Journal of Great Lakes Research 40 (2014) 712–720

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Journal of Great Lakes Research

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Age and growth of round gobies in Lake Michigan, with preliminarymortality estimation

Bin Huo a, Charles P. Madenjian b,⁎, Cong X. Xie a, Yingming Zhao c, Timothy P. O’Brien b, Sergiusz J. Czesny d

a Huazhong Agricultural University, College of Fisheries, Wuhan, Hubei 430070, Chinab U.S. Geological Survey, Great Lakes Science Center, 1451 Green Road, Ann Arbor, MI 48105, USAc Ontario Ministry of Natural Resources, Aquatic Research and Development Section, 320 Milo Road, Wheatley, ON N0P 2P0, Canadad Illinois Natural History Survey, University of Illinois, Lake Michigan Biological Station, 400 17th Street, Zion, IL 60099, USA

⁎ Corresponding author. Tel.: +1 734 214 7259.E-mail address: cmadenjian@usgs.gov (C.P. Madenjian

http://dx.doi.org/10.1016/j.jglr.2014.07.0030380-1330/Published by Elsevier B.V. on behalf of Interna

a b s t r a c t

a r t i c l e i n f o

Article history:Received 17 March 2014Accepted 17 June 2014Available online 19 July 2014

Communicated by Ed Rutherford

Index words:Age structureGrowth variationMortalityRound gobyTop-down control

The round goby (Neogobius melanostomus) is a prevalent invasive species throughout Lake Michigan, as well asother Laurentian Great Lakes, yet little information is available on spatial variation in round goby growth withinone body ofwater. Age and growth of round goby at three areas of LakeMichiganwere studied by otolith analysisfrom a sample of 659 specimens collected from 2008 to 2012. Total length (TL) ranged from 48 to 131 mm forSturgeon Bay, from 50 to 125 mm for Waukegan, and from 54 to 129 mm for Sleeping Bear Dunes. Ages rangedfrom 2 to 7 years for Sturgeon Bay, from 2 to 5 years for Waukegan, and from 2 to 6 years for Sleeping BearDunes. Area-specific and sex-specific body–otolith relationships were used to back-calculate estimates of totallength at age, which were fitted to von Bertalanffymodels to estimate growth rates. For both sexes, round gobiesat Sleeping BearDunes andWaukegan grew significantly faster than those at Sturgeon Bay. However, round gobygrowth did not significantly differ between Sleeping Bear Dunes andWaukegan for either sex. At all three areas ofLake Michigan, males grew significantly faster than females. Based on catch curve analysis, estimates of annualmortality rates ranged from 0.79 to 0.84. These relatively high mortality rates suggested that round gobiesmay be under predatory control in Lake Michigan.

Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction

Development of global transportation and trade has led to an ac-celerating pace of biological invasions, causing an increasing level ofecological and economic concern (Mack et al., 2000; Pimentel et al.,2005). Understanding the nature and consequences of these inva-sions continues to be an urgent challenge for the scientific communi-ty (Kolar and Lodge, 2001; Sakai et al., 2001). An influx of alienspecies from the Ponto-Caspian Region of Eurasia (Claudi andRavishankar, 2006) has resulted from the discharge of ballast waterinto the Laurentian Great Lakes by transoceanic ships. In the lasttwo decades, these invasive species have become incorporated intoGreat Lakes food webs (Ricciardi and MacIsaac, 2000). The roundgoby (Neogobius melanostomus), which was first observed in the St.Clair River in 1990 (Jude et al., 1992), is one of these invasive species.As a result of shipping ballast transport, recreational anglers, andnatural dispersal, this species has spread into all five LaurentianGreat Lakes (Bronnenhuber et al., 2011; Brown and Stepien, 2009;LaRue et al., 2011; Schaeffer et al., 2005; Steingraeber and Thiel,2000; Walsh et al., 2007), and has also colonized tributary streams

).

tional Association for Great Lakes Re

and rivers (Kornis and Vander Zanden, 2010; Krakowiak andPennuto, 2008; Phillips et al., 2003).

