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Article Behavioural Response of Juvenile Common ( carpio) and Juvenile Channel Catfish ( punctatus) to Strobe Light

Jaewoo Kim 1,2,3,* , Caitlyn Bondy 1, Catherine M. Chandler 1,4 and Nicholas E. Mandrak 2

1 Great Lakes Laboratory for and Aquatic Sciences, Fisheries and Oceans , 867 Lakeshore Road, Burlington, ON L7S 1A1, Canada; [email protected] (C.B.); [email protected] (C.M.C.) 2 Department of Biological Sciences, University of Toronto Scarborough, 1265 Military Trail, Toronto, ON M1C 1A4, Canada; [email protected] 3 Golder Associates, Ltd., 2535-3rd Avenue S.E., Calgary, AB T2A 7W5, Canada 4 Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, ON K1N 6N5, Canada * Correspondence: [email protected]

 Received: 6 March 2019; Accepted: 28 April 2019; Published: 4 May 2019 

Abstract: The movement of can be regulated by behavioural manipulation through non-physical barrier systems. Aquatic are becoming one of the major management issues in , and threaten native aquatic ecosystems, including . Placements of non-physical barriers in waterways can help disrupt the movement of invasive fish. This study examined the effect of a strobe-light stimulus on the avoidance behaviour of two proxy species, juvenile (Cyprinus carpio) and juvenile channel (Ictalurus punctatus), in a controlled laboratory environment. For each species, three sequential treatments of pre-stimulus, strobe-light stimulus, and post-stimulus for 30 min periods were recorded on acclimated groups of 5 juvenile common carp and 5 juvenile using 15 and 13 replicates, respectively. The distribution of juvenile common carp individuals throughout the tank did not change significantly with treatment, nor did cohesive grouping behaviour. Similarly, there were no significant differences across experimental treatments in average location/distance of juvenile channel catfish relative to the strobe light or degree of cohesion in response to the strobe light. Non-physical barriers have been widely reported to vary between species and environmental conditions. These results suggest that strobe lights evoke no avoidance or attractive responses in juvenile common carp and juvenile channel catfish, and will likely not be an effective barrier to inhibit movements of juvenile invasive fishes.

Keywords: fish barrier; deterrence; invasive species; juvenile life stages; fisheries management; conservation

1. Introduction In recent years, aquatic invasive species has become one of the major management concerns, given their negative impact on our ecosystems, and increasing population size and habitat ranges [1–3]. Physical barriers in aquatic environments are common, effective management techniques that can physically obstruct fish movement [4]. Physical barrier technologies may be useful in managing fishes in reservoir environments, however, areas with high debris loads increase maintenance requirements, rendering the application of such barriers impractical [5]. By contrast, non-physical deterrence systems do not constrain flow or restrict navigation and, in some cases, allow the movement of non-target organisms [6]. Non-physical deterrence systems can be defined as any stimuli that discourages or prevents a species from moving into specified areas [6]. Non-physical deterrence systems rely on the

