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Seasonal abundance of two important forage species in the North Pacific Ocean, Pacific herring and walleye pollock
Fisheries Research 83 (2007) 319–331
Seasonal abundance of two important forage species in the North Pacific Ocean, Pacific herring and walleye pollock Michael F. Sigler ∗ , David J. Csepp National Oceanic and Atmospheric Association, National Marine Fisheries Service, Alaska Fisheries Science Center, Auke Bay Laboratory, 11305 Glacier Highway, Juneau, AK 99801-8626, USA Received 8 March 2006; received in revised form 29 September 2006; accepted 8 October 2006
Abstract Pacific herring (Clupea pallasii) and walleye pollock (Theragra chalcogramma) are important forage species in the North Pacific Ocean, but their seasonal abundance patterns are poorly known. During three consecutive years of monthly acoustic surveys in Lynn Canal, southeastern Alaska, large schools of herring dominated during winter and were present in a 60-km long submarine gully; this gully appears to provide critical winter habitat for herring when their prey are less available and energy expenditure must be reduced. The salient change in pollock distribution is a shift from shallow waters during summer to deeper waters during winter, such that shallow (<40 m) waters are nearly devoid of pollock during winter. The shift presumably occurs in response to the build-up of secondary productivity during summer and predator avoidance during winter. The seasonal changes in herring abundance drove seasonal changes in predator abundance, as Steller sea lions (Eumetopias jubatus) and humpback whales (Megaptera novaeangliae) preyed upon the winter aggregation of herring. Such seasonal links likely serve an important role in structuring trophic relationships in the North Pacific Ocean ecosystem. Published by Elsevier B.V. Keywords: Forage fish; Pacific herring; Walleye pollock; Seasonality; Ecology
1. Introduction Forage species are a critical part of the North Pacific Ocean ecosystem. However, few studies have quantified seasonality of forage species availability despite evidence that foraging pinnipeds (Sinclair and Zepplin, 2002) and odontocetes (Simil¨a et al., 1996) take advantage of seasonally concentrated prey. Well-known examples of forage species in the North Pacific Ocean are anadromous fishes such as Pacific salmon (Oncorhynchus spp.; e.g. Willson and Halupka, 1995) and eulachon (Thaleichthys pacificus; e.g. Marston et al., 2002; Sigler et al., 2004), whose spawning aggregations provide important seasonal food resources for mammalian and avian predators. Pacific herring (Clupea pallasii) and walleye pollock (Theragra chalcogramma) also are important forage species in the North Pacific Ocean and they are prey of marine fish, birds, and mammals (Livingston, 1993). Predation rates can vary season-
∗
Corresponding author. Tel.: +1 907 789 6037; fax: +1 907 789 6094. E-mail addresses: [email protected] (M.F. Sigler), [email protected] (D.J. Csepp). 0165-7836/$ – see front matter. Published by Elsevier B.V. doi:10.1016/j.fishres.2006.10.007
ally. For example, Pacific cod (Gadus macrocephalus) predation rates on herring are highest during winter (Walters et al., 1986); great sculpins (Myoxocephalus polyacanthocephalus) prey upon young-of-the-year pollock once they are demersal (Carlson, 1995). Predation rates also can vary annually. For example, groundfish predators appear to track strong year classes of pollock (Livingston, 1993). The goal of this study was to improve our understanding of seasonal predator–prey relationships for major forage species in the North Pacific Ocean. Predator–prey relationships involving forage species are poorly described for the North Pacific Ocean, especially in seasons other than summer. We measured the abundance of Pacific herring and walleye pollock each month for three consecutive years in Lynn Canal in southeastern Alaska, an area occupied by Steller sea lions (Eumetopias jubatus), an important marine predator in the North Pacific Ocean. Herring and pollock are by far the most common prey species found in Steller sea lion scats in this area, with percent frequency of occurrence of more than 80% for each species year-round (Womble and Sigler, 2006). Our study area also contains a Steller sea lion haulout at Benjamin Island. The number of sea lions at Benjamin Island varies seasonally, with counts peaking at
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Fig. 1. Map of study area. Boundaries between strata are indicated by dotted lines. From north to south, the strata for the standard survey area are Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench. Strata for occasionally sampled strata are not shown.
several hundred sea lions during winter (Womble and Sigler, 2006). Our objectives were: (1) to quantify Pacific herring and walleye pollock monthly abundance, and (2) to describe the role of seasonal abundance changes in the life history of Pacific herring and walleye pollock. The research described here is part of a broader study to explain decreases in Steller sea lion abundance. 2. Materials and methods 2.1. Study area Acoustic surveys were conducted in Favorite Channel (Fig. 1) in lower Lynn Canal between Tee Harbor (58◦ 25 N, 134◦ 46 W) and Vanderbilt Reef (58◦ 36 N, 135◦ 01 W) on a monthly basis between June 2001 and May 2004. This area was chosen because it includes Benjamin Island which is used as a seasonal haulout (a terrestrial site used by pinnipeds for breeding, caring for young, and molting) by Steller sea lions from October to April. The area also is relatively sheltered, facilitating year-round surveys, and encompasses a variety of habitats (depth range between 5 and 305 m; average depth = 60 m) typical of southeastern Alaska. 2.2. Acoustic surveys To estimate pollock and herring abundance, we used a portable 38-kHz Simrad1 echo-integration system with a 12◦ beam angle, towed beside the 11-m long F/V Williwaw at 11 km h−1 . We simultaneously collected location data with 1 Reference to trade names does not imply endorsement by the U.S. Government.
a Garmin global positioning system with location accuracy ±10 m. From June 2001 to May 2002, acoustic surveys followed a 36-km-long path that ran parallel to the mainland or offshore islands, or perpendicular between the two. Thereafter, surveys followed a longer 56-km zigzag path across the same area (Fig. 1) to increase sampling coverage of the study area. All surveys began after daybreak and concluded before dusk. Some fish species, particularly herring, undergo diurnal migrations through the water column that can affect acoustic density estimates (Huse and Korneliussen, 2000; Hjellvik et al., 2004). We chose to sample only during daylight because of the diel variation in acoustic density estimates and to facilitate observations of foraging sea lions while collecting acoustic data. Usually one survey was completed each month. Two of the monthly surveys were replicated to estimate variance of the abundance estimates. Opportunistic trawl samples were collected to identify the acoustic targets in the echograms and to provide biological information about the target species. Length, weight, and species composition data were collected quarterly with midwater trawls deployed from the 18-m long F/V Solstice from September 2001 to March 2002, the 31-m long F/V Viking Storm from May 2002 to September 2003, and the 37-m long R/V Medeia from January 2004 to March 2004. Two midwater trawls were used: (1) a 164 Nordic rope trawl with 1.5-m2 alloy doors, 7-m height, and 17-m width with a 19-mm mesh codend liner, and (2) a mesh wing 25/21/64 trawl with 3.0-m2 alloy doors, 11-m height, and 29-m width with a 32-mm mesh codend liner. The larger midwater trawl generally was used with the larger vessels to match their larger trawl-handling equipment. Size selectivity likely was unaffected by using two different nets because fish as small as 4-cm fork length (FL) commonly were caught by both nets. Typical characteristics of trawling operations were sinking rate
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331
during deployment of 11 m min−1 , rising rate during retrieval of 15 m min−1 , and towing speed at target depth of 5.6 km h−1 . All catches were sorted to the lowest taxonomic order practicable, usually species, then weighed. The total number caught also was counted, except for small, numerically abundant fish, which were subsampled for mean weight to estimate total number caught. The acoustic data were classified by species using the identification information from midwater trawls. Midwater trawls targeting herring and pollock were dominated by catches of these species. Herring comprised 87% of the catch by weight when herring was targeted and pollock comprised 84% of the catch by weight when pollock was targeted. The corresponding echogram patterns showed that herring during summer characteristically formed dense, round or tall pelagic schools, typically of small size. During winter, herring formed a consistent, dense layer associated with the bottom in submarine gullies. In contrast to herring, juvenile and adult pollock formed loose aggregations. Juvenile pollock typically were shallower than adult pollock. Pollock were classified as juvenile if their gonads were immature. In addition, juvenile and adult pollock sometimes were differentiated by comparing the single-target virtual echogram (from the echo-integration software SonarData Echoview) to published target strength (TS) values by fish species and size. Questionable acoustic targets were highlighted and then analyzed by using minimum, maximum, and mean TS, TS frequency distributions, and TS versus depth plots that were compared with published values (Traynor, 1996; Ona, 2003). Species classification of monthly acoustic data from the quarterly midwater trawl samples was reasonable because echogram patterns attributable to herring and pollock were consistent from month-to-month and year-to-year. An echo-integrator summed the returning echoes from fish observed beneath the vessel. The acoustic data were classified by species using the identification information from midwater trawls, integrated for 0.183-km length intervals (transects) and 10-m depth intervals, and corrected for instrument calibration using the software SonarData Echoview. The output of acoustic scattering (NASC) is proportional to fish density (MacLennan and Simmonds, 1992). To convert NASC to fish density in numbers, estimates of acoustic reflectivity for single fish were needed by species. Target strength refers to the acoustic reflectivity of a single echo or fish and depends on length (L in cm): TS = 20 log10 L + b (MacLennan and Simmonds, 1992). For pollock, b = −66 (Traynor, 1996) and for herring, b = −65.4 (Ona, 2003). Similar b-values were reported for herring in two other recent studies: −66 in fall by Thomas et al. (2002) and −65.1 by Gauthier and Horne (2004). In addition, NASC and TS values for herring were adjusted for depth compression of the air bladder (Ona, 2003) and acoustic shadowing (Zhao and Ona, 2003) by methods described in the next two sections of this paper. Herring gonad size also may influence herring target strength, but we chose to ignore this effect based on Ona (2003) recommendation. Target strength was transformed to backscattering cross-section by σ bs = 4π10TS/10 . Fish density in numbers was computed by dividing NASC by σ bs . Fish density in weight equals density in number multiplied by average weight. Fish density in weight
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is expressed by 0.183-km length interval (transect) and 10-m depth interval in units of kg km−2 . Fish density in weight was converted to nutritional energy density using season-, size-, and species-specific energy conversions determined in a companion study (Vollenweider et al., submitted for publication). Whereas seasonal energy content varied approximately two-fold (5.7–10.6 kJ g−1 for herring and 3.5–4.8 kJ g−1 for pollock), biomass density in an area could vary by several orders of magnitude. Therefore, the variation in prey energy density (kJ km−2 ) was due mostly to variation in biomass present, rather than differences in mass-specific energy content. Nutritional energy density is expressed by 0.183-km length interval (transect) and 10-m depth interval in units of kJ km−2 . We summed each transect’s data across 10-m depth intervals, such that each 0.183-km long transect had an estimate of biomass density (in kg km−2 ) and energy density (in kJ km−2 ). The transect data were grouped by strata, where each stratum encompassed similar habitat, and average biomass density and average energy density were computed by strata. For each stratum, total biomass (in t) was computed by multiplying biomass density (in kg km−2 ) by the area of the stratum (in km2 ). Total energy was computed by multiplying energy density (in kJ km−2 ) by the area of the stratum (in km2 ). Four strata (Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench) were sampled during standard monthly surveys. Five additional strata (Lena Point, Portland Trench, North Douglas, Douglas Trench, and Fritz Cove) were sampled occasionally during winter. 2.3. Target strength adjustment for depth compression Herring are physostomous (have an open swim bladder) and are incapable of gas secretion (Blaxter and Batty, 1984), so swim bladder compression with depth cannot be compensated for by gas secretion. We adjusted herring TS for the effect of depth following Ona (2003). Ona (2003) reported a TS for Atlantic herring of 20 log10 L − 65.4 − 2.3 log10 (1 + z/10) where z is the water depth (in m). Thomas et al. (2002) also reported a TS equation adjusted for depth for Pacific herring of 20 log10 L − 66 − 6.7 log10 (1 + z/10) (reformulated to match that of Ona (2003)). The equation in Thomas et al. (2002) implies a greater depth effect than the equation in Ona (2003) (multipliers of 6.7 and 2.3, respectively). We chose the equation of Ona (2003) rather than Thomas et al. (2002) because Ona tested a greater depth range (near surface to 500 m) than Thomas’s estimate (near surface to 43 m). Thomas et al. (2002) also assumed that the swim bladder acts like a free, spherical balloon in responding to increased pressure with depth, whereas Ona (2003) hypothesized that the herring swim bladder has fixed end positions and pressure-sensitive diameter, which accounts for less depth effect than predicted by Boyle’s Law. 2.4. Shadow coefficient The shadow coefficient is a measure of the attenuation of sound energy due to fish density. Fish nearest the transducer
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Table 1 Acoustic properties of reference seafloor used to estimate shadow coefficient Reference area
Average depth (m)
Average angle (◦ )
S.E. angle
Average NASC
S.E. NASC
Sample size (# transects)
A B
111 108
1.0 0.9
0.010 0.008
2,039,759 1,349,117
3600 1378
152 180
Transect length is 20 m.
attenuate the acoustic energy so that more distant fish contribute less to the received signal; thus, the shadow coefficient is a measure of the energy removed from the beam by each fish (MacLennan and Simmonds, 1992). An estimate of the shadow coefficient is needed for abundance estimation of densely schooling fish like herring. Foote (1999) estimated a shadow coefficient for Atlantic herring of 2.41 ± 0.33. No estimate has been reported for Pacific herring. We estimated the shadow coefficient for Pacific herring from our survey data by applying the methods of Foote et al. (1992) to select the data, and the methods of Zhao and Ona (2003) to analyze the data. Foote et al. (1992) stipulated that the bottom in the study area be flat and acoustically uniform, the range of fish observations span a range of acoustic (NASC) values, and the range of NASC include areas with fish absent. We chose data from two areas with nearly flat (average bottom angle ≤1◦ ), homogeneous (average NASC = 2,039,759 ± 3600 and 1,349,117 ± 1378 m2 nmi−2 ) bottom (Table 1). The maximum NASC due to herring was 644,562 m2 nmi−2 (Table 2). The shadow coefficient was estimated from the observed reduction in bottom NASC due to herring NASC. 3. Results 3.1. Species composition A total of 34 monthly acoustic surveys were conducted between June 2001 and May 2004. No data were collected in June and July 2002 due to logistical and equipment problems. The standard transects were surveyed during daylight hours and totaled 1621 km of acoustic transiting. Opportunistic surveys occasionally were conducted outside the standard survey area during winter when herring were abundant and totaled 219 km of acoustic transiting. A total of 96 midwater trawl tows were completed during 11 quarterly midwater trawl cruises.