Establishment of the round goby in new habitats is likely due to itsdiverse diet and its tolerance of a wide range of environmental condi-tions including depths, substrata, salinities, oxygen deficiencies, and adiverse diet (Charlebois et al., 2001). Moreover, their behavioral andreproductive characteristics have allowed round gobies to quickly in-crease in number and become a significant component of Great Lakesfood webs (Corkum et al., 1998; Johnson et al., 2005; Kornis et al.,2012; MacInnis and Corkum, 2000a; Ricciardi and MacIsaac, 2000).Some ecological impacts of the round goby invasions included declinesin native benthic fishes due to competition for habitat and dietaryresources (Janssen and Jude, 2001; Jude et al., 1995; Lauer et al.,2004), alteration in benthic communities by removal of invertebratesand cascade effects on benthic plants and nutrient cycles (Kuhns andBerg, 1999), and predation on eggs and fry of certain native fishes(Chotkowski and Marsden, 1999; Phillips et al., 2003; Steinhart et al.,2004). However, much more research is needed to fully determine theeffects of round goby invasions on food webs of the invaded aquaticecosystems.

Understanding life-history characteristics, such as growth, agestructure, and mortality, is vital for evaluating long-term effects ofinvaders on food webs and for developing practical managementtechniques for the control of invaders (Veitch and Clout, 2002). In

search.

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previous studies, round goby growth has been determined bylength–frequency distributions, by back-calculated length at age,and by observed length at age from otoliths (French and Black,2009; Gümüs and Kurt, 2009; MacInnis and Corkum, 2000a,2000b;Phillips et al., 2003; Sokołowska and Fey, 2011; Taraborelli et al.,2010). Results from these studies indicated that size within an agegroup was highly variable and males grew faster and attained a larg-er maximum size than females. Furthermore, life history characteris-tics can vary over the course of an invasion due to different selectionpressures during the early invasion stages (when population densityis volatile) compared with the late invasion stages (when populationdensity is stable). For example, Gruľa et al. (2012) demonstrated thatround gobies in the middle Danube River negative allometric growthin newly established populations, but positive allometric growth inlonger established populations. Lynch and Mensinger (2013) usedmark-recapture methods to investigate seasonal changes in roundgoby growth in Duluth Harbor of Lake Superior. Maximum growthrate was observed during July and August, whereas virtually nogrowth was observed between October and March.

Estimation of round goby mortality rates in invaded aquatic ecosys-tems has been limited to a few studies. Lynch andMensinger (2013) es-timated that round gobies in a confined area of Duluth Harborexperienced an annual mortality of 0.33. Similarly, Vélez-Espino et al.(2010) estimated that annual mortality of round gobies in HamiltonHarbour of Lake Ontario ranged from0.26 to 0.44. Neither of these stud-ies investigated round goby mortality in the non-harbor waters of themain basins of the Laurentian Great Lakes. Annual mortality rate ofround gobies in the central basin of Lake Erie was estimated to be0.62, on average (Bunnell et al., 2005). To date, growth rates andmortal-ity rates for round gobies in Lake Michigan have not been determined.

Although several studies have focused on age and growth of roundgoby in invaded aquatic ecosystems, none have directly investigatedspatial variation in round goby growth within one body of water. Suc-cessful invaders, including the round goby, typically have broad adap-tive abilities indicating high variation in life-history characteristics.Whether life-history variables, e.g. age distribution and growth param-eters, can vary between different locations of the same body of waterremains an open question. The primary goal of our study was to deter-mine whether round goby growth in Lake Michigan showed significantspatial variation. The secondary goal of our studywas to estimate roundgoby mortality rates for Lake Michigan. Our specific objectives were to:(1) age round gobies from three different areas of Lake Michigan usingotoliths, (2) establish body–otolith relationships and growth equationsfor each combination of area and sex, (3) compare growth between thethree areas, (4) compare growth between the sexes, and (5) estimatemortality rates at the three areas using catch curve analysis.

