Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby

JGLR-01013; No. of pages: 8; 4C: Journal of Great Lakes Research xxx (2016) xxx–xxx

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Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby Derek P. Crane a,⁎, Donald W. Einhouse b a b

Lake Superior State University, 650 West Easterday Avenue, Sault Ste. Marie, MI 49783, USA New York State Department of Environmental Conservation, Lake Erie Fisheries Research Unit, Dunkirk, NY 14048, USA

a r t i c l e

i n f o

Article history: Received 5 January 2015 Accepted 14 November 2015 Available online xxxx Communicated by John Janssen Index words: Invasive species Round goby Growth Great Lakes Smallmouth bass

a b s t r a c t Upon invading the Great Lakes, the round goby (Neogobius melanostomus) was rapidly incorporated in the diet of native predators. The smallmouth bass (Micropterus dolomieu) is an abundant nearshore predator and readily consumes round goby; however, the effects of round goby on growth of smallmouth bass have not been examined for a wide range of smallmouth bass ages. We compared smallmouth bass diets from New York waters of Lake Erie before and after the invasion of round goby and analyzed 19 years (pre-round goby = 1993–1998; post-round goby = 2001–2013) of length-at-age data (ages 2–10) to investigate the effects of round goby on growth of smallmouth bass. Analysis of variance was used to test hypotheses about the effects of sex, age, and round goby presence on length-at-age of smallmouth bass, and von Bertalanffy models were used to identify changes in growth patterns. Crayfish (Decapoda spp.) were the most common prey of smallmouth bass prior to invasion of round goby (observed in 53.5% of diets). Round goby became the dominant prey of smallmouth bass after its invasion (observed in 73.3% of diets), and crayfish were only observed in 5.8% of diets in the postround goby time period. Length-at-age increased following invasion of round goby and the greatest increases in length (11–15%) were observed for ages 2–4. The von Bertalanffy growth coefficient, K, increased for both male and female smallmouth bass. Results from this study demonstrate how aquatic invaders can rapidly change population characteristics of native predators. © 2015 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

Introduction Invasive species can have substantial effects on population characteristics and life histories of native fauna. The Great Lakes is one of the most invaded aquatic ecosystems in the world (Ricciardi, 2006), and the round goby (Neogobius melanostomus) is one of the most successful invaders of the Great Lakes and its tributaries. Round goby were first detected in the St. Clair River in 1990 (Jude et al., 1992) and have continued to spread throughout the Great Lakes, its connecting channels, tributaries, and adjacent lakes over the past 25 years (Kornis et al., 2012). Densities of 1–14 round goby m− 2 are frequently reported (Barton et al., 2005; Johnson et al., 2005a; Ray and Corkum, 2001), and densities of N 100 individuals m−2 have been observed (Chotkowski and Marsden, 1999). The round goby is a benthic dwelling species and able to successfully occupy a variety of habitats spanning a broad range of thermal regimes, salinities, dissolved oxygen levels, and physical structure (Kornis et al., 2012). In the Great Lakes round goby are found in habitats ranging from coastal wetlands (Cooper et al., 2007; Farrell et al., 2010) to 150 m deep profundal zones (Walsh ⁎ Corresponding author at: Coastal Carolina University, 111 Chanticleer Drive East, Conway, SC 29526, USA. Tel.: +1 843 349 4065. E-mail address: [email protected] (D.P. Crane).

et al., 2007). Restructuring of energy (Campbell et al., 2009; Johnson et al., 2005b) and contaminant pathways (Hogan et al., 2007), extirpation and decreased abundance of native benthic fishes (Janssen and Jude, 2001; Kornis et al., 2012; Lauer, 2004), dramatic shifts in diet (Johnson et al., 2005b), and associated changes in body condition (Crane et al., 2015) and growth of piscivores (Stapanian et al., 2011; Steinhart et al., 2004a) have been attributed to the round goby. Growth is a defining life-history characteristic and is frequently studied by biologists. Growth characteristics can have important implications for other life history traits such as age-at-maturity and mortality, as has been well studied for fishes (He and Stewart, 2001; He and Stewart, 2002; Madenjian et al., 1996; Pauly, 1980). Resource managers often evaluate growth of fishes to assess management practices or productivity of a body of water for a particular species. Somatic growth of fishes is dictated by a number of factors including competition, environmental conditions, forage availability and quality, maturity status, and activity (Diana, 2004). Invasive prey fishes have the potential to alter growth of native piscivores by causing shifts in diet and foraging strategies and affecting the availability of native prey. Although the round goby has resulted in decreased abundance of native benthic prey fishes in some regions of the Great Lakes (J.M. Farrell, State University of New York – College of Environmental Science and Forestry, unpublished data, March 2014; Janssen and Jude, 2001; Lauer, 2004), it has also

