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Energy content of young yellow perch and walleye in Saginaw Bay
JGLR-00635; No. of pages: 6; 4C: Journal of Great Lakes Research xxx (2013) xxx–xxx
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Energy content of young yellow perch and walleye in Saginaw Bay Steven A. Pothoven a,⁎, Tomas O. Höök b,1, Charles R. Roswell b a b
National Oceanic and Atmospheric Administration, Great Lakes Environmental Research Laboratory, 1431 Beach Street, Muskegon, MI 49441, USA Purdue University, Department of Forestry and Natural Resources, 195 Marstellar St., West Lafayette, IN 47907, USA
a r t i c l e
i n f o
Article history: Received 27 February 2013 Accepted 25 September 2013 Available online xxxx Communicated by Scott Peacor Index words: Allometry Lake Huron Energy allocation Seasonality Winter survival
a b s t r a c t We evaluated seasonal energy content of age-0 yellow perch Perca flavescens and walleye Sander vitreus in Saginaw Bay, Lake Huron in 2009 and 2010. We also determined the energy content of age-1 fish from the 2009 and 2010 cohorts the following spring (i.e., for fish that had survived one winter) to evaluate overwinter energy losses. As expected, larger fish within each species had disproportionately higher energy content (i.e., slope relating length and energy N 3.0) than smaller conspecifics. By contrast to expectations, allometric slopes were N 3.0 in nearly all months, not just the fall, and were higher for age-0 yellow perch than for walleye, even though increased allocation to growth would have seemingly been beneficial to even the largest yellow perch during summer. Seasonal energy allocation patterns differed between years. In 2009, length specific energy content increased from late summer to fall for both species. However, for the 2010 cohorts of fish, length specific energy content decreased between late summer and fall for yellow perch and did not change for walleye. There were 13–17% overwinter declines in length specific energy content between the fall (October or November) and the spring (May) with no major differences between cohorts within a species or between species for a given year. Because young yellow perch and walleye are similar physiologically but differ in size (i.e., yellow perch are smaller), it is possible that overwinter energy losses are more important for yellow perch than for walleye. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.
Introduction Yellow perch Perca flavescens and walleye Sander vitreus are two native cool-water fishes that support important fisheries in Saginaw Bay, Lake Huron. The abundance of age-0 yellow perch and walleye in Saginaw Bay increased after the nearly complete disappearance of the non-native planktivore alewife Alosa pseudoharengus from Lake Huron (Fielder and Thomas, 2006; Fielder et al., 2007; Ivan et al., 2011). Formerly, predation and competition from alewife are thought to have limited walleye and yellow perch (Fielder and Thomas, 2006; Fielder et al., 2007). The recent high survival of age-0 walleye led to large year classes and resulted in a strong sport fishery (Fielder and Thomas, 2006; Fielder et al., 2007; Ivan et al., 2011). On the other hand, despite high production of age-0 yellow perch, recruitment of fish to the fishery has remained low (Fielder and Thomas, 2006; Ivan et al., 2011). Poor survival due to slow growth and predation by walleyes are both thought to be contributing to poor recruitment of yellow perch (Ivan et al., 2011; Roswell et al., in this issue). Energy content is a measure of the physiological status of a fish and can help elucidate mechanisms underlying variable vital rates such as mortality and growth. Energy content can change rapidly with ontogeny, and seasonal shifts in energy content can provide information on how ⁎ Corresponding author. Tel.: +1 231 759 9035. E-mail addresses: [email protected] (S.A. Pothoven), [email protected] (T.O. Höök), [email protected] (C.R. Roswell). 1 Tel.: +1 765 496 6799.
energy allocation strategies are adapted to environments where conditions for growth and survival vary over the year (Hurst and Conover, 2003; Höök and Pothoven, 2009). These strategies can be particularly useful to understanding fish growth in temperate environments where overwinter mortality can have large influences for age-0 fish energy allocation (Post and Evans, 1989; Post and Parkinson, 2001; Hurst and Conover, 2003). Age-0 fish in the temperate zone face a trade-off between energy allocation to growth and storage (Schultz and Conover, 1997; Hurst and Conover, 2003). Early in the growing season, survival is generally enhanced by allocating energy toward structural growth, because size selective predation pressure is high and resources are plentiful (Schultz and Conover, 1997). During winter, predation pressure is likely lower and resources are scarce, so selective pressures should favor energy allocation toward storage tissues later in the growing season (Schultz and Conover, 1997). In addition to season, the size of fish can determine how energy is apportioned between growth and storage, with large fish tending to allocate energy toward storage at the expense of increases in length (i.e., structural tissue), especially during the fall (Hurst and Conover, 2003). Larger size provides advantages to fish, including lower mass specific metabolic rates, access to larger prey, and lower risk of size selective predation (Post and Evans, 1989; Shuter and Post, 1990; Borcherding et al., 2007). Larger fish tend to suffer lower mortality rates overwinter than smaller conspecifics (Post and Evans, 1989; Heermann et al., 2009). The goal of this study was to evaluate seasonal energy content for age-0 yellow perch and walleye in Saginaw Bay in 2009 and 2010. We expected that fish would focus on somatic growth early in the summer
0380-1330/$ – see front matter. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. http://dx.doi.org/10.1016/j.jglr.2013.10.002
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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S.A. Pothoven et al. / Journal of Great Lakes Research xxx (2013) xxx–xxx
and energy storage in the fall, a pattern seen for other fish species in the temperate zone (Schultz and Conover, 1997). We also expected that larger fish would have disproportionately higher length specific energy content than smaller fish (Hurst and Conover, 2003). Yellow perch and walleye are closely related species and many physiological parameters for the two species are similar (Hanson et al., 1997). However, owing to the relatively larger size of age-0 walleye, we expected that they would allocate more energy toward storage than the relatively smaller yellow perch. To evaluate overwinter energy losses, we also determined the energy content of age-1 fish from the 2009 and 2010 cohorts the following spring (i.e., individual fish that had survived their first winter). We expected that energy content for both species would decrease overwinter, but that decreases would be more severe for yellow perch based on their current slow growth rates and poor recruitment (Fielder and Thomas, 2006; Ivan et al., 2011; Roswell et al., in this issue). Methods Age-0 and age-1 yellow perch and walleye were collected in bottom trawls (7.6 m semi-balloon trawl with a 13 mm mesh cod liner) at 5 sites in Saginaw Bay, Lake Huron (see Roswell et al., 2013; Pothoven et al., in this issue). Age-0 fish were collected during July–November 2009 and 2010, and age-1 fish (i.e., survivors of one winter) were collected in May 2010 and 2011. Fish were sorted by species, placed in bags with water, and immediately put on ice in coolers. Upon returning to shore, bags of fish were frozen at −20 °C. In the laboratory, total length (nearest mm) and wet weight (nearest 0.01 g) were measured for all fish or a subsample of fish from larger catches. We separated age-0 and age-1 fish using total length, based on clear divisions in length frequency data. After stomach contents were removed, individual fish were dried for 3 days at 70 °C. Subsamples of individual dried fish from each month of sampling (15–46 randomly selected fish/month) were further homogenized with a mortar and pestle. Entire homogenized fish (or a 1 g subsample for fish N 1 g dry weight) from each month of sampling were individually combusted in a Parr 1261 isoperibol calorimeter standardized with benzoic acid. Each individual fish's proportional dry to wet weight, energy density (based on wet weight), and total body energy content (J/g wet weight × total wet weight) were determined. Energy density was regressed as a function of the dry: wet weight ratio for each species and these regressions were used to estimate energy density for all dried fish as done in other studies (e.g., Pothoven et al., 2011; Jacobs et al., 2012). To evaluate seasonal and ontogenetic patterns of energy dynamics, allometric relationships (i.e., E = aLb) between total length (L; mm) and total body energy (E; J) were used to compare energy across months for each cohort of yellow perch and walleye (i.e., fish born in 2009 and 2010). Length-specific total body energy content is a particularly useful index of condition because it encapsulates both length-specific tissue composition and weight (both of which influence condition). Previous studies suggest that both allometric slopes and constants provide insight
as to seasonal and ontogenetic patterns of energy allocation (e.g., Hurst and Conover, 2003). We also determined the size distribution of fish to determine if there were shifts in the size structure of fish overwinter. For this, all fish (i.e., not just those used for energy analysis) were placed into 10 mm size classes so that the 30 mm class was 31–40 mm, 40 mm class = 41–50 mm, etc. The size distributions of fish were compared between the last sampling in the fall (October and November) and the spring (May) using a 2-sample Kolmogorov–Smirnov test. A general linear model was used to evaluate the homogeneity of slopes relating logeE to logeL by determining whether there was a significant interaction between the covariate (logeL) and the factor (month). An ANCOVA was used to compare adjusted mean energy content (adjusted to mean length) between months within a cohort of fish for both species. An ANCOVA was also used to compare adjusted mean energy content between the last sampling in the fall (October or November) and the spring sampling for each cohort of fish. To determine whether the slopes relating length and energy were N 3 (i.e., energy allocation was not isometric), we examined the 95% CI of slopes from the regressions relating logeE to logeL. All statistical comparisons were done using SYSTAT 11, with p b 0.05 considered significant.