The largest midwater trawl catches were walleye pollock (1472 kg of 3465 kg total weight and 9912 of 72,534 total number) and Pacific herring (682 kg and 8641). Acoustic estimates of abundance were completed for these two species because the catches consistently confirmed delineations of these species in the echograms. Other species with large catches by total weight (>100 kg) or total number (>1000) were squid, eulachon, myctophids (especially northern lampfish (Stenobrachius leucopsarus)), Pacific hake (Merluccius productus), capelin, pallid eelpout (Lycodapus mandibularis), northern smoothtongue (Leuroglossus schmidti), and shrimp (especially Pacific glass shrimp (Pasiphaea pacifica)). These species were also widely caught and their percent occurrence exceeded ∼10%. 3.2. Herring shadow coefficient The estimated mean shadow coefficient was 0.94 ± 0.16 (Table 2). The fitted linear model reasonably represented the data. The estimated shadow coefficient implies a relatively small correction for acoustic shadowing. We applied this shadow coefficient to the example data in Table 1 of Zhao and Ona (2003) and found that the corresponding correction factor is 1.07 for the example herring NASC of 224,396. The shadow coefficients for Atlantic and Pacific herring appear substantially different: 2.41 versus 0.94. However, the corresponding correction factors are closer than implied by the difference between the shadow coefficients. The correction factor for the example data in Zhao and Ona (2003) is 1.21 versus 1.07 for shadow coefficients of 2.41 and 0.94, respectively. 3.3. Sensitivity of herring abundance estimates We compared the sensitivity of herring biomass estimates using three methods: (1) the standard target strength equation applied to Pacific herring acoustic measurements from Alaska,
Table 2 Shadow coefficient estimates for Pacific herring Data set
Area
Date
Maximum NASC
Shadow coefficient
Sample size (# transects)
1 2 3 4 5 6 7 8
A A A A B B B B
16 January 2002 16 January 2002 18 January 2002 13 February 2004 16 January 2002 18 December 2002 13 January 2003 13 February 2004
244,527 69,080 143,859 644,562 327,664 485,628 442,144 317,539
1.24 1.57 1.47 0.41 0.59 1.09 0.63 0.51
41 64 222 176 206 294 267 275
Mean S.E.M.
0.94 0.16
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(2) the standard equation adjusted for acoustic shadowing, and (3) Ona (2003) equation and accounting for depth and acoustic shadowing (the method applied in this paper). In previous studies, the standard TS equation applied to Pacific herring acoustic measurements from Alaska has been TS = 26.5 log10 L − 76.4 (Thomas et al., 2002). Method 3 explicitly accounts for depth differences between herring schools and explicitly adjusts for acoustic shadowing, whereas Method 1 does not. Differences in biomass estimates by the three methods were small during winter when herring were most abundant (≤9%; Table 3). The standard equation adjusted for acoustic shadowing increased biomass estimates only by small amounts (Method 1 versus Method 2; ≤8%). The greatest differences occurred for months when herring are less abundant (Method 1 versus Method 3; ≥−29%). Herring were at shallower depths during these months. The depth adjustment for Method 3 increases the
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TS estimate for each herring; thus, the estimated biomass is less for Method 3 than for Method 1. 3.4. Prey composition and seasonal variation Forage species biomass varied dramatically among months and among species (Table 4). For herring, biomass in the standard survey area ranged between 6 t (June 2001) and 33,000 t (December 2001). In all 3 years, biomass peaked between December and February due to the presence of large herring aggregations. In contrast, walleye pollock biomass in the study area was much less than herring, varying between 3 t (February 2002) and 655 t (July 2001). Pollock biomass peaked between July and October. Opportunistic acoustic surveys conducted outside the standard survey area sometimes found significant quantities of herring (>1000 t) in Lena Point, North Douglas,
Table 3 Comparison of herring biomass estimates (t) from three computational methods: (1) standard target strength equation (TS = 26.5 log10 L − 76.4, Thomas et al., 2002); (2) standard equation and account for acoustic shadowing; (3) explicitly account for depth effect on TS and adjust for acoustic shadowing (the method applied in this paper) Year and month
Method 1
Method 2
Percent difference, Methods 1 and 2 (%)
Method 3
Percent difference, Methods 1 and 3 (%)
2001 June July August September October November December
7 528 1,332 2,977 782 1,337 30,239
7 530 1,340 3,139 787 1,345 32,264
0 0 1 5 1 1 7
6 406 994 2,506 716 1,347 32,976
−15 −23 −25 −16 −8 1 9
2002 January February March April May August September October November December
14,720 3,803 260 1,206 161 6,956 2,084 1,274 2,141 12,241
15,079 3,855 261 1,212 161 7,279 2,109 1,287 2,173 12,524
2 1 0 1 0 5 1 1 1 2
15,874 3,244 203 883 139 5,795 2,129 1,173 2,244 12,492
8 −15 −22 −27 −14 −17 2 −8 5 2
2003 January February March April May June July August September October November December
17,833 6,143 797 83 1,089 227 228 747 1,600 1,027 5,538 19,747
18,410 6,290 803 83 1,107 227 230 754 1,614 1,047 5,971 20,580
3 2 1 0 2 0 1 1 1 2 8 4
19,272 6,045 757 59 837 186 191 580 1,443 941 5,309 20,139
8 −2 −5 −29 −23 −18 −16 −22 −10 −8 −4 2
2004 January February March April May
4,188 23,599 949 138 43
4,380 25,279 1,004 138 43
5 7 6 0 0
4,319 25,026 988 128 39
3 6 4 −7 −10
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Table 4 Biomass estimates (t) by year, month, strata, species and area size (km2 ) by strata Year and month
Pacific herring
Walleye pollock
Vanderbilt Reef
Benjamin Island
Eagle Beach
Amalga Trench
Total
Vanderbilt Reef
Benjamin Island
2001 June July August September October November December
0 132 129 0 0 0 0
0 0 251 0 698 1,148 12,019
1 0 193 1,462 0 111 85
5 274 421 1,044 18 88 20,873
6 406 994 2,506 716 1,347 32,976
39 37 85 85 37 9 51
8 70 5 17 67 13 2
2002 January February March April May August September October November December
0 na na 0 0 0 na na 0 0
120 219 156 34 13 0 1,884 0 1,997 5,258
2 1 43 155 2 0 70 312 0 371
15,713 3,146 4 694 123 5,795 175 861 248 6,863
15,835 3,367 203 883 139 5,795 2,129 1,173 2,245 12,492
23 na na 18 106 45 na na 67 47
2003 January February March April May June July August September October November December
0 27 0 0 84 0 0 0 0 0 0 0
240 237 0 12 86 23 1 79 66 941 1,082 0
592 3 115 19 362 63 1 41 376 0 4,227 0
18,439 5,849 642 28 304 100 188 459 1,006 0 0 20,139
19,272 6,117 757 59 837 186 191 580 1,448 941 5,309 20,139
2004 January February March April May
na na 0 0 0
0 0 4 0 3
0 0 0 44 28
4,319 25,026 984 84 8
4,319 25,026 988 128 39
6.2
8.1
22.9
47.5
Area size (km2 )
10.3
and Fritz Cove strata, but not in Portland Trench or Douglas Trench strata (Table 5). Patterns of total nutritional energy followed the biomass patterns (Fig. 2). For herring, total energy ranged between 51 million kJ (June 2001) and 285,000 million kJ (December 2001). For pollock, total energy ranged between 11 million kJ (February 2002) and 2800 million kJ (September 2002). Consequently, herring constituted most of the total energy available in most months. Averaged across all months, herring represented 81% of the total energy available to sea lions, compared to 19% for pollock. The disparity in total energy attributed to herring was even greater during the winter months. Between November and February, herring constituted an average of 99% of the total energy, compared to 1% for pollock.
Eagle Beach
Amalga Trench
Total
13 58 6 108 41 3 3
42 491 128 427 270 54 143
102 655 225 637 415 79 199
3 0 1 3 61 19 24 9 10 4
2 2 2 7 43 41 28 25 26 11
45 1 101 84 262 448 471 389 184 257
73 3 104 113 473 553 523 422 287 319
43 46 10 9 18 15 27 31 30 24 32 32
7 1 6 16 11 16 30 63 20 22 56 6
2 1 0 58 4 31 11 97 58 94 33 7
21 7 70 159 29 64 253 266 347 172 81 61
74 55 86 242 61 126 321 457 455 313 203 106
na na 2 4 8
2 14 1 7 33
1 1 0 6 30
77 6 56 109 106
80 21 60 126 177
Herring were found at greater depths in winter than in summer, as were pollock, although depth ranges differed between species. Herring biomass density was greatest at 75–125 m depths from December to March, at 15–85 m depths from April to August, and at 35–115 m depths from September to November (Fig. 3). The depth distribution usually was unimodal, except from April to June, when the depth distribution was bimodal with distinct modes at 15–25 and 65–75 m. Pollock primarily were found from 65 to 235 m depths from November to March and from 35 to 235 m depths from April to October. The depth distribution was bimodal for several months (e.g. July). The deeper modes (165–235 m) were due to adult pollock biomass and the shallower modes were due to juvenile pollock biomass based on midwater trawl catches and TS values.
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Table 5 Biomass estimates (t) by year, month, strata, and species for opportunistic surveys, and area size (km2) by strata Year and month
Lena Point
Portland Trench
North Douglas
Douglas Trench
Fritz Cove
Standard strata
Total
Pacific herring 2002 January February March
2844 1180 na
na na 60
na 455 0
na 656 17
3256 79 0
15,835 3,367 203
21,935 5,737 281
na na na
na na na
na na 3136
na 258 251
1555 26 18
19,272 6,117 757
20,827 6,400 4,163
na
na
na
na
0
4,319
4,319
6.2
6.0
4.4
5.7
4.5
47.5
74.2
Walleye pollock 2002 January February March
3 0 na
na na 20
na 7 1
na 42 0
1 4 3
73 3 104
78 56 128
2003 January February March
na na na
na na na
na na 1
na 185 4
7 5 1
74 55 86
81 244 92
2004 January
na
na
na
na
6
80
86
2003 January February March 2004 January Area size
(km2 )
The sums of biomass estimates for strata sampled during standard surveys also are displayed. Standard strata are Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench (Table 4).
Herring and juvenile pollock were segregated from adult pollock. Average depths of herring and juvenile pollock (based on biomass density) were less than 100 m, whereas average depths of adult pollock were 150–200 m (Fig. 4). Herring and juvenile pollock overlapped from September to April, but separated somewhat from May to August. During these months, average depths of herring were about 50 m and average depths of juvenile pollock were about 80 m.
Herring size ranged from 8 to 27 cm FL in midwater trawl samples (Table 6). Most herring were 16–25 cm FL, except for March 2002 when smaller (12–17 cm FL) herring were more common. Pollock size ranged from 11 to 69 cm FL in midwater trawl samples (Table 7). Most pollock were less than 35 cm FL. Larger pollock were uncommon in all strata except Vanderbilt Reef where bottom depths were greater (mean 199 m) than the other strata (mean 99 m). 3.5. Variance estimates
Fig. 2. Nutritional energy (millions kJ) by year, month and species: Pacific herring () and walleye pollock ().
The estimates of herring abundance sometimes were highly variable. The coefficient of variation (CV) from replicate surveys ranged from 11% to 141% (Table 8). The CV values sometimes were large because herring were aggregated and the size and density of each aggregation were variable. Greater abundance and further survey replication improved precision of abundance estimates for Pacific herring. Abundance was intermediate for February 2002 for Amalga Trench; the CV was 42%. Abundance was high for January 2002 for Amalga Trench and three surveys were conducted; the CV was 11%. The estimates of pollock abundance generally were less variable than the estimates of herring abundance. Most CV values were between 22% and 68% (Table 8). The CV values were lower because spatial distributions of juvenile and adult pollock were relatively homogeneous. Only young-of-the-year and age 1+ pollock were aggregated, although not as tightly as herring.
