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MARINE PROGRESS SERIES Vol. 167: 215-226, 1998 Published June 18 Mar Ecol Prog Ser l

Effect of light on juvenile shoaling and their interaction with predators

CliffordH. Ryer*, Bori L. Olla

Fisheries Group, Science Center, National Marine Fisheries Service, NOAA, Hatfield Marine Science Center, Newport, Oregon 97365, USA

ABSTRACT: Research was undertaken to examine the influence of light lntenslty on the shoaling behavior, activity and anti-predator behavior of juvenlle walleye pollock Theragra chalcogramrna. Under a 12 h light/l2 h dark photoperiod, juveniles displayed a diurnal shoaling and activity pattern, characterized by swimming in cohesive groups during the day, with a cessation of shoaling and decreased swlmmlng speeds at nlght. Prior studies of school~ngfishes have demonstrated distinct light thresholds below which school~ngabruptly ceases. To see if this threshold effect occurs in a predomi- nantly shoaling , like juvenile walleye pollock, another experiment was undertaken in which illumination was lourered by orders of magnitude, glrrlng fish 20 mln to adapt to each light intensity Juvenlle walleye pollock were not characterized by a d~stinctlight threshold for shoaling; groups grad- ually dispersed as light levels decreased and gradually recoalesced as light levels increased. At light levels below 2.8 X 10.~pE SS' m-" juvenile walleye pollock were so dispersed as to no longer constitute a . Exposure to simulated risk had differing effects upon fish behavior under light and dark cond~tionsBrief exposure to a mndc! prerlst~r:E !he .'ark c;i;ssd fish to ~WIIIIidsier, ior 5 or 6 min, than fish which had been similarly startled In the light. Chronic exposure to a l~vingpredator produced simllar results; fish tended to swlm slower when a predator was present in the light, but faster when a predator was present in the dark. In the light, shoallng and/or school~ngprovide protection against predators. But in the dark, with f~shunable to see one another, increased prey activlty resulting from predator may lead to accelerated dispersal of prey Thus, perceived predation risk may have different effects upon the spatial d~stnbutionof luvenlle walleye pollock under light and dark conditions. This has implications for surv~val,as f~shwh~ch have become widely scattered durlng the darkness may take longer to reform shoals at dawn, resulting in greater predation nsk.

KEYWORDS Schooling Spat~aldistnbut~on Tw~lighthypothesis Predator-prey Swimming speed Illumination

INTRODUCTION dividuals within a school (Partridge & Pitcher 19801, it is unlikely that in the wild many species are capable of The means by which fish forin and maintain shoals schooling in the absence of sufficient light. Thls impres- and schools has long been of interest to fisheries scien- sion is supported by observational (Emery 1973, Helf- tists and behavioral ecologists. Since the early investi- man 1979) and bioacoustical studies which generally gations of schooling, it has been evident that the show that shoals and schools disperse at night (Appen- amount of light reaching the fish's largely deter- zeller & Leggett 1992, Brodeur & Wilson 1996). Since mines whether or not it is able to school (Breder 1951, ambient light in marine and aquatic may vary Atz 1953, Shaw 1961, Hunter 1968). Although other greatly according to depth, , season, lunar senses, such as the system, may play an im- stage and cloud cover (McFarland 1986), the meaning portant role in the spatial and angular orientation of in- of 'night', relative to light levels, 1s rather ambiguous. Numerous studies have been directed towards deter- mining the relationship between light intensity and some measure of the ability or inclination of fish to form

O Inter-Research 1998 Resale offull article not pei-n~itted 216 Mar Ecol Prog Ser 167: 215-226, 1998