Results There was a close relationship between energy density and dry: wet weight for both yellow perch (J/g = (23,231 × dry:wet ratio) − 658.7); n = 148, R2 = 0.87 and walleye (J/g = (22,649 × dry:wet ratio) − 474.3); n = 423, R2 = 0.92. Based on these equations, energy density was estimated for 573 yellow perch ranging in length from 31 to 101 mm, and 1705 walleye ranging in length from 37 to 206 mm (Tables 1 and 2). For age-0 yellow perch, energy density (J/g) increased between July and October 2009 and between July and September 2010 then declined in November 2010 (Table 1). Energy density increased between July and November for age-0 walleye (Table 2). Mean energy density decreased overwinter for both the 2009 and 2010 cohorts of yellow perch. Energy density decreased overwinter for the 2009 cohort of walleye, but remained relatively constant over winter for the 2010 cohort. Mean total energy (J) generally increased each month between July and October or November for age-0 yellow perch and walleye (Tables 1 and 2). Unlike energy density, mean total energy only decreased overwinter for the 2010 cohort of yellow perch, and actually increased overwinter for the 2009 cohort of yellow perch and 2010 cohort of walleye (Tables 1 and 2). Overall, larger fish had disproportionately higher energy content (i.e., allometric slope relating length and energy N3.0) for both yellow perch (slope = 3.57; 95% CI = 3.53–3.60) and walleye (slope = 3.30; 95% CI = 3.28–3.32). Within each month, allometric slopes were N3.0 for yellow perch and walleye, although the 95% CI overlapped 3.0 in May 2010, November 2010, and May 2011 for yellow perch and September 2009 and May 2010 for walleye (Fig. 1).
Table 1 Energy density (J/g), total energy (J), mean length (mm), mean weight (g) (all ± 1 SE), sample size (n) and equation relating energy (E, J) to total length (L, mm) for age-0 (July–November) and age-1 (May) yellow perch from Saginaw Bay, Lake Huron in 2009 and 2010. DOY = day of year fish were collected. Month
DOY
Year
Energy density
Total energy
Length
Weight
July August September October May July August September November May
188–189 216–217 244–245 278–279 130–139 187–188 222–223 266 314 131
2009 2009 2009 2009 2010 2010 2010 2010 2010 2011
3975 4573 4991 5218 4323 4358 4626 5180 4529 4439
1645 ± 7037 ± 13,800 ± 17,610 ± 19,524 ± 4128 ± 12,686 ± 24,933 ± 28,985 ± 24,006 ±
38 ± 56 ± 69 ± 72 ± 78 ± 48 ± 66 ± 80 ± 86 ± 85 ±
0.42 1.54 2.77 3.41 4.49 0.95 2.70 4.81 6.40 5.39
± ± ± ± ± ± ± ± ± ±
45 30 43 66 58 26 29 36 32 42
65 323 663 774 1836 207 857 1097 1693 1526
1 1 1 1 2 1 1 1 1 1
± ± ± ± ± ± ± ± ± ±
0.02 0.07 0.13 0.15 0.39 0.05 0.17 0.21 0.37 0.32
n
Equation
87 82 85 64 16 75 79 63 18 22
loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E
= = = = = = = = = =
3.59 loge L-5.72 (r2 3.66 loge L-5.95 (r2 3.63 loge L-5.91 (r2 3.42 loge L-4.88 (r2 3.35 loge L-4.78 (r2 4.02 loge L-7.29 (r2 3.57 loge L-5.57 (r2 3.59 loge L-5.65 (r2 3.20 loge L-4.03 (r2 3.41 loge L-5.10 (r2
= = = = = = = = = =
0.94) 0.94) 0.91) 0.91) 0.91) 0.93) 0.96) 0.87) 0.95) 0.86)
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
S.A. Pothoven et al. / Journal of Great Lakes Research xxx (2013) xxx–xxx
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Table 2 Energy density (J/g), total energy (J), mean length (mm), mean weight (g) (all ± 1 SE), sample size (n) and equation relating energy (E, J) to total length (L, mm) for age-0 (July–November) and age-1 (May) walleye from Saginaw Bay, Lake Huron in 2009 and 2010. DOY = day of year fish were collected. Month
DOY
Year
Energy density
Total energy
Length
July August September October November April/May July August September November May
188–189, 204 216–217 244–245 278–279 307 130–139 187–189 221–223 265–266 314 131
2009 2009 2009 2009 2009 2010 2010 2010 2010 2010 2011
2762 3333 3709 4286 4503 4380 3405 3769 4440 4597 4534
3681 10,805 28,036 58,163 70,058 70,831 8384 23,066 81,045 78,941 106,256
52 74 97 117 121 130 67 93 131 130 151
± ± ± ± ± ± ± ± ± ± ±
14 20 13 23 44 40 60 18 32 43 25
± ± ± ± ± ± ± ± ± ± ±
122 348 553 2014 4538 4534 377 960 3869 5924 3002
For the 2009 cohort of yellow perch, length-specific energy content differed among months (F4, 328 = 4,108, p b 0.001). Energy content of yellow perch was fairly similar between July and September, and then increased in October prior to an overwinter decrease to its lowest level in May (Fig. 2). For the 2009 cohort of walleye, there was a significant interaction between the factor and the covariate, confounding analysis. Therefore, we examined whether energy content changed between late summer (September) and fall (October and/or November) for both species. For yellow perch, length specific energy content increased 12% between September and October 2009 (Table 3). Similarly, for walleye, energy content increased 8% between September and October 2009, and continued to increase into November (Table 3). For the 2010 cohort of yellow perch, there was a significant interaction between the factor and the covariate. For the 2010 cohort of walleye, length specific energy content differed among months (F4, 564 = 7750, p b 0.001) (Fig. 2). For walleye, energy content decreased slightly between July and August and then returned to July levels for September and November before decreasing overwinter into May (Fig. 2). Between September and November, length specific energy content decreased 7% for yellow perch and did not change for walleye (Table 3).