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Table 6 Length frequencies (%) by year and month for Pacific herring Fork length (mm)
2001 September
80 90 100 120 130 140 150 160 170 180 190 200 210 220 230 240 250 260 270
0.0 0.0 0.0 0.0 0.0 0.0 1.1 5.6 27.8 23.3 13.3 16.7 8.9 2.2 0.0 0.0 1.1 0.0 0.0
Sample size
90
2002 December 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.9 0.0 5.7 10.4 22.6 21.7 21.7 12.3 3.8 0.0 0.0 106
March 0.0 0.0 1.5 5.4 17.7 18.2 21.2 16.7 9.4 2.5 3.0 3.0 1.5 0.0 0.0 0.0 0.0 0.0 0.0 203
2003 May 0.8 0.8 0.0 0.0 0.0 0.0 4.0 5.6 12.8 8.0 11.2 15.2 16.0 8.8 8.0 6.4 2.4 0.0 0.0 125
September 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.0 6.6 21.9 23.8 13.2 9.3 8.6 7.9 3.3 1.3 151
December 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 2.8 2.8 7.7 12.6 22.4 25.2 20.3 6.3 0.0 0.0 143
2004 March 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 23.3 26.7 33.3 10.0 6.7 0.0 0.0 0.0 0.0 0.0 30
May 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.9 16.2 25.1 33.0 14.5 6.7 0.0 0.6 0.0 179
September 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 20.0 40.0 20.0 20.0 0.0 0.0 0.0 0.0 0.0 0.0 5
January 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.0 1.7 12.2 19.4 24.1 20.7 11.4 6.8 2.5 0.4 0.4 0.0
March 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.6 3.6 5.5 20.0 21.8 23.6 18.2 3.6 0.0 0.0 0.0 0.0
237
55
January
March
0.0 47.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 23.8 23.8 0.0 0.3 0.2 0.0 0.8 0.4 0.6 0.6 0.8 0.2 0.6 0.2 0.0 0.0 0.1 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 44.4 22.2 0.0 22.2 0.0 0.0 0.0 0.0 11.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Values greater than 5% are bold. Table 7 Length frequencies (%) by year and month for walleye pollock Fork length (mm)
2001 September
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 Sample size
0.0 0.0 0.0 1.6 17.6 45.2 13.8 0.0 2.1 8.0 6.4 0.7 0.0 0.1 0.5 0.9 1.0 1.3 0.5 0.2 0.2 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 240
2002 December 3.5 1.4 0.3 0.0 2.4 22.8 31.8 12.1 1.0 1.0 1.0 0.7 0.9 2.3 0.7 1.8 0.0 1.8 0.9 3.6 6.3 1.8 0.9 0.9 0.0 0.0 0.0 0.0 0.0 0.0 254
March 12.2 67.3 12.2 0.0 0.0 6.1 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.2 0.0 0.1 0.0 0.8 0.2 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.0 38
2003 May 0.0 0.5 6.3 5.8 0.0 2.4 11.1 24.7 27.1 7.8 3.4 1.5 2.9 1.7 1.6 0.9 0.5 0.4 0.2 0.4 0.2 0.4 0.1 0.0 0.1 0.0 0.0 0.0 0.0 0.0 264
September 0.0 0.0 0.0 0.0 1.7 23.7 13.5 4.5 9.0 18.0 15.8 6.2 1.7 2.3 1.1 0.1 0.0 0.2 0.0 0.4 0.6 0.1 0.4 0.3 0.0 0.1 0.0 0.1 0.0 0.0 196
December 0.0 0.0 0.0 0.0 1.7 24.8 38.0 10.3 6.6 9.1 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.4 0.9 0.4 0.0 0.9 3.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 241
2004 March 0.0 0.0 0.0 0.0 0.9 5.3 25.9 8.8 9.7 8.8 16.7 5.7 5.3 3.5 3.1 0.7 1.2 1.9 0.4 0.7 0.8 0.2 0.4 0.1 0.0 0.0 0.0 0.0 0.0 0.0 274
May 0.0 0.0 0.0 0.0 0.0 0.0 9.1 20.7 12.3 6.7 8.1 9.1 9.2 5.3 6.2 4.5 4.2 1.9 1.0 0.6 0.3 0.2 0.3 0.1 0.1 0.0 0.0 0.0 0.0 0.0 407
September 0.0 0.0 0.0 0.0 0.0 0.7 0.7 2.1 17.8 22.8 17.1 13.5 11.4 9.2 1.4 0.8 0.1 0.3 0.3 0.3 0.5 0.3 0.5 0.0 0.0 0.0 0.1 0.0 0.0 0.0 156
Values greater than 5% are bold. Lengths are pooled into 2-cm groups to compact the table. The mid-point of the length interval is displayed.
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Fig. 3. Percent frequency of biomass density attributable to depth interval by species and month. The range of each depth interval is 10 m; the mid-point is shown. For example, the value 5 represents the depth interval 0–9.9 m. Percent frequency is the average of three survey years.
4. Discussion 4.1. Abundance estimation Survey replication improved precision of abundance estimates for Pacific herring. The most precise abundance estimate was based on three surveys conducted in January 2002 for Amalga Trench, where herring were abundant (CV = 11%, Table 8). Replicate surveys have a long history as an approach to estimate precision of herring abundance estimates (e.g. Thorne, 1977). This approach is best-suited for a herring school that already has been located or where the available herring habitat is small; in either case, the herring usually can be surveyed quickly. For example, replicate surveys in southeastern Alaska lasted 20 min for Thorne (1977). In contrast, our surveys lasted
several hours in order to monitor abundance of both herring and pollock and to relocate the herring schools that moved within the available herring habitat from month-to-month. In addition, the available herring habitat was large. An advantage of longer surveys is that herring schools are less likely to be missed, whereas short surveys may miss schools separate from major aggregations, especially if the available herring habitat is large or marine mammals are not foraging on the herring school and thus serving as a cue for biologists to locate the herring school. An alternate approach combining both large and small surveys is to complete a large survey of the available herring habitat to locate herring aggregations and then to replicate small, fine-scale surveys of the aggregations. The large surveys can be completed by echosounder surveys as we did, by sonar surveys that cover a larger water volume on each vessel transect, or by aerial surveys
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Fig. 4. Average depth of biomass density by month and species: (—) Pacific herring, (- - -) juvenile walleye pollock, and (– – –) adult walleye pollock. Depth is the average of three survey years.
to search for marine mammal activity often associated with herring aggregations. The choice of approach depends on variation in school size and location, and the spatial scale of the variation (e.g. a few km versus tens of km). The quantitative effects of acoustic shadowing on abundance estimates of Pacific herring and Atlantic herring are similar. The correction factor for acoustic shadowing for Pacific herring is only 12% less than the value for Atlantic herring from the example data set in Zhao and Ona (2003), which is a small difference in biological terms. There are a few possible reasons for the difference in estimated shadow coefficients. First, estimates of the shadow coefficient are variable. Foote (1999) found that shadow coefficient values by data set ranged from 1.97 to 3.71 (and averaged 2.41). Second, fish in our study area were smaller (22 cm versus 33 cm FL) and shallower (80–90 m versus >200 m water depth) than the Atlantic herring in the other studies (Foote, 1999; Zhao and Ona, 2003). Finally, fish behavior (school shape and structure and fish orientation) may differ between the two areas. Table 8 Variability of biomass estimates by year, month, and species based on replicate surveys Month and year
Substrata
Average
Sample size
S.D.
CV
January 2002
Amalga Trench Benjamin Island Eagle Beach
15,713 120 0.9
3 2 2
1739 84 1.2
0.11 0.70 1.41
February 2002
Amalga Trench Benjamin Island Eagle Beach
3,146 110 0.6
2 2 2
1328 155 0.8
0.42 1.41 1.41
January 2002
Amalga Trench Benjamin Island Eagle Beach
34 2.4 2.0
3 2 2
19 1.6 0.7
0.57 0.68 0.36
February 2002
Amalga Trench Benjamin Island Eagle Beach
0.8 0.3 1.7
2 2 2
0.2 0.2 2.0
0.22 0.62 1.14
Pacific herring
Walleye pollock
Herring abundance estimates during winter are similar regardless of whether abundance estimates are adjusted for depth and acoustic shadowing. In contrast, herring abundance estimates during summer are sensitive to the adjustments, probably because herring are located at shallower depths during summer. Not adjusting the TS for depth causes a bias in abundance estimates. Of the three methods used to compare the sensitivity of herring biomass estimates, Method 3 (the method used in this paper) explicitly accounts for depth differences between herring schools and explicitly adjusts for acoustic shadowing, whereas Method 1 does not. Method 2 adjusts for acoustic shadowing but not depth differences. Method 1 was developed during winter surveys when herring were at deeper depths and were concentrated in large schools, and appears appropriate for winter surveys but not for other times of the year. Method 3 accounts for the seasonal depth difference for herring schools. The depth adjustment increases the TS estimate for each herring, so that estimated biomass was less for Method 3 than for Method 1 by up to 29% during seasons when herring were shallower. Therefore, the depth effect on TS should be incorporated into the abundance calculations to avoid bias. We chose a standard sampling time during daylight hours so that surveys accurately tracked relative abundance. A further question remains as to whether the abundance estimates accurately represent absolute abundance estimates. The TS equations we referenced (Traynor, 1996; Ona, 2003) do not adjust for diurnal variation in acoustic density. Understanding of the diel effect on acoustic surveys for herring is growing (Huse and Korneliussen, 2000; Hjellvik et al., 2004), but this information is not definitive enough to quantitatively adjust acoustic data for this effect. 4.2. Herring ecology Large schools of herring began to form in the study area in November; herring biomass peaked in January and decreased sharply in February during all survey years. Consequently, the total pelagic prey biomass and energy were considerably higher during the winter months and were dominated by herring. The schools formed in the Benjamin Island stratum in November, then shifted southward to the Amalga Trench stratum in December and January. The Benjamin Island stratum contained nearly 65% of the herring biomass found in the study area in November, but an average of only 3% by February. By February, the Amalga Harbor stratum contained nearly 96% of the biomass in the study area, due mostly to the movement of the large herring schools into this area. We presume that the herring in the Benjamin Island stratum were the same as those in the Amalga Trench stratum because there was no evidence of large herring concentrations outside these areas based on the lack of marine mammal activity. The Lynn Canal stock that we studied is one of 12 stocks of Pacific herring identified in southeastern Alaska based on their spawning locations (Pritchett and Walker, 2005); the nearest stocks to the Lynn Canal stock are geographically distinct, occurring more than 100 km away. In addition, the herring were found in the same submarine gully, though the submarine gully is interrupted at one point by outwash from a glacial
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river lying between the Benjamin Island and Amalga Harbor strata. These results are consistent with known herring ecology in that herring generally follow the same annual migration paths and utilize the same areas (Hourston, 1982; Wheeler and Winters, 1984; Corten, 2002), though shifts may occur on decadal and longer scales (Corten, 2002). In summer, herring form small, dynamic feeding schools, which move extensively to utilize relatively ephemeral aggregations of copepods (Kvamme et al., 2000). In late fall, copepod densities are reduced, and herring begin to aggregate into large schools and migrate to wintering areas (Huse and Ona, 1996). The shift to wintering depths appears linked to the break-up of the thermocline (Carlson, 1980), which occurred during November in our study. Once in wintering areas, herring move little, as feeding is reduced (Huse and Ona, 1996) and energy conservation is necessary. For example, all 30 stomachs that we examined in January 2004 were empty; an earlier study in Lynn Canal also found little or no food during winter (Carlson, 1980). The location of the wintering herring areas in Lynn Canal differed somewhat between 1973–1975 (Carlson, 1980) and 2001–2004 (this study). During 2001–2004, herring were concentrated in the Benjamin Island and Amalga Harbor strata and sometimes were found in the Fritz Cove stratum, whereas during 1973–1975, herring were concentrated in Auke Bay and Fritz Cove (Carlson, 1980). We found juvenile herring schools only in the inner part of Auke Bay, but no overwintering schools of adult herring. Carlson (1980) noted that the center of herring abundance was Fritz Cove. Carlson (1980) searched Lynn Canal in August, November, and January and found only a few herring, most of which were juveniles. Acoustic surveys may miss wintering herring schools with the narrow echosounder beam and even with the wider sonar search path. However, it would be difficult to miss the marine mammal activity typically associated with herring schools as long as Carlson (1980) searched the eastern shore of Lynn Canal, where we found large wintering herring schools. Thus, over three decades, it appears that herring usually occupy Fritz Cove, are reduced in Auke Bay, and have increased in Benjamin Island and Amalga Trench strata. The finding that herring were concentrated in the submarine gully in two different study periods separated by three decades (1973–1975 and 2001–2004) is evidence that herring have concentrated in this area during winter for several decades. This recurring use implies that the submarine gully in the study area is critical habitat for the Lynn Canal stock of herring in southeastern Alaska. The gully extends nearly continuously within our study area (including the opportunistically sampled strata) and is oriented north–south from the Douglas Trench stratum to the Benjamin Island stratum with a branch extending eastward into Fritz Cove. The water depth of the bottom of the gully is 80–130 m. The recurrence of wintering herring in this area was highly predictable over our 3-year study period. Furthermore, the recurrence appeared over a three-decade span (1973–1975 to 2001–2004), even though the distribution center has shifted somewhat. Because herring feed little during winter, the gully presumably offers benefits by reducing energy expenditure and