cohesive groups. In some species there is a gradual de- In this paper we examine the influence of light on the crease in schooling or shoaling as light levels decrease shoaling and anti-predator behavior of juvenile wall- (John 1964), while for others, there is a threshold light eye pollock Theragra chalcogramma. The walleye pol- level at which this behavior abruptly ceases. This lock is a pelagic species of the northern Pacific threshold varies from 3.7 X 10-2 pE S-' m-* for the which supports a large commercial and, in its Hawaiian silverside Pranesus insularurn (Major 1977) juvenile phase, is preyed upon by numerous species of to 1.8 X lO-? pE S-' m-2 for the Atlantic groundfish, and marine mammals (Livingston scombrus (Glass et al. 1986), with most other 1993). For juveniles, gregarious behavior typically con- species examined falling somewhere between these sists of shoaling (Pitcher 1980), with fish forming extremes (Higgs & Fuiman 1996).Putting this in an eco- loosely structured groups (Ryer & Olla 1995).Juveniles logical context, Glass et al. (1986) concluded that At- will form more highly structured schools (Pitcher lantic mackerel should be able to school to depths of 1980),but only when they are rapidly moving from one 20 m on clear starlit nights and perhaps to 80 or 100 m location to another. In the Bering Sea, juvenile walleye on clear moonlit nights, whereas cloud cover could pollock have been reported to exhibit a diel pattern of make schooling at night impossible, even at the surface. vertical migration, moving upwards into surface wa- One of the well-established functions of gregarious ters during dusk, followed by a return to depth around behavior, e.g. shoaling, schooling, and - dawn (Bailey 1989, Tang et al. 1996). In the western ing, is to facilitate the individual's ability to detect and Gulf of Alaska, Brodeur & Wilson (1996) observed a mitigate predatory threat (Lazarus 1979). Individuals similar diel migration, but also reported that juveniles in groups are likely to detect predators at greater dis- formed highly cohesive aggregations near the bottom tances (Magurran et al. 1985) and are often less vul- during the day and dispersed in the surface waters nerable due to coordinated escape responses (Pitcher during the night. Without knowledge of the in situ light & Parrish 1993) which result in predator confusion levels and light thresholds for shoaling behavior, it is (Neill & Cullen 1974, Landeau & Terborgh 1986) as impossible to know whether such dispersive behavior well as dilutiodattack abatement effects (Bertram results from fish actively leaving social groups to indi- 1978, Turner & Pitcher 1986). Attacks by predators are vidually seek out prey (Ryer & Olla 1995), or from the frequently concentrated during twilight periods (Major inability of fish to maintain shoals at the ambient light 1977, Parrish 1992),when prey are silhouetted against levels involved. A prior laboratory study demonstrated the downwelling light from the surface and predators that juvenile walleye pollock shoals become less cohe- approaching from below are difficult for prey to detect sive at night (Sogard & Olla 1996). But, this study uti- against the darkness of the depths (Munz & McFarland lized a night-time light level of 0.1 pE S-' m-', which is 1973). Yet, little is known about how predators and more typical of twilight than night-time, leaving open prey interact in darkness and how this will influence the question of how lower light levels influence shoal- the spatial distribution of prey. With their dependence ing. Beyond its interest from a purely ecological per- upon vision, it is clearly not feasible for most shoaling spective, knowledge of distribution patterns in juve- and schooling species to maintain, much less form, nile , and the underlying more cohesive groups in the dark. However, fish may mechanisms which produce them, may aid in design- have evolved other behaviors that minimize their noc- ing the sampling protocols needed to predict future turnal vulnerability and perhaps facilitate the reforma- of these species (Neilson & Perry 1990). tion of groups at dawn. Some fish species decrease To address the relationship between light and shoal- their activity during the night (Emery 1973, Helfman ing in juvenile walleye pollock, we examined the 1993) to conserve energy and possibly to reduce con- shoaling intensity and swimming speeds of juvenile spicuousness to predators. For shoaling and schooling walleye pollock over 2 consecutive days under a 12 h fish, this may also minimize group dispersal and light/l2 h dark photoperiod, to elucidate diel patterns decrease the time required for individuals to locate of behavior in the laboratory. Next, we conducted an conspecifics and reform shoals or schools at dawn. Sev- experiment to see if there is a distinct threshold light eral stud.ies have shown that, with the onset of morning level at which shoaling ceases, decreasing illumination twilight, fish begin forming groups before they com- from 3.9 pES-' m-2 to darkness in incremental order of mence other activities such as feeding (Helfman 1979, magnitude steps, and then incrementally increasing Pitcher & Turner 1986). Since twilight is a period of light back to the 3.9 pE S-' m-2 level. At each level we intense predation, any influence that predators have monitored shoal behavior and activity. upon the dispersal of prey during the darkness, If the dispersal of juvenile walleye pollock in dark- thereby influencing the speed of group reforma.tion at ness results from an inability to shoal, the rate of dis- dawn, should influence individual vulnerability to pre- persal may be influenced by any factor which affects dation at dawn. fish activity. When there is adequate light for shoaling, Ryer & Olla: Light, predat~onand shoaling In a

the presence of predators has been shown to decrease CCD Camera juvenile walleye pollock swimming speeds (Ryer & - Incandescenl Olla 1997). However, in preliminary experiments we k tighk , noted that juvenile walleye pollock startled by , activity in the darkness tended to become agitated and more active than juveniles startled in the light. We hypothesized that juvenile walleye pollock would also become more active in response to predators in the darkness. To test this, we conducted 2 experiments; '1''!, LED Lights first, juvenile walleye pollock were exposed to a simu- Transparent .. lated attack by a model predator under both light and dark conditions, and second, juveniles were exposed to the more persistent threat of a live predator in both the light and the dark. For both experiments we monitored shoal cohesiveness and swimming speeds of the fish.