± ± ± ± ± ± ± ± ± ± ±
Weight 1 1 1 1 2 2 1 1 2 3 1
1.29 3.20 7.49 13.42 15.17 16.04 2.43 6.05 17.96 16.86 23.18
± ± ± ± ± ± ± ± ± ± ±
0.04 0.09 0.13 0.42 0.87 0.94 0.08 0.23 0.78 1.13 0.62
n
Equation
390 164 302 181 69 29 69 107 84 43 267
loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E
= = = = = = = = = = =
3.28 loge L-4.88 (r2 3.34 loge L-5.13 (r2 3.08 loge L-3.88 (r2 3.38 loge L-5.19 (r2 3.47 loge L-5.56 (r2 3.14 loge L-4.15 (r2 3.37 loge L-5.18 (r2 3.29 loge L-4.95 (r2 3.34 loge L-5.08 (r2 3.27 loge L-4.72 (r2 3.42 loge L-5.68 (r2
= = = = = = = = = = =
0.93) 0.92) 0.89) 0.93) 0.97) 0.90) 0.88) 0.94) 0.96) 0.98) 0.92)
The comparison of overwinter energy loss between cohorts is somewhat confounded by the fact that yellow perch were not caught as late in the year for 2009 as in 2010. For yellow perch, length specific energy declined 16% between early October 2009 and May 2010, and 13% between November 2010 and May 2011 (Table 4), although the overwinter decrease was 19% between late September 2010 and May 2011. For walleye, which were caught in November each year, overwinter energy losses were similar between November and May for the 2009 cohort (16%) and the 2010 cohort (17%) (Table 4). The size distribution of yellow perch changed overwinter for the 2009 cohort (p b 0.001). Most yellow perch (84%) in the 2009 cohort were in the 61–80 mm size range in October, but the size distribution shifted overwinter so that 88% of the fish were in the 71–90 mm size range in May (Fig. 3). For the 2010 cohort of yellow perch, the size distribution did not change overwinter (p = 0.53), with a mode at the 80 mm size class in both November and May (Fig. 3). The size distribution of walleye differed between fall and spring for both the 2009 and 2010 cohorts (p ≤ 0.01). For the 2009 cohort of walleye, the size distribution was fairly wide in November, with a mode at the 110 mm size class which shifted to the 120 mm class overwinter (Fig. 3). For the 2010 cohort of walleye, there was again a fairly broad size distribution of fish in November, with a mode at 130 mm size class which shifted to the 150 mm size class overwinter (Fig. 3). Discussion
Fig. 1. Monthly allometric exponents relating energy density to total length for the 2009 and 2010 cohorts of yellow perch and walleye in Saginaw Bay, Lake Huron. Error bars represent 95% CI.
We expected that both age-0 yellow perch and walleye would adopt season specific energy allocation strategies to deal with varying conditions for survival over the year. Specifically, we expected that fish would focus on somatic growth in the summer and energy storage in the fall, a pattern seen for other fish species in the temperate zone (Schultz and Conover, 1997; Post and Parkinson, 2001; Hurst and Conover, 2003). However, our expectations were only partially confirmed for both age-0 yellow perch and walleye. Specifically, for age-0 yellow perch and walleye, length specific energy content did increase between late summer and fall in 2009. On the other hand, between late summer and fall 2010, length specific energy content declined for age-0 yellow perch and did not change for age-0 walleye. Seasonal allocation of energy for age-0 yellow perch and walleye in Saginaw Bay is not a fixed pattern based on variation in seasonal patterns between years. One factor that might have played a role in the inter-annual differences in energy allocation for yellow perch and walleye is the relatively high growth and energy content of fish in 2010 compared to 2009, possibly reducing the need for increased allocation to energy in the fall in 2010. Age-0 largemouth bass Micropterus salmoides allocated a high proportion of energy to storage regardless of season when a high ration was available in a raceway experiment, but fish with a low ration only allocated a high proportion of energy to storage in the fall (Jacobs et al., 2012). Similarly, for age-0 rainbow trout Oncorhynchus mykiss, fast growing fish were found to maximize survival by maximizing energy storage, whereas slow growing fish
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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Fig. 2. Regression lines showing the relationship between loge total energy and loge total length for each month of sampling for the 2009 and 2010 cohorts of age-0 yellow perch and walleye (July–November) and for age-1 fish from the same cohorts (May) in Saginaw Bay, Lake Huron.
optimized survival by allocating energy to somatic growth rather than to storage (Post and Parkinson, 2001). Perhaps, given the faster growth in 2010, fish had sufficient energy reserves and there was less need to allocate more to storage than in 2009. The inter-annual variation in seasonal energy allocation patterns do not appear related to diet differences. Age-0 yellow perch mainly consumed Daphnia in both late summer and fall and did not undergo strong ontogenetic shifts to benthic macroinvertebrates during 2009 or 2010 (Roswell et al., in this issue) and most age-0 walleye (N 80%) were piscivorous by September in both years (S. Pothoven, unpubl. data). As expected, larger fish within each species had disproportionately higher energy content (i.e., slope relating length and energy N3.0) than smaller conspecifics. Contrary to expectations, larger fish tended to allocate disproportionate energy toward storage over increased length in all months even prior to the fall, even though it seems that there would be benefits for even the largest fish to continue growing in the summer (i.e., increased access to larger prey, reduced size selective predation). Interestingly, allometric slopes for yellow perch declined in
the fall, when one would expect them to increase. This could be related to the persistence of Daphnia as a main prey into the fall, rather than shift to benthic macroinvertebrates, which would have been beneficial for larger yellow perch (Roswell et al., in this issue). By contrast to this study, other species have relatively isometric allocation of energy toward storage early in the year and switch to allometric allocation as winter approached (Hurst and Conover, 2003). Allometric slopes for the yellow perch each month were generally higher than those for walleye. This is in contradiction to our expectation that larger fish (i.e., walleye) would put more energy toward growth than smaller fish (i.e., yellow perch). Energy density for each month was also higher for yellow perch than walleye. Thus, it appears that even though yellow perch growth is slow relative to historical rates and a likely factor limiting their survival (Roswell et al., in this issue), yellow perch have an energy allocation strategy in Saginaw Bay that strongly favors energy storage over somatic growth compared to walleye.
Table 3 Percent change in mean length adjusted energy content (from ANCOVA) between late summer (September) and fall (October or November) for the 2009 and 2010 cohorts of age-0 yellow perch and walleye in Saginaw Bay, Lake Huron.
Table 4 Percent decline in mean length adjusted energy content (from ANCOVA) between fall (October or November) and the following spring (May) for the 2009 and 2010 cohorts of age-0 yellow perch and walleye in Saginaw Bay, Lake Huron.
