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Journal of Experimental Marine Biology and Ecology 292 (2003) 43 – 59 www.elsevier.com/locate/jembe

Biological structures and bottom type influence habitat choices made by Alaska flatfishes Allan W. Stoner *, Richard H. Titgen Fisheries Behavioral Ecology Program, Alaska Fisheries Science Center, National Marine Fisheries Service, NOAA, 2030 S. Marine Science Drive, Newport, OR 97365, USA Received 7 November 2002; received in revised form 20 January 2003; accepted 12 March 2003

Abstract Habitats of flatfishes are ordinarily characterized on the basis of depth, sediment type, and temperature. However, features of the benthic environment such as structures created by sessile organisms and different bedforms may also influence habitat suitability. In this investigation, we tested the hypothesis that habitat choices made by juveniles of two economically important flatfishes, Pacific halibut (Hippoglossus stenolepis Schmidt) and northern rock sole (Lepidopsetta polyxystra Orr and Matarese), are influenced by structures on the sea floor. In the laboratory, age-0 individuals of both species demonstrated high positive selectivity for habitats with structure (natural sponges, bryozoan mimics, bivalve shells, and sand waves) over smooth sand substratum. The degree of choice was influenced significantly by density of structures, particularly sponges. Small halibut (48 – 77 and 90 – 144 mm) were more selective than larger juveniles (270 – 337 mm), and in sponge habitat juvenile halibut were more selective than comparably sized rock sole. Preference for habitat with structure increased significantly with increasing light level, suggesting that choices were made partially on the basis of visual cues or as related to perceived threat. However, the preference for structured habitat was maintained in darkness. Beam trawl collections made in a flatfish nursery ground near Kodiak, Alaska, revealed that the abundances of age-0 Pacific halibut and rock sole were closely correlated with amounts of shell and echinoderm bycatch in the tows, corroborating the laboratory observations of affinity for habitat structure. Strong preferences for structured habitat in young halibut and rock sole indicate the importance of benthic structures that are frequently removed by fishing gear. Published by Elsevier Science B.V. Keywords: Habitat complexity; Habitat preference; Behavior; Halibut; Rock sole; Crypsis

* Corresponding author. Tel.: +1-541-867-0165; fax: +1-541-867-0136. E-mail address: [email protected] (A.W. Stoner). 0022-0981/03/$ - see front matter. Published by Elsevier Science B.V. doi:10.1016/S0022-0981(03)00144-8

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1. Introduction Structurally complex habitats in nearshore marine environments such as coral reefs, kelp forests, seagrass meadows, and salt marshes often support high abundance and species richness of fishes and invertebrates compared with low-relief, soft-sediment habitats. It is generally believed that complex habitats provide shelter from predation and abundant food resources for small fishes. Because of their ecological role and importance as habitat for ecologically and economically significant species, complex biotopes in estuarine and marine systems are protected by environmental regulations in many nations. Complex habitats in offshore regions and in deeper and/or colder waters are less well studied. However, the increasing use of ROVs (remotely operated vehicles) and submersibles for direct observations has shown that fishes are not uniformly distributed over lowrelief continental shelf environments (e.g., Auster et al., 1991; Malatesta and Auster, 1999; Moran and Stephenson, 2000; Lindholm et al., 2001). Certain demersal fishes and age groups of fishes are at least loosely associated with benthic habitat features such as cobble, sand waves, sessile invertebrates, shell material, and other biogenic structures that provide structural complexity to otherwise homogeneous sea floor. Using the basic understanding of ecological processes in complex nearshore habitats and some of the same rationale for conservation, there has been a call for the protection of structurally complex shelf habitats (Auster and Langton, 1999). However, functional relationships between fishes and structures in low-relief shelf environments are poorly studied. Associations between flatfishes and benthic habitats are ordinarily determined from trawl surveys that do not consider structural features of the bottom, and most researchers classify habitat for flatfishes on the basis of sediment characteristics, bottom temperature, and depth strata (Rogers, 1992; Swartzman et al., 1992; Jager et al., 1993; Gibson, 1994, 1997; Abookire and Norcross, 1998; Norcross et al., 1999; McConnaughey and Smith, 2000). Direct field observations on flatfishes are relatively rare (Gibson et al., 1998; Sullivan et al., 2000), but ROV observations made by Norcross and Mueter (1999) in bays of Kodiak, Alaska, revealed that the highest probability of observing juvenile flatfishes occurred in sand-wave habitat and that flatfish were ‘‘very often associated with specific structures in their habitat.’’ Also, recent laboratory experiments have shown that age-0 winter flounder (Pseudopleuronectes americanus Walbaum) gain significant protection from predation while occupying locations with even small amounts of seagrass or macroalgae, and that sediment grain size had no effect (Manderson et al., 2000). Winter flounder also have a high preference for vegetated habitats over bare sand (Phelan, 2000). These recent studies suggest that we need to carefully assess what constitutes critical habitat for flatfishes on a species- and size-specific basis. Understanding the role of habitat structure for fishes on the continental shelf is important because the physical structures created by sessile invertebrates and sediment surface features can be impacted by fishing gear and other human activities (Collie et al., 1997; Freese et al., 1999; Kaiser et al., 2000; McConnaughey et al., 2000). In this investigation, we tested the null hypothesis that habitat choices by juveniles of two flatfish species are independent of physical structure created by different bedforms and sessile biota. We also examined the interaction between habitat choice