Materials and methods

Round gobies were caught during 2008–2012 in three areas of LakeMichigan, includingWaukegan, Sturgeon Bay, and Sleeping Bear Dunes(Fig. 1). Round gobies fromWaukeganwere caught using graded small-mesh gill nets (mesh sizes of 6, 8, 10, and 12 mm, bar measure), whichwere set at depths of 3–11mwith soak times ranging from 2 to 6 h dur-ing June through October, 2008–2011. Round gobies from Sturgeon Baywere caught during early October 2012 using a 12-m headrope bottomtrawl towed at depths of 46–91 m. Round gobies from Sleeping BearDunes were caught using minnow traps at depths ranging from 10 to20 m from August through September 2012 (Table 1). All fish were im-mediately frozen and transported back to the laboratory. After the spec-imens were thawed, total length (TL) was measured to the nearest1 mm. Sagittal otoliths were extracted, washed with water, air-dried,and then stored in labeled tubes. All individuals were sexed based onthe shape of the urogenital papilla (Kornis et al., 2012).

Both right and left sagittal otoliths were removed from each individ-ual, but usually just the left otolith was used for aging. Otoliths were cut

along the transverse sectioning plane using an IsoMet low speed saw(Secor et al., 1991). Sectioned otoliths were mounted on a glass slideusing clear fingernail polish with anterior–posterior axis perpendicularto the slide plane. The otoliths were then ground using wet sandpaper(600–2000 grit) and polished with alumina paste (3 μm) until thecore was visible under a compound microscope. The otoliths were re-moved from the glass slide by dissolving the fingernail polish with ace-tone, and then the otoliths were re-affixed to the glass slides, with thepolished face down, using fingernail polish. The sectioned otolithswere then ground and polished until the core was exposed again.

Age was estimated by counting annuli on the otolith using a micro-scope (×100) under transmitted light. The reader had no prior knowl-edge of the length, sex, or time of capture before the age estimation.All ages were determined twice by the same reader, with one monthof time elapsing between the two readings. If both readings were inagreement, the agreed-upon age was assigned to the round goby. Ifthe two readings differed, then the otolith was read a third time. If thethird reading did not agree with either of the other readings, then noage assignmentwasmade to the round goby. If the third reading agreedwith one of the previous two readings, the age for which there wasagreement was assigned to the round goby.

A digital picture of each otolith was taken using an Olympus BX51photo-microscope. We measured the distances between successive an-nuli along the central axis of the otolith, which extended from the focusto the ventral edge (Fig. 2). In addition, we measured the distance fromthe latest annulus to the ventral edge of the otolith. Measurements tonearest 0.001 mm were carried out using Imagine Pro Plus V6.0 soft-ware on a personal computer. The relationship between log-transformed total length (TL) and log-transformed otolith radius (OR)was characterized using simple linear regression, and we refer to thisrelationship as the body–otolith relationship in the discussions below.

We used the back-calculation procedure which is based on the pro-portional hypothesis (Francis, 1990) to reconstruct the growth historyof each round goby. This hypothesis states that the ratio of the otolith ra-dius at one age to the otolith radius at another age is a function of thefish length at these two ages. This function could be linear or nonlinear(Francis, 1990). Preliminary analysis of the total length–otolith radiusdata revealed that the logarithm of total length could be described bya linear function of the logarithm of otolith radius. Thus, we back-calculated round goby total lengths at age using the following relation-ship:

TLn ¼ TL � ORn

OR

� �a

where TLn, total length at annulus n; TL, observed total length; ORn,otolith radius at annulus n;OR, otolith radius; a, the slope of linear func-tion between logarithm of total length and logarithm of otolith radius.