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predation. Tidal currents may be reduced near the bottom of the gully where the herring lie, thus reducing energy consumption. Typically, currents due to tidal flows are reduced near the sea floor due to friction and disruption of laminar flow from bottom irregularities. The gully offers shelter from tidal currents by providing a break from strong currents above. The northern half of the gully lies outside the main channel of Lynn Canal and flows likely are reduced there. Light levels also are lower because the floor of the gully is relatively deep, reducing predation by visual predators. 4.3. Pollock ecology Juvenile pollock were segregated from adult pollock by depth. Adult pollock cannibalize young-of-the-year pollock (Dwyer et al., 1987; Bailey, 1989) and sometimes age-1 pollock (13–24 cm SL) (Dwyer et al., 1987), so avoiding predation by adult pollock may be one reason for the depth segregation. Juvenile pollock were shallower (average depth about 70 m) during July–September and deeper (average depth about 100 m) during January–March, whereas adult pollock depth distribution did not vary seasonally (Fig. 4). Brodeur and Wilson (1996) also found the same seasonal depth pattern for juvenile (young-of-the-year) pollock. Juvenile pollock primarily are zooplankton feeders (Clausen, 1983; Dwyer et al., 1987; Brodeur and Wilson, 1996). Zooplankton abundance is reduced in shallow water during winter (e.g. for southeastern Alaska, Carlson, 1980; Paul and Coyle, 1993) because primary productivity is negligible there during winter and zooplankton move to deeper water. Zooplankton sampling nearby our study area (50 km away) that overlapped our study period (May–September 1997–2002) found that monthly zooplankton standing stock peaked during May or June then typically decreased thereafter (Park et al., 2004). With less prey available, juvenile pollock may move to greater depths to reach lower light levels and reduce detection by visual predators, but not so deep as to mix with adult pollock. Juvenile (young-of-theyear) pollock avoided bright light under laboratory conditions, a behavior modulated by temperature, fish size, and the presence of predators (Olla et al., 1996). 4.4. Habitat selection, segregation, and predator avoidance Herring, like juvenile pollock, were found at shallower depths during summer and greater depths during winter. During summer, juvenile pollock were segregated from herring by depth. Juvenile pollock and herring may segregate to reduce competition because both prey upon zooplankton. In southeastern Alaska, herring feed upon copepods (Carlson, 1980), whereas juvenile pollock feed primarily upon euphausiids, mysids, and shrimp; copepods were a minor diet item (Clausen, 1983). Differences in depth distributions of herring and juvenile pollock during summer also may reflect differences in their coloration and predator avoidance strategies. Herring formed small, dynamic schools and individuals were counter-shaded (dark above, light below, with reflective sides), a common strategy for reducing predation in a visual environment. In contrast, juvenile pollock were spread out and their coloration was mottled,
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a possible strategy for reducing predation in a lower light environment. Occupying deeper depths during winter likely is an energy conservation strategy. Juvenile (young-of-the-year) pollock under laboratory conditions fed ad libitum rations remained primarily in warmer surface waters, whereas when rations were low enough to prohibit growth, fish occurrence in colder, deeper waters significantly increased; lowering body temperature by 3 ◦ C can lead to a 30–40% decrease in metabolic rate (Olla et al., 1996). Bailey (1989) found that pollock migrated into deeper, colder waters of the Bering Sea only when prey abundance was reduced. Cold temperatures increased survival rates of starved juvenile (young-of-the-year) pollock under laboratory conditions (Sogard and Olla, 2000). Forage species such as herring are the focus of marine predators, especially when the forage species are aggregated at predictable times (Marston et al., 2002; Willson and Halupka, 1995; Sigler et al., 2004). Typically these spawning or pre-spawning aggregations last for short periods (days to weeks). In contrast, winter herring aggregations persist over longer periods (weeks to months) and the aggregations are not required for reproduction. In addition, there is evidence that herring have concentrated during winter in the same general place and time over decades. This predictability would seem to increase their predation risk, especially because the aggregation is large. Steller sea lions and humpback whales (Megaptera novaeangliae) prey upon the winter herring aggregation (Womble and Sigler, 2006). The number of sea lions at Benjamin Island varies seasonally, with counts near zero during summer and peaking at several hundred sea lions during winter (Womble and Sigler, 2006). Similarly, killer whales (Orcinus orca) in Norway prey upon winter herring aggregations in the northeast Atlantic Ocean (Simil¨a et al., 1996). By selecting the submarine gully habitat in winter, herring must derive some benefit that is sufficient to outweigh the predation risk. Marine predators may depend on seasonally available forage species for much of their annual energy requirements, yet research in this area began only recently for the North Pacific Ocean. More research is required to document the relationships between seasonally important forage species such as pollock and herring and their predators in the North Pacific Ocean. Such seasonal links likely serve an important role in structuring trophic relationships in the North Pacific Ocean ecosystem. Acknowledgements We thank Peter Ord of the F/V Williwaw for boat support and Dave Carlile, Dave Clausen, Phil Rigby, Alex Wertheimer, Matt Wilson and two anonymous reviewers for reviewing this paper. References Bailey, K.M., 1989. Interaction between the vertical distribution of juvenile pollock Theragra chalcogramma in the eastern Bering Sea, and cannibalism. Mar. Ecol. Prog. Ser. 53, 205–213. Blaxter, J.H.S., Batty, R.S., 1984. The herring swimblader: loss and gain of gas. J. Mar. Biol. Assoc. U.K. 64, 441–459.
Brodeur, R.D., Wilson, M.T., 1996. Mesoscale acoustic patterns of juvenile walleye pollock (Theragra chalcogramma) in the western Gulf of Alaska. Can. J. Fish. Aquat. Sci. 53, 1951–1963. Carlson, H.R., 1980. Seasonal distribution and environment of Pacific herring near Auke Bay, Lynn Canal, southeastern Alaska. Trans. Am. Fish. Soc. 109, 71–78. Carlson, H.R., 1995. Consistent yearly appearance of age-0 walleye pollock, Theragra chalcogramma, at a coastal site in southeastern Alaska, 1973–1994. Fish. Bull. U.S. 93, 386–390. Clausen, D.M., 1983. Food of walleye pollock, Theragra chalcogramma, in an embayment of southeastern Alaska. Fish. Bull. U.S. 81, 637–642. Corten, A., 2002. The role of “conservatism” in herring migrations. Rev. Fish. Biol. Fish. 11, 339–361. Dwyer, D.A., Bailey, K.M., Livingston, P.A., 1987. Feeding habits and daily ration of walleye pollock (Theragra chalcogramma) in the eastern Bering Sea, with special reference to cannibalism. Can. J. Fish. Aquat. Sci. 44, 1972–1984. Foote, K.G., Ona, E., Toresen, R., 1992. Determining the extinction cross-section of aggregating fish. J. Acoust. Soc. Am. 91, 1983–1989. Foote, K.G., 1999. Extinction cross-section of Norwegian spring-spawning herring. ICES J. Mar. Sci. 56, 606–612. Gauthier, S., Horne, J.K., 2004. Acoustic characteristics of forage fish species in the Gulf of Alaska and Bering Sea based on Kirchhoff-approximation models. Can. J. Fish. Aquat. Sci. 61, 1839–1850. Hourston, A.S., 1982. Homing by Canada’s West Coast herring to management units and divisions as indicated by tag recoveries. Can. J. Fish. Aquat. Sci. 39, 1414–1422. Huse, I., Korneliussen, R., 2000. Diel variation in acoustic density measurements of overwintering herring (Clupea harengus L.). ICES J. Mar. Sci. 57, 903–910. Huse, I., Ona, E., 1996. Tilt angle distribution and swimming speed of overwintering Norwegian spring-spawning herring. ICES J. Mar. Sci. 53, 863– 873. Hjellvik, V., Godø, O.R., Tjøstheim, D., 2004. Diurnal variation in acoustic densities: why do we see less in the dark? Can. J. Fish. Aquat. Sci. 61, 2237–2254. Kvamme, C., Nottestad, L., Ferno, A., Misund, O.A., Dommasnes, A., Axelsen, B.E., 2000. A sonar study of the migration pattern of Norwegian springspawning herring (Clupea harengus L.) in July. ICES CM2000, 1–24. Livingston, P.A., 1993. Importance of predation by groundfish, marine mammals and birds on walleye pollock Theragra chalcogramma and Pacific herring Clupea pallasi in the eastern Bering Sea. Mar. Ecol. Prog. Ser. 102, 205–215. MacLennan, D.N., Simmonds, E.J., 1992. Fisheries Acoustics. Chapman and Hall, New York, 325 pp. Marston, B.H., Willson, M.F., Gende, S.M., 2002. Predator aggregations during eulachon Thaleichthys pacificus spawning runs. Mar. Ecol. Prog. Ser. 231, 229–236. Olla, B.L., Davis, M.W., Ryer, C.H., Sogard, S.M., 1996. Behavioural determinants of distribution and survival in early stages of walleye pollock Theragra chalcogramma: a synthesis of experimental studies. Fish. Oceanogr. 5 (Suppl. 1), 167–178. Ona, E., 2003. An expanded target-strength relationship for herring. ICES J. Mar. Sci. 60, 493–499. Paul, A.J., Coyle, K.O., 1993. Taxa composition and biomass of the surfacedwelling crustaceans during spring pycnocline formation in Auke Bay, southeastern Alaska. J. Crustac. Biol. 13, 594–600. Park, W., Sturdevant, M., Orsi, J., Wertheimer, A., Fergusson, E., Heard, W., Shirley, T., 2004. Interannual abundance patterns of copepods during an ENSO event in Icy Strait, southeastern Alaska. ICES J. Mar. Sci. 61, 464–477. Pritchett, M., Walker, S., 2005. Southeast Alaska/Yakutat Annual Herring Research Report, 2003/2004 Season. Alaska Department of Fish and Game, Commercial Fisheries Management and Development Division, Juneau, Alaska. Sigler, M.F., Womble, J.N., Vollenweider, J.J., 2004. Availability to Steller sea lions (Eumetopias jubatus) of a seasonal prey resource: a prespawning aggregation of eulachon (Thaleichthys pacificus). Can. J. Fish. Aquat. Sci. 61, 1475–1484.
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331 Simil¨a, T., Holst, J.C., Christensen, I., 1996. Occurrence and diet of killer whales in northern Norway: seasonal patterns relative to the distribution and abundance of Norwegian spring-spawning herring. Can. J. Fish. Aquat. Sci. 53, 769–779. Sinclair, E.H., Zepplin, T.K., 2002. Seasonal and spatial differences in diet in the western stock of Steller sea lions (Eumetopias jubatus). J. Mammol. 83, 973–990. Sogard, S.M., Olla, B.L., 2000. Endurance of simulated winter conditions by age-0 walleye pollock: effects of body size, water temperature and energy stores. J. Fish. Biol. 56, 1–21. Thomas, G.L., Kirsch, J., Thorne, R.E., 2002. Ex situ target strength measurements of Pacific herring and Pacific sand lance. N. Am. J. Fish. Manage. 22, 1136–1145. Thorne, R.E., 1977. Acoustic assessment of hake and herring stocks in Puget Sound, Washington and southeastern Alaska. Rapports et Process-Verbaux des Reunions. Conseil Int. Explor. Mer. 170, 265–278. Traynor, J.J., 1996. Target-strength measurements for walleye pollock (Theragra chalcogramma) and Pacific whiting (Merluccius productus). ICES J. Mar. Sci. 53, 253–258.
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Vollenweider, J.J., Heintz, R.A., Kelly, B.P., submitted for publication. Seasonal variation in whole-body proximate composition and energy content of forage fish in southeastern Alaska. Mar. Ecol. Prog. Ser. Walters, C.J., Stocker, M., Tyler, A.V., Westrheim, S.J., 1986. Interaction between Pacific cod (Gadus macrocephalus) and herring (Clupea harengus pallasi) in the Hecate Strait, British Columbia. Can. J. Fish. Aquat. Sci. 43, 830–837. Wheeler, J.P., Winters, G.H., 1984. Homing of Atlantic herring (Clupea harengus harengus) in Newfoundland waters as indicated by tagging data. Can. J. Fish. Aquat. Sci. 41, 108–117. Willson, M.F., Halupka, K.C., 1995. Anadromous fish as keystone species in vertebrate communities. Conserv. Biol. 9, 489–497. Womble, J.N., Sigler, M.F., 2006. Seasonal availability of abundant, energyrich prey influences the abundance and diet of a marine predator, the Steller sea lion Eumetopias jubatus. Mar. Ecol. Prog. Ser. 325, 281– 293. Zhao, X., Ona, E., 2003. Estimation and compensation models for the shadowing effect in dense fish aggregations. ICES J. Mar. Sci. 60, 155–163.