http://dx.doi.org/10.1016/j.jglr.2015.12.005 0380-1330/© 2015 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

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D.P. Crane, D.W. Einhouse / Journal of Great Lakes Research xxx (2016) xxx–xxx

become an important food resource for many native piscivores (Dietrich et al., 2006; Jacobs et al., 2010; Johnson et al., 2005b; Kornis et al., 2012; Madenjian et al., 2011). Thus, the round goby has the potential to significantly change the growth of predatory fishes in the Great Lakes (Stapanian et al., 2011; Steinhart et al., 2004a). The smallmouth bass (Micropterus dolomieu) is a relatively abundant predator in many shallow water areas (defined here as water depth b 15 m) of the Great Lakes, its connecting channels, and tributaries (Einhouse et al., 2002; Fielder et al., 2013; Lantry, 2014; McCullough and Gordon, 2014). Smallmouth bass are most frequently found in areas with coarse rocky substrate (Brown et al., 2009) which are also preferred by round goby (Johnson et al., 2005a; Kornis et al., 2012; Kornis et al., 2013; Ray and Corkum, 2001). Following invasion of Lake Erie by the round goby, round goby quickly became the dominant prey item of smallmouth bass (Johnson et al., 2005b; Steinhart et al., 2004a). Based on proportion of diet, round goby is consumed more by smallmouth bass than any other Lake Erie fish, except burbot (Lota lota), which consume round goby in similar proportions as smallmouth bass (Johnson et al., 2005b). The effect of round goby on growth of smallmouth bass in the Great Lakes has not been investigated for most smallmouth bass ages. Steinhart et al., (2004a) investigated changes in growth of age-0 smallmouth bass in western Lake Erie following invasion of round goby, and McCullough (2012) and Lantry (2014) documented longterm trends in smallmouth bass length-at-age for St. Lawrence River and Lake Ontario populations. However, examining the effects of round goby on smallmouth bass growth in the St. Lawrence River and eastern Lake Ontario was confounded by compensatory growth observed prior to invasion of round goby (Lantry, 2014). Sex-based differences in the response of smallmouth bass growth to the presence of round goby have also not been explored. The round goby is an egg predator and its presence has energetic costs for male smallmouth bass during nest guarding, which are not incurred by females (Steinhart et al., 2005). Here, we examine changes in diet and growth of smallmouth bass following invasion of eastern Lake Erie by round goby. The objectives of this study were to (1) describe the diet of smallmouth bass prior to and after invasion of round goby, (2) identify changes in smallmouth bass length-at-age and differences in growth trends between the pre- and post-invasion time periods, and (3) determine if growth responses to the invasion of round goby differed between male and female smallmouth bass. We hypothesized that (1) similar to other areas of the Great Lakes (Johnson et al., 2005b; Lantry, 2014; Reyjol et al., 2010; Steinhart et al., 2004a; Taraborelli et al., 2010), round goby is an important part of smallmouth bass diets in New York waters of eastern Lake Erie, (2) smallmouth bass growth increased following round goby invasion, (3) and females experienced greater increases in growth than males. Methods Study system and fish collection Lake Erie is the shallowest and most productive of the Laurentian Great Lakes. The nearshore zone of the eastern basin of Lake Erie (Fig. 1) is classified as oligotrophic to mesotrophic (Markham, 2014) and supports a diverse community of warm- and coolwater fishes. Smallmouth bass were collected from 1981 to 2013 as part of the New York State Department of Environmental Conservation (NYSDEC) Eastern Lake Erie Warmwater Fish Community Assessment. From 1981 to 1992, fish were collected with multifilament gill nets during early September through early October. Nets were fished overnight at fixed stations in water b 12 m. Beginning in 1993, the sampling strategy was altered to align with an interagency gill net assessment for Lake Erie (Ryan et al., 1993). This investigation primarily focuses on the 1993–2013 time period. Sampling during 1993–2013 was conducted with monofilament gill nets from early September through early October at fixed and randomly