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and light level because the study species occupy turbid coastal waters that are subject to low-light conditions associated with depth and the subarctic winter season. Observations under conditions of darkness provided insights into the mechanisms of habitat choice.

2. Materials and methods 2.1. Collection and maintenance of subject species Experiments were conducted with two commercially important pleuronectid flatfishes: the Pacific halibut (Hippoglossus stenolepis Schmidt) and the northern rock sole (Lepidopsetta polyxystra Orr and Matarese). Although relatively little is known about the early stages of these fishes, juveniles of both are found in the Gulf of Alaska and Bering Sea, primarily in shallow water (< 50 m) (IPHC, 1998; Norcross et al., 1999). Pacific halibut and northern rock sole in the age-0 and age-1 groups (35 – 170 and 12 – 80 mm total length, respectively) for our laboratory experiments were collected with a beam trawl (2 m wide, 3-mm mesh) towed at f 1 m s 1 in Chiniak Bay, Kodiak Island, Alaska (57j40VN, 152j30VW) in August 2000, and in June and August 2001. Bottom temperatures were 8 –10 jC at the trawl sites. The fish were held in flow-through seawater tanks (f 9 jC) at the Kodiak Laboratory of the National Marine Fisheries Service for 2 days prior to air transport to the Hatfield Marine Science Center in Newport, OR. Shipping generally took < 30 h and temperatures remained near 9 jC in insulated containers. Very few fish died in transport, and most fed within 24 h of arrival in Newport. Age-0 halibut were maintained in tanks 1.3 m in diameter, with 0.5 cm of sand on the bottom and supplied with flow-through seawater maintained at 9 jC ( F 1.5 jC). Halibut were transferred to larger tanks (4.5 m in diameter) as they grew to the largest size tested (f 330 mm). Rock sole, which were smaller than halibut, were held in 0.75-m square tanks (35 cm deep), with environmental conditions similar to those for halibut. Small halibut and rock sole were fed to satiation 3 days/week on diets of chopped frozen shrimp and dry pellet foods high in protein and lipid. Halibut >150 mm were fed a gel food comprised of squid, herring, krill, amino acid supplements, and vitamins. Three size classes of Pacific halibut and two size classes of rock sole were tested for habitat choice (Table 1). All of the fish were tested within 12 weeks after being collected except for the largest halibut, which were held for f 1 year to reach 30 cm TL. 2.2. Substrata tested All observations of habitat preference were made in pairwise combinations of smooth bare sand and structured habitat created on opposite halves of circular tanks (Table 1). Three sizes of quartz sand (fine: 0.2 mm; medium: 0.5 mm; coarse: 1.0 mm) were mixed in equal proportions and covered the bottom of each tank for experiments with rock sole and the two smallest size classes of Pacific halibut. Only medium and coarse sand were mixed for the large halibut because of their increased burial capabilities and because they prefer