Seasonal abundance of two important forage species in the North Pacific Ocean, Pacific herring and walleye pollock Michael F. Sigler ∗ , David J. Csepp National Oceanic and Atmospheric Association, National Marine Fisheries Service, Alaska Fisheries Science Center, Auke Bay Laboratory, 11305 Glacier Highway, Juneau, AK 99801-8626, USA Received 8 March 2006; received in revised form 29 September 2006; accepted 8 October 2006
Abstract Pacific herring (Clupea pallasii) and walleye pollock (Theragra chalcogramma) are important forage species in the North Pacific Ocean, but their seasonal abundance patterns are poorly known. During three consecutive years of monthly acoustic surveys in Lynn Canal, southeastern Alaska, large schools of herring dominated during winter and were present in a 60-km long submarine gully; this gully appears to provide critical winter habitat for herring when their prey are less available and energy expenditure must be reduced. The salient change in pollock distribution is a shift from shallow waters during summer to deeper waters during winter, such that shallow (<40 m) waters are nearly devoid of pollock during winter. The shift presumably occurs in response to the build-up of secondary productivity during summer and predator avoidance during winter. The seasonal changes in herring abundance drove seasonal changes in predator abundance, as Steller sea lions (Eumetopias jubatus) and humpback whales (Megaptera novaeangliae) preyed upon the winter aggregation of herring. Such seasonal links likely serve an important role in structuring trophic relationships in the North Pacific Ocean ecosystem. Published by Elsevier B.V. Keywords: Forage fish; Pacific herring; Walleye pollock; Seasonality; Ecology
1. Introduction Forage species are a critical part of the North Pacific Ocean ecosystem. However, few studies have quantified seasonality of forage species availability despite evidence that foraging pinnipeds (Sinclair and Zepplin, 2002) and odontocetes (Simil¨a et al., 1996) take advantage of seasonally concentrated prey. Well-known examples of forage species in the North Pacific Ocean are anadromous fishes such as Pacific salmon (Oncorhynchus spp.; e.g. Willson and Halupka, 1995) and eulachon (Thaleichthys pacificus; e.g. Marston et al., 2002; Sigler et al., 2004), whose spawning aggregations provide important seasonal food resources for mammalian and avian predators. Pacific herring (Clupea pallasii) and walleye pollock (Theragra chalcogramma) also are important forage species in the North Pacific Ocean and they are prey of marine fish, birds, and mammals (Livingston, 1993). Predation rates can vary season-
∗
Corresponding author. Tel.: +1 907 789 6037; fax: +1 907 789 6094. E-mail addresses: [email protected] (M.F. Sigler), [email protected] (D.J. Csepp). 0165-7836/$ – see front matter. Published by Elsevier B.V. doi:10.1016/j.fishres.2006.10.007
ally. For example, Pacific cod (Gadus macrocephalus) predation rates on herring are highest during winter (Walters et al., 1986); great sculpins (Myoxocephalus polyacanthocephalus) prey upon young-of-the-year pollock once they are demersal (Carlson, 1995). Predation rates also can vary annually. For example, groundfish predators appear to track strong year classes of pollock (Livingston, 1993). The goal of this study was to improve our understanding of seasonal predator–prey relationships for major forage species in the North Pacific Ocean. Predator–prey relationships involving forage species are poorly described for the North Pacific Ocean, especially in seasons other than summer. We measured the abundance of Pacific herring and walleye pollock each month for three consecutive years in Lynn Canal in southeastern Alaska, an area occupied by Steller sea lions (Eumetopias jubatus), an important marine predator in the North Pacific Ocean. Herring and pollock are by far the most common prey species found in Steller sea lion scats in this area, with percent frequency of occurrence of more than 80% for each species year-round (Womble and Sigler, 2006). Our study area also contains a Steller sea lion haulout at Benjamin Island. The number of sea lions at Benjamin Island varies seasonally, with counts peaking at
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Fig. 1. Map of study area. Boundaries between strata are indicated by dotted lines. From north to south, the strata for the standard survey area are Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench. Strata for occasionally sampled strata are not shown.
several hundred sea lions during winter (Womble and Sigler, 2006). Our objectives were: (1) to quantify Pacific herring and walleye pollock monthly abundance, and (2) to describe the role of seasonal abundance changes in the life history of Pacific herring and walleye pollock. The research described here is part of a broader study to explain decreases in Steller sea lion abundance. 2. Materials and methods 2.1. Study area Acoustic surveys were conducted in Favorite Channel (Fig. 1) in lower Lynn Canal between Tee Harbor (58◦ 25 N, 134◦ 46 W) and Vanderbilt Reef (58◦ 36 N, 135◦ 01 W) on a monthly basis between June 2001 and May 2004. This area was chosen because it includes Benjamin Island which is used as a seasonal haulout (a terrestrial site used by pinnipeds for breeding, caring for young, and molting) by Steller sea lions from October to April. The area also is relatively sheltered, facilitating year-round surveys, and encompasses a variety of habitats (depth range between 5 and 305 m; average depth = 60 m) typical of southeastern Alaska. 2.2. Acoustic surveys To estimate pollock and herring abundance, we used a portable 38-kHz Simrad1 echo-integration system with a 12◦ beam angle, towed beside the 11-m long F/V Williwaw at 11 km h−1 . We simultaneously collected location data with 1 Reference to trade names does not imply endorsement by the U.S. Government.
a Garmin global positioning system with location accuracy ±10 m. From June 2001 to May 2002, acoustic surveys followed a 36-km-long path that ran parallel to the mainland or offshore islands, or perpendicular between the two. Thereafter, surveys followed a longer 56-km zigzag path across the same area (Fig. 1) to increase sampling coverage of the study area. All surveys began after daybreak and concluded before dusk. Some fish species, particularly herring, undergo diurnal migrations through the water column that can affect acoustic density estimates (Huse and Korneliussen, 2000; Hjellvik et al., 2004). We chose to sample only during daylight because of the diel variation in acoustic density estimates and to facilitate observations of foraging sea lions while collecting acoustic data. Usually one survey was completed each month. Two of the monthly surveys were replicated to estimate variance of the abundance estimates. Opportunistic trawl samples were collected to identify the acoustic targets in the echograms and to provide biological information about the target species. Length, weight, and species composition data were collected quarterly with midwater trawls deployed from the 18-m long F/V Solstice from September 2001 to March 2002, the 31-m long F/V Viking Storm from May 2002 to September 2003, and the 37-m long R/V Medeia from January 2004 to March 2004. Two midwater trawls were used: (1) a 164 Nordic rope trawl with 1.5-m2 alloy doors, 7-m height, and 17-m width with a 19-mm mesh codend liner, and (2) a mesh wing 25/21/64 trawl with 3.0-m2 alloy doors, 11-m height, and 29-m width with a 32-mm mesh codend liner. The larger midwater trawl generally was used with the larger vessels to match their larger trawl-handling equipment. Size selectivity likely was unaffected by using two different nets because fish as small as 4-cm fork length (FL) commonly were caught by both nets. Typical characteristics of trawling operations were sinking rate
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331
during deployment of 11 m min−1 , rising rate during retrieval of 15 m min−1 , and towing speed at target depth of 5.6 km h−1 . All catches were sorted to the lowest taxonomic order practicable, usually species, then weighed. The total number caught also was counted, except for small, numerically abundant fish, which were subsampled for mean weight to estimate total number caught. The acoustic data were classified by species using the identification information from midwater trawls. Midwater trawls targeting herring and pollock were dominated by catches of these species. Herring comprised 87% of the catch by weight when herring was targeted and pollock comprised 84% of the catch by weight when pollock was targeted. The corresponding echogram patterns showed that herring during summer characteristically formed dense, round or tall pelagic schools, typically of small size. During winter, herring formed a consistent, dense layer associated with the bottom in submarine gullies. In contrast to herring, juvenile and adult pollock formed loose aggregations. Juvenile pollock typically were shallower than adult pollock. Pollock were classified as juvenile if their gonads were immature. In addition, juvenile and adult pollock sometimes were differentiated by comparing the single-target virtual echogram (from the echo-integration software SonarData Echoview) to published target strength (TS) values by fish species and size. Questionable acoustic targets were highlighted and then analyzed by using minimum, maximum, and mean TS, TS frequency distributions, and TS versus depth plots that were compared with published values (Traynor, 1996; Ona, 2003). Species classification of monthly acoustic data from the quarterly midwater trawl samples was reasonable because echogram patterns attributable to herring and pollock were consistent from month-to-month and year-to-year. An echo-integrator summed the returning echoes from fish observed beneath the vessel. The acoustic data were classified by species using the identification information from midwater trawls, integrated for 0.183-km length intervals (transects) and 10-m depth intervals, and corrected for instrument calibration using the software SonarData Echoview. The output of acoustic scattering (NASC) is proportional to fish density (MacLennan and Simmonds, 1992). To convert NASC to fish density in numbers, estimates of acoustic reflectivity for single fish were needed by species. Target strength refers to the acoustic reflectivity of a single echo or fish and depends on length (L in cm): TS = 20 log10 L + b (MacLennan and Simmonds, 1992). For pollock, b = −66 (Traynor, 1996) and for herring, b = −65.4 (Ona, 2003). Similar b-values were reported for herring in two other recent studies: −66 in fall by Thomas et al. (2002) and −65.1 by Gauthier and Horne (2004). In addition, NASC and TS values for herring were adjusted for depth compression of the air bladder (Ona, 2003) and acoustic shadowing (Zhao and Ona, 2003) by methods described in the next two sections of this paper. Herring gonad size also may influence herring target strength, but we chose to ignore this effect based on Ona (2003) recommendation. Target strength was transformed to backscattering cross-section by σ bs = 4π10TS/10 . Fish density in numbers was computed by dividing NASC by σ bs . Fish density in weight equals density in number multiplied by average weight. Fish density in weight
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is expressed by 0.183-km length interval (transect) and 10-m depth interval in units of kg km−2 . Fish density in weight was converted to nutritional energy density using season-, size-, and species-specific energy conversions determined in a companion study (Vollenweider et al., submitted for publication). Whereas seasonal energy content varied approximately two-fold (5.7–10.6 kJ g−1 for herring and 3.5–4.8 kJ g−1 for pollock), biomass density in an area could vary by several orders of magnitude. Therefore, the variation in prey energy density (kJ km−2 ) was due mostly to variation in biomass present, rather than differences in mass-specific energy content. Nutritional energy density is expressed by 0.183-km length interval (transect) and 10-m depth interval in units of kJ km−2 . We summed each transect’s data across 10-m depth intervals, such that each 0.183-km long transect had an estimate of biomass density (in kg km−2 ) and energy density (in kJ km−2 ). The transect data were grouped by strata, where each stratum encompassed similar habitat, and average biomass density and average energy density were computed by strata. For each stratum, total biomass (in t) was computed by multiplying biomass density (in kg km−2 ) by the area of the stratum (in km2 ). Total energy was computed by multiplying energy density (in kJ km−2 ) by the area of the stratum (in km2 ). Four strata (Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench) were sampled during standard monthly surveys. Five additional strata (Lena Point, Portland Trench, North Douglas, Douglas Trench, and Fritz Cove) were sampled occasionally during winter. 2.3. Target strength adjustment for depth compression Herring are physostomous (have an open swim bladder) and are incapable of gas secretion (Blaxter and Batty, 1984), so swim bladder compression with depth cannot be compensated for by gas secretion. We adjusted herring TS for the effect of depth following Ona (2003). Ona (2003) reported a TS for Atlantic herring of 20 log10 L − 65.4 − 2.3 log10 (1 + z/10) where z is the water depth (in m). Thomas et al. (2002) also reported a TS equation adjusted for depth for Pacific herring of 20 log10 L − 66 − 6.7 log10 (1 + z/10) (reformulated to match that of Ona (2003)). The equation in Thomas et al. (2002) implies a greater depth effect than the equation in Ona (2003) (multipliers of 6.7 and 2.3, respectively). We chose the equation of Ona (2003) rather than Thomas et al. (2002) because Ona tested a greater depth range (near surface to 500 m) than Thomas’s estimate (near surface to 43 m). Thomas et al. (2002) also assumed that the swim bladder acts like a free, spherical balloon in responding to increased pressure with depth, whereas Ona (2003) hypothesized that the herring swim bladder has fixed end positions and pressure-sensitive diameter, which accounts for less depth effect than predicted by Boyle’s Law. 2.4. Shadow coefficient The shadow coefficient is a measure of the attenuation of sound energy due to fish density. Fish nearest the transducer
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Table 1 Acoustic properties of reference seafloor used to estimate shadow coefficient Reference area
Average depth (m)
Average angle (◦ )
S.E. angle
Average NASC
S.E. NASC
Sample size (# transects)
A B
111 108
1.0 0.9
0.010 0.008
2,039,759 1,349,117
3600 1378
152 180
Transect length is 20 m.
attenuate the acoustic energy so that more distant fish contribute less to the received signal; thus, the shadow coefficient is a measure of the energy removed from the beam by each fish (MacLennan and Simmonds, 1992). An estimate of the shadow coefficient is needed for abundance estimation of densely schooling fish like herring. Foote (1999) estimated a shadow coefficient for Atlantic herring of 2.41 ± 0.33. No estimate has been reported for Pacific herring. We estimated the shadow coefficient for Pacific herring from our survey data by applying the methods of Foote et al. (1992) to select the data, and the methods of Zhao and Ona (2003) to analyze the data. Foote et al. (1992) stipulated that the bottom in the study area be flat and acoustically uniform, the range of fish observations span a range of acoustic (NASC) values, and the range of NASC include areas with fish absent. We chose data from two areas with nearly flat (average bottom angle ≤1◦ ), homogeneous (average NASC = 2,039,759 ± 3600 and 1,349,117 ± 1378 m2 nmi−2 ) bottom (Table 1). The maximum NASC due to herring was 644,562 m2 nmi−2 (Table 2). The shadow coefficient was estimated from the observed reduction in bottom NASC due to herring NASC. 3. Results 3.1. Species composition A total of 34 monthly acoustic surveys were conducted between June 2001 and May 2004. No data were collected in June and July 2002 due to logistical and equipment problems. The standard transects were surveyed during daylight hours and totaled 1621 km of acoustic transiting. Opportunistic surveys occasionally were conducted outside the standard survey area during winter when herring were abundant and totaled 219 km of acoustic transiting. A total of 96 midwater trawl tows were completed during 11 quarterly midwater trawl cruises.