Fig. 1. Map of New York waters of eastern Lake Erie.

selected locations. Sampling occurred in two depth strata: b 15 m (9 fixed and 16 randomly selected locations per year) and 15–b 30 m (15 randomly selected locations per year). Nets were set from 1200 to 1700 h and retrieved from sunrise through 1200 h. All waters b30 m in the New York portion of Lake Erie were available for sampling. Nets were fished on the bottom at all locations but were not set if an area selected for sampling included the thermocline. The gill nets were 213.4 m long and consisted of 14, 15.2 m long × 1.8 m deep panels. Each panel contained a single size stretch mesh ranging from 3.2 to 15.2 cm and the panels were randomly ordered. The 15.2 cm panel was discontinued in 2005 due to poor performance and excessive net damage. Tangled, damaged, or fouled nets were omitted. The total length (TL; nearest mm) and sex of each smallmouth bass were recorded, and scales and sagittal otoliths were collected for age determination. Beginning in 2000, smallmouth bass were infrequently sub-sampled if the catch was N10 for a particular mesh size, during a single net set. The smallmouth bass dataset was divided into pre- and post-round goby time periods based on annual forage trawl survey data. Round goby were first detected in annual forage trawls in New York waters of eastern Lake Erie in 1999 (Markham and Einhouse, 2014). Therefore, prior to 1999 was defined as the pre-round goby time period and 1999–2013 was defined as the post-round goby time period. Diet data were collected opportunistically and available for 1985–1987, 1992, 1999–2002, and 2006–2007. Because the main objective of the diet analysis was to demonstrate change in smallmouth bass diet following invasion of the round goby in eastern Lake Erie, all available diet data were included. For growth analyses, the 1981–2013 dataset was reduced to prevent potential biases related to age determination methods, gear selectivity, and age distribution of the catch in relation to invasion of round goby. First, samples collected prior to 1993 were removed due to changes in age determination protocols beginning in 1993. Prior to 1993, scales were used to estimate ages of all fish. From 1993 to 2013 scales were used to estimate ages of small fish and otoliths were used to estimate ages of larger fish (see below). Next, smallmouth bass that lived in both the pre- and post-round goby time periods were removed to make more reliable growth comparisons between time periods. Finally, fish bage-2 and N age-10 were removed because smallmouth bass were not fully recruited to the gill nets until age-2 and catches for individuals N age-10 were rare (only 2% of smallmouth bass included in the pre−/post-round goby time periods were N age-10). Subsequently, all fish collected during 1999 and 2000 were omitted from growth analyses (except for use in time series plots of length-at-age) because no fish could satisfy the requirements of being ≥age-2 and only living during either the pre- or post-round goby time period.