For each combination of area and sex, we used simple linear regres-sion analysis to estimate the slope of the body–otolith relationship. Inaddition, we used an F test for equality of slopes to determine if theslopes of the body–otolith relationship differed between the sexes ateach of the three areas. For each sex, we also tested for pairwise differ-ences betweenWaukegan, Sturgeon Bay, and Sleeping Bear Dunes, anda Bonferroni correction was applied to α for these three pairwise com-parisons between areas. Analyses were carried out using R (R coreteam, Vienna Austria), Lab Origin pro 8.5 (Originlab, Northampton,MA, USA), and Photoshop CS5 Extended (Adobe, San Jose, CA, USA).We set α = 0.05 for all of our statistical testing.

For each combination of area and sex,we alsofitted a von Bertalanffygrowthmodel to the total lengths calculated from the above equation. ANewton–Gaussian nonlinear regression algorithmwas used to estimateparameters in the von Bertalanffy growth model. We used the maxi-mum likelihood ratio test, as described by Quinn and Deriso (1999), todetermine whether the fitted von Bertalanffy growth models differedsignificantly between the sexes for each of the three areas. In addition,

Fig. 1. Sampling locations at Sleeping Bear Dunes (circles), Sturgeon Bay (diamonds), and Waukegan (triangles) of Lake Michigan for round gobies used in the aging study.

Table 1Number of round gobies caught at three areas of Lake Michigan on different samplingdates.

Sampling time Number of Samples

Sturgeon Bay Waukegan Sleeping Bear Dunes

Aug-08 50Sep-08 26Oct-08 44Jun-09 1Jul-09 4Sep-09 71Jun-10 1Aug-10 48Sep-10 2Oct-10 11Jun-11 1Sep-11 7Aug-12 81Sep-12 119Oct-12 200Total 200 266 200

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for each sex, we tested for pairwise differences in the fitted vonBertalanffy growth models between Waukegan, Sturgeon Bay, andSleeping Bear Dunes, and a Bonferroni correction was applied to thesethree pairwise comparisons between areas.

Catch curve analysis was used to estimate round goby mortalityrates at the three areas of LakeMichigan (Ricker, 1975).We first identi-fied the age at which the round gobies were fully recruited to the sam-pling gear by examining the catch curves for each of the areas (Quinnand Deriso, 1999; Ricker, 1975). Simple catch curves were used forSleeping Bear Dunes and Sturgeon Bay because the round gobies weresampled for just one year (2012) in both areas (Ricker, 1975); whereas,cohort catch curves were used forWaukegan (Quinn and Deriso, 1999).Because sampling effort varied with year at Waukegan, construction ofcohort catch curves involved calculation of catch per unit effort(CPUE). If sufficient data were available, simple linear regression wasused to fit a regression line to log-transformed catch (or CPUE) at ageas a function of age. Simple linear regression yielded an estimate of in-stantaneousmortality rate Z, and annual survival S is equal to e−Z. How-ever, if only two data points were available on the descending limb of

Fig. 2. Sectioned sagittal otolith of round goby with 131 mm TL and estimated age of7 years. White dots mark the annuli. ORn = annulus radius at age n; OR= otolith radius.

Fig. 3. Total length composition, by sex, of round gobies caught in three areas of LakeMichigan.

715B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

the catch curve, we simply calculated the ratio of catch at the older ageto peak catch or the ratio of CPUE at the older age to peak CPUE to esti-mate annual survival. Annual mortality is equal to 1− S. We were ableto generate annual survival estimates for both the 2005 and 2006 year-classes of round gobies at Waukegan, and we used an average to repre-sent annual survival at Waukegan. Variance of the annual survivalestimate was calculated either by directly estimating the variancearound the mean or by the delta method (Seber, 1982). For a particulararea, variance and standard error (SE) for the annual survival estimatewere equal to variance and SE, respectively, for the annual mortalityestimate.

Results

Length composition

For each sex, size distributions were generally similar among thethree areas (Fig. 3). For females, Sturgeon Bay round gobies ranged intotal length from 48 to 119 mm, with the most dominant classes from70 to 100 mm (Fig. 3). Waukegan round gobies ranged in total lengthfrom 50 to 107 mm, with the most dominant classes from 60 to90 mm, and Sleeping Bear Dunes round gobies ranged in total lengthfrom 55 to 112 mm, with the most frequent classes from 70 to100 mm (Fig. 3).