Fishes 2019, 4, 29; doi:10.3390/fishes4020029 www.mdpi.com/journal/fishes Fishes 2019, 4, 29 2 of 10 manipulation of sensory systems that drive species behaviour. Various external stimuli have been used to manipulate fish behaviour, such as stroboscopic lights [7,8], broadband sound [9,10], and chemical cues (e.g., alarm cue) [11–13]. The effectiveness of various non-physical deterrence systems is variable across species, and success is dependent on the nature of the behavioural response [5–7,14–17]. Such variation suggests that no single deterrence method will be a ‘one-size fits all’ solution, and that the installation of non-physical deterrence systems must be tailored towards specific project goals [6]. While barrier success varies with objective, species, device, and location, strobe lights have been effective for the greatest number of species perhaps due to their relatively easier deployment [4,7,8,17]. Fish use several sources to gather information from their external environment [18]. The cues most often used for daily activity (feeding, mating, avoiding predators) are light, sound, temperature, vibration, and chemicals [18]. Therefore, the sensory systems to detect these cues can be well-developed [18]. The aquatic environment is full of visual indicators, and teleost fishes are highly adapted to detect changes in the visual environment [7,13]. Strobe lights are a form of non-physical deterrence system and can be defined as intermittent high-intensity light for short durations [14,19]. The use of strobe lights as a deterrence system for common carp (Cyprinus carpio) aims to manipulate this anatomical characteristic [7]. The strobe light provides sufficient light for orientation, however, the abnormal pulsating changes in brightness stimulate avoidance reactions [6,16]. Strobe lights have received greater attention as a behavioural stimulus, predominantly in guiding migrating salmonids [14,20]. Strobe lights have been shown to deter a variety of species (e.g., chinook (Oncorhynchus tshawytscha), common carp, gizzard shad (Dorosoma cepedianum), (Micropterus salmoides), rainbow smelt (Osmerus mordax), and (Perca flavescens)) [7,14,15,17,18,21]. For example, adult common carp stayed away from strobe lights [7]. In general, most studies to date have evaluated sensitivity of fishes to strobe lights in adults or sub-adults, but not juvenile stages. Moreover, most studies tend to focus only on target species, hence limited information is available for potential impacts on non-target or native species including channel catfish [6]. The development of non-physical barrier technologies aims to deter invasive species by disrupting potential dispersal routes. Prevention of aquatic invasive species entering new regions provides a higher probability of conservation success, as removing established populations is nearly impossible [3,22]. For our research, juvenile (i.e., age-0) common carp were used as a model organism for target species, and juvenile (i.e., age-0) channel catfish (Ictalurus punctatus) as non-target species. Common carp is an in Canada, , , Kenya, and elsewhere in the world [23–25]. They are considered harmful to native fishes and plants as they destroy submerged aquatic plants and increase the turbidity of surrounding water [24–26]. Channel catfish are native to North America, including the Great Lakes [26]. This study used juvenile common carp and juvenile channel catfish to determine the effectiveness of a strobe-light system on avoidance behaviour in juvenile fishes.

2. Results The mean number of fishes differed significantly between grid sections (A, B, and C) but not between treatments (pre-stimulus, stimulus, and post-stimulus) for both juvenile channel catfish and juvenile common carp. There was no significant difference on the mean score of cohesive groupings between treatments.

2.1. Juvenile Channel Catfish There was no significant interaction between grid sections (A, B, and C) and treatments (pre-stimulus, stimulus, and post-stimulus) on the mean number of fish (ANOVA: F4, 126 = 0.83, p = 0.51, Figure1). The mean number of fish did differ significantly between sections (ANOVA: F2, 126 = 78.60, p < 0.001). Fish spent more time in section A and C compared to B (Figure1). However, the mean number of fish did not differ significantly between treatments (ANOVA: F2, 126 = 0.17, p = 0.85; Figure1). Moreover, a two-factor repeated-measures ANOVA yielded no significant difference in the mean score of cohesive Fishes 2019, 4, x FOR PEER REVIEW 3 of 10

1). Moreover, a two-factor repeated-measures ANOVA yielded no significant difference in the mean score of cohesive groupings between treatments (p > 0.05). In general, juvenile channel catfish stayed in a group of three or more most of the time.

2.2. Juvenile Common Carp There was no significant interaction between sections and treatments on the mean number of fish (ANOVA: F4, 108 = 0.66, p = 0.62; Figure 2). The mean number of fish significantly differed between sections (ANOVA: F2, 108 = 21.3, p < 0.001), where fish spent more time in location A and C, compared to B (Figure 2). However, the mean number of fish did not differ significantly between treatments (ANOVA: F2, 108 = 0.30, p = 0.74; Figure 2). In addition, the mean score of cohesive groupings did not differ significantly between treatments (ANOVA: F2, 21 = 0.93, p = 0.41). Much like juvenile channel catfish, juvenile common carp stayed in a group of three or more most of the time.

3. Discussion Although juvenile channel catfish and common carp did not exhibit significant responses to the three treatments (pre-stimulus, stimulus, post-stimulus), they did exhibit a preference to certain sections within the experimental tank. All grid sections were assumed to be equal, however, the results suggest that the average distributions per grid section were different during the pre-stimulus treatment. This may be an inevitable result of protective cover [27,28] as sections A & C both included Fishescorners2019, 4of, 29 the tank that offered more security than the center grid section. Furthermore, the tank3 of 10 drainpipe was also located in grid section A, which could have caused an attractive effect. This may be a more appropriate test of avoidance behaviour, as the test groups demonstrated preference within groupingsthe tank. between Conclusions treatments about (pthe> 0.05).ability In of general, the stimulus juvenile to channel remove catfish fish from stayed previous in a group areas of threeof orpreference more most can of theclearly time. demonstrate stimulus aversion [29].