The largest midwater trawl catches were walleye pollock (1472 kg of 3465 kg total weight and 9912 of 72,534 total number) and Pacific herring (682 kg and 8641). Acoustic estimates of abundance were completed for these two species because the catches consistently confirmed delineations of these species in the echograms. Other species with large catches by total weight (>100 kg) or total number (>1000) were squid, eulachon, myctophids (especially northern lampfish (Stenobrachius leucopsarus)), Pacific hake (Merluccius productus), capelin, pallid eelpout (Lycodapus mandibularis), northern smoothtongue (Leuroglossus schmidti), and shrimp (especially Pacific glass shrimp (Pasiphaea pacifica)). These species were also widely caught and their percent occurrence exceeded ∼10%. 3.2. Herring shadow coefficient The estimated mean shadow coefficient was 0.94 ± 0.16 (Table 2). The fitted linear model reasonably represented the data. The estimated shadow coefficient implies a relatively small correction for acoustic shadowing. We applied this shadow coefficient to the example data in Table 1 of Zhao and Ona (2003) and found that the corresponding correction factor is 1.07 for the example herring NASC of 224,396. The shadow coefficients for Atlantic and Pacific herring appear substantially different: 2.41 versus 0.94. However, the corresponding correction factors are closer than implied by the difference between the shadow coefficients. The correction factor for the example data in Zhao and Ona (2003) is 1.21 versus 1.07 for shadow coefficients of 2.41 and 0.94, respectively. 3.3. Sensitivity of herring abundance estimates We compared the sensitivity of herring biomass estimates using three methods: (1) the standard target strength equation applied to Pacific herring acoustic measurements from Alaska,
Table 2 Shadow coefficient estimates for Pacific herring Data set
Area
Date
Maximum NASC
Shadow coefficient
Sample size (# transects)
1 2 3 4 5 6 7 8
A A A A B B B B
16 January 2002 16 January 2002 18 January 2002 13 February 2004 16 January 2002 18 December 2002 13 January 2003 13 February 2004
244,527 69,080 143,859 644,562 327,664 485,628 442,144 317,539
1.24 1.57 1.47 0.41 0.59 1.09 0.63 0.51
41 64 222 176 206 294 267 275
Mean S.E.M.
0.94 0.16
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331
(2) the standard equation adjusted for acoustic shadowing, and (3) Ona (2003) equation and accounting for depth and acoustic shadowing (the method applied in this paper). In previous studies, the standard TS equation applied to Pacific herring acoustic measurements from Alaska has been TS = 26.5 log10 L − 76.4 (Thomas et al., 2002). Method 3 explicitly accounts for depth differences between herring schools and explicitly adjusts for acoustic shadowing, whereas Method 1 does not. Differences in biomass estimates by the three methods were small during winter when herring were most abundant (≤9%; Table 3). The standard equation adjusted for acoustic shadowing increased biomass estimates only by small amounts (Method 1 versus Method 2; ≤8%). The greatest differences occurred for months when herring are less abundant (Method 1 versus Method 3; ≥−29%). Herring were at shallower depths during these months. The depth adjustment for Method 3 increases the
323
TS estimate for each herring; thus, the estimated biomass is less for Method 3 than for Method 1. 3.4. Prey composition and seasonal variation Forage species biomass varied dramatically among months and among species (Table 4). For herring, biomass in the standard survey area ranged between 6 t (June 2001) and 33,000 t (December 2001). In all 3 years, biomass peaked between December and February due to the presence of large herring aggregations. In contrast, walleye pollock biomass in the study area was much less than herring, varying between 3 t (February 2002) and 655 t (July 2001). Pollock biomass peaked between July and October. Opportunistic acoustic surveys conducted outside the standard survey area sometimes found significant quantities of herring (>1000 t) in Lena Point, North Douglas,
Table 3 Comparison of herring biomass estimates (t) from three computational methods: (1) standard target strength equation (TS = 26.5 log10 L − 76.4, Thomas et al., 2002); (2) standard equation and account for acoustic shadowing; (3) explicitly account for depth effect on TS and adjust for acoustic shadowing (the method applied in this paper) Year and month
Method 1
Method 2
Percent difference, Methods 1 and 2 (%)
Method 3
Percent difference, Methods 1 and 3 (%)
2001 June July August September October November December
7 528 1,332 2,977 782 1,337 30,239
7 530 1,340 3,139 787 1,345 32,264
0 0 1 5 1 1 7
6 406 994 2,506 716 1,347 32,976
−15 −23 −25 −16 −8 1 9
2002 January February March April May August September October November December
14,720 3,803 260 1,206 161 6,956 2,084 1,274 2,141 12,241
15,079 3,855 261 1,212 161 7,279 2,109 1,287 2,173 12,524
2 1 0 1 0 5 1 1 1 2
15,874 3,244 203 883 139 5,795 2,129 1,173 2,244 12,492
8 −15 −22 −27 −14 −17 2 −8 5 2
2003 January February March April May June July August September October November December
17,833 6,143 797 83 1,089 227 228 747 1,600 1,027 5,538 19,747
18,410 6,290 803 83 1,107 227 230 754 1,614 1,047 5,971 20,580
3 2 1 0 2 0 1 1 1 2 8 4
19,272 6,045 757 59 837 186 191 580 1,443 941 5,309 20,139
8 −2 −5 −29 −23 −18 −16 −22 −10 −8 −4 2
2004 January February March April May
4,188 23,599 949 138 43
4,380 25,279 1,004 138 43
5 7 6 0 0
4,319 25,026 988 128 39
3 6 4 −7 −10
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Table 4 Biomass estimates (t) by year, month, strata, species and area size (km2 ) by strata Year and month
Pacific herring
Walleye pollock
Vanderbilt Reef
Benjamin Island
Eagle Beach
Amalga Trench
Total
Vanderbilt Reef
Benjamin Island
2001 June July August September October November December
0 132 129 0 0 0 0
0 0 251 0 698 1,148 12,019
1 0 193 1,462 0 111 85
5 274 421 1,044 18 88 20,873
6 406 994 2,506 716 1,347 32,976
39 37 85 85 37 9 51
8 70 5 17 67 13 2
2002 January February March April May August September October November December
0 na na 0 0 0 na na 0 0
120 219 156 34 13 0 1,884 0 1,997 5,258
2 1 43 155 2 0 70 312 0 371
15,713 3,146 4 694 123 5,795 175 861 248 6,863
15,835 3,367 203 883 139 5,795 2,129 1,173 2,245 12,492
23 na na 18 106 45 na na 67 47
2003 January February March April May June July August September October November December
0 27 0 0 84 0 0 0 0 0 0 0
240 237 0 12 86 23 1 79 66 941 1,082 0
592 3 115 19 362 63 1 41 376 0 4,227 0
18,439 5,849 642 28 304 100 188 459 1,006 0 0 20,139
19,272 6,117 757 59 837 186 191 580 1,448 941 5,309 20,139
2004 January February March April May
na na 0 0 0
0 0 4 0 3
0 0 0 44 28
4,319 25,026 984 84 8
4,319 25,026 988 128 39
6.2
8.1
22.9
47.5
Area size (km2 )
10.3
and Fritz Cove strata, but not in Portland Trench or Douglas Trench strata (Table 5). Patterns of total nutritional energy followed the biomass patterns (Fig. 2). For herring, total energy ranged between 51 million kJ (June 2001) and 285,000 million kJ (December 2001). For pollock, total energy ranged between 11 million kJ (February 2002) and 2800 million kJ (September 2002). Consequently, herring constituted most of the total energy available in most months. Averaged across all months, herring represented 81% of the total energy available to sea lions, compared to 19% for pollock. The disparity in total energy attributed to herring was even greater during the winter months. Between November and February, herring constituted an average of 99% of the total energy, compared to 1% for pollock.
Eagle Beach
Amalga Trench
Total
13 58 6 108 41 3 3
42 491 128 427 270 54 143
102 655 225 637 415 79 199
3 0 1 3 61 19 24 9 10 4
2 2 2 7 43 41 28 25 26 11
45 1 101 84 262 448 471 389 184 257
73 3 104 113 473 553 523 422 287 319
43 46 10 9 18 15 27 31 30 24 32 32
7 1 6 16 11 16 30 63 20 22 56 6
2 1 0 58 4 31 11 97 58 94 33 7
21 7 70 159 29 64 253 266 347 172 81 61
74 55 86 242 61 126 321 457 455 313 203 106
na na 2 4 8
2 14 1 7 33
1 1 0 6 30
77 6 56 109 106
80 21 60 126 177
Herring were found at greater depths in winter than in summer, as were pollock, although depth ranges differed between species. Herring biomass density was greatest at 75–125 m depths from December to March, at 15–85 m depths from April to August, and at 35–115 m depths from September to November (Fig. 3). The depth distribution usually was unimodal, except from April to June, when the depth distribution was bimodal with distinct modes at 15–25 and 65–75 m. Pollock primarily were found from 65 to 235 m depths from November to March and from 35 to 235 m depths from April to October. The depth distribution was bimodal for several months (e.g. July). The deeper modes (165–235 m) were due to adult pollock biomass and the shallower modes were due to juvenile pollock biomass based on midwater trawl catches and TS values.
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331
325
Table 5 Biomass estimates (t) by year, month, strata, and species for opportunistic surveys, and area size (km2) by strata Year and month
Lena Point
Portland Trench
North Douglas
Douglas Trench
Fritz Cove
Standard strata
Total
Pacific herring 2002 January February March
2844 1180 na
na na 60
na 455 0
na 656 17
3256 79 0
15,835 3,367 203
21,935 5,737 281
na na na
na na na
na na 3136
na 258 251
1555 26 18
19,272 6,117 757
20,827 6,400 4,163
na
na
na
na
0
4,319
4,319
6.2
6.0
4.4
5.7
4.5
47.5
74.2
Walleye pollock 2002 January February March
3 0 na
na na 20
na 7 1
na 42 0
1 4 3
73 3 104
78 56 128
2003 January February March
na na na
na na na
na na 1
na 185 4
7 5 1
74 55 86
81 244 92
2004 January
na
na
na
na
6
80
86
2003 January February March 2004 January Area size
(km2 )
The sums of biomass estimates for strata sampled during standard surveys also are displayed. Standard strata are Vanderbilt Reef, Benjamin Island, Eagle Beach, and Amalga Trench (Table 4).
Herring and juvenile pollock were segregated from adult pollock. Average depths of herring and juvenile pollock (based on biomass density) were less than 100 m, whereas average depths of adult pollock were 150–200 m (Fig. 4). Herring and juvenile pollock overlapped from September to April, but separated somewhat from May to August. During these months, average depths of herring were about 50 m and average depths of juvenile pollock were about 80 m.
Herring size ranged from 8 to 27 cm FL in midwater trawl samples (Table 6). Most herring were 16–25 cm FL, except for March 2002 when smaller (12–17 cm FL) herring were more common. Pollock size ranged from 11 to 69 cm FL in midwater trawl samples (Table 7). Most pollock were less than 35 cm FL. Larger pollock were uncommon in all strata except Vanderbilt Reef where bottom depths were greater (mean 199 m) than the other strata (mean 99 m). 3.5. Variance estimates
Fig. 2. Nutritional energy (millions kJ) by year, month and species: Pacific herring () and walleye pollock ().
The estimates of herring abundance sometimes were highly variable. The coefficient of variation (CV) from replicate surveys ranged from 11% to 141% (Table 8). The CV values sometimes were large because herring were aggregated and the size and density of each aggregation were variable. Greater abundance and further survey replication improved precision of abundance estimates for Pacific herring. Abundance was intermediate for February 2002 for Amalga Trench; the CV was 42%. Abundance was high for January 2002 for Amalga Trench and three surveys were conducted; the CV was 11%. The estimates of pollock abundance generally were less variable than the estimates of herring abundance. Most CV values were between 22% and 68% (Table 8). The CV values were lower because spatial distributions of juvenile and adult pollock were relatively homogeneous. Only young-of-the-year and age 1+ pollock were aggregated, although not as tightly as herring.