MATERIALS AND METHODS

Fish collection and maintenance. During June of 1995 and 1996,juvenile walleye pollock were collected at night from , Port Townsend, WA, USA, by dipnetting them as they aggregated around a light suspended above the water's surface. At the time of Bottom Support IRIlluminator collection, juveniles ranged from 20 to 50 mm total length. Fish were transported back to our laboratory in Fig 1 Exper~mental lnfrared (IR) arena Surrounded by a Newport, OR, USA, and maintained in 3000 1 circular bl~ndIn a dark room, fish were vlewed as s~lhouettesagainst a un~formbright background from above wlth an IR sens~tive tanks provided with a continuous flow of seawater; --- LuLILcLo :K ~IY~ILIIIYwds proviaea by tour bOW LED lllumlna- sdiirliiy range 28 to 33x0, temperature range 9 to 13OC. tors located below the transparent bottom of the arena The 1R Juvenile sablefish Anaploponla firnbria, used as preda- lllumlnators were almed downwards, so the11 light was tors, were captured during April 1996 using a neuston bounced off reflective fo11 on the floor beneath the aiena and net during the night, approximately 32 km off New- upward thlough the transparent arena bottom An inner transparent wall (cylinder) was positioned lnside the arena port. Both species were fed pelletized food daily, and and prevented f~shfrom swlmmng along the arena walls, while the exact ration was not measured, it was suffi- where they would not be sllhouetted from below Visible light cient to promote growth. was provlded by a combination of incandescent and green Infrared observation arena. The arena consisted of LED illuminators located above the arena a fiberglass circular tank (190 X 76 cm, W X H) with a 19 mm thick plexiglass bottom (Fig. 1). It was posi- in overhead fluorescent fixtures, thereby producing a tioned 64 cm off the floor, supported around its periph- uniformly illuminated background against which fish ery by cinder blocks and across its center by a narrow could be viewed from above. A video camera, with support wall that bisected the tank bottom. The area spectral sensitivity well into the IR range, was posi- under the arena was lined with aluminum foil to pro- tioned 2.4 m above the arena and cabled to a video vide a reflective surface and then surrounded with recorder and monitor in another room. A circular clear black plastic to prevent light leakage. The tank was plexiglass inner wall (150 X 76 cm, W X H) was cen- illuminated from below with four 60 W LED infrared trally positioned in the arena to keep fish away froin (IR) illuminators. The wavelength of emitted light the outer arena wall where they would not be visible peaked at 880 nm, with no emissions below 760 nm. to the camera. This inner wall had numerous 5 mm Previous studies indicate that fish are insensitive to holes in it, which allowed water to pass from this inner light in this range (John 1964,Pitcher & Turner 1986, area to the outer area of the arena. Four seawater Higgs & Fuiman 1996).The IR illuminators were posi- inflow pipes extending vertically to within 3 cm of the tioned under the arena around its periphery and arena bottom were positioned at equal distances aimed downward onto the aluminum foil, which scat- around the periphery of the inner wall, supplying sea- tered and reflected the IR light upwards through the water to the central area of the arena, while a single arena bottom. The bottom of the arena was also lined drain hole in the outer arena wall at a height of 30 cm with a plastic light-diffusing material, commonly used allowed outflow of water. 218 Mar Ecol Prog Ser 167: 215-226, 1998

Six 60 W incandescent lights with aluminum reflec- all subsequent experiments, swimming speeds were tor cones were positioned 2.4 m above the floor, converted to body lengths S-', dividing swimming equally spaced in a 3.6 m diameter circle centered on speed by the average fish length for a given group. All the arena. Lights were controlled by a timer set to a data were homoscedastic (F,,,,-test; Sokal & Rohlf photoperiod of 12 h light/l2 h dark. Rather than 1969) and appeared normally distributed (rankit plots; instantly turning the lights on or off, the timer initiated Sokal & Rohlf 1969). Data were analyzed using a gradual dimming or raising of the lights which lasted repeated-measures ANOVA (Hicks 1982), examining roughly 75 min, simulating morning and evening twi- the effect of hour (17:00, 21:00, 01:00, 05:00, 09:00, light. At full illumination, these lights produced 2.1 pE 13:OO h) and day (1, 2). Where statistical effects were S-' m-', measured at the water's surface with a re- considered significant (p i 0.05), a postenori multiple search radiometer equipped with a detector sensitive comparisons were conducted utilizing Ryan's Q-test to 1 X IO-~pE S-' m-'. This lighting arrangement was (Day & Quinn 1989). utilized for the shoaling and activity periodicity exper- Light-shoaling threshold determination. Six fish iment conducted during the fall of 1995. For subse- were haphazardly selected from stock tanks and intro- quent experiments, conducted during the summer of duced to the arena at approximately 15:OO h. The fol- 1996, a set of 10 equally spaced LED illuminators was lowing morning, at approximately 09:OO h, we began added to the ring of lighting, allowing more precise to incrementally lower the illumination in order of control of low illuminations. Each illuminator consisted magnitude steps, pausing at each level for 20 mi.n and of 10 individual green LEDs. These illuminators emit- videotaping the group. The light was manipulated ted at 555 nm and, when operated independently of using both incandescent and green LED lights in tan- the incandescent lighting, allowed incremental manip- dem. The starting level was 3.9 pE s-' m-2, achieved ulation of light from 4.2 X 10-3 to 4.0 X 10-' pE S-' m-', with both incandescent and green LED lights on full. measured at the water's surface. Operated in tandem, For each of the next 2 steps, 3.9 X 10-' and 3.9 X 10-* pE the incandescent and green LED lights allowed mani.p- s-I m-2 , the incandescent lights were dimmed while the ulation of illumination in the range of 3.9 to 4.0 X 10'7 green LEDs remained on full. This resulted in some ~.IES-' m-2. degree of spectral shift as the light dimmed, which we Periodicity of shoaling and activity. Four juvenile did not measure. For subsequent light levels, 4.2 X IO-~, walleye pollock were haphazardly selected from hold- 4.3 X IO-~,4.5 X 10-', 4.1 X 10'~and