Figure 1. Mean ( SE) number of juvenile common carp per minute per grid (N = 15). Figure 1. Mean ±(±SE) number of juvenile common carp per minute per grid (N = 15). 2.2. Juvenile Common Carp There was no significant interaction between sections and treatments on the mean number of fish (ANOVA: F4, 108 = 0.66, p = 0.62; Figure2). The mean number of fish significantly di ffered between sections (ANOVA: F2, 108 = 21.3, p < 0.001), where fish spent more time in location A and C, compared to B (Figure2). However, the mean number of fish did not di ffer significantly between treatments (ANOVA: F2, 108 = 0.30, p = 0.74; Figure2). In addition, the mean score of cohesive groupings did not differ significantly between treatments (ANOVA: F2, 21 = 0.93, p = 0.41). Much like juvenile channel catfish,Fishes 2019 juvenile, 4, x FOR PEER common REVIEW carp stayed in a group of three or more most of the time. 4 of 10

FigureFigure 2. 2.MeanMean (±SE) ( SE) number number of of juvenile juvenile channel channel catfishcatfish perper minuteminute per per grid grid (N (N= =13). 13). ± The avoidance of the strobe-light stimulus was quantified by the spatial distribution of individuals during the 30 min stimulus treatment. The lack of significance between average frequencies of fish distribution within the tank demonstrates that the strobe light had no effect on the test individuals. While Figures 2 and 3 suggest that there was a decline in the distribution of both species in section A, and an increase in section C, marginal overlap demonstrates no significant change (i.e., p > 0.05). Königson et al. [18] suggested that it is not necessary to startle fish, but to provide a component of the response that controls movement in a specific direction. The flash duration of the strobe light is a more important factor rather than the spectral composition of the light source, potential changes to flash duration in the present study could have yielded dramatically different results [17,19].

Figure 3. Layout of experimental tanks with scoring grid. Dashed lines represent the grid sections used to determine fish distributions. The black square represents the strobe-light stimulus. The grey circle represents the submerged GoPro camera.

Table 1. Rules and examples for cohesion scoring based on number and formation of fishes in the tank.

Cohesion Group Number of Fish Example Configurations and Points

Fishes 2019, 4, x FOR PEER REVIEW 4 of 10

Fishes 2019, 4, 29 4 of 10

3. Discussion Although juvenile channel catfish and common carp did not exhibit significant responses to the three treatments (pre-stimulus, stimulus, post-stimulus), they did exhibit a preference to certain sections within the experimental tank. All grid sections were assumed to be equal, however, the results suggest that the average distributions per grid section were different during the pre-stimulus treatment. This may be an inevitable result of protective cover [27,28] as sections A & C both included corners of the tank that offered more security than the center grid section. Furthermore, the tank drainpipe was also located in grid section A, which could have caused an attractive effect. This may be a more appropriate test of avoidance behaviour, as the test groups demonstrated preference within the tank.

ConclusionsFigure about 2. the Mean ability (±SE) of number the stimulus of juvenile to remove channel fish catfish from per previous minute areasper grid of preference(N = 13). can clearly demonstrate stimulus aversion [29]. TheThe avoidance avoidance of theof strobe-lightthe strobe-light stimulus stimulus was quantified was quantified by the spatialby the distribution spatial distribution of individuals of duringindividuals the 30 minduring stimulus the 30 treatment. min stimulus The lacktreatment. of significance The lack between of significance average between frequencies average of fish distributionfrequencies within of fish the distribution tank demonstrates within the tank that demon the strobestrates light that had the nostrobe effect light on had the no test effect individuals. on the Whiletest Figuresindividuals.2 and While3 suggest Figures that 2 thereand 3 was suggest a decline that there in the was distribution a decline in of the both distribution species in of section both A, andspecies an increasein section in A, section and an C, increase marginal in overlap section demonstratesC, marginal overlap no significant demonstrates change no (i.e., significantp > 0.05). Königsonchange et(i.e., al. [p18 > ]0.05). suggested Königson that itet isal. not [18] necessary suggested to startlethat it fish,is not but necessary to provide to startle a component fish, but of to the provide a component of the response that controls movement in a specific direction. The flash response that controls movement in a specific direction. The flash duration of the strobe light is a more duration of the strobe light is a more important factor rather than the spectral composition of the light important factor rather than the spectral composition of the light source, potential changes to flash source, potential changes to flash duration in the present study could have yielded dramatically duration in the present study could have yielded dramatically different results [17,19]. different results [17,19].