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Table 6 Length frequencies (%) by year and month for Pacific herring Fork length (mm)
2001 September
80 90 100 120 130 140 150 160 170 180 190 200 210 220 230 240 250 260 270
0.0 0.0 0.0 0.0 0.0 0.0 1.1 5.6 27.8 23.3 13.3 16.7 8.9 2.2 0.0 0.0 1.1 0.0 0.0
Sample size
90
2002 December 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.9 0.9 0.0 5.7 10.4 22.6 21.7 21.7 12.3 3.8 0.0 0.0 106
March 0.0 0.0 1.5 5.4 17.7 18.2 21.2 16.7 9.4 2.5 3.0 3.0 1.5 0.0 0.0 0.0 0.0 0.0 0.0 203
2003 May 0.8 0.8 0.0 0.0 0.0 0.0 4.0 5.6 12.8 8.0 11.2 15.2 16.0 8.8 8.0 6.4 2.4 0.0 0.0 125
September 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4.0 6.6 21.9 23.8 13.2 9.3 8.6 7.9 3.3 1.3 151
December 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 2.8 2.8 7.7 12.6 22.4 25.2 20.3 6.3 0.0 0.0 143
2004 March 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 23.3 26.7 33.3 10.0 6.7 0.0 0.0 0.0 0.0 0.0 30
May 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.9 16.2 25.1 33.0 14.5 6.7 0.0 0.6 0.0 179
September 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 20.0 40.0 20.0 20.0 0.0 0.0 0.0 0.0 0.0 0.0 5
January 0.0 0.0 0.0 0.0 0.0 0.4 0.0 0.0 1.7 12.2 19.4 24.1 20.7 11.4 6.8 2.5 0.4 0.4 0.0
March 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3.6 3.6 5.5 20.0 21.8 23.6 18.2 3.6 0.0 0.0 0.0 0.0
237
55
January
March
0.0 47.6 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 23.8 23.8 0.0 0.3 0.2 0.0 0.8 0.4 0.6 0.6 0.8 0.2 0.6 0.2 0.0 0.0 0.1 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 44.4 22.2 0.0 22.2 0.0 0.0 0.0 0.0 11.1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0
Values greater than 5% are bold. Table 7 Length frequencies (%) by year and month for walleye pollock Fork length (mm)
2001 September
11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 Sample size
0.0 0.0 0.0 1.6 17.6 45.2 13.8 0.0 2.1 8.0 6.4 0.7 0.0 0.1 0.5 0.9 1.0 1.3 0.5 0.2 0.2 0.0 0.0 0.1 0.0 0.0 0.0 0.0 0.0 0.0 240
2002 December 3.5 1.4 0.3 0.0 2.4 22.8 31.8 12.1 1.0 1.0 1.0 0.7 0.9 2.3 0.7 1.8 0.0 1.8 0.9 3.6 6.3 1.8 0.9 0.9 0.0 0.0 0.0 0.0 0.0 0.0 254
March 12.2 67.3 12.2 0.0 0.0 6.1 0.0 0.0 0.0 0.0 0.0 0.1 0.0 0.2 0.0 0.1 0.0 0.8 0.2 0.1 0.1 0.2 0.1 0.1 0.1 0.1 0.0 0.0 0.0 0.0 38
2003 May 0.0 0.5 6.3 5.8 0.0 2.4 11.1 24.7 27.1 7.8 3.4 1.5 2.9 1.7 1.6 0.9 0.5 0.4 0.2 0.4 0.2 0.4 0.1 0.0 0.1 0.0 0.0 0.0 0.0 0.0 264
September 0.0 0.0 0.0 0.0 1.7 23.7 13.5 4.5 9.0 18.0 15.8 6.2 1.7 2.3 1.1 0.1 0.0 0.2 0.0 0.4 0.6 0.1 0.4 0.3 0.0 0.1 0.0 0.1 0.0 0.0 196
December 0.0 0.0 0.0 0.0 1.7 24.8 38.0 10.3 6.6 9.1 3.3 0.0 0.0 0.0 0.0 0.0 0.0 0.4 0.9 0.4 0.0 0.9 3.5 0.0 0.0 0.0 0.0 0.0 0.0 0.0 241
2004 March 0.0 0.0 0.0 0.0 0.9 5.3 25.9 8.8 9.7 8.8 16.7 5.7 5.3 3.5 3.1 0.7 1.2 1.9 0.4 0.7 0.8 0.2 0.4 0.1 0.0 0.0 0.0 0.0 0.0 0.0 274
May 0.0 0.0 0.0 0.0 0.0 0.0 9.1 20.7 12.3 6.7 8.1 9.1 9.2 5.3 6.2 4.5 4.2 1.9 1.0 0.6 0.3 0.2 0.3 0.1 0.1 0.0 0.0 0.0 0.0 0.0 407
September 0.0 0.0 0.0 0.0 0.0 0.7 0.7 2.1 17.8 22.8 17.1 13.5 11.4 9.2 1.4 0.8 0.1 0.3 0.3 0.3 0.5 0.3 0.5 0.0 0.0 0.0 0.1 0.0 0.0 0.0 156
Values greater than 5% are bold. Lengths are pooled into 2-cm groups to compact the table. The mid-point of the length interval is displayed.
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Fig. 3. Percent frequency of biomass density attributable to depth interval by species and month. The range of each depth interval is 10 m; the mid-point is shown. For example, the value 5 represents the depth interval 0–9.9 m. Percent frequency is the average of three survey years.
4. Discussion 4.1. Abundance estimation Survey replication improved precision of abundance estimates for Pacific herring. The most precise abundance estimate was based on three surveys conducted in January 2002 for Amalga Trench, where herring were abundant (CV = 11%, Table 8). Replicate surveys have a long history as an approach to estimate precision of herring abundance estimates (e.g. Thorne, 1977). This approach is best-suited for a herring school that already has been located or where the available herring habitat is small; in either case, the herring usually can be surveyed quickly. For example, replicate surveys in southeastern Alaska lasted 20 min for Thorne (1977). In contrast, our surveys lasted
several hours in order to monitor abundance of both herring and pollock and to relocate the herring schools that moved within the available herring habitat from month-to-month. In addition, the available herring habitat was large. An advantage of longer surveys is that herring schools are less likely to be missed, whereas short surveys may miss schools separate from major aggregations, especially if the available herring habitat is large or marine mammals are not foraging on the herring school and thus serving as a cue for biologists to locate the herring school. An alternate approach combining both large and small surveys is to complete a large survey of the available herring habitat to locate herring aggregations and then to replicate small, fine-scale surveys of the aggregations. The large surveys can be completed by echosounder surveys as we did, by sonar surveys that cover a larger water volume on each vessel transect, or by aerial surveys
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Fig. 4. Average depth of biomass density by month and species: (—) Pacific herring, (- - -) juvenile walleye pollock, and (– – –) adult walleye pollock. Depth is the average of three survey years.
to search for marine mammal activity often associated with herring aggregations. The choice of approach depends on variation in school size and location, and the spatial scale of the variation (e.g. a few km versus tens of km). The quantitative effects of acoustic shadowing on abundance estimates of Pacific herring and Atlantic herring are similar. The correction factor for acoustic shadowing for Pacific herring is only 12% less than the value for Atlantic herring from the example data set in Zhao and Ona (2003), which is a small difference in biological terms. There are a few possible reasons for the difference in estimated shadow coefficients. First, estimates of the shadow coefficient are variable. Foote (1999) found that shadow coefficient values by data set ranged from 1.97 to 3.71 (and averaged 2.41). Second, fish in our study area were smaller (22 cm versus 33 cm FL) and shallower (80–90 m versus >200 m water depth) than the Atlantic herring in the other studies (Foote, 1999; Zhao and Ona, 2003). Finally, fish behavior (school shape and structure and fish orientation) may differ between the two areas. Table 8 Variability of biomass estimates by year, month, and species based on replicate surveys Month and year
Substrata
Average
Sample size
S.D.
CV
January 2002
Amalga Trench Benjamin Island Eagle Beach
15,713 120 0.9
3 2 2
1739 84 1.2
0.11 0.70 1.41
February 2002
Amalga Trench Benjamin Island Eagle Beach
3,146 110 0.6
2 2 2
1328 155 0.8
0.42 1.41 1.41
January 2002
Amalga Trench Benjamin Island Eagle Beach
34 2.4 2.0
3 2 2
19 1.6 0.7
0.57 0.68 0.36
February 2002
Amalga Trench Benjamin Island Eagle Beach
0.8 0.3 1.7
2 2 2
0.2 0.2 2.0
0.22 0.62 1.14
Pacific herring
Walleye pollock
Herring abundance estimates during winter are similar regardless of whether abundance estimates are adjusted for depth and acoustic shadowing. In contrast, herring abundance estimates during summer are sensitive to the adjustments, probably because herring are located at shallower depths during summer. Not adjusting the TS for depth causes a bias in abundance estimates. Of the three methods used to compare the sensitivity of herring biomass estimates, Method 3 (the method used in this paper) explicitly accounts for depth differences between herring schools and explicitly adjusts for acoustic shadowing, whereas Method 1 does not. Method 2 adjusts for acoustic shadowing but not depth differences. Method 1 was developed during winter surveys when herring were at deeper depths and were concentrated in large schools, and appears appropriate for winter surveys but not for other times of the year. Method 3 accounts for the seasonal depth difference for herring schools. The depth adjustment increases the TS estimate for each herring, so that estimated biomass was less for Method 3 than for Method 1 by up to 29% during seasons when herring were shallower. Therefore, the depth effect on TS should be incorporated into the abundance calculations to avoid bias. We chose a standard sampling time during daylight hours so that surveys accurately tracked relative abundance. A further question remains as to whether the abundance estimates accurately represent absolute abundance estimates. The TS equations we referenced (Traynor, 1996; Ona, 2003) do not adjust for diurnal variation in acoustic density. Understanding of the diel effect on acoustic surveys for herring is growing (Huse and Korneliussen, 2000; Hjellvik et al., 2004), but this information is not definitive enough to quantitatively adjust acoustic data for this effect. 4.2. Herring ecology Large schools of herring began to form in the study area in November; herring biomass peaked in January and decreased sharply in February during all survey years. Consequently, the total pelagic prey biomass and energy were considerably higher during the winter months and were dominated by herring. The schools formed in the Benjamin Island stratum in November, then shifted southward to the Amalga Trench stratum in December and January. The Benjamin Island stratum contained nearly 65% of the herring biomass found in the study area in November, but an average of only 3% by February. By February, the Amalga Harbor stratum contained nearly 96% of the biomass in the study area, due mostly to the movement of the large herring schools into this area. We presume that the herring in the Benjamin Island stratum were the same as those in the Amalga Trench stratum because there was no evidence of large herring concentrations outside these areas based on the lack of marine mammal activity. The Lynn Canal stock that we studied is one of 12 stocks of Pacific herring identified in southeastern Alaska based on their spawning locations (Pritchett and Walker, 2005); the nearest stocks to the Lynn Canal stock are geographically distinct, occurring more than 100 km away. In addition, the herring were found in the same submarine gully, though the submarine gully is interrupted at one point by outwash from a glacial
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river lying between the Benjamin Island and Amalga Harbor strata. These results are consistent with known herring ecology in that herring generally follow the same annual migration paths and utilize the same areas (Hourston, 1982; Wheeler and Winters, 1984; Corten, 2002), though shifts may occur on decadal and longer scales (Corten, 2002). In summer, herring form small, dynamic feeding schools, which move extensively to utilize relatively ephemeral aggregations of copepods (Kvamme et al., 2000). In late fall, copepod densities are reduced, and herring begin to aggregate into large schools and migrate to wintering areas (Huse and Ona, 1996). The shift to wintering depths appears linked to the break-up of the thermocline (Carlson, 1980), which occurred during November in our study. Once in wintering areas, herring move little, as feeding is reduced (Huse and Ona, 1996) and energy conservation is necessary. For example, all 30 stomachs that we examined in January 2004 were empty; an earlier study in Lynn Canal also found little or no food during winter (Carlson, 1980). The location of the wintering herring areas in Lynn Canal differed somewhat between 1973–1975 (Carlson, 1980) and 2001–2004 (this study). During 2001–2004, herring were concentrated in the Benjamin Island and Amalga Harbor strata and sometimes were found in the Fritz Cove stratum, whereas during 1973–1975, herring were concentrated in Auke Bay and Fritz Cove (Carlson, 1980). We found juvenile herring schools only in the inner part of Auke Bay, but no overwintering schools of adult herring. Carlson (1980) noted that the center of herring abundance was Fritz Cove. Carlson (1980) searched Lynn Canal in August, November, and January and found only a few herring, most of which were juveniles. Acoustic surveys may miss wintering herring schools with the narrow echosounder beam and even with the wider sonar search path. However, it would be difficult to miss the marine mammal activity typically associated with herring schools as long as Carlson (1980) searched the eastern shore of Lynn Canal, where we found large wintering herring schools. Thus, over three decades, it appears that herring usually occupy Fritz Cove, are reduced in Auke Bay, and have increased in Benjamin Island and Amalga Trench strata. The finding that herring were concentrated in the submarine gully in two different study periods separated by three decades (1973–1975 and 2001–2004) is evidence that herring have concentrated in this area during winter for several decades. This recurring use implies that the submarine gully in the study area is critical habitat for the Lynn Canal stock of herring in southeastern Alaska. The gully extends nearly continuously within our study area (including the opportunistically sampled strata) and is oriented north–south from the Douglas Trench stratum to the Benjamin Island stratum with a branch extending eastward into Fritz Cove. The water depth of the bottom of the gully is 80–130 m. The recurrence of wintering herring in this area was highly predictable over our 3-year study period. Furthermore, the recurrence appeared over a three-decade span (1973–1975 to 2001–2004), even though the distribution center has shifted somewhat. Because herring feed little during winter, the gully presumably offers benefits by reducing energy expenditure and