illumination set at 2.1pE S-' m-2, we began videotap- control trials, fish were videotaped for 5 h, starting at ing the arena After 30 min a 25 cm generic model fish 16:30 h. From these tapes we quantified juvenile wall- 'predator', on a 1 m string attached to a stick, was eye pollock behavior during 30 rnin periods beginning plunged into the center of the arena and surged back at 17:30 h (light = 2.1 pE S-' m-', 90 rnin before the and forth for 5 S, then rapidly removed. Videotaping beginning of evening twilight) and 21:OO h (45 min was continued for another 90 min. The next day, the after darkness, light < 1 X 10-"E S-' m-' ). We mea- procedure was repeated in the dark (lean nearest-neighbor distances (+SE). on the next day. In both predator and (b)Mean swimming speeds (+SE)over 2 consecutive 24 h periods Mar Ecol Prog Ser 167: 215-226, 1.998

lowed by a significant increase during the morning, which was then followed by a decrease during the day to interme- diate levels that did not differ from either the morning high or the night-time lows (multiple comparisons; ANOVA: F = 5.79, df = 5, p = 0.001). As was the case for nearest-neighbor distances, the pat- for swimming speed was similar during both days of the experiment (F = 16' 'E 02.06. df = 5. p = 0.099). suggesting that 10' walleye pollock behavior did not change over the 2 d expenment as a result of acclimation to the arena.

Influence of illumination on shoaling and swimming speed 20 40 60 80 100 120 140 1-80180 200 220 240 260 280 300 Time since start of experiment (min) Juvenile walleye pollock did not ex- hibit a distinct illumination threshold for shoaling or activity. As illumination was lowered by orders of magnitude from full light to darkness, with fish given 20 mln to adapt to each illumination level, juve- nile walleye pollock exhibited a gradual 0.0 10' 10' I rl~0.3 c31 PI 0.~1PI c71od 4l o2 decrease in shoal cohesiveness, as Light ( pe m.'s '1 demonstrated by increasing nearest- neighbor distances (Fig. 3a). Subsequent order of magnitude increases in illumi- nation produced corresponding in- creases in shoal cohesion. Nearest- neighbor distances changed significantly through the expenment (ANOVA: F = 2.62, df = 14, p = 0.003), but in a graded manner, with multiple comparisons re- vealing 3 largely overlapping homoge- neous subgroups of means. More impor- tantly, in 12 out of 14 changes in illumination, the observed direction of Time since start of experiment (min) change in mean nearest-neighbor dis- tance was consistent with that predicted Fig. 3. Light threshold experiment. (a) Mean nearest-neighbor distances by assuming a negative relationship be- (+SE) as light levels were incrementally decreased and then increased again. tween nearest-neighbor distance and Fish were given 20 min acclimation at each light level. (b) meannearest- light level, This represents a significant neighbor distances (+SE)plotted as a function of illumination (cl hlean swim- rnmg speeds (*SE)wlth incremental llght. change. (d) Mean swimming departure the of as- speeds as a function of ~llumination sociation between light and nearest- neighbor distance (Sign test, p = 0.006), days of the experiment (time X day interaction: F = further indicating that shoaling decreases with de- 2.55, df = 5, p = 0.049), nearest-neighbor distances creasing illumination. The 2 exceptions to this pattern were consistently greater in the dark than in the light occurred at 4.3 X 10-4 IJE S-' m-2, on both the ascending during both days (multiple comparisons). Changes in and descending limbs of the light response curve activity also reflected a die1 periodicity, but one which (Fig. 3a). When nearest-neighbor distance is plotted as was less pronounced than that observed for schooling a function of the natural log of light level, the mean (Fig. 2b). Low swimming speeds at night were fol- nearest-neighbor distance at 4.3 X 10-4 pE ss' m-2 is Ryer & Olla: Light, predation and shoaling in a pelagic fish 221

suggestive of a discontinuity in what otherwise would appear to be a linear relationship (Fig. 3b) Comparing nearest-neighbor distances between Fig. 3a and Fig. 2a, it would appear that group cohesion was greater in the dark during the day than it was in the dark during the night. This is most probably an artifact of the differing numbers of fish used in these 2 experi- ments. The arena size was the same for both, but in the periodicity study, groups of 4 fish were utilized, com- pared to groups of 6 in the threshold study. Swimming speed was less clearly related to illumina- tion than shoaling (Fig. 3c). The only significant effect was that swimming speed at the beginning of the i 0 experiment, i.e. 20 min, was higher than during the 30 20 10 0 10 20 30 40 50 60 70 80 90 remainder of the experiment (multiple comparisons, Time beforelafter simulated predator attack (min) ANOVA: F= 7.64, df = 14, p 0.001).Further, although 9 out of 14 illumination changes were consistent with a positive relationship between swimming speed and light level, this result did not differ significantly from the null model of no association (Sign test, p = 0.212). Similarly, plotting swimming speed by natural-log- transformed light level suggests no obvious relation- (Fig. 3d). - / Time (min)