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Table 1 Summary of experimental tests for substratum preference using Pacific halibut and northern rock sole Fish species

Fish size class

Tests for substratum preference Pacific halibut small medium

Northern rock sole

Tests for light effects Pacific halibut

large very small small

medium

Mean fish size (range) (mm TL)

Substratum tested

Arena diameter (m)

No. of observations per run

60 (48 – 75) 61 (49 – 77) 112 (90 – 134) 112 (91 – 136) 111 (90 – 135) 114 (92 – 140) 114 (93 – 142) 116 (95 – 144) 331 (270 – 337) 20 (15 – 25) 57 (42 – 74) 57 (42 – 74)

high-density sponges bivalve shells high-density sponges low-density sponges high-density bryozoans low-density bryozoans bivalve shells sand waves high-density sponges high-density sponges high-density sponges bivalve shells

1.1

2

1.9

4

2.9 0.7 1.1

8 2 2

112 (90 – 134)

high-density sponge

1.9

4

Each substratum listed was used in a pairwise test against smooth bare sand. Eight runs were made with five naı¨ve fish in each run (total of 40 fish).

larger grain sizes (Stoner and Ottmar, 2003). In all cases, sediment depth was such that the fish could bury completely without touching the bottom of the tank. Structured habitats were created to mimic several different forms observed in shallow shelf environments of the Bering Sea and Gulf of Alaska where Pacific halibut and rock sole have nursery grounds, and to mimic the structures that are removed or reduced by fishing trawls (McConnaughey et al., 2000). A commercial sponge (Hippospongia sp.) was used to mimic Halichondria sp., which is common in the Bering Sea. The approximately spherical sponges (mean diameter = 12 cm) provided a low, solid profile. Two densities were tested (5 and 15 m 2) resulting in bottom coverages of 6% and 16%. To simulate the form and color of the feathery bryozoan Eucratea loricata, 30-cm lengths of gold polypropylene rope (9 mm in diameter) were bound on one end and frayed to produce an open-structured canopy with an average individual area of 353 cm2. Two densities were tested (5 and 15 m 2) producing 19% and 55% coverage of the bottom. Both sponges and bryozoan mimics were anchored to threaded nylon rods (95 mm in diameter) that were screwed into acrylic sheets placed beneath the sand. Empty bivalve shells were used to create a low-profile structure. We mixed an equal number of smooth clam and cockleshells (mean diameter = 80 and 67 mm, respectively) to yield a bottom coverage of 8%. The fourth kind of structured habitat was a sand-wave substratum (wave height = 10 cm, wavelength = f 30 cm). Waves were formed manually with a rake on one half of the tank at the beginning of each run. Wave crests were oriented in a diagonal to the interface between the smooth and textured surfaces. Wave height was similar to sponge height used in other tests, and the shape of the waves was sufficiently gentle that the fish could settle anywhere along the wavelength.