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

D.P. Crane, D.W. Einhouse / Journal of Great Lakes Research xxx (2016) xxx–xxx

Ages of smallmouth bass were determined by counting scale annuli (smallmouth bass b430 mm TL) or otolith annuli (smallmouth bass ≥ 430 mm TL), and the same individual conducted age determination for all fish. Scales were pressed on acetate and then viewed on a microfiche reader. Otoliths were prepared using the crack-and-burn technique (Christensen, 1964), mounted in modeling clay, dabbed with immersion oil, and viewed under a dissecting microscope. Otoliths are the preferred structure for age determination of smallmouth bass (Long and Fisher, 2001) because scales can lead to underestimation of age. However, Maceina and Sammons (2006) observed that scale and otolith-based age estimates generally agreed for Hudson River smallmouth bass estimated to be up to age-6 (otolith estimate). In this study, 39% of male smallmouth bass (5% of total male sample) and 32% of female smallmouth bass (4% of total female sample) estimated to be N6 years old, using scales or otoliths, were b the 430 mm cutoff used for determining age based on otoliths. Any potential bias from using scales for age determination should not have affected comparisons between time periods in this study because (1) the low number of fish N age-6 and b430 mm relative to the total sample size, (2) the same individual examined all fish to assign ages, and (3) the same methods were used throughout the study period. Diet Diets were examined for a subsample of smallmouth bass. Stomach contents were removed from each fish, and prey items were visually identified to the lowest practical taxonomic level. Alewife (Alosa pseudoharengus) and gizzard shad (Dorosoma cepedianum) were collectively referred to as clupeids, and white bass (Morone chrysops) and white perch (Morone americana) were referred to as Morone spp. Unidentifiable fishes were referred to as “other fish” and macroinvertebrates were referred to as crayfish or “other macroinvertebrates.” Percent occurrence of each prey taxa in non-empty stomachs (based on count) was calculated for the pre- and post-round goby time periods.

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Table 1 Coefficient estimates for the ANOVA model of smallmouth bass length-at-age. Smallmouth bass were collected from eastern Lake Erie during 1993–1998 (pre-round goby) and 2001–2013 (post-round goby). The model contained coefficients for age, round goby presence, and interactions between age and round goby presence and age and sex. All variables were treated as categorical predictors. Each age was treated as a separate parameter and the intercept indicates the length (mm) of an age-2 female smallmouth bass. The length of a fish for a given age, sex, and time period can be estimated by the equation: Lt, s, rg = Intercept + Age + RG present (0 = absent, 1 = present) + Age * RG present + Age * sex (0 = female, 1 = male). For example, the estimated length of an age-5, male smallmouth bass in the post-round goby time period (RG present) would be 407.6 = 250.3 + 121.9 + 34.1 − 2.8 + 4.1. Adjusted R2 = 0.87. Variable

Estimate

SE

Intercept Age-3 Age-4 Age-5 Age-6 Age-7 Age-8 Age-9 Age-10 RG present Age-3 * RG present Age-4 * RG present Age-5 * RG present Age-6 * RG present Age-7 * RG present Age-8 * RG present Age-9 * RG present Age-10 * RG present Age-2 * male Age-3 * male Age-4 * male Age-5 * male Age-6 * male Age-7 * male Age-8 * male Age-9 * male Age-10 * male

250.3 49.0 87.6 121.9 142.6 163.9 181.4 195.4 205.6 34.1 9.7 5.3 −2.8 −7.7 −7.7 −11.1 −17.6 −15.7 2.8 4.5 6.4 4.1 8.6 6.6 −0.1 −0.4 −8.3

1.22 1.60 1.73 1.69 2.01 2.05 2.55 3.00 3.56 1.22 1.64 1.83 1.94 2.23 2.35 3.13 3.49 5.06 0.89 1.03 1.35 1.46 1.87 2.00 2.88 3.24 4.35

Growth and length-at-age analyses Pre- and post-round goby comparisons of smallmouth bass growth were investigated using three analyses of length-at-age data. First, analysis of variance (ANOVA) and was used to identify important factors affecting smallmouth bass length. Next, differences between pre- and post-round goby lengths-at-age were tested for and effect sizes were estimated using Dunnett's modified Tukey–Kramer test. Finally, time period specific von Bertalanffy growth models (Beverton and Holt, 1957; von Bertalanffy, 1938) were fitted for female and male smallmouth bass. All analyses were conducted in R (R version 3.0.2; R Core Team, 2013), and an alpha level of 0.05 was used to determine statistical significance. We used ANOVA in the car package (Fox and Weisberg, 2015; ANOVA function; type III sum of squares) to examine the effects of sex, round goby presence, age, and the interaction of these factors on smallmouth bass length. Age was treated as a categorical factor and sex and round goby time period were treated as binary categorical factors. Once we identified factors that significantly affected smallmouth bass length, we removed all nonsignificant factors and fitted the reduced ANOVA model using the lm function. This allowed us to estimate treatment effects for each model parameter in relation to the base level for each factor (Crawley, 2013). For example, all treatment effects for the age factor (i.e., parameters for ages 3–10) were in relation to the coefficient for an age-2 fish (see Table 1). Results from ANOVA indicated that the interaction between sex and age was an important predictor of length. Therefore, differences in mean length-at-age between pre- and post-round goby time periods were estimated separately for male and female smallmouth bass. Differences in length-at-age between time periods and 95% confidence intervals were estimated using Dunnet's modified Tukey–Kramer test in R