FigureFigure 3. Layout3. Layout of of experimental experimental tanks tanks with with scoringscoring grid.grid. Dashed lines lines represent represent the the grid grid sections sections usedused to determineto determine fish fish distributions. distributions. The The black black squaresquare representsrepresents the strobe-light strobe-light stimulus. stimulus. The The grey grey circlecircle represents represents the the submerged submerged GoPro GoPro camera. camera. Cohesive behaviour among is an attempt to dilute predation risk [30]. A higher number Table 1. Rules and examples for cohesion scoring based on number and formation of fishes in the of individualstank. in a group decreases the probability that an individual will be harmed [30]. This research showed that the frequency of cohesive grouping between test individuals did not vary with treatment. Fish in dense aggregations often produce different responses in comparison to individuals and may Cohesion Group respond to light stimuli differentlyNumber [14 of]. Fish Cohesive behaviour Example is used Configurations for various activities among and Points species, the formation of temporary or permanent groups allows for potential fitness advantages as a result of higher quality reproduction, foraging or defense [31]. For example, sticklebacks often inspect a predator in pair groupings, as the probability of predation during inspection is reduced by 50% when a partner is present [30]. As the strobe-light barrier provides no harm to individuals, it is possible that experimental individuals evaluated their interactions with the barrier. In escape studies, fish often swim parallel to the barrier, turn away and retreat, and then approach the barrier again [32]. These behaviours were thought to be testing the barrier and when no harm was encountered individuals escaped confinement [32]. The relative indifference of juvenile channel catfish and juvenile common carp to strobe lights suggests that strobe lights would not be an effective barrier. In contrast, adult common carp stayed away Fishes 2019, 4, 29 5 of 10 from strobe-lights [7]. Channel catfish also showed low sensitivity to strobe lights when compared to largemouth bass, , and yellow perch [15]. Previous literature as suggested that foraging schedules and activity rates may be linked to the efficacy of non-physical barriers [32]. For example, largemouth bass had higher foraging success during daylight hours while also having greater escape rates during that time [33]. Pelagic fishes, such as alewife ( pseudoharengus), gizzard shad, and rainbow smelt, were repelled by bubble barriers, while demersal fishes, such as the white sucker (Catostomus commersonii), were attracted [16]. The flash rate of the strobe light was set to random flash (manufacturer setting), which could have been too similar to natural conditions. Strobe-light efficacy depends on a flash rate that is distinguishable from natural light fluctuations produced by waves and clouds [34]. Many studies note lower strobe-light efficacy during daylight hours, suggesting that ambient light dilutes the effect of the strobe light [4,14,19,29]. Furthermore, light as a deterrence system varies with wavelength and turbidity [14,18,19]. The wide range of studies presenting variable degrees of barrier efficacy with environmental and species traits suggests that there must be a case-by-case analysis to determine suitability. Strobe-light barriers are well known in fish management for their low cost and simplicity, and have attracted much attention in the application of invasive species management. This study suggests that strobe lights will not be an effective barrier to the spread of invasive common carp juveniles, however, studies examining the different frequencies of strobe light or using different tank size may provide more reliable results.