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2.3. Experimental apparatus and light experiments All of the habitat preference experiments were conducted in circular tanks with flowthrough seawater at 9.0 jC ( F 1 jC). Experiments with rock sole and the smallest halibut were conducted in four fiberglass tanks (1.2 m diameter with center standpipes) (seawater flow = 3 l min 1). Sediment depth was 2 cm and water depth was 26 cm. Clear acrylic rings (71 and 108 cm in diameter, 30 cm high) were placed inside the tanks to scale arena dimensions to fish size (Table 1). These rings extended above the water level and were perforated with small holes to allow an even flow of water from all sides. Overhead fluorescent lighting provided a daylight illumination of 10 1 Amol photons m 2 s 1, as determined with an International Light IL1700 using an SHUD 033 sensor submerged at the bottom center of the tank. Nighttime illumination ranged 10 5 –10 7 Amol photons m 2 s 1. Experiments with medium halibut (90 – 144 mm TL) were conducted in two polyethylene tanks (1.9 m in diameter) covered on the outside with black PVC sheets to prevent motion in the area from disturbing the fish. Water depth was 32 cm (flow = 9 l min 1) and sediment depth was 7 cm. The deep sand layer was used in this apparatus so that sand waves could be created while leaving sand for burial in the wave troughs. Each tank was located within a separate light-controlled area so that light-level effects could be tested in relation to habitat choice. To reduce shadowing, all lighting in the two areas was attached to an overhead ring suspended 1.8 m above the tank bottom and 0.7 m outside the tank circumference (tank height = 105 cm). Six 60-W incandescent bulbs and 10 green LED clusters (10 LEDs per cluster) were mounted at uniform spacing on the ring. The incandescent bulbs, guarded by conical metal shades, were directed away from the tank to avoid glare and hot spots and controlled by an electronic timer set to a 12-h schedule (all experiments were run under a 0700 – 1900 h lighting schedule). The dimmer LED clusters were directed toward the center of the tanks and were controlled by a microcomputer. Light experiments were conducted with four illumination levels, measured at sediment level. Bright daylight (10 1 Amol photons m 2 s 1) was simulated with the incandescent lamps. Low light (10 3 Amol photons m 2 s 1) and moonlight (10 5 Amol photons m 2 s 1) were simulated with the LED clusters. Dark in the light-controlled areas measured 0.08  10 7 Amol photons m 2 s 1. All of the experimental substrata were tested with medium halibut in this apparatus. However, because halibut showed a positive response to all of the structured habitats, the light experiments were conducted only with high density sponge. Habitat choice experiments with large halibut (Table 1) were conducted in four insulated fiberglass tanks (2.9 m in diameter). Sediment depth was 3 cm and water depth was 83 cm (flow = 12 l min 1). Bright daylight (10+ 0 Amol photons m 2 s 1) was simulated by fluorescent lights circling the tops of the laboratory walls (3.9 m high), and night illumination was 10 7 Amol photons m 2 s 1. 2.4. Experimental protocol Gibson and Robb (2000) recommended that knowledge of activity patterns in fish is desirable when using point measurements in habitat preference studies. Preliminary video

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recordings of young halibut and rock sole revealed that their locomotory activities and diurnal rhythms were somewhat different, and that both species were strongly affected by feeding history. Juvenile halibut were active primarily at night. However, when fed to satiation, they are normally buried in the sediment and remained essentially motionless for 12– 24 h. Juvenile rock sole were active both day and night, cleared their stomachs more slowly than halibut, and remained relatively inactive for 36 h or more after heavy feeding. After handling or transfers, both species buried into the sediment and remained motionless for several hours. Exploration of the experimental tank normally resumed during hours of darkness, and habitat choices were made during that time, with fewer explorations occurring during daytime in both species. The following protocol was established for habitat preference experiments on the basis of preliminary observations to insure that the fish had adequate opportunity to choose between the habitats offered. Halibut were fed in the afternoon prior to testing, and transferred to the experimental apparatus between 1300 and 1500 h the next day. Rock sole were handled in the same way except that they were starved for 2 days rather than 1. These starvation periods insured that the fish would become active and search the available substrata, yet they did not swim constantly in search of food. For all experiments, five fish were released on the two sides of the tank in subsets of two and three fish, alternating the release pattern on each test. Observations of fish location (side occupied) and their degree of burial were made beginning the next morning. Burial was scored according to the percentage of body covered with sediment, where 0 = < 5% coverage, 1 = 5 – 25%, 2 = 25– 50%, 3 = 50 –75%, 4 = 75– 100%. Most of the experiments were conducted with age-0 Pacific halibut in two size classes because of the number of fish available and because their relatively large size and dark coloration allowed easy observation and videotaping (Table 1). Rock sole were also tested in two size classes, but this is a smaller and more cryptic species than halibut, and thus more difficult to observe. However, similar tests were made with the two species for two different treatments using high-density sponge and shell as substrata. Eight runs with five fish each were made for every pairwise test of substrata (flat bare sand vs. structured habitat), yet the number of individual observations made during each run varied with fish size (Table 1). The largest fish (30-cm halibut) were observed most frequently because no disturbance was necessary to make observations. On the day following introduction to the test arenas, fish were observed hourly between 0800 and 1500 h for a total of eight observations. Medium-sized halibut were observed four times at approximately equal intervals between 0800 and 1600 h, and small fish, both halibut and rock sole, were observed twice, at 0800 and 1200 h. Location of the smallest fish required probing of the sediment in most cases. This sometimes resulted in flights by the fish across the tank, and hence, longer recovery periods were required between observations. However, video recordings showed that the fish continued to explore the tanks and consistently chose particular habitats. In all cases, the repeated observations were averaged for a run to avoid problems of pseudoreplication. Heterogeneity G-tests were performed to test for variation in observed choices among runs within experiments, and then the total value for the G statistic was used to accept or reject the null hypothesis that fish were distributed equally between the test substrata. Loglikelihood ratio tests were applied to contingency tables to test for the effects of light level,