(Lau, 2013; R package: DTK). Significant differences in length-at-age between time periods were observed when 95% confidence intervals did not overlap zero. Dunnett's modified Tukey–Kramer test was selected for estimating differences because of unequal sample sizes between time periods (Table 2). After estimating differences in length-at-age between time periods, sex-specific von Bertalanffy growth models were fitted for the preand post-round goby time periods to investigate the effects of round goby presence on growth patterns of male and female smallmouth bass. Mean length-at-age was described using the equation Lt(s, rg) = L∞(s, rg)(1 − e(−K(s,rg)(t − t0))),where Lt(s,rg) = mean length at age-t for a smallmouth bass of sex s, in round goby time period rg; L∞(s,rg) = mean asymptotic maximum length for a smallmouth bass of sex s, in round goby time period rg; K(s,rg) = the rate that smallmouth

Table 2 Sex, age, time period specific counts of smallmouth bass used in growth and length-at-age analyses. Males

Females

Age

Pre-round goby

Post-round goby

Pre-round goby

Post-round goby

2 3 4 5 6 7 8 9 10 Total

206 286 228 265 136 128 60 54 37 1400

1035 569 266 163 112 92 39 36 13 2325

175 302 226 282 142 139 78 49 37 1430

974 662 340 181 163 122 59 43 14 2558

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

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bass of sex s, in round goby time period rg approaches L∞; and t0 = theoretical constant that represents the age at a mean length of zero. A single t0 value was estimated based on the entire data set and used in each sex and time period specific growth model to simplify between sex and time period comparisons of L∞ and K (parameters of interest). Using a universal t0 value was justified because (1) t0 does not have biological meaning; (2) L∞, K, and t0 are correlated; therefore, using a single value for t0 standardized comparisons among models, and (3) t0 is a constant used to adjust the model for the extrapolated y-intercept (Ogle, 2013). All parameters were estimated using the nonlinear least squares method in R. Ellipse plots of pairwise 95% confidence intervals (Murdoch and Chow, 2013; R package: ellipse) for L∞ and K were created to visualize sex and time period specific parameter estimates. Examination of sex and time period specific mean length-at-age and standard deviations indicated that the assumption of equal variance across ages was met, and a histogram of combined residuals from all four growth models indicated that errors were normally distributed. Results Diet Stomach contents were identified for 142 smallmouth bass in the pre-round goby time period and 345 smallmouth bass in the postround goby time period. Crayfish were the most frequently observed diet item prior to invasion of round goby (observed in 53.5% of stomachs with identifiable prey; Fig. 2). Other macroinvertebrates, clupeids, Morone spp., and rainbow smelt (Osmerus mordax) were also prevalent (Fig. 2). Round goby were the most common prey identified in postinvasion diets (73.3% of diets), and crayfish were observed at a much lower frequency (5.8% of diets) during the post-round goby time period compared to the pre-round goby time period.

Table 3 Analysis of variance table examining factors potentially affecting total length of smallmouth bass from Lake Erie. Age, sex, and round goby were treated as categorical factors. Statistically significant factors at α = 0.05 are in bold. Variable

Sum of squares

Intercept Age Sex Round goby Age × sex Age × round goby Sex × round goby Age × sex × round goby Residuals