4. Materials and Methods

4.1. Experimental Subject and Set-Up The study was conducted in the Aquatic Life Research Facility at the Canada Center for Inland Waters in Burlington, Ontario, Canada. One experimental tank (3.04 m 1.06 m 0.42 m) was used × × to conduct 1.5 h trials for either juvenile common carp (15 replicates) and juvenile channel catfish (13 replicates). Only one-half of the experimental tank was used, to ensure that individuals could be recorded by camera (Figure3). Each trial consisted of three sequential 30 min treatment periods on groups of 5 randomly selected juveniles (i.e., age-0) common carp (n = 75, length = 6.12 0.67 cm) ± or juvenile (i.e., age-0) channel catfish (n = 65, length = 7.60 0.45 cm). For the experiment, each ± individual fish was only used once. The three treatments included a pre-stimulus period (strobe light off), a stimulus period (strobe light on), and a post-stimulus period (strobe light off). Prior to the study in July 2015, juvenile common carp and juvenile channel catfish were purchased from Osage Catfisheries (Osage Beach, MO, USA). Fishes were housed in a series of large recirculating tanks (~689 L). Water temperatures were maintained at approximately 14 ◦C. Fishes were fed (1.0%–1.5% of fish weight) daily with commercial fish food (Profishent Chow, Martin Mills, Inc., Elmira, ON, Canada) and maintained in a 12 h/12 h (dark/light) cycle. The experimental tank was enclosed with blackout blinds to maintain controlled lighting conditions. Above-tank lighting was automated on a daylight-hour schedule, dimming from 25% to zero by 21:00, and increasing from zero to 25% by 07:00. For each species, test groups of juvenile fishes were transferred to the experimental tank using disinfected dip nets 17 h before the sequential treatments were applied. Water temperature was maintained at 12–14 ◦C, and water flow was provided at all times to keep consistent temperatures. An aeration bar was placed on the side of the tank where fish were not present. The physical barrier placed to divide the tank prevented fish from moving out of the filming area without disrupting water flow. The submerged strobe light (See Brite LED Underwater light, IAS Products Ltd., North Vancouver, BC, Canada) with random flashes (0.05–1.0 s flash rate, where each flash lasts 1.5 ms) was placed opposite the barrier and attached to the center of the wall of the experimental tank (Figure3). This strobe light (See Brite LED Underwater light, IAS Products Ltd., North Vancouver, BC, Canada) uses 110 volt AC 10% at 50/60 Hz and consists of 4 LED (light intensity ± = 13,402 lumens) circuit board panels radiating light at 360◦ with a full spectrum (400–700 nm), and had a 1.8 ampere demand. Strobe-light strength (LED light intensity = 13,402 lumens) was measured Fishes 2019, 4, 29 6 of 10 using a portable lux meter with a waterproof probe (Millwaukee Instruments, Inc.). In ambient light conditions (i.e., with experimental room lights on but strobe light turned off), light levels within the tank ranged from 0 to 66 lux in the experimental tank (mean light level = 15.58 lux, n = 12), whereas with strobe lights including experimental room lights turned on, light levels ranged from 783 to 31,600 lux (mean light level = 6176.00 lux, n = 6) [7]. Due to strobing, precision of the portable light meter, and a relatively small size of tank, we only reported the ranges of light levels measured within the tank. Light levels were kept consistent and appropriate for this experimental design; light levels were highest near the strobe light when flashing and decreased as the distance from the strobe light increased, with the lowest light levels observed at the far end of the tank. At the end of each trial, the experimental tank was drained and rinsed before the next test group was introduced to reduce the potential effect of chemical cues that may have been produced during the previous trial.

4.2. Data Collection and Analysis Each trial was recorded for the full duration using a submerged camcorder (GoPro Hero) and overhead camcorder (Canon XA-25). Trial recordings were used to quantify juvenile common carp and juvenile channel catfish behaviour during treatment sessions. Within the experimental tank, red waterproof tape was applied to laterally divide the filming arena into three sections, labeled A to C, starting closest to the camera’s field of view (Figure3). The spatial distribution of fish during each treatment session was analyzed using a time-sampling approach. At 1 min intervals, the number of fish in each grid section of the tank was recorded manually, totaling 30 observations per treatment. The total number of fish observed in each grid section over the 1 min interval was totaled and averaged across all trials. Group cohesion is also a measure of avoidance behaviour in animals [35,36]. Cohesive behaviour was evaluated using JWatcher [37,38] scoring software for behavioural analyses. The ethogram for the analysis aimed to identify a continuous tally of grouping interactions within each treatment session. A grouping was defined as two or more individuals within one body length or less distance, for at least five seconds. The five second duration of grouping ensured that positions were intentional by the individuals in the group, and not a byproduct of passive movement within the tank [35,39,40]. Average total body length of test individuals was 6.12 0.67 cm, representing 4% of the tank length. ± It was assumed that individual position within less than one body length indicated intentional positioning [7,35,40,41]. Cohesion groups were denoted as ‘2’ through ‘5’, corresponding directly to the number of individuals in the group as events (Table1). The cohesion group ‘1’ described states where all fish in sight were greater than one body length away from all other individuals (no grouping behaviour present). The ‘0’ cohesion group represented states where no individuals were in the camera’s field of view and, thus, no observations of cohesive behaviour could be recorded. The proportion of time spent out of sight was totaled, and treatment sessions that exceeded 15 min were excluded from the analysis. The frequency of grouping type was determined by totaling the number of observations of a grouping and dividing by the total number of observations made during the treatment session. The average frequency was calculated across all trials for each treatment. For statistical analyses, two-way ANOVAs were used to examine the differences between mean number of fish per minute, per grid, between all treatments. The predictor variables were treatments and grid sections, and the response variable was the total number of fish per grid section. The null hypothesis was that there were no significant differences in the frequencies of fish per grid section between treatments and grid sections. Moreover, single-factor repeated-measures ANOVA was used to determine if there was a significant difference in the mean frequency of a grouping type between treatments. The predictor variable was treatment type, and the response variable was the average frequency of grouping type. The null hypothesis was that there were no significant differences between treatments. All statistical tests used a significance level of 0.05 and were conducted using SPSS v23.0. Fishes 2019, 4, x FOR PEER REVIEW 5 of 10 Fishes 2019, 4, x FOR PEER REVIEW 5 of 10