Species
Cohort Period
Percent change
F-ratio
Yellow perch Yellow perch Walleye
2009
+12
F1, 146 = 31.1 b0.001 4.24
Walleye
2009
Walleye
2010
2010 2009
September to October September to November September to October September to November September to November
p
Mean loge mm
Species
Cohort
Period
Percent decline
2009
October to May November to May October to May November to May November to May
16
−7
F1, 78 = 6.0
0.02
4.40
+8
F1, 82 = 7.9
0.01
4.67
Yellow perch Yellow perch Walleye
+18
F1, 77 = 31.6 b0.001 4.69
Walleye
2009
−2
F1, 57 = 0.4
Walleye
2010
0.54
4.86
2010 2009
F-ratio
p
Mean loge mm
F1, 77 = 34.73
b0.001
4.28
13
F1, 37 = 25.74
b0.001
4.44
13
F1, 207 = 41.65
b0.001
4.77
16
F1, 95 = 57.54
b0.001
4.81
17
F1, 307 = 86.99
b0.001
4.99
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
S.A. Pothoven et al. / Journal of Great Lakes Research xxx (2013) xxx–xxx
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Fig. 3. Percent distribution of age-0 yellow perch and walleye in the fall (October or November) and age-1 yellow perch and walleye in the spring (May) for the 2009 and 2010 cohorts of fish in Saginaw Bay.
For both yellow perch (2009 cohort only) and walleye (2009 and 2010 cohorts), there was a shift toward larger fish between fall and spring that could indicate size selective overwinter mortality was occurring for both species. Previous studies have demonstrated that overwinter mortality is more severe for small yellow perch than larger conspecifics (Shuter and Post, 1990; Post and Parkinson, 2001; Heermann et al., 2009). Because both yellow perch and walleye feed during winter (Shuter and Post, 1990; Bandow and Anderson, 1993; Fitzgerald et al., 2006), we cannot entirely eliminate the possibility that growth occurred overwinter, which would produce a shift in the size structure that would resemble size selective mortality. However, evidence for yellow perch (Post and Evans, 1989; Shuter and Post, 1990; Fitzgerald et al., 2006) and walleye (Bandow and Anderson, 1993) suggests that even if they feed they are not likely to grow much during winter. Growth might also have occurred later in the fall after our sampling occurred or early in spring prior to our sampling. Length specific energy content decreased overwinter for both small and large yellow perch and walleye and for both 2009 and 2010 cohorts of fish. The percent energy loss overwinter was not markedly different between the 2009 and 2010 cohorts for either species despite seasonal differences in energy allocation patterns. Furthermore, it appears that the differences in energy loss between species are relatively minor. However, because young yellow perch and walleye are similar physiologically but differ in size (i.e., yellow perch are smaller), the possibility of overwinter energy losses are more important for yellow perch is consistent with the idea that overwinter energy losses are most important for smaller fish. There does not appear to be any strong relationship between age-0 yellow perch abundance in the fall and recruitment to age-1 in Saginaw Bay (Ivan et al., 2011), so overwinter mortality could be particularly important for this species compared to walleye. On the other hand, there is a relationship between age-0 walleye abundance in the fall and recruitment to age-1 in Saginaw Bay (Ivan et al., 2011), so overwinter energy losses might not be as important for walleye as for yellow perch. Overwinter mortality can be due to starvation, predation, or a combination of the two factors (Fitzgerald et al., 2006). Even though we can't conclusively confirm that size structure shifts between fall and spring were due to size selective overwinter mortality, larger fish are
generally less susceptible to starvation and predation (Shuter and Post, 1990; Garvey et al., 2004; Heermann et al., 2009). For yellow perch and walleye, instances where starvation occurs might be rare because both species will feed during winter if food is available (Shuter and Post, 1990; Bandow and Anderson, 1993; Fitzgerald et al., 2006). Starvation might not be likely because it appears that food was available during winter, based on relatively high densities of chironomids in the spring (C. Foley, Purdue University, unpubl. data). Chironomids were the main prey for age-1 yellow perch and walleye in the spring (Staton et al., in this issue; S. Pothoven, unpubl. data). However, fish that have low energy reserves are more likely to forage overwinter, putting them at increased risk of predation (Garvey et al., 2004; Fitzgerald et al., 2006). Predation was probably a bigger factor for yellow perch than walleye because age-0 walleye are larger than age yellow perch, and no young walleye were found in adult walleye stomachs during the summer (S. Pothoven, unpubl. data); whereas small yellow perch were an important diet item (S. Pothoven, unpubl. data; Roswell et al., in this issue). Therefore, losses of energy during winter, although not dramatically different between age-0 walleye and yellow perch, could have differing implications for the survival of each species and recruitment into the fishery of Saginaw Bay.
Acknowledgments We thank those who helped in the field and laboratory, especially B. Coggins, J. Militello, A. Roswell, J. Comben, J. Cavaletto, J. Elliott, A. Zantello, A. Yagiela, and J. Workman. Project funding provided by National Oceanic and Atmospheric Administration Center for Sponsored Coastal Ocean Research. GLERL contribution 1690.
References Bandow, F., Anderson, C.S., 1993. Weight–length relationships, proximate body composition, and winter survival of stocked walleye fingerlings. Minnesota Department of Natural Resources Investigational Report., 425, pp. 1–23 (St. Paul, MN). Borcherding, J., Hermasch, B., Murawski, P., 2007. Field observations and laboratory experiments on growth and lipid content of young-of-the-year perch. Ecol. Freshw. Fish 16, 198–209.
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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Fielder, D.G., Thomas, M.V., 2006. Fish population dynamics of Saginaw Bay, Lake Huron 1998–2004. Fisheries Research Report 2083. Michigan Department of Natural Resources, Ann Arbor, MI, pp. 1–76. Fielder, D.G., Schaeffer, J.S., Thomas, M.V., 2007. Environmental and ecological conditions surrounding the production of large year classes of walleye (Sander vitreus) in Saginaw Bay, Lake Huron. J. Great Lakes Res. 33 (Suppl. 1), 118–132. Fitzgerald, D.G., Forney, J.L., Rudstam, L.G., Irwin, B.J., VanDeValk, A.J., 2006. Gizzard shad put a freeze on winter mortality of age-0 yellow perch but not white perch. Ecol. Appl. 16, 1487–1501. Garvey, J.E., Ostrand, K.G., Wahl, D.H., 2004. Energetics, predation, and ration affect size-dependent growth and mortality of fish during winter. Ecology 85, 2860–2871. Hanson, P.C., Johnson, T.B., Schindler, D.E., Kitchell, J.F., 1997. Fish Bioenergetics 3.0. University of Wisconsin, Sea Grant Institute, Madison, Wisconsin (WISCU-T-97-001). Heermann, L., Eriksson, L.-O., Magnhagen, C., Borcherding, J., 2009. Size-dependent energy storage and winter mortality of perch. Ecol. Freshw. Fish 18, 560–571. Höök, T.O., Pothoven, S.A., 2009. Energy content of young alewives in eastern Lake Michigan and Muskegon Lake, a connected drowned river mouth lake. N. Am. J. Fish Manag. 29, 378–387. Hurst, T.P., Conover, D.O., 2003. Seasonal and interannual variation in the allometry of energy allocation in juvenile striped bass. Ecology 84, 3360–3369. Ivan, L.N., Höök, T.O., Thomas, M.V., Fielder, D.G., 2011. Long-term and interannual dynamics of walleye and yellow perch in Saginaw Bay, Lake Huron. Trans. Am. Fish. Soc. 140, 1078–1092.