Effect of simulated predator attack upon shoaling and swimming speed

As seen in ii~e2 prior experiments, juvenile walleye pollock shoaled in the light, but swam about indepen- dently in the dark (Fig. 4a). Throughout the pre-expo- Time beforelafter simulated predator attack(min) sure period, nearest-neighbor distances were lower in the light than in the darkness (multiple comparisons; Fig. 4. 'Model predator experiment. (a) Mean nearest-neigh- bor distances (&SE)before and after a 5 S exposure to a model time X light level interaction: F = 1.97, df = 24, p = fish predator both in the light and in the dark. (b) Mean swim- 0.007).The model predator had a transitory effect upon rmng speeds (*SE). Insets in both (a) and (b) show, in an this light/dark difference in shoaling. During the 5 S expanded time scale, the period immediately following simu- model predator presentation, fish scattered and darted lated attack by the model predator about, after which some individuals remained motion- less on the arena bottom for up to 90 s, often aggregat- Model presentation had a pronounced effect upon ac- ing next to or behind water inflow pipes. As a result, tivity, particularly for fish in the dark (Fig. 4b; time X light 2 min after the model presentation, nearest-neighbor level interaction: F= 5.80, df = 24, p < 0.001). Prior to the distances were equal under both light and dark condi- presentation, swimming speed tended to be lower in the tions (multiple comparisons). However, 4 min after the dark than In the light (significantly so 14and 11 min be- simulated attack, fish in the light were again shoaling, forehand, multiple comparison). After the presentation, with their nearest-neighbor distances lower than those swimming speed increased under both light and dark of fish in the darkness (multiple comparisons). This dif- conditions (multiple comparisons). However, this in- ference in shoaling behavior persisted through the crease was greater in the dark, so that by 3 min after the remainder of the experiment (multiple comparisons). presentation, fish in the dark were swimming faster than Other than the brief period immediately after the sim- those in the light (significant differences at minutes 3,4, ulated attack, there was no difference in nearest- 5 and 7, multiple comparisons) This sharp increase in neighbor distances between before and after periods the swimming speed in the dark was transitory and in the darkness (multiple comparison). In the light, 8 min after the attack fish had slowed to speeds compa- there was a trend towards more cohesive shoaling rable to those exhibited by fish in the light (no significant after the simulated attack, but this was not statistically differences for minutes 8 to 26, multiple comparisons). significant (multiple comparisons). Forty-one min after the model predator presentation, fish Mar Ecol Prog Ser 167: 215-226, 1998

in the dark again tended to swim slower than fish in the light (significant differences at minutes 41, 56 and 71, multiple comparisons).

Effect of a live predator upon shoaling and swimming speed

An average of 1.55 ju.venile walleye pollock (SD = light dark 1..42) were consumed in the predator trials, although none were consumed during the two 30 min observa- control tion periods, and none were consumed in the darkness. Attacks by the predator were frequent in the light (36.4 h-', SD = 30.2). but no attacks were observed in the darkness. Although the predator appeared able to detect and approach prey from a range of several cm in the darkness, these approaches were infrequent (3.5 h-', SD = 3.4) and juvenile walleye pollock darted away as soon as the predator drew near, with no 5 light dark attempted pursuit by the predator. Other than these infrequent close encounters, juvenile walleye pollock Fig. 5. Live predator experiment. (a) Mean nearest-neiyhbor did not appear to actively avoid predators in the dark. distances (+SE) in both the light and the dark, with and with- In contrast, in the light, walleye pollock shoaling was out a predator present. (b) Mean swimming speeds (+SE) frequently disrupted, as individuals and small groups of fish moved in different directions to avoid the approaching predator. In addition, individual fish SE = 1.2; predator: Z = 3.6, SE = 1.0). Chases were not would often separate from the shoal, approach, and enumerated in the dark. sometimes follow the predator. This inspection behav- ior was most prevalent when the fish had not recently been chased. DISCUSSION Beyond an obvious effect of light on shoaling (F = 73.21, df = l, p < 0.001), there was no statistically signif- The diurnal pattern of shoaling we observed in fish icant effect of predator presence on shoaling (Fig. 5a) subjected to a 12 h light/l2 h dark photoperiod sup- (F = 0.22, df = l, p = 0.651), under either light or dark ports prior field and laboratory observations on juve- conditions, although in the light there was a trend for nile walleye pollock (Brodeur & Wilson 1996, Sogard & more cohesive shoaling in the presence of a predator Olla 1996) and is similar to those observed in other (F= 2.52, df = l, p = 0.144). Nearest-neighbor distances shoaling and schooling fish (Shaw 1961, Blaxter & Par- in the dark were generally lower than those in the prior rish 1965, Major 1977, McFarland et al. 1979). While it experiments. Again, this was most probably an artifact is unclear to what extent endogenous rhythms influ- of our having used more fish in the live predator exper- ence this diurnal behavior (Neilson & Perry 1990), it is iment than were used in the prior experiments. Swim- clear that juvenile walleye pollock do not shoal in the ming speed was influenced by preda.tor presence darkness. Using lateral line systems, some fish appear (Fig. 5b);in the light, swimming speed decreased when to have limited ability to maintain social groupings a predator was present, while in the dark it increased without vision. For example, temporarily blinded (light X predator interaction: F= 13.44, df = 1, p = 0.004; saithe Pollachiusvirens are able to swim with a sighted multiple comparisons: Ryan's Q equaled the critical school, but tend to maintain greater nearest-neighbor value, i.e. p = 0.05, for comparisons in both the light and distances (Partridge & Pitcher 1980). Similarly, olfac- the dark). This increased swimming speed in the dark- tion may allow some species to stay congregated in the ness did not appear to directly result from observable dark (Keenleyside 1955).We observed pairs of juvenile interactions between predator and prey. walleye pollock occasionally swimming together in Aggressive interactions between juvenile walleye darkness, with one fish altering its speed and direction pollock were also influenced by predation risk. In the to match the other's, falling in somewhat behind and light, instances of walleye pollock chasing each other off to one side of the leader. However, such pairing were less frequent when a predator was present never lasted more than 4 or 5 s before a change in (l-tailed t= 1.81, df = 10, p = 0.025; no predator: P= 6.5, direction by one fish or the other resulted in separa- Ryer & Olla: Light, predation and shoaling in a pelagic fish 223

