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Effect of Light on Juvenile Walleye Pollock Shoaling and Their Interaction with Predators

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Effect of Light on Juvenile Walleye Pollock Shoaling and Their Interaction with Predators MARINE ECOLOGY PROGRESS SERIES Vol. 167: 215-226, 1998 Published June 18 Mar Ecol Prog Ser l Effect of light on juvenile walleye pollock shoaling and their interaction with predators Clifford H. Ryer*, Bori L. Olla Fisheries Behavioral Ecology Group, Alaska Fisheries 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 fish 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 species, 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 shoal. Exposure to simulated predation 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 disturbance may lead to accelerated dispersal of prey shoals 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. KEY WORDS 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 eye 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 habitats may vary Atz 1953, Shaw 1961, Hunter 1968). Although other greatly according to depth, turbidity, season, lunar senses, such as the lateral line 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 Ocean threshold varies from 3.7 X 10-2 pE S-' m-* for the which supports a large commercial fishery 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 mackerel groundfish, birds and marine mammals (Livingston Scomber 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, flocking and herd- 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 shoaling and schooling fishes, 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- abundance 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 pE S-' 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 pelagic fish 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 ,tighk , noted that juvenile walleye pollock startled by human k activity in the darkness tended to become agitated and more active than juveniles startled in the light.
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