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substratum type, fish size, and fish species on habitat selection. Standard analysis of variance was used to test for differences in burial scores with Levene’s test and box plots to test for homogeneity of variance and normal distributions. 2.5. Field test Field collections were made to test for the association of fishes with habitats containing physical structures observed in the laboratory. Age-0 rock sole and halibut have been found consistently during summer in Holiday Beach Cove in Chiniak Bay on the east side of Kodiak Island, Alaska (57j41.3VN, 152j28.0VW). Beam trawl (2 m wide, 3-mm mesh) collections made on 25 – 28 July 2002 revealed that rock sole were abundant over a wide depth range (3 to >20 m) while halibut were restricted to < 15 m. Consequently, on 29 July 2002, 14 short tows (5 min at < 1 m s 1) were made within the preferred depth range for both species (6 –14 m) to test for relationships between the fishes and habitat structure. Fish were counted for each tow along with the numbers of large bivalve shells and gastropod shells (both living and dead) (>5 cm in diameter), and sea stars, urchins, and sand dollars (living) which comprised the primary structure-forming materials on sand habitat in the cove. Scatter plots and standard regression analysis were used to test associations.

3. Results 3.1. Effects of light Medium-sized Pacific halibut (90 –134 mm TL) demonstrated a strongly positive choice for habitat with high-density sponge over flat bare sand at all light levels ( p < 0.05) (Fig. 1). The log-likelihood ratio test for the 2  4 contingency table indicated that selectiveness was not independent of light level ( G = 33.65, p < 0.001). Affinity for structured habitat increased from 60% in darkness and dimly lit conditions (10 5 Amol photons m 2 s 1) to 90% at the highest light level. The fish did not ordinarily move, rest, or bury in direct contact with the sponges, but they were found on or in the sand in the vicinity of sponges. The cryptic behavior of halibut was also influenced by light level. General observations during the experiments revealed that they were more active during the daytime in conditions of low light and darkness than at higher light levels. Also, the effect of light level on burial score (Fig. 1) was significant (ANOVA, F = 11.534, p < 0.001), with highest burial in highlight conditions (Scheffe’s multiple range test, p < 0.05) and approximately equal burial scores for fish in the light range 10 3 –10 7 Amol photons m 2 s 1 ( p>0.05). 3.2. Effects of substratum type and density A significant preference for structured habitat over smooth bare sand occurred in medium-sized juvenile halibut (90 – 144 mm TL) regardless of structure type (Fig. 2) ( p < 0.001 in all cases). Highest selectivity (90%) occurred with high-density sponge,

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Fig. 1. Effect of light level on the choice of habitat with sponge vs. bare sand by medium-sized juvenile Pacific halibut (90 – 134 mm TL) (top), and their burial. Choice is reported as the mean percentage ( F S.E.) of fish choosing each of the paired substrata in eight replicated runs of five fish each and observed four times. Burial was scored from 0 to 4 (see text). Burial is reported as the mean F S.E., where a score of 1 means that < 25% of the body was covered with sediment and 2 means there was 25 – 50% coverage.