tion. Given the size of our experimental arena, we can- no abrupt change in the light-shoaling relationship not discount the possibility that juvenile walleye pol- between 3.9 X 10-2 and 4.2 X 10-' pE S-' m-', as the light lock may utilize other senses to maintain loose congre- went from mixed white and green to green only. Thus, gations in the darkness, but for shoaling, vision is while the precise shape and slope of this upper portion essential. of the light-response curve remains suspect, we feel Ambient light levels in the ocean vary with time of that our overall conclusion, that shoaling decreases day, latitude, season, cloud cover, surface turbulence, gradually as illumination decreases, is supported by depth and turbidity, to name but a few factors (McFar- our data. land 1986). As such, using 'night-time' as a synonym The lack of a discrete light threshold for shoaling for darkness is ambiguous and potentially misleading. may be a general characteristic of fish which routinely Accordingly, numerous studies have attempted to engage in shoaling, as opposed to schooling 'behavior. quantify the precise light levels at which various spe- Schooling fish continue to maintain precise distances cies no longer engage in shoaling and schooling be- and angular relationships between individuals as illu- havior, with values ranging from 3.7 X 10-2 yE S-' m-2 mination decreases, but when illumination falls below for Hawaiian silversides Pranesus insularum (Major the threshold, schooling abruptly ceases. Shoals are 1977) to 1.8 X 10-7 pE ss' m-' for Atlantic mackerel more chaotic in , with distances, angles and Scomber scombrus (Glass et al. 1986). Most of the spe- even direction of movement differing considerably cies for which thresholds have been reported are fish between individuals. The less rigid behavior of which routinely engage in schooling, i.e. fish that move shoalers, combined with the tendency of individual in polarized groups, in a highly synchronized manner juvenile walleye pollock to continually leave and Although juvenile walleye pollock will occasionally rejoin shoals, is likely to be responsible for the lack of school, shoaling is more the norm in this species. Our a distinct light threshold for shoaling in this species. A results indicate that juvenile walleye pollock gradually gradual decrease in shoaling with lowered light has decrease shoaling as illumination decreases, rather also been observed In Astyanax mexicanus (John than displaying a distinct light threshold. Although 1964). It would be instructive to examine whether or light at a given depth in the ocean can change by as not a light threshold is manifest in species like the much as 50% min-' during twilight periods (McFar- walleye pollock, when the fish are motivated to land 1986), at the high latitudes where juvenile wall- engage in more rigid schooling behavior. eye poiioc~ occur, twiiight periods are more pro- Although we observed that shoal cohesion changes longed, wlth more gradual changes in illumination at linearly with the natural log of illumination, we also any given depth. In addition, juvenile walleye pollock saw what appeared to be a discontinuity in shoal cohe- migrate vertically (Bailey 1989, Merati & Brodeur 1996, sion occurring at 4.0 X 10s4 PE S-' m-2 (Fig. 3b). Tang et al. 1996), and since light attenuates with Although we can ascribe no statistical significance to depth, this will also lessen the magnitude of changes in this discontinuity, its occurrence on both the ascending illumination they experience. These factors combined and descending limbs of the light response curve suggest that walleye pollock may experience only 2 or (Fig. 3a) suggests that some aspect of vision or behav- 3 orders of magnitude change in illumination over pro- ior changes at this light level. One possibility is that longed periods of time during their crepuscular migra- this is the light level at which walleye pollock switch tlons. Hence, the transition from shoaling to non-shoal- from photopic to scotopic vision. While highly specula- ing is also likely to be a gradual one. tive, this hypothesis could be tested by studying the The spectral composition of ambient light also varies retinomotor responses of juvenile walleye pollock to temporally, with meteorological conditions and with various illuminations. depth (McFarland 1986), and the fish eye is differen- Our laboratory data suggest that at light levels below tially sensitive to various spectra (Blaxter 1964, 1969). 2.8 X 10-~pE S-' m-', those likely to be encountered in In our threshold experiment, we utilized green light for North Pacific surface waters on a clear moonless night, illuminations of 4.2 X 10-"E S-' m-2 and below, since juvenile walleye pollock would be so dispersed as to no this is the most ubiquitous wavelength in coastal longer constitute a distinct shoal. However, with moon- marine waters (McFarland 1986). Unfortunately, for light, shoaling could occur at greater depths, depend- higher illun~inationswe had to add additional incan- ing on lunar stage, cloud cover and water clarity. descent lighting, which resulted in a shifting of spec- Brodeur & Wilson (1996) reported that juvenile walleye tral composition. Without knowing the spectral sensi- pollock in the western Gulf of Alaska dispersed at a tivity of the juvenile walleye pollock eye, it is depth of 35 m during the night and actively fed .upon impossible to evaluate precisely how this shifting of larvaceans, and euphausiids (Merati & wavelengths may have influenced the shape of Brodeur 1996). Without data on ambient light levels at response curve shown in Fig. 3b. However, there was these depths on the nights concerned, it is impossible Mar Ecol Prog Ser 167: 215-226,1998