Jacobs, G.R., Breck, J.E., Höök, T.O., 2012. Growth mediated seasonal energy allocation patterns of young-of-year largemouth bass (Micropterus salmoides). J. Freshw. Ecol. 27, 63–76. Post, J.R., Evans, D.O., 1989. Size-dependent overwinter mortality of young-of-the-year yellow perch (Perca flavescens): laboratory, in situ enclosure, and field experiments. Can. J. Fish. Aquat. Sci. 46, 1958–1968. Post, J.R., Parkinson, E.A., 2001. Energy allocation strategy in young fish: allometry and survival. Ecology 82, 1040–1051. Pothoven, S.A., Hondorp, D.W., Nalepa, T.F., 2011. Declines in deepwater sculpin Myoxocephalus thompsonii energy density associated with the disappearance of Diporeia spp. in lakes Huron and Michigan. Ecol. Freshw. Fish 20, 14–22. Pothoven, S.A., Höök, T.O., Roswell, C.R., 2013. Feeding ecology of lake whitefish in Saginaw Bay, Lake Huron. J. Great Lakes Res. (in this issue). Roswell, C.R., Pothoven, S.A., Höök, T.O., 2013. Spatio-temporal, ontogenetic, and inter-individual variation of age-0 diets in a population of yellow perch. Ecol. Freshw. Fish 22, 479–493. Roswell, C.R., Pothoven, S.A., Höök, T.O., 2013. Patterns of age-0 yellow perch growth, diets, and mortality in Saginaw Bay, Lake Huron. J. Great Lakes Res. (in this issue). Schultz, E.T., Conover, D.O., 1997. Latitudinal differences in somatic energy storage: adaptive responses to seasonality in an estuarine fish (Atherinidae: Menidia menidia). Oecologia 109, 516–529. Shuter, B.J., Post, J.R., 1990. Climate, population viability, and the zoogeography of temperate fishes. Trans. Am. Fish. Soc. 119, 314–336. Staton, J.M., Roswell, C.R., Fielder, D.G., Thomas, M.V., Pothoven, S.A., Höök, T.O., 2013. Evaluating differences in condition of yellow perch in Saginaw Bay, Lake Huron (1970–2011). J. Great Lakes Res. (in this issue).
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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Energy content of young yellow perch and walleye in Saginaw Bay Steven A. Pothoven a,⁎, Tomas O. Höök b,1, Charles R. Roswell b a b
National Oceanic and Atmospheric Administration, Great Lakes Environmental Research Laboratory, 1431 Beach Street, Muskegon, MI 49441, USA Purdue University, Department of Forestry and Natural Resources, 195 Marstellar St., West Lafayette, IN 47907, USA
a r t i c l e
i n f o
Article history: Received 27 February 2013 Accepted 25 September 2013 Available online xxxx Communicated by Scott Peacor Index words: Allometry Lake Huron Energy allocation Seasonality Winter survival
a b s t r a c t We evaluated seasonal energy content of age-0 yellow perch Perca flavescens and walleye Sander vitreus in Saginaw Bay, Lake Huron in 2009 and 2010. We also determined the energy content of age-1 fish from the 2009 and 2010 cohorts the following spring (i.e., for fish that had survived one winter) to evaluate overwinter energy losses. As expected, larger fish within each species had disproportionately higher energy content (i.e., slope relating length and energy N 3.0) than smaller conspecifics. By contrast to expectations, allometric slopes were N 3.0 in nearly all months, not just the fall, and were higher for age-0 yellow perch than for walleye, even though increased allocation to growth would have seemingly been beneficial to even the largest yellow perch during summer. Seasonal energy allocation patterns differed between years. In 2009, length specific energy content increased from late summer to fall for both species. However, for the 2010 cohorts of fish, length specific energy content decreased between late summer and fall for yellow perch and did not change for walleye. There were 13–17% overwinter declines in length specific energy content between the fall (October or November) and the spring (May) with no major differences between cohorts within a species or between species for a given year. Because young yellow perch and walleye are similar physiologically but differ in size (i.e., yellow perch are smaller), it is possible that overwinter energy losses are more important for yellow perch than for walleye. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.
Introduction Yellow perch Perca flavescens and walleye Sander vitreus are two native cool-water fishes that support important fisheries in Saginaw Bay, Lake Huron. The abundance of age-0 yellow perch and walleye in Saginaw Bay increased after the nearly complete disappearance of the non-native planktivore alewife Alosa pseudoharengus from Lake Huron (Fielder and Thomas, 2006; Fielder et al., 2007; Ivan et al., 2011). Formerly, predation and competition from alewife are thought to have limited walleye and yellow perch (Fielder and Thomas, 2006; Fielder et al., 2007). The recent high survival of age-0 walleye led to large year classes and resulted in a strong sport fishery (Fielder and Thomas, 2006; Fielder et al., 2007; Ivan et al., 2011). On the other hand, despite high production of age-0 yellow perch, recruitment of fish to the fishery has remained low (Fielder and Thomas, 2006; Ivan et al., 2011). Poor survival due to slow growth and predation by walleyes are both thought to be contributing to poor recruitment of yellow perch (Ivan et al., 2011; Roswell et al., in this issue). Energy content is a measure of the physiological status of a fish and can help elucidate mechanisms underlying variable vital rates such as mortality and growth. Energy content can change rapidly with ontogeny, and seasonal shifts in energy content can provide information on how ⁎ Corresponding author. Tel.: +1 231 759 9035. E-mail addresses: [email protected] (S.A. Pothoven), [email protected] (T.O. Höök), [email protected] (C.R. Roswell). 1 Tel.: +1 765 496 6799.