lowest selectivity (70%) occurred with low-density sponge, and approximately equal selectivity (81 –85%) was observed in treatments with bryozoan mimics (high and low density), bivalve shells, and sand waves. In sand waves, most fish were observed lying in the troughs. Significant heterogeneity in selectiveness occurred in runs associated with low-density sponge ( G = 18.27, p < 0.05), low-density bryozoan ( G = 20.47, p < 0.01), and sand waves ( G = 39.28, p < 0.001); therefore, a complete contingency table analysis to test for differences in choices among the treatments was not valid. The log-likelihood ratio test for the 2  3 contingency table comparing the other three substrata revealed no significant difference in the degree of selectiveness by structure type (83 – 90%) ( G = 2.81, p>0.1). 3.3. Effects of fish size and species Small halibut (48 – 77 mm TL) had positive responses to sponge and shell substrata (Fig. 3) similar to the responses of medium-sized fish (Fig. 2). Responses to both substrata

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Fig. 2. Effect of substratum type on the choice of habitat by medium-sized juvenile Pacific halibut (90 – 144 mm TL). Choices were made between structured habitats and bare sand. SH = high-density sponge, SL = low-density sponge, BH = high-density bryozoan mimics, BL = low-density bryozoan mimics, Sh = bivalve shells, SW = sand waves. Choice is reported as the mean percentage ( F S.E.) of fish choosing each of the paired substrata in eight replicated runs of five fish each and observed four times.

were homogeneous among runs ( p>0.1) and highly significant ( p < 0.001). The choice of sponge habitat (91%) was significantly higher than that for shell (79%) ( G = 5.80, p < 0.05). Large Pacific halibut (270 – 337 mm TL) had a significant positive response to highdensity sponge ( G = 42.73, p < 0.001) with 63% of observations in the complex habitat, despite significant heterogeneity among runs ( G = 27.40, p < 0.001) (Fig. 4). Because of that heterogeneity, the response of large fish could not be compared statistically with

Fig. 3. Effect of substratum type on the choice of habitat by small juvenile Pacific halibut (48 – 77 mm TL). Choices were made between structured habitats and bare sand. SH = high-density sponge, Sh = bivalve shells. Choice is reported as the mean percentage ( F S.E.) of fish choosing each of the paired substrata in eight replicated runs of five fish each and observed two times.

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Fig. 4. Effect of substratum type on the choice of habitat by large juvenile Pacific halibut (270 – 337 mm TL). Choices were made between bare sand and high density sponge habitat (SH). Choice is reported as the mean percentage ( F S.E.) of fish choosing each of the paired substrata in eight replicated runs of five fish each and observed eight times.

responses of the two smaller fish groups. It is clear, however, that large halibut were less selective in their choice of sponge over sand than the smaller fish (90 – 91% choice for sponge habitat). Rock sole were tested for choice of sponge and shell substrata over smooth bare sand (Fig. 5). The smallest fish (15 – 25 mm TL) chose sponge over sand ( G = 25.22, p < 0.01). The response by larger individuals (42 – 74 mm TL) was also positive ( G = 35.85,

Fig. 5. Effect of substratum type on the choice of habitat by small juvenile rock sole (15 – 25 mm TL and 42 – 74 mm TL). Choices were made between structured habitats and bare sand. SH = high-density sponge, Sh = bivalve shells. Choice is reported as the mean percentage ( F S.E.) of fish choosing each of the paired substrata in eight replicated runs of five fish each and observed two times.

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p < 0.001) with no significant size effect observed ( G = 4.61, p>0.1). The larger rock sole also demonstrated a positive choice for shell substratum over bare sand ( G = 55.55, p < 0.001).

Fig. 6. Relationships between catch-per-unit-effort of age-0 Pacific halibut and age-0 rock sole, and bycatch of large shells and invertebrates in beam trawl tows made in a Kodiak, Alaska, nursery ground.

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Small Pacific halibut and rock sole of comparable size (42 –74 mm TL) were compared for habitat selectivities. Halibut made stronger choices for complex habitat in high-density sponge trials (91 vs. 69%; G = 5.43, p < 0.05) but there was no species difference in trials with shell (79 vs. 73%; G = 0.32, p>0.1). 3.4. Field associations Field sampling yielded 87 age-0 Pacific halibut and 437 age-0 rock sole, which were the numerically dominant fishes in the collections. Catch-per-unit-effort of fishes was positively correlated with habitat structure provided by shells and echinoderms in the habitat (Fig. 6).