10,970,525 5,021,084 658 171,330 8973 68,916 4 6119 3,655,463

Degrees of freedom 1 8 1 1 8 8 1 8 7677

F

P

23,039.7 1318.1 1.4 359.8 2.4 18.1 0.0 1.6

b0.0001 b0.0001 0.2398 b0.0001 0.0158 b0.0001 0.9235 0.1173

bass for ages 2 through 7 (2.8–8.6 mm; Table 1), but slightly shorter for ages 8 through 10 (0.1–8.3 mm; Table 1). Sex-specific von Bertalanffy models also indicated changes in growth of smallmouth bass following round goby invasion (Fig. 5). Parameter estimates for K increased for female and male smallmouth bass, with a greater increase observed for females than males (Fig. 6). Estimates of K prior to invasion of round goby indicated that male smallmouth bass (K = 0.2754) approached their mean asymptotic maximum length at a faster rate than female smallmouth bass (K = 0.2592); however, female smallmouth (K = 0.3375) approached their mean asymptotic maximum at a slightly faster rate than males (K = 0.3288)

Growth and length-at-age Growth and length-at-age analyses were based on data from 7713 smallmouth bass (Table 2). Age, round goby presence, and interactions between age and round goby presence and age and sex were identified as significant factors affecting smallmouth bass length (Tables 1, 3). Length-at-age increased for both male and female smallmouth bass following round goby invasion, and younger smallmouth bass experienced the greatest increases in length (Fig. 3). Time series plots of length-atage for age-2, 3, and 4 smallmouth bass indicated that increases in length-at-age coincided with the invasion of round goby (Fig. 4). Male smallmouth bass tended to be slightly longer than female smallmouth

Fig. 2. Diet (percent occurrence, by count, in non-empty stomachs) of smallmouth bass before and after the invasion of New York waters of Lake Erie by the round goby.

Fig. 3. Estimated differences and 95% CIs for mean lengths-at-age of female (A) and male (B) smallmouth bass following the invasion of New York waters of eastern Lake Erie by the round goby. Differences and 95% CI's were estimated using Dunnett's modified Tukey– Kramer test. Percent change in length-at-age is list above each point. Significantly different lengths-at-age between time periods are indicated by 95% CI's that do not overlap zero.

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

D.P. Crane, D.W. Einhouse / Journal of Great Lakes Research xxx (2016) xxx–xxx

Fig. 4. Estimated mean (±SE) lengths-at-age for age-2, age-3, and age-4 female (A) and male (B) smallmouth bass from New York waters of eastern Lake Erie (1993–2013).

once round goby became available as a food source. The invasion of round goby had contrasting effects on female and male smallmouth bass L∞ estimates. Mean asymptotic maximum length was slightly greater for females (L∞ = 481 mm) than males (L∞ = 473 mm) prior to the invasion of round goby. Following the invasion of round goby, L∞ increased for males and decreased for females, resulting in males (L∞ = 485 mm) having a slightly greater estimated L∞ than females (L∞ = 473 mm; Fig. 5; Fig. 6). Discussion The round goby has substantially affected smallmouth bass growth in eastern Lake Erie. Other factors that typically result in changes in growth such as change in water temperature or compensatory mechanisms are unlikely. Greater than 99% of smallmouth bass included in this study belonged to cohorts hatched from 1987 to 2011; therefore, water temperatures for 1987–2013 can be considered the growing conditions for fish included in the analyses. Observed increases in smallmouth bass growth were not related to water temperature because eastern Lake Erie's mean summer epilimnetic water temperature did not significantly change during 1987–2013 (Fig. 7). Furthermore, examination of the length of age-2–4 fish over time indicates an abrupt increase in length following invasion of round goby (Fig. 4). Compensatory growth mechanisms (e.g., increased growth of smallmouth bass associated with decreased abundance of smallmouth bass) can be ruled out because annual gillnet assessments indicate increased abundance of smallmouth bass ≥ age-2 in eastern Lake Erie following invasion of round goby (Einhouse, 2014). Additionally, abundance of other