to characterize this dispersal as being the result of The importance of shoaling and/or schooling in active or passive processes, but our laboratory data predator avoidance has been clearly established and it clearly suggest that the ability of juvenile walleye pol- has been widely observed that when there is adequate lock to shoal will be greatly affected by astronomical light for such behavior, the presence of predators typi- and meteorological conditions, and that the ability of cally results in shoals or schools becoming more com- fish to shoal at this depth will probably vary from night pact (Maguran & Pitcher 1987, Morgan 1988, Ryer & to night. Olla 1996). The 'many ' in a cohesive group are Whereas the diurnal pattern of shoaling behavior in able to detect predators more efficiently than individu- juvenile walleye pollock appears to represent a simple als (Maguran et al. 1985) and coordinated escape response to available light, the diel pattern of swim- responses produce predator confusion (Neill & Cullen ming speed was more complex. There was a tendency 1974, Partridge & Pitcher 1980, Landeau & Terborgh for swimming speeds to be lower in the dark than in 1986). However, prior studies of predation risk and the light, although the statistical significance of this group cohesiveness in juvenile walleye pollock have effect varied between experiments. Many species of produced mixed results. Ryer & Olla (1997) demon- fish decrease their activity or swimming speed at night strated that juvenile walleye pollock exposed to preda- (Helfman 1993). For visually oriented species, de- tory sablefish shoaled more cohesively, but that the creased activity may lower energetic costs during peri- extent of this effect was influenced by whether or not ods when fish are not actively feeding (Neilson & Perry the walleye pollock were , as well as the spa- 1990, Sogard & Olla 1996).Decreased activity may also tial and temporal distribution of their food. Similarly, facilitate the maintenance of congregations when Sogard & Olla (1998) reported that whether or not there is insufficient light for visually mediated shoaling group cohesion increased in the face of predation risk (Emery 1973). In addition to this modest light/dark depended upon juvenile walleye pollock size and effect, there was also a strong diel pattern of swim- hunger state. In the live predator trials of the present ming speed, characterized by peak speeds during the study, we saw only a weak trend for greater group early morning, which decreased through the day and cohesiveness. The small size of our infrared arena and then decreased further to uniformly low levels during the large number of fish used in this experiment, com- the night. This pattern may represent an endogenous pared, that is, to our prior study utilizing the sable- rhythm, superimposed upon the light/dark effect. fish/walleye pollock predator/prey pairing (Ryer & Alternatively, increased morning activity may simply Olla 199?), may have influenced our results. The be stimulated by the end of an extended period of predator was often intermingled with the juvenile darkness. Whatever its proximal causation, increased walleye pollock and, with fish moving in different morning activity may facilitate shoal reformation, as directions to avoid the predator, this often disrupted individuals and small groups seek to locate one shoaling. We also failed to see a strong effect of preda- another and form a larger shoal. If shoaling represents tion risk upon shoal cohesion in our model predator the primary defense against predation, increased experiment. Sogard & Olla (1998) found that, although energy expenditure to quickly reform shoals in the juveniles will shoal more cohesively after presentation morning would be advantageous. Pitcher & Turner of a model predator, this response is weaker than that (1986) observed that European forgo feeding elicited by a living predator. Cumulatively, these stud- untll they have formed shoals at dawn, suggesting that ies indicate that juvenile walleye pollock do tend to mitigation of predation risk takes precedence over shoal in the presence of predators; however, this is not feeding during this vulnerable twilight. an immutable relationship, as other environmental and This superimposition of a diel pattern upon a gener- motivational factors also help determine the structure alized light/dark effect may explain the confusing and cohesiveness of fish shoals. results obtained in our threshold experiment, where In the light, the effect of predation risk upon juvenile swimming speed tended to decrease as the lights were walleye pollock swimming speed differed between the dimmed, but did not increase again as the lights were simulated and live predator trials. In simulated predator turned back up. These trials commenced at 09:OO h, trials, where the model predator made a brief but dra- when fish were engaged in their most rapid swimming matic appearance, fish increased their swimming of the day, as indicated by our periodicity experiment, speed. However, in live predator trials, fish decreased but ended in the afternoon, when fish would typically swimming speed; the same effect as that observed in a have been swimming more slowly. This diel pattern, prior study where juvenile walleye pollock experienced combined w~ththe variability of our data, may have persistent exposure to sablefish predation risk (Ryer & confounded our ability to clearly discriminate the Olla 1997). This difference between predator treat- effect of light intensity upon swimming speed in this ments could be attributable to any of a number of fac- particular experiment. tors. It may simply represent an acclimation to predator Ryer & Olla: Light, predation and shoaling in a pelagic fish 225