4. Discussion Traditionally, the habitats of flatfishes have been characterized on the basis of depth, temperature, and sediment type because of their direct association with the bottom and burial in sediment (Gibson and Robb, 1992; Gibson, 1994). In the laboratory, age-0 Pacific halibut had strong affinity for physical structure, from small sand waves and bivalve shells to sponges and open forms providing canopy. Age-0 rock sole and large halibut had weaker but significant preferences for structured habitats. These preferences are not completely unexpected in flatfishes. Other laboratory experiments have shown that small to moderate amounts of vegetation are preferred by age-0 winter flounder (Phelan, 2000), and Murphy et al. (2000) found several flatfish species associated with beds of filamentous algae, eelgrass, and kelp in southeast Alaska. Kaiser et al. (1999) reported that plaice (Pleuronectes platessa L.) and dab (Limanda limanda L.) in the North Sea and English Channel were often associated with habitats containing sessile epibenthos such as bryozoans and soft corals, and juvenile flatfishes in Kodiak, Alaska, have been observed in biogenic depressions and in habitats containing bivalve shells (Norcross and Mueter, 1999). While densities of halibut and rock sole were correlated with invertebrate and shell bycatch in beam trawl collections, we routinely collect these species in substantial numbers on bare sand where there is no appreciable bycatch. Consequently, we conclude that the associations observed are not obligatory. Nevertheless, the behavioral response was strong and small flatfishes may profit from such an association. Shelter from predators is the most likely advantage to both halibut and rock sole for choice of structured habitats over bare sand substratum. Age-0 flatfishes are vulnerable to a host of predators (Bailey, 1994; Ellis and Gibson, 1995; Witting and Able, 1995; Van der Veer et al., 1997; Wennhage, 2000), and numerous experimental studies show that complex habitats protect small fishes from predators (e.g., Tupper and Boutilier, 1995; Beukers and Jones, 1998; Halpin, 2000). Both Manderson et al. (2000) and Wennhage (2002) have shown that structured habitats reduce predation rates for age-0 winter flounder and plaice, respectively. Less strong preference for structure in juvenile rock sole than Pacific halibut may be related to different defense mechanisms. Personal observations reveal that rock sole are more cryptic on sediment than halibut. They are less motile and relatively slow, and have

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the ability to match color and pattern of sandy substrata more exactly than halibut. These characteristics make rock sole less subject to detection and pursuit by visual predators. Experiments in laboratory mesocosms have shown that predation rates by age-2 halibut on age-0 rock sole are lower than those on similar-sized halibut (Ryer et al., in preparation). These experiments also show that the presence of sponges significantly reduced the vulnerability of the two prey species, with the strongest effect on survivorship of halibut. The primary mechanism for the species difference was a significantly larger decrease in the predator – prey encounter rate for halibut prey than for rock sole when habitat complexity was increased. We conclude that the strong preference for structured habitat in age-0 halibut is related to its high vulnerability to visual predators. Exactly how halibut and rock sole make the selection for structured habitat is unknown, but two lines of evidence for halibut suggest a shelter-seeking response. First, while sponge habitat was always chosen over sand, the strength of the response decreased with decreasing light level. Second, burial also decreased with decreasing light. These observations indicate that young halibut possess behavioral responses that reduce their visibility and vulnerability to visual predators. The structures used in our experiments cast very small shadows and the fish did not shelter under the structures, so it seems unlikely that the fish were seeking low light microhabitats. However, the environment created by sponges and other vertical habitat features served to reduce the visual field for the fish, which may be preferred. The choice for sponge habitat over bare sand remained positive even in total darkness and some element of tactile perception must also be functioning. Affinity for structured habitat in the field could also be related to availability of foods. Age-0 halibut and rock sole consume primarily motile crustaceans such as mysids, amphipods, cumaceans, and small shrimps (Holladay and Norcross, 1995; Holladay, 2001). Small crustaceans such as these are often most abundant in structurally complex habitats (Orth et al., 1984; Bostro¨m and Bonsdorff, 2000). In laboratory experiments, Phelan et al. (2001) found that presence of food overwhelmed sediment preferences exhibited by winter flounder. While there were no food cues in our experiments, fishes may choose habitats that typically carry large numbers of appropriate prey. Expanded field work related to interactions between young flatfishes, habitat structure, and food availability is warranted for the future. The laboratory studies discussed here represent only a beginning for understanding the mechanisms that affect relationships between juvenile flatfishes and their benthic habitats. Future investigations should include more in situ field observations, particularly with respect to microhabitat associations (see Norcross and Mueter, 1999). Field assessments of habitat-specific growth and survivorship are also warranted, and field manipulations, including experimental enhancement of habitat complexity, may be possible in shallow water. Measures of habitat complexity are commonly incorporated into habitat suitability models for roundfishes such as trout (Bozek and Rahel, 1992), pike (Minns et al., 1996), salmon (Roni et al., 1999), and spotted seatrout (Rubec et al., 1999), but benthic features other than sediment type are rarely considered for flatfishes (e.g., Kaiser et al., 1999; Stoner et al., 2001). It is increasingly evident, however, that predictive models of habitat for some flatfishes such as Pacific halibut and winter flounder may improve with the