energy allocation strategies are adapted to environments where conditions for growth and survival vary over the year (Hurst and Conover, 2003; Höök and Pothoven, 2009). These strategies can be particularly useful to understanding fish growth in temperate environments where overwinter mortality can have large influences for age-0 fish energy allocation (Post and Evans, 1989; Post and Parkinson, 2001; Hurst and Conover, 2003). Age-0 fish in the temperate zone face a trade-off between energy allocation to growth and storage (Schultz and Conover, 1997; Hurst and Conover, 2003). Early in the growing season, survival is generally enhanced by allocating energy toward structural growth, because size selective predation pressure is high and resources are plentiful (Schultz and Conover, 1997). During winter, predation pressure is likely lower and resources are scarce, so selective pressures should favor energy allocation toward storage tissues later in the growing season (Schultz and Conover, 1997). In addition to season, the size of fish can determine how energy is apportioned between growth and storage, with large fish tending to allocate energy toward storage at the expense of increases in length (i.e., structural tissue), especially during the fall (Hurst and Conover, 2003). Larger size provides advantages to fish, including lower mass specific metabolic rates, access to larger prey, and lower risk of size selective predation (Post and Evans, 1989; Shuter and Post, 1990; Borcherding et al., 2007). Larger fish tend to suffer lower mortality rates overwinter than smaller conspecifics (Post and Evans, 1989; Heermann et al., 2009). The goal of this study was to evaluate seasonal energy content for age-0 yellow perch and walleye in Saginaw Bay in 2009 and 2010. We expected that fish would focus on somatic growth early in the summer
0380-1330/$ – see front matter. Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. http://dx.doi.org/10.1016/j.jglr.2013.10.002
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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and energy storage in the fall, a pattern seen for other fish species in the temperate zone (Schultz and Conover, 1997). We also expected that larger fish would have disproportionately higher length specific energy content than smaller fish (Hurst and Conover, 2003). Yellow perch and walleye are closely related species and many physiological parameters for the two species are similar (Hanson et al., 1997). However, owing to the relatively larger size of age-0 walleye, we expected that they would allocate more energy toward storage than the relatively smaller yellow perch. To evaluate overwinter energy losses, we also determined the energy content of age-1 fish from the 2009 and 2010 cohorts the following spring (i.e., individual fish that had survived their first winter). We expected that energy content for both species would decrease overwinter, but that decreases would be more severe for yellow perch based on their current slow growth rates and poor recruitment (Fielder and Thomas, 2006; Ivan et al., 2011; Roswell et al., in this issue). Methods Age-0 and age-1 yellow perch and walleye were collected in bottom trawls (7.6 m semi-balloon trawl with a 13 mm mesh cod liner) at 5 sites in Saginaw Bay, Lake Huron (see Roswell et al., 2013; Pothoven et al., in this issue). Age-0 fish were collected during July–November 2009 and 2010, and age-1 fish (i.e., survivors of one winter) were collected in May 2010 and 2011. Fish were sorted by species, placed in bags with water, and immediately put on ice in coolers. Upon returning to shore, bags of fish were frozen at −20 °C. In the laboratory, total length (nearest mm) and wet weight (nearest 0.01 g) were measured for all fish or a subsample of fish from larger catches. We separated age-0 and age-1 fish using total length, based on clear divisions in length frequency data. After stomach contents were removed, individual fish were dried for 3 days at 70 °C. Subsamples of individual dried fish from each month of sampling (15–46 randomly selected fish/month) were further homogenized with a mortar and pestle. Entire homogenized fish (or a 1 g subsample for fish N 1 g dry weight) from each month of sampling were individually combusted in a Parr 1261 isoperibol calorimeter standardized with benzoic acid. Each individual fish's proportional dry to wet weight, energy density (based on wet weight), and total body energy content (J/g wet weight × total wet weight) were determined. Energy density was regressed as a function of the dry: wet weight ratio for each species and these regressions were used to estimate energy density for all dried fish as done in other studies (e.g., Pothoven et al., 2011; Jacobs et al., 2012). To evaluate seasonal and ontogenetic patterns of energy dynamics, allometric relationships (i.e., E = aLb) between total length (L; mm) and total body energy (E; J) were used to compare energy across months for each cohort of yellow perch and walleye (i.e., fish born in 2009 and 2010). Length-specific total body energy content is a particularly useful index of condition because it encapsulates both length-specific tissue composition and weight (both of which influence condition). Previous studies suggest that both allometric slopes and constants provide insight
as to seasonal and ontogenetic patterns of energy allocation (e.g., Hurst and Conover, 2003). We also determined the size distribution of fish to determine if there were shifts in the size structure of fish overwinter. For this, all fish (i.e., not just those used for energy analysis) were placed into 10 mm size classes so that the 30 mm class was 31–40 mm, 40 mm class = 41–50 mm, etc. The size distributions of fish were compared between the last sampling in the fall (October and November) and the spring (May) using a 2-sample Kolmogorov–Smirnov test. A general linear model was used to evaluate the homogeneity of slopes relating logeE to logeL by determining whether there was a significant interaction between the covariate (logeL) and the factor (month). An ANCOVA was used to compare adjusted mean energy content (adjusted to mean length) between months within a cohort of fish for both species. An ANCOVA was also used to compare adjusted mean energy content between the last sampling in the fall (October or November) and the spring sampling for each cohort of fish. To determine whether the slopes relating length and energy were N 3 (i.e., energy allocation was not isometric), we examined the 95% CI of slopes from the regressions relating logeE to logeL. All statistical comparisons were done using SYSTAT 11, with p b 0.05 considered significant.
Results There was a close relationship between energy density and dry: wet weight for both yellow perch (J/g = (23,231 × dry:wet ratio) − 658.7); n = 148, R2 = 0.87 and walleye (J/g = (22,649 × dry:wet ratio) − 474.3); n = 423, R2 = 0.92. Based on these equations, energy density was estimated for 573 yellow perch ranging in length from 31 to 101 mm, and 1705 walleye ranging in length from 37 to 206 mm (Tables 1 and 2). For age-0 yellow perch, energy density (J/g) increased between July and October 2009 and between July and September 2010 then declined in November 2010 (Table 1). Energy density increased between July and November for age-0 walleye (Table 2). Mean energy density decreased overwinter for both the 2009 and 2010 cohorts of yellow perch. Energy density decreased overwinter for the 2009 cohort of walleye, but remained relatively constant over winter for the 2010 cohort. Mean total energy (J) generally increased each month between July and October or November for age-0 yellow perch and walleye (Tables 1 and 2). Unlike energy density, mean total energy only decreased overwinter for the 2010 cohort of yellow perch, and actually increased overwinter for the 2009 cohort of yellow perch and 2010 cohort of walleye (Tables 1 and 2). Overall, larger fish had disproportionately higher energy content (i.e., allometric slope relating length and energy N3.0) for both yellow perch (slope = 3.57; 95% CI = 3.53–3.60) and walleye (slope = 3.30; 95% CI = 3.28–3.32). Within each month, allometric slopes were N3.0 for yellow perch and walleye, although the 95% CI overlapped 3.0 in May 2010, November 2010, and May 2011 for yellow perch and September 2009 and May 2010 for walleye (Fig. 1).