Fishes 2019, 4, x FOR PEER REVIEW 5 of 10

0 1 Fishes 2019, 4, x FOR PEER REVIEW 5 of 10 0 1 Fishes 2019, 4, 29 Fishes 2019, 4, x FOR0 PEER REVIEW 1 5 of 10 7 of 10

Fishes 2019, 4, x FOR PEER REVIEW 5 of 10 Table 1. Rules and examples for cohesion10 scoring based on21number and formation of fishes in the tank. 1 2 Cohesion Group and Points Number0 of Fish1 Example Configurations 1 2

0 10 1 21 3 in a2 line 2 3 in a line 11 2 2 2 3 in a line

1 2 2 3 in a line 2 3 in 3tight in a groupline 3 3 inor tight 4 in agroup line

23 3 in a line or 4 in a line 3 3 in tight group or 4 in a line 3 in tight group 3 2 or 3 4 in in a a line line 3 in tight group 3 4 in tight group 4 or 4 in a line 34 inor tight 5 in agroup line 4 4 in tight group4 or 5 in a line 3 or 5 in a line 4 inor tight4 in a group line 4 3 in tight group 3 or 5 in a line or 4 in a line 4 in tight group 4 5 5 in tight5 group 5 inor tight 5 in agroup line 5 4 5 in tight group 4 or 5 in a line 5 5 in tight group 4 in tight group 4 Cohesive behaviour amongor animals5 in a line is an attempt to dilute predation risk [30]. A higher number Cohesive 5behaviour among 5 in animals tight group is an attempt to dilute predation risk [30]. A higher number of individuals in a group decreases the probability that an individual will be harmed [30]. This ofresearch individuals showed in thata group the frequency decreases of the cohesive probability grouping that betweenan individual test individuals will be harmed did not [30].vary Thiswith Cohesive5 behaviour among 5 in animals tight group is an attempt to dilute predation risk [30]. A higher number researchtreatment. showed Fish in that dense the aggregations frequency of oftencohesive produc groupinge different between responses test individuals in comparison did notto individuals vary with of individuals in a group decreases the probability that an individual will be harmed [30]. This treatment.and may respond Fish in dense to light aggregations stimuli differently often produc [14].e Co differenthesive responsesbehaviour inis comparisonused for various to individuals activities researchCohesive showed5 behaviour that the frequency among 5 in tightanimals of groupcohesive is an attemptgrouping to between dilute predation test individuals risk [30]. did A highernot vary number with andamong may species, respond the to lightformation stimuli of differently temporary [14]. or Copermanenthesive behaviour groups isallows used forfor variouspotential activities fitness treatment.of individuals Fish in in dense a group aggregations decreases often the producprobabilitye different that an responses individual in comparison will be harmed to individuals [30]. This amongadvantagesCohesive species, as behaviour athe result formation amongof higher animalsof temporaryquality is an reprod attempt or permanentuction, to dilute foraging groupspredation or allowsdefense risk [30]. for [31]. Apotential higher For example,number fitness andresearch may respond showed tothat light the stimulifrequency differently of cohesive [14]. gr Cooupinghesive between behaviour test isindividuals used for various did not activitiesvary with ofadvantagessticklebacks individuals asoften ina aresult inspectgroup of decreasesahigher predator quality the in probability pairreprod groupings,uction, that an foragingas individual the probability or defense will be of [31].harmed predation For [30].example, during This amongtreatment. species, Fish inthe dense formation aggregations of temporary often produc or permanente different responsesgroups allows in comparison for potential to individuals fitness researchsticklebacksinspectionCohesive showed is often reduced behaviour that inspect the by frequencyamong50% a predator when animals of a cohesivepartnerin is pair an attemptis grgroupings, presoupingent to [30]. dilutebetween as Asthe predation the testprobability strobe-light individuals risk [30]. of barrier predationdid A higher not provides vary numberduring with no advantagesand may respond as a result to light of stimulihigher differentlyquality reprod [14].uction, Cohesive foraging behaviour or defense is used for[31]. various For example, activities treatment.inspectionofharm individuals to individuals, Fishis reduced in densea group itby is aggregations 50%possible decreases when that a oftenpartnerthe experimental probability produc is prese differentindividualsent that [30]. an responsesAs individual evaluatedthe strobe-light in comparisonwill their be interactionsbarrier harmed to provides individuals [30]. with This theno sticklebacksamong species, often theinspect formation a predator of temporary in pair groupings, or permanent as the groups probability allows of for predation potential during fitness andharmresearchbarrier. may to individuals, In showedrespond escape that tostudies, itlight the is possible frequency stimuli fish often thatdifferently of swim experimentalcohesive parallel [14]. gr oupingCo individualstohesive the between barrier, behaviour evaluated test turn individualsis away usedtheir and forinteractions did variousretreat, not vary activities andwith withthen the inspectionadvantages is reducedas a result by 50% of higherwhen aquality partner reprodis presuction,ent [30]. foraging As the strobe-light or defense barrier [31]. Forprovides example, no amongbarrier.treatment.approach species,In theFishescape barrier in