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inclusion of nontraditional variables such as shells, large epibenthic biota, and sediment bedforms. Low-relief continental shelf habitats are subject to intensive fishing for demersal fishes and invertebrates with a variety of gear types. For example, Auster et al. (1996) estimated that an area equivalent to 200– 400% of the surface area of Georges Bank was swept by towed fishing gear on an annual basis between 1976 and 1991. Other traditionally important fishing grounds such as those in the North Sea, the Bering Sea, and the Gulf of Mexico have also been heavily fished for decades. The impacts of fishing gear on benthic communities and habitat are now well documented (see reviews by Jennings and Kaiser, 1998; Auster and Langton, 1999; Collie et al., 2000), and it is clear that fishing gear can alter bedforms, affect changes in the benthic infauna, and remove or dislodge sessile invertebrates. The larger invertebrates such as sponges, bryozoans, ascidians, and anthozoans are among the most vulnerable (Collie et al., 1997; Freese et al., 1999; Kaiser et al., 2000; Pitcher et al., 2000). In one study directly relevant to juvenile halibut and rock sole, McConnaughey et al. (2000) quantified the abundance of large benthic invertebrates in previously unfished and heavily fished softbottom areas of the eastern Bering Sea. Virtually all sedentary invertebrates including sponges, anemones, bryozoans, tunicates, as well as empty shells of bivalves and gastropods were significantly less abundant in the fished area than in the unfished area. We can only hypothesize the potential impacts of such habitat alterations on juvenile fishes because experimental field studies including small fishes and habitat structure have not been conducted. Nevertheless, impacts of lost habitat structure can be either direct or indirect. First, the fishes that prefer structured habitat may not settle or recruit to habitats where physical structures have been lost, or they may emigrate upon habitat disturbance. Second, small fishes may be lost to predation in the absence of shelter provided by habitat with physical structure, as observed in a number of experiments with both Atlantic cod (Tupper and Boutilier, 1995; Lindholm et al., 1999) and flatfishes (Manderson et al., 2000; Wennhage, 2002; Ryer et al., in preparation). Links between habitat structure and growth, survivorship and recruitment of fishes to fisheries need to be explored. However, our experiments on habitat preference make it clear that the presence of bedforms and biological structures in low-relief sedimentary habitats can have critical functional significance even for flatfishes. These important habitat features may need to be identified and protected.

Acknowledgements We thank Eric Munk for logistical support in Kodiak, boat operation, and assistance with collections. Collections were also made with the help of Captain Tim Tripp, T. Hurst, M. Ottmar, E. Sturm, S. Sogard, and M. Spencer. A. Abookire helped with fish identifications. B. Stevens, R. Otto, and the Borough of Kodiak provided laboratory space for holding fish. M. Ottmar and E. Sturm assisted with laboratory set-ups. M. Davis arranged for collecting and transport permits and supervised quarantine procedures. F. Scharf and G. Stauffer, B. Norcross, and anonymous reviewers provided helpful criticisms on the manuscript. [SS]

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