Table 1 Energy density (J/g), total energy (J), mean length (mm), mean weight (g) (all ± 1 SE), sample size (n) and equation relating energy (E, J) to total length (L, mm) for age-0 (July–November) and age-1 (May) yellow perch from Saginaw Bay, Lake Huron in 2009 and 2010. DOY = day of year fish were collected. Month
DOY
Year
Energy density
Total energy
Length
Weight
July August September October May July August September November May
188–189 216–217 244–245 278–279 130–139 187–188 222–223 266 314 131
2009 2009 2009 2009 2010 2010 2010 2010 2010 2011
3975 4573 4991 5218 4323 4358 4626 5180 4529 4439
1645 ± 7037 ± 13,800 ± 17,610 ± 19,524 ± 4128 ± 12,686 ± 24,933 ± 28,985 ± 24,006 ±
38 ± 56 ± 69 ± 72 ± 78 ± 48 ± 66 ± 80 ± 86 ± 85 ±
0.42 1.54 2.77 3.41 4.49 0.95 2.70 4.81 6.40 5.39
± ± ± ± ± ± ± ± ± ±
45 30 43 66 58 26 29 36 32 42
65 323 663 774 1836 207 857 1097 1693 1526
1 1 1 1 2 1 1 1 1 1
± ± ± ± ± ± ± ± ± ±
0.02 0.07 0.13 0.15 0.39 0.05 0.17 0.21 0.37 0.32
n
Equation
87 82 85 64 16 75 79 63 18 22
loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E
= = = = = = = = = =
3.59 loge L-5.72 (r2 3.66 loge L-5.95 (r2 3.63 loge L-5.91 (r2 3.42 loge L-4.88 (r2 3.35 loge L-4.78 (r2 4.02 loge L-7.29 (r2 3.57 loge L-5.57 (r2 3.59 loge L-5.65 (r2 3.20 loge L-4.03 (r2 3.41 loge L-5.10 (r2
= = = = = = = = = =
0.94) 0.94) 0.91) 0.91) 0.91) 0.93) 0.96) 0.87) 0.95) 0.86)
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
S.A. Pothoven et al. / Journal of Great Lakes Research xxx (2013) xxx–xxx
3
Table 2 Energy density (J/g), total energy (J), mean length (mm), mean weight (g) (all ± 1 SE), sample size (n) and equation relating energy (E, J) to total length (L, mm) for age-0 (July–November) and age-1 (May) walleye from Saginaw Bay, Lake Huron in 2009 and 2010. DOY = day of year fish were collected. Month
DOY
Year
Energy density
Total energy
Length
July August September October November April/May July August September November May
188–189, 204 216–217 244–245 278–279 307 130–139 187–189 221–223 265–266 314 131
2009 2009 2009 2009 2009 2010 2010 2010 2010 2010 2011
2762 3333 3709 4286 4503 4380 3405 3769 4440 4597 4534
3681 10,805 28,036 58,163 70,058 70,831 8384 23,066 81,045 78,941 106,256
52 74 97 117 121 130 67 93 131 130 151
± ± ± ± ± ± ± ± ± ± ±
14 20 13 23 44 40 60 18 32 43 25
± ± ± ± ± ± ± ± ± ± ±
122 348 553 2014 4538 4534 377 960 3869 5924 3002
For the 2009 cohort of yellow perch, length-specific energy content differed among months (F4, 328 = 4,108, p b 0.001). Energy content of yellow perch was fairly similar between July and September, and then increased in October prior to an overwinter decrease to its lowest level in May (Fig. 2). For the 2009 cohort of walleye, there was a significant interaction between the factor and the covariate, confounding analysis. Therefore, we examined whether energy content changed between late summer (September) and fall (October and/or November) for both species. For yellow perch, length specific energy content increased 12% between September and October 2009 (Table 3). Similarly, for walleye, energy content increased 8% between September and October 2009, and continued to increase into November (Table 3). For the 2010 cohort of yellow perch, there was a significant interaction between the factor and the covariate. For the 2010 cohort of walleye, length specific energy content differed among months (F4, 564 = 7750, p b 0.001) (Fig. 2). For walleye, energy content decreased slightly between July and August and then returned to July levels for September and November before decreasing overwinter into May (Fig. 2). Between September and November, length specific energy content decreased 7% for yellow perch and did not change for walleye (Table 3).
± ± ± ± ± ± ± ± ± ± ±
Weight 1 1 1 1 2 2 1 1 2 3 1
1.29 3.20 7.49 13.42 15.17 16.04 2.43 6.05 17.96 16.86 23.18
± ± ± ± ± ± ± ± ± ± ±
0.04 0.09 0.13 0.42 0.87 0.94 0.08 0.23 0.78 1.13 0.62
n
Equation
390 164 302 181 69 29 69 107 84 43 267
loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E loge E
= = = = = = = = = = =
3.28 loge L-4.88 (r2 3.34 loge L-5.13 (r2 3.08 loge L-3.88 (r2 3.38 loge L-5.19 (r2 3.47 loge L-5.56 (r2 3.14 loge L-4.15 (r2 3.37 loge L-5.18 (r2 3.29 loge L-4.95 (r2 3.34 loge L-5.08 (r2 3.27 loge L-4.72 (r2 3.42 loge L-5.68 (r2
= = = = = = = = = = =
0.93) 0.92) 0.89) 0.93) 0.97) 0.90) 0.88) 0.94) 0.96) 0.98) 0.92)
The comparison of overwinter energy loss between cohorts is somewhat confounded by the fact that yellow perch were not caught as late in the year for 2009 as in 2010. For yellow perch, length specific energy declined 16% between early October 2009 and May 2010, and 13% between November 2010 and May 2011 (Table 4), although the overwinter decrease was 19% between late September 2010 and May 2011. For walleye, which were caught in November each year, overwinter energy losses were similar between November and May for the 2009 cohort (16%) and the 2010 cohort (17%) (Table 4). The size distribution of yellow perch changed overwinter for the 2009 cohort (p b 0.001). Most yellow perch (84%) in the 2009 cohort were in the 61–80 mm size range in October, but the size distribution shifted overwinter so that 88% of the fish were in the 71–90 mm size range in May (Fig. 3). For the 2010 cohort of yellow perch, the size distribution did not change overwinter (p = 0.53), with a mode at the 80 mm size class in both November and May (Fig. 3). The size distribution of walleye differed between fall and spring for both the 2009 and 2010 cohorts (p ≤ 0.01). For the 2009 cohort of walleye, the size distribution was fairly wide in November, with a mode at the 110 mm size class which shifted to the 120 mm class overwinter (Fig. 3). For the 2010 cohort of walleye, there was again a fairly broad size distribution of fish in November, with a mode at 130 mm size class which shifted to the 150 mm size class overwinter (Fig. 3). Discussion
Fig. 1. Monthly allometric exponents relating energy density to total length for the 2009 and 2010 cohorts of yellow perch and walleye in Saginaw Bay, Lake Huron. Error bars represent 95% CI.
We expected that both age-0 yellow perch and walleye would adopt season specific energy allocation strategies to deal with varying conditions for survival over the year. Specifically, we expected that fish would focus on somatic growth in the summer and energy storage in the fall, a pattern seen for other fish species in the temperate zone (Schultz and Conover, 1997; Post and Parkinson, 2001; Hurst and Conover, 2003). However, our expectations were only partially confirmed for both age-0 yellow perch and walleye. Specifically, for age-0 yellow perch and walleye, length specific energy content did increase between late summer and fall in 2009. On the other hand, between late summer and fall 2010, length specific energy content declined for age-0 yellow perch and did not change for age-0 walleye. Seasonal allocation of energy for age-0 yellow perch and walleye in Saginaw Bay is not a fixed pattern based on variation in seasonal patterns between years. One factor that might have played a role in the inter-annual differences in energy allocation for yellow perch and walleye is the relatively high growth and energy content of fish in 2010 compared to 2009, possibly reducing the need for increased allocation to energy in the fall in 2010. Age-0 largemouth bass Micropterus salmoides allocated a high proportion of energy to storage regardless of season when a high ration was available in a raceway experiment, but fish with a low ration only allocated a high proportion of energy to storage in the fall (Jacobs et al., 2012). Similarly, for age-0 rainbow trout Oncorhynchus mykiss, fast growing fish were found to maximize survival by maximizing energy storage, whereas slow growing fish
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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S.A. Pothoven et al. / Journal of Great Lakes Research xxx (2013) xxx–xxx
Fig. 2. Regression lines showing the relationship between loge total energy and loge total length for each month of sampling for the 2009 and 2010 cohorts of age-0 yellow perch and walleye (July–November) and for age-1 fish from the same cohorts (May) in Saginaw Bay, Lake Huron.