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common piscivores in eastern Lake Erie, such as yellow perch (Perca flavescens) and walleye (Sander vitreus), also increased following invasion of round goby (Einhouse, 2014). Therefore, the availability of round goby as a new food resource is the most plausible factor explaining the recent increases in growth of smallmouth bass. The change in diet and increased length-at-age of smallmouth bass following invasion of round goby was likely the result of (1) the abundance of round goby in the preferred habitat of smallmouth bass; (2) reduced foraging, handling, and digestion costs associated with consuming round goby compared to other prey (e.g., crayfish); and (3) differences in energy density between round goby and other prey. The abundance of round goby as a prey may have decreased intraspecific competition for food. Crayfish can also reach high abundances in the rocky habitats preferred by smallmouth bass; however, Carter et al. (2010) observed that smallmouth bass selected for round goby over crayfish at low turbidity levels (0–5 NTU). Since the invasion of dreissenid mussels in Lake Erie, water clarity has dramatically increased, and Secchi depths typically exceed 4.0 m in nearshore areas (Markham, 2014). Therefore, water clarity levels in Lake Erie may have facilitated the transition from a crayfish to round goby dominated diet. Consumption of round goby has likely resulted in complex changes to the bioenergetics of smallmouth bass in eastern Lake Erie. The round goby has a greater energy density (3.2–4.8 kJ/g for 5–50 g wet weight round goby; Johnson et al., 2005b) than crayfish (3.1 kJ/g wet weight; Kelso, 1973), and the chitonous exoskeleton of crayfish has energetic costs during the digestion process that are not incurred when consuming round goby. The body composition of intermolt crayfish ranges from 25 to 65% indigestible matter (by weight), while forage fishes average only 3% indigestible matter (Beauchamp et al., 2007; Stein, 1977). Crayfish also possess defense mechanisms such as chelipeds, which increase foraging costs compared to round goby. Hoyle and Keast (1987) observed that crayfish had the longest handling time of six prey taxa consumed by largemouth bass. Although crayfish have a lower energy density than round goby, round goby are similar to or less energetically rich than prey fishes previously consumed by smallmouth bass (Kelso, 1972; Johnson et al., 2005b; Rand et al., 1994;Strange and Pelton, 1987). However, many of the forage fishes available to smallmouth bass (e.g., emerald shiner (Notropis atherinoides), rainbow smelt, gizzard shad) in Lake Erie are schooling, pelagic, or occupy areas higher in the water column compared to the benthic oriented smallmouth bass. Johnson et al. (2005b) hypothesized that observed increases in mean length-at-age for smallmouth bass and burbot (Lota lota) in Lake Erie were the result of reduced foraging costs associated with round goby. Switching to a diet dominated by round goby, a species readily available in the preferred habitat of smallmouth bass, likely decreased the smallmouth bass' energetic costs of seeking, chasing, or capturing prey. However, the bioenergetic changes associated with switching to a round goby dominated diet are not well understood and warrant further investigation (Robinson, 2015). For example, energy density comparisons between prey species do not necessarily correspond to relationships in total energy content of prey items (i.e., energy content of prey is dependent on size as well as energy density). A more thorough examination of smallmouth diets, compared to this investigation, may provide information necessary to develop a mechanistic understanding of the effects of consuming round goby on smallmouth bass bioenergetics. Increased K values in von Bertalanffy growth models for both male and female smallmouth bass and the observation that increases in length-at-age peaked at age-3 suggest an increased growth rate of juvenile fish following invasion of round goby. Our results corroborate previous findings on the effects of round goby on growth of Great Lakes piscivores. Steinhart et al., (2004a) observed increased growth of age0 smallmouth bass in western Lake Erie following invasion of round goby and concluded that it was the result of round goby facilitating an earlier transition to piscivory. Stapanian et al., (2011) hypothesized that consuming round goby is most beneficial (in terms of somatic