the densestudies, formationagain aggregations fish [32]. often ofThese temporary swimoften behaviours producparallel or e permanent were todifferent the thought barrier, responses groups to turn be allowsintestingaway comparison andthefor barrierretreat,potential to individuals andand fitness whenthen harmsticklebacks to individuals, often inspectit is possible a predator that experimental in pair groupings, individuals as evaluatedthe probability their interactionsof predation with during the advantagesapproachandno harm may wasrespondthe as barrierencountered a resultto lightagain of stimuli individu[32].higher These differently qualityals escapedbehaviours reprod [14]. confinement Couction,werehesive thought foraging behaviour[32]. to beor testingisdefense used the for [31]. barriervarious For and example,activities when barrier.inspection In escape is reduced studies, by 50%fish whenoften swima partner parallel is pres toent the [30]. barrier, As the turn strobe-light away and barrier retreat, provides and then no sticklebacksnoamong harmThe species, was relative often encountered the indifference inspect formation individua predator of ofjuvenile alstemporary escapedin channelpair confinementgroupings,or catfishpermanent and as [32]. juvenilethegroups probability commonallows offor carp predation potential to strobe duringfitness lights approachharm to individuals,the barrier again it is possible [32]. These that behavioursexperimental were individuals thought evaluatedto be testing their the interactions barrier and with when the inspectionadvantagessuggestsThe relativethat is asreduced strobe a indifferenceresult lights by 50%of wouldhigher whenof juvenile not qualitya partnerbe anchannel reprodeffe is presctive catfishuction,ent barrier. [30]. and foraging AsInjuvenile contrast,the strobe-lightor common defense adult common carpbarrier[31]. to For strobeprovides carp example, stayedlights no nobarrier. harm wasIn escape encountered studies, individu fish oftenals escapedswim parallel confinement to the barrier,[32]. turn away and retreat, and then harmsuggestssticklebacksaway to from individuals, that strobe-lights oftenstrobe inspect lightsit is possible [7]. woulda predatorCha thatnotnnel beexperimental incatfish an pair effe ctivegroupings,also individuals showedbarrier. as Inlow the evaluatedcontrast, sensitivityprobability adult their to commoninteractionsof strobe predation lightscarp with duringstayed when the approachThe relative the barrier indifference again [32]. of juvenile These behaviours channel catfish were and thought juvenile to be common testing thecarp barrier to strobe and lights when barrier.awayinspectioncompared from In escapeis tostrobe-lights reduced largemouth studies, by 50%[7]. fishbass, whenCha often chinooknnel a swim partner catfish salmon,parallel is also pres toandshowedent the [30].yellow barrier, lowAs the perch sensitivityturn strobe-light away[15]. toPreviousand strobebarrier retreat, lightsliteratureprovides and when then noas suggestsno harm that was strobe encountered lights would individu notals be escaped an effective confinement barrier. In[32]. contrast, adult common carp stayed approachcomparedharmsuggested to individuals, the tothat barrierlargemouth foraging itagain is possibleschedules bass,[32]. These chinookthat and experimental behaviours activity salmon, rates were andindividuals may thoughtyellow be linked evaluated perchto be to testing [15].the their efficacyPrevious the interactions barrier of literaturenon-physical and with when theas away Thefrom relative strobe-lights indifference [7]. Cha of juvenilennel catfish channel also catfishshowed and low juvenile sensitivity common to strobecarp to lights strobe when lights nosuggestedbarrier.barriers harm In[32].was thatescape encounteredFor foraging example, studies, schedules individu largemouthfish often alsand swim escaped bassactivity parallelhad confinement rateshigh toer may theforaging bebarrier, [32]. linked success turn to theawayduring efficacy and daylight retreat, of non-physical hours and whilethen comparedsuggests thatto largemouthstrobe lights bass, would chinook not be ansalmon, effective and barrier. yellow In perchcontrast, [15]. adult Previous common literature carp stayed as barriersapproachalso Thehaving [32]. relative the For greaterbarrier example,indifference againescape largemouth [32]. ofrate juvenileTheses during bassbehaviours channel hadthat high timecatfish wereer foraging[33]. thoughtand Pela juvenile success gicto befishes, common testing during such the daylightcarp barrieras to alewife strobe hours and lightswhilewhen(Alosa suggestedaway from that strobe-lights foraging schedules [7]. Cha andnnel activity catfish ratesalso showedmay be linkedlow sensitivity to the efficacy to strobe of non-physical lights when suggestsalsonopseudoharengus harm having thatwas greaterstrobeencountered), gizzard lights escape shad, wouldindividu rate and snot alsrainbowduring be escaped an thateffe smelt, confinementctive time were barrier. [33]. repelled Pela [32].In contrast,gic by bubblefishes, adult barriers,such common as whilealewife carp demersal stayed(Alosa barrierscompared [32]. toFor largemouth example, largemouth bass, chinook bass hadsalmon, high erand foraging yellow success perch during [15]. 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Fishes 2019, 4, 29 8 of 10