optimized survival by allocating energy to somatic growth rather than to storage (Post and Parkinson, 2001). Perhaps, given the faster growth in 2010, fish had sufficient energy reserves and there was less need to allocate more to storage than in 2009. The inter-annual variation in seasonal energy allocation patterns do not appear related to diet differences. Age-0 yellow perch mainly consumed Daphnia in both late summer and fall and did not undergo strong ontogenetic shifts to benthic macroinvertebrates during 2009 or 2010 (Roswell et al., in this issue) and most age-0 walleye (N 80%) were piscivorous by September in both years (S. Pothoven, unpubl. data). As expected, larger fish within each species had disproportionately higher energy content (i.e., slope relating length and energy N3.0) than smaller conspecifics. Contrary to expectations, larger fish tended to allocate disproportionate energy toward storage over increased length in all months even prior to the fall, even though it seems that there would be benefits for even the largest fish to continue growing in the summer (i.e., increased access to larger prey, reduced size selective predation). Interestingly, allometric slopes for yellow perch declined in
the fall, when one would expect them to increase. This could be related to the persistence of Daphnia as a main prey into the fall, rather than shift to benthic macroinvertebrates, which would have been beneficial for larger yellow perch (Roswell et al., in this issue). By contrast to this study, other species have relatively isometric allocation of energy toward storage early in the year and switch to allometric allocation as winter approached (Hurst and Conover, 2003). Allometric slopes for the yellow perch each month were generally higher than those for walleye. This is in contradiction to our expectation that larger fish (i.e., walleye) would put more energy toward growth than smaller fish (i.e., yellow perch). Energy density for each month was also higher for yellow perch than walleye. Thus, it appears that even though yellow perch growth is slow relative to historical rates and a likely factor limiting their survival (Roswell et al., in this issue), yellow perch have an energy allocation strategy in Saginaw Bay that strongly favors energy storage over somatic growth compared to walleye.
Table 3 Percent change in mean length adjusted energy content (from ANCOVA) between late summer (September) and fall (October or November) for the 2009 and 2010 cohorts of age-0 yellow perch and walleye in Saginaw Bay, Lake Huron.
Table 4 Percent decline in mean length adjusted energy content (from ANCOVA) between fall (October or November) and the following spring (May) for the 2009 and 2010 cohorts of age-0 yellow perch and walleye in Saginaw Bay, Lake Huron.
Species
Cohort Period
Percent change
F-ratio
Yellow perch Yellow perch Walleye
2009
+12
F1, 146 = 31.1 b0.001 4.24
Walleye
2009
Walleye
2010
2010 2009
September to October September to November September to October September to November September to November
p
Mean loge mm
Species
Cohort
Period
Percent decline
2009
October to May November to May October to May November to May November to May
16
−7
F1, 78 = 6.0
0.02
4.40
+8
F1, 82 = 7.9
0.01
4.67
Yellow perch Yellow perch Walleye
+18
F1, 77 = 31.6 b0.001 4.69
Walleye
2009
−2
F1, 57 = 0.4
Walleye
2010
0.54
4.86
2010 2009
F-ratio
p
Mean loge mm
F1, 77 = 34.73
b0.001
4.28
13
F1, 37 = 25.74
b0.001
4.44
13
F1, 207 = 41.65
b0.001
4.77
16
F1, 95 = 57.54
b0.001
4.81
17
F1, 307 = 86.99
b0.001
4.99
Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002
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Fig. 3. Percent distribution of age-0 yellow perch and walleye in the fall (October or November) and age-1 yellow perch and walleye in the spring (May) for the 2009 and 2010 cohorts of fish in Saginaw Bay.
For both yellow perch (2009 cohort only) and walleye (2009 and 2010 cohorts), there was a shift toward larger fish between fall and spring that could indicate size selective overwinter mortality was occurring for both species. Previous studies have demonstrated that overwinter mortality is more severe for small yellow perch than larger conspecifics (Shuter and Post, 1990; Post and Parkinson, 2001; Heermann et al., 2009). Because both yellow perch and walleye feed during winter (Shuter and Post, 1990; Bandow and Anderson, 1993; Fitzgerald et al., 2006), we cannot entirely eliminate the possibility that growth occurred overwinter, which would produce a shift in the size structure that would resemble size selective mortality. However, evidence for yellow perch (Post and Evans, 1989; Shuter and Post, 1990; Fitzgerald et al., 2006) and walleye (Bandow and Anderson, 1993) suggests that even if they feed they are not likely to grow much during winter. Growth might also have occurred later in the fall after our sampling occurred or early in spring prior to our sampling. Length specific energy content decreased overwinter for both small and large yellow perch and walleye and for both 2009 and 2010 cohorts of fish. The percent energy loss overwinter was not markedly different between the 2009 and 2010 cohorts for either species despite seasonal differences in energy allocation patterns. Furthermore, it appears that the differences in energy loss between species are relatively minor. However, because young yellow perch and walleye are similar physiologically but differ in size (i.e., yellow perch are smaller), the possibility of overwinter energy losses are more important for yellow perch is consistent with the idea that overwinter energy losses are most important for smaller fish. There does not appear to be any strong relationship between age-0 yellow perch abundance in the fall and recruitment to age-1 in Saginaw Bay (Ivan et al., 2011), so overwinter mortality could be particularly important for this species compared to walleye. On the other hand, there is a relationship between age-0 walleye abundance in the fall and recruitment to age-1 in Saginaw Bay (Ivan et al., 2011), so overwinter energy losses might not be as important for walleye as for yellow perch. Overwinter mortality can be due to starvation, predation, or a combination of the two factors (Fitzgerald et al., 2006). Even though we can't conclusively confirm that size structure shifts between fall and spring were due to size selective overwinter mortality, larger fish are
generally less susceptible to starvation and predation (Shuter and Post, 1990; Garvey et al., 2004; Heermann et al., 2009). For yellow perch and walleye, instances where starvation occurs might be rare because both species will feed during winter if food is available (Shuter and Post, 1990; Bandow and Anderson, 1993; Fitzgerald et al., 2006). Starvation might not be likely because it appears that food was available during winter, based on relatively high densities of chironomids in the spring (C. Foley, Purdue University, unpubl. data). Chironomids were the main prey for age-1 yellow perch and walleye in the spring (Staton et al., in this issue; S. Pothoven, unpubl. data). However, fish that have low energy reserves are more likely to forage overwinter, putting them at increased risk of predation (Garvey et al., 2004; Fitzgerald et al., 2006). Predation was probably a bigger factor for yellow perch than walleye because age-0 walleye are larger than age yellow perch, and no young walleye were found in adult walleye stomachs during the summer (S. Pothoven, unpubl. data); whereas small yellow perch were an important diet item (S. Pothoven, unpubl. data; Roswell et al., in this issue). Therefore, losses of energy during winter, although not dramatically different between age-0 walleye and yellow perch, could have differing implications for the survival of each species and recruitment into the fishery of Saginaw Bay.
Acknowledgments We thank those who helped in the field and laboratory, especially B. Coggins, J. Militello, A. Roswell, J. Comben, J. Cavaletto, J. Elliott, A. Zantello, A. Yagiela, and J. Workman. Project funding provided by National Oceanic and Atmospheric Administration Center for Sponsored Coastal Ocean Research. GLERL contribution 1690.
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Please cite this article as: Pothoven, S.A., et al., Energy content of young yellow perch and walleye in Saginaw Bay, J Great Lakes Res (2013), http:// dx.doi.org/10.1016/j.jglr.2013.10.002