presence in live, as opposed to the simulated, predator der lower predation regimes. Thus, our results suggest trials, or subtle differences in the perceived risk associ- that predation risk may have very different influences ated with the 2 treatments. Alternatively, there may be upon the spatial distribution of fish under light versus a fundamental difference in how fish respond to in- dark conditions. In the light, predation may, depending tense, but brief, interactions with predators, compared upon environmental conditions and fish motivational to persistent interaction. Fish scattered and then froze state, cause greater contagion in fish spatial distribu- in response to model predator exposure. Afterwards, tion, while in the darkness it likely results in greater fish were unable to relocate the source of perceived spatial dispersion. threat, and may have increased swimming speed to While it is unclear whether predator-accelerated dis- 'leave the area' before another attack could occur. In persal of prey would influence prey vulnerability in the contrast, in the live predator trial, fish were in continual darkness, these prey may find themselves particularly contact with the predator and may have decreased vulnerable the following morning. During morning speed to increase their vigilance, while also decreasing twilight, fish are silhouetted against downwelling light their conspicuousness (Lazarus 1979). Predators have from the surface, rendering them particularly vulnera- evolved preferences that exploit vulnerabilities in their ble to predatory attack from below (Munz & McFar- prey, as suggested by a study of the predatory cichlid land 1973). Attacks by are often concen- Aequidens pulcher, which exhibited greater attraction trated at twilight (Major 1977, Parrish 1992) when for more active, as opposed to less active, groups of predators have this visual advantage over their prey Poecilia reticulata (Krause & Godin 1995). (Helfinan 1993) and when prey are less likely to detect Whatever the reason for the differences between our stalking predators (Pitcher & Turner 1986). With the predation treatments, a more exhaustive investigation onset of morning twilight, widely dispersed individuals into how fish respond to differing types of perceived will presumably take longer to locate conspecifics and risk, expanding on the work of Helfman (1989)' would reform shoals and schools, resulting in prolonged vul- be of great assistance in the synthesis of a predator- nerability and greater probability of being eaten. prey literature which has staged and/or simulated pre- In summary, juvenile walleye pollock are not charac- dation risk using a wide variety of techniques. terized by a distinct light threshold at which shoaling Since light plays a pivotal role in shoaling and school- ceases; rather, fish gradually disperse as illumination ing, it also determines how fish respond to predators. At decreases. Our data indicate that juvenile walleye pol- -.-.L'ILyl~r or at deptii, wiii~insufficient iight for fish to see lock would be unlikely to maintain any degree of one another, shoals and schools tend to disperse (Smith shoaling in the ocean at illuminations below 2.8 X 10-6 et al. 1993, present study). Even in the presence of a PE S-' n1r2, conditions that could be expected in surface predator, when the n~otivation to maintain groups waters on a starlit night. Illunlination may also influ- should be high, juvenile walleye pollock were unable ence how juvenile walleye pollock respond to preda- to do so. This is similar to behavior reported for black- tors. Exposure to either model or live predators in the nose dace, which shoal in response to predators in the dark caused juvenile walleye pollock to swim faster. light, but fail to do so in the dark, irrespective of preda- This may result in more rapid and complete dispersal tor presence or absence (Cerri 1983). However, this of shoals during the night, making individuals more does not mean that in the darkness, prey behavior is vulnerable to predation at dawn. unaffected by predator presence. Juvenile walleye pol- lock exposed to either model or living predators in the dark swam faster than fish which were not so exposed, LITERATURE CITED the opposite of what was seen in the light. This was not because they were chased by the predator in the dark- Appenzeller AR. Leggett WC (1992) Bias in hydroacoustic estimates of fish abundance due to acoustic shadowing: ness, or exhibited frequent overt avoidance behavior. evidence from day-night surveys of vertically migrating Rather, the mere presence of larger fish swimming fish. Can J Fish Aquat SCI49:2179-2189 about in the tank appeared to stimulate more rapid Atz JW (1953) Onentation in school~ng fishes. Proc Conf swimming by juvenile walleye pollock. 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Editorial responsib~llty Otto Kinne (Editor), Suhmttcd: October 21, 1997; Accepted: April 1, 1998 Oldendorf/Luhe, Germany Proofs received from author(s1. June 2, 1998