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predation. Tidal currents may be reduced near the bottom of the gully where the herring lie, thus reducing energy consumption. Typically, currents due to tidal flows are reduced near the sea floor due to friction and disruption of laminar flow from bottom irregularities. The gully offers shelter from tidal currents by providing a break from strong currents above. The northern half of the gully lies outside the main channel of Lynn Canal and flows likely are reduced there. Light levels also are lower because the floor of the gully is relatively deep, reducing predation by visual predators. 4.3. Pollock ecology Juvenile pollock were segregated from adult pollock by depth. Adult pollock cannibalize young-of-the-year pollock (Dwyer et al., 1987; Bailey, 1989) and sometimes age-1 pollock (13–24 cm SL) (Dwyer et al., 1987), so avoiding predation by adult pollock may be one reason for the depth segregation. Juvenile pollock were shallower (average depth about 70 m) during July–September and deeper (average depth about 100 m) during January–March, whereas adult pollock depth distribution did not vary seasonally (Fig. 4). Brodeur and Wilson (1996) also found the same seasonal depth pattern for juvenile (young-of-the-year) pollock. Juvenile pollock primarily are zooplankton feeders (Clausen, 1983; Dwyer et al., 1987; Brodeur and Wilson, 1996). Zooplankton abundance is reduced in shallow water during winter (e.g. for southeastern Alaska, Carlson, 1980; Paul and Coyle, 1993) because primary productivity is negligible there during winter and zooplankton move to deeper water. Zooplankton sampling nearby our study area (50 km away) that overlapped our study period (May–September 1997–2002) found that monthly zooplankton standing stock peaked during May or June then typically decreased thereafter (Park et al., 2004). With less prey available, juvenile pollock may move to greater depths to reach lower light levels and reduce detection by visual predators, but not so deep as to mix with adult pollock. Juvenile (young-of-theyear) pollock avoided bright light under laboratory conditions, a behavior modulated by temperature, fish size, and the presence of predators (Olla et al., 1996). 4.4. Habitat selection, segregation, and predator avoidance Herring, like juvenile pollock, were found at shallower depths during summer and greater depths during winter. During summer, juvenile pollock were segregated from herring by depth. Juvenile pollock and herring may segregate to reduce competition because both prey upon zooplankton. In southeastern Alaska, herring feed upon copepods (Carlson, 1980), whereas juvenile pollock feed primarily upon euphausiids, mysids, and shrimp; copepods were a minor diet item (Clausen, 1983). Differences in depth distributions of herring and juvenile pollock during summer also may reflect differences in their coloration and predator avoidance strategies. Herring formed small, dynamic schools and individuals were counter-shaded (dark above, light below, with reflective sides), a common strategy for reducing predation in a visual environment. In contrast, juvenile pollock were spread out and their coloration was mottled,
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a possible strategy for reducing predation in a lower light environment. Occupying deeper depths during winter likely is an energy conservation strategy. Juvenile (young-of-the-year) pollock under laboratory conditions fed ad libitum rations remained primarily in warmer surface waters, whereas when rations were low enough to prohibit growth, fish occurrence in colder, deeper waters significantly increased; lowering body temperature by 3 ◦ C can lead to a 30–40% decrease in metabolic rate (Olla et al., 1996). Bailey (1989) found that pollock migrated into deeper, colder waters of the Bering Sea only when prey abundance was reduced. Cold temperatures increased survival rates of starved juvenile (young-of-the-year) pollock under laboratory conditions (Sogard and Olla, 2000). Forage species such as herring are the focus of marine predators, especially when the forage species are aggregated at predictable times (Marston et al., 2002; Willson and Halupka, 1995; Sigler et al., 2004). Typically these spawning or pre-spawning aggregations last for short periods (days to weeks). In contrast, winter herring aggregations persist over longer periods (weeks to months) and the aggregations are not required for reproduction. In addition, there is evidence that herring have concentrated during winter in the same general place and time over decades. This predictability would seem to increase their predation risk, especially because the aggregation is large. Steller sea lions and humpback whales (Megaptera novaeangliae) prey upon the winter herring aggregation (Womble and Sigler, 2006). The number of sea lions at Benjamin Island varies seasonally, with counts near zero during summer and peaking at several hundred sea lions during winter (Womble and Sigler, 2006). Similarly, killer whales (Orcinus orca) in Norway prey upon winter herring aggregations in the northeast Atlantic Ocean (Simil¨a et al., 1996). By selecting the submarine gully habitat in winter, herring must derive some benefit that is sufficient to outweigh the predation risk. Marine predators may depend on seasonally available forage species for much of their annual energy requirements, yet research in this area began only recently for the North Pacific Ocean. More research is required to document the relationships between seasonally important forage species such as pollock and herring and their predators in the North Pacific Ocean. Such seasonal links likely serve an important role in structuring trophic relationships in the North Pacific Ocean ecosystem. Acknowledgements We thank Peter Ord of the F/V Williwaw for boat support and Dave Carlile, Dave Clausen, Phil Rigby, Alex Wertheimer, Matt Wilson and two anonymous reviewers for reviewing this paper. References Bailey, K.M., 1989. Interaction between the vertical distribution of juvenile pollock Theragra chalcogramma in the eastern Bering Sea, and cannibalism. Mar. Ecol. Prog. Ser. 53, 205–213. Blaxter, J.H.S., Batty, R.S., 1984. The herring swimblader: loss and gain of gas. J. Mar. Biol. Assoc. U.K. 64, 441–459.
Brodeur, R.D., Wilson, M.T., 1996. Mesoscale acoustic patterns of juvenile walleye pollock (Theragra chalcogramma) in the western Gulf of Alaska. Can. J. Fish. Aquat. Sci. 53, 1951–1963. Carlson, H.R., 1980. Seasonal distribution and environment of Pacific herring near Auke Bay, Lynn Canal, southeastern Alaska. Trans. Am. Fish. Soc. 109, 71–78. Carlson, H.R., 1995. Consistent yearly appearance of age-0 walleye pollock, Theragra chalcogramma, at a coastal site in southeastern Alaska, 1973–1994. Fish. Bull. U.S. 93, 386–390. Clausen, D.M., 1983. Food of walleye pollock, Theragra chalcogramma, in an embayment of southeastern Alaska. Fish. Bull. U.S. 81, 637–642. Corten, A., 2002. The role of “conservatism” in herring migrations. Rev. Fish. Biol. Fish. 11, 339–361. Dwyer, D.A., Bailey, K.M., Livingston, P.A., 1987. Feeding habits and daily ration of walleye pollock (Theragra chalcogramma) in the eastern Bering Sea, with special reference to cannibalism. Can. J. Fish. Aquat. Sci. 44, 1972–1984. Foote, K.G., Ona, E., Toresen, R., 1992. Determining the extinction cross-section of aggregating fish. J. Acoust. Soc. Am. 91, 1983–1989. Foote, K.G., 1999. Extinction cross-section of Norwegian spring-spawning herring. ICES J. Mar. Sci. 56, 606–612. Gauthier, S., Horne, J.K., 2004. Acoustic characteristics of forage fish species in the Gulf of Alaska and Bering Sea based on Kirchhoff-approximation models. Can. J. Fish. Aquat. Sci. 61, 1839–1850. Hourston, A.S., 1982. Homing by Canada’s West Coast herring to management units and divisions as indicated by tag recoveries. Can. J. Fish. Aquat. Sci. 39, 1414–1422. Huse, I., Korneliussen, R., 2000. Diel variation in acoustic density measurements of overwintering herring (Clupea harengus L.). ICES J. Mar. Sci. 57, 903–910. Huse, I., Ona, E., 1996. Tilt angle distribution and swimming speed of overwintering Norwegian spring-spawning herring. ICES J. Mar. Sci. 53, 863– 873. Hjellvik, V., Godø, O.R., Tjøstheim, D., 2004. Diurnal variation in acoustic densities: why do we see less in the dark? Can. J. Fish. Aquat. Sci. 61, 2237–2254. Kvamme, C., Nottestad, L., Ferno, A., Misund, O.A., Dommasnes, A., Axelsen, B.E., 2000. A sonar study of the migration pattern of Norwegian springspawning herring (Clupea harengus L.) in July. ICES CM2000, 1–24. Livingston, P.A., 1993. Importance of predation by groundfish, marine mammals and birds on walleye pollock Theragra chalcogramma and Pacific herring Clupea pallasi in the eastern Bering Sea. Mar. Ecol. Prog. Ser. 102, 205–215. MacLennan, D.N., Simmonds, E.J., 1992. Fisheries Acoustics. Chapman and Hall, New York, 325 pp. Marston, B.H., Willson, M.F., Gende, S.M., 2002. Predator aggregations during eulachon Thaleichthys pacificus spawning runs. Mar. Ecol. Prog. Ser. 231, 229–236. Olla, B.L., Davis, M.W., Ryer, C.H., Sogard, S.M., 1996. Behavioural determinants of distribution and survival in early stages of walleye pollock Theragra chalcogramma: a synthesis of experimental studies. Fish. Oceanogr. 5 (Suppl. 1), 167–178. Ona, E., 2003. An expanded target-strength relationship for herring. ICES J. Mar. Sci. 60, 493–499. Paul, A.J., Coyle, K.O., 1993. Taxa composition and biomass of the surfacedwelling crustaceans during spring pycnocline formation in Auke Bay, southeastern Alaska. J. Crustac. Biol. 13, 594–600. Park, W., Sturdevant, M., Orsi, J., Wertheimer, A., Fergusson, E., Heard, W., Shirley, T., 2004. Interannual abundance patterns of copepods during an ENSO event in Icy Strait, southeastern Alaska. ICES J. Mar. Sci. 61, 464–477. Pritchett, M., Walker, S., 2005. Southeast Alaska/Yakutat Annual Herring Research Report, 2003/2004 Season. Alaska Department of Fish and Game, Commercial Fisheries Management and Development Division, Juneau, Alaska. Sigler, M.F., Womble, J.N., Vollenweider, J.J., 2004. Availability to Steller sea lions (Eumetopias jubatus) of a seasonal prey resource: a prespawning aggregation of eulachon (Thaleichthys pacificus). Can. J. Fish. Aquat. Sci. 61, 1475–1484.
M.F. Sigler, D.J. Csepp / Fisheries Research 83 (2007) 319–331 Simil¨a, T., Holst, J.C., Christensen, I., 1996. Occurrence and diet of killer whales in northern Norway: seasonal patterns relative to the distribution and abundance of Norwegian spring-spawning herring. Can. J. Fish. Aquat. Sci. 53, 769–779. Sinclair, E.H., Zepplin, T.K., 2002. Seasonal and spatial differences in diet in the western stock of Steller sea lions (Eumetopias jubatus). J. Mammol. 83, 973–990. Sogard, S.M., Olla, B.L., 2000. Endurance of simulated winter conditions by age-0 walleye pollock: effects of body size, water temperature and energy stores. J. Fish. Biol. 56, 1–21. Thomas, G.L., Kirsch, J., Thorne, R.E., 2002. Ex situ target strength measurements of Pacific herring and Pacific sand lance. N. Am. J. Fish. Manage. 22, 1136–1145. Thorne, R.E., 1977. Acoustic assessment of hake and herring stocks in Puget Sound, Washington and southeastern Alaska. Rapports et Process-Verbaux des Reunions. Conseil Int. Explor. Mer. 170, 265–278. Traynor, J.J., 1996. Target-strength measurements for walleye pollock (Theragra chalcogramma) and Pacific whiting (Merluccius productus). ICES J. Mar. Sci. 53, 253–258.
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Vollenweider, J.J., Heintz, R.A., Kelly, B.P., submitted for publication. Seasonal variation in whole-body proximate composition and energy content of forage fish in southeastern Alaska. Mar. Ecol. Prog. Ser. Walters, C.J., Stocker, M., Tyler, A.V., Westrheim, S.J., 1986. Interaction between Pacific cod (Gadus macrocephalus) and herring (Clupea harengus pallasi) in the Hecate Strait, British Columbia. Can. J. Fish. Aquat. Sci. 43, 830–837. Wheeler, J.P., Winters, G.H., 1984. Homing of Atlantic herring (Clupea harengus harengus) in Newfoundland waters as indicated by tagging data. Can. J. Fish. Aquat. Sci. 41, 108–117. Willson, M.F., Halupka, K.C., 1995. Anadromous fish as keystone species in vertebrate communities. Conserv. Biol. 9, 489–497. Womble, J.N., Sigler, M.F., 2006. Seasonal availability of abundant, energyrich prey influences the abundance and diet of a marine predator, the Steller sea lion Eumetopias jubatus. Mar. Ecol. Prog. Ser. 325, 281– 293. Zhao, X., Ona, E., 2003. Estimation and compensation models for the shadowing effect in dense fish aggregations. ICES J. Mar. Sci. 60, 155–163.