Author Contributions: J.K.: Experimental planning, main writing, review & writing, statistical analysis; C.B.: experiment, data analysis, writing; C.M.C.: experiment, data analysis, writing; N.E.M.: writing, review & editing, funding acquisition. Funding: This research was funded by the Program at Fisheries and Oceans Canada (DFO). JK was funded by a visiting fellowship from Natural Sciences and Engineering Research Council (NSERC), funded by the DFO Asian Carp Program. Acknowledgments: This research was funded by Asian Carp Program at Fisheries and Oceans Canada (DFO). Becky Cudmore and Gavin Christie provided program oversight. Field crews at DFO included David Marson, D’Arcy Campbell, Erin Gertzen, Brad Doyle, Monica Choy, Hadi Dhiyebi, Paul Bzonek, and many summer student technicians through DFO’s Federal Student Work Experience Program (FSWEP). Experiments were conducted at Aquatic Life Research Facility, Canada Centre for Inland Waters with logistic support from Alicia Mehlenbacher, Quintin Rochfort, and Jaclyn Gugelyk at Environment and Climate Change Canada (ECCC). We also thank Frances Pick at University of Ottawa for her comments on the manuscript and supervision of C.M.C.’s honour thesis. This study was conducted according to Use Protocol approved by Animal Care Committee at Canada Centre for Inland Waters. Conflicts of Interest: The authors declare no conflict of interest.

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