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

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gonads in fall surveys suggests that age-at-maturity has decreased since round goby invaded Lake Erie, and males now mature at ages 2–3 and females mature at ages 3–4 (D. W. Einhouse, NYSDEC, unpublished data). Maturation of smallmouth bass at ages 2–4 explains the peak increase in length for age-3 smallmouth bass in this study. Although we identified a significant interaction between sex and age that affected smallmouth bass length, differences between male and female smallmouth bass mean length-at-age were not large and unlikely to be biologically meaningful. Additionally, differences in L∞ estimates between males and females were similarly small during both time periods. Although L∞ estimates for male and female smallmouth bass were reasonable, they may have been affected by small numbers of age-10 fish in the post-invasion time period (n b 15 for both sexes) and changes in L∞ between time periods should be interpreted with caution. Finally, the interaction between sex and presence of round goby was not identified as an important predictor of length-at-age, indicating that net energetic trade-offs associated with presence of round goby did not differ between males and females (i.e., food resource vs. potential increased energetic costs to nest-guarding males). Because scales were used in addition to otoliths to determine ages of smallmouth bass, there is potential that some age estimates may be inaccurate, particularly for fish N age-6 and b430 mm. Maceina and Sammons (2006) found that scale-based methods for age determination resulted in an underestimation of age for smallmouth bass N age6 compared to otoliths, and lower agreement between readers, particularly for fish N age-4. Given that the greatest observed changes in smallmouth bass length in this study were for fish ages 2–4 and the same individual estimated ages for all samples in this study, we are confident that the observed increases in length-at age were not the result of bias in age estimates. However, because age estimates for fish N age-6 and b 430 mm may be biased, comparisons of length-at-age and von Bertalanffy parameter estimates from this study with estimates from other populations may not be valid. Fig. 5. von Bertalanffy growth models plotted against mean lengths-at-age for female (A) and male (B) smallmouth bass from New York waters of eastern Lake Erie. Separate models were fit for smallmouth bass that lived during the pre- and post-round goby time periods. L∞ and K parameters were allowed to vary for sex and time period, but a single t0 was estimated for all models.

growth) to juvenile burbot because energy available for growth is allocated solely to somatic growth. Although definitive smallmouth bass age-at-maturity data are not available for Lake Erie, examination of

Conclusion The results presented here provide further evidence that transition to a round goby dominated diet has increased growth of juvenile smallmouth bass. Although we focused on eastern Lake Erie, smallmouth bass are likely consuming round goby throughout the Great Lakes–St. Lawrence River and its tributaries (Hirethota, 2015; Johnson et al., 2005b; Reyjol et al., 2010; Steinhart et al., 2004a; Taraborelli et al., 2010), and resource agency reports (Hansen and Kroeff, 2014; Lantry, 2014; McCullough, 2012), peer-reviewed investigations (Crane et al., 2015; Steinhart et al., 2004a), and anecdotal evidence from anglers suggest that changes in growth and body condition of smallmouth bass are widespread. The overall effect of round goby on smallmouth bass in the Great Lakes is not fully realized and is a function of interacting ecological trade-offs. For example, consumption of round goby has increased growth of juveniles and may allow for higher survival from the juvenile stage to maturity, but the benefits of increased survival from the juvenile stage to maturity may be offset by consumption of smallmouth bass eggs by round goby (Steinhart et al., 2004b). Additionally, K is positively correlated with the natural mortality rate of fishes (Pauly, 1980); therefore, increases in growth may result in decreased average longevity. Decreased longevity of fish may have important implications for lifetime fecundity. Consumption of round goby may also affect other life history traits such as age-at-maturity and annual fecundity. Future research should continue to investigate the ecological trade-offs associated with the smallmouth bass-round goby dynamic to better understand the overall effect of a highly abundant invasive species on this important Great Lakes predator. Acknowledgments

Fig. 6. Combined 95% CIs for L∞ and K parameters in von Bertalanffy growth models for female and male smallmouth bass, before and after round goby invaded New York waters of eastern Lake Erie.

We would like to thank the many dedicated NYSDEC employees who were integral in collecting and maintaining the data used in this

Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005

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Fig. 7. Mean June–August epilimnetic water temperatures (°C) for eastern Lake Erie at Buffalo, New York (1987–2013). Data were provided by the National Weather Service (available online: www.erh.noaa.gov/buf/laketemps/laketemps.php). No significant trend in water temperature was observed for 1987–2013 (linear regression; F1,25 = 1.44; P = 0.24).

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Please cite this article as: Crane, D.P., Einhouse, D.W., Changes in growth and diet of smallmouth bass following invasion of Lake Erie by the round goby, J. Great Lakes Res. (2016), http://dx.doi.org/10.1016/j.jglr.2015.12.005