For males, Sturgeon Bay round gobies ranged in total length from 49to 131mm,with themost frequent classes from 70 to 100mm.Wauke-gan round gobies ranged in total length from 51 to 125 mm, with themost dominant classes from 60 to 100 mm, and Sleeping Bear Dunes

round gobies ranged in total length from 54 to 129 mm, with the mostdominant classes from 70 to 110 mm (Fig. 3).

Age composition

Of 666 otoliths examined, only 7 (approximately 1%) of the roundgobies were not assigned an age due to failure to reach agreementfrom multiple readings. For females, age estimates ranged from 2 to5 years for Sturgeon Bay, from 2 to 6 years for Sleeping Bear Dunes,and from2 to 4 years forWaukegan (Fig. 4). Formales, the age estimatesranged from 2 to 7 years for Sturgeon Bay, from 2 to 5 years for SleepingBear Dunes, and from 2 to 5 years forWaukegan (Fig. 4). Maximum ageswere 6 years and 7 years for females and males, respectively.

Body–otolith relationship

For bothmales and females, slopes of the body–otolith relationshipsdid not significantly differ between the three areas of Lake Michigan(Fig. 5; Table 2). In addition, the slopes for males were significantly

Fig. 4. Age composition, by sex, of round gobies caught in three areas of Lake Michigan.

Table 2Statistial F tests for equality of slopes from the body–otolith relationships among the threeareas of LakeMichigan for each sex; refer to theAREA:ORmodel terms. AREAdenotes area,OR denotes otolith radius and AREA:OR is the interaction term.

Sex ModelTerm

Degrees offreedom

Sum ofsquares

Meansquare

F-value P-value

Female AREA 2 0.1721 0.0861 49.9336 b0.001⁎⁎⁎

OR 1 0.7909 0.7909 458.9773 b0.001⁎⁎⁎

AREA:OR 2 0.0034 0.0017 0.9893 0.373Residuals 347 0.5980 0.0017

Male AREA 2 0.2255 0.1128 50.6040 b0.001⁎⁎⁎

OR 1 1.1019 1.1019 494.4982 b0.001⁎⁎⁎

AREA:OR 2 0.0026 0.0013 0.5864 0.557Residuals 295 0.6574 0.0022

⁎ denotes significance at α = 0.05.⁎⁎ denotes significance at α = 0.01.⁎⁎⁎ denotes significance at α = 0.001.

716 B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

greater than the slopes for females at Sturgeon Bay and Sleeping BearDunes, whereas the slope for males was not significantly differentfrom the slope for females at Waukegan (Table 3). We pooled growth

Fig. 5. Body–otolith relationships of round gobies in Lake Michigan, by area and sex. Linesrepresent fitted regression lines. Symbols represent observed values. TL and OR are mea-sured in millimeters.

data across the three areas to obtain the logarithmic regressionequations for each sex:

for females:

log TLð Þ ¼ 0:946 � log ORð Þ þ 2:008 n ¼ 353;R2 ¼ 0:565� �

:

for males:

log TLð Þ ¼ 1:174 � log ORð Þ þ 2:041 n ¼ 301;R2 ¼ 0:622� �

:

Growth

For both males and females, Sleeping Bear Dunes round gobies andWaukegan round gobies grew significantly faster than Sturgeon Bayround gobies (Fig. 6; Table 4). However, round goby growth did not sig-nificantly differ between Sleeping Bear Dunes andWaukegan for eithersex (Table 4). At all three areas of Lake Michigan, males grew signifi-cantly faster than females (Fig. 6; Table 5). In addition, asymptoticlength, L∞, of males exceeded that of females at all three areas (Table 6).

Mortality

Round gobies fully recruited to the gear at age 3 for Sleeping BearDunes and Waukegan and at age 4 for Sturgeon Bay (Fig. 4). Annualinstantaneous mortality rate from the catch curve analysis for theround goby population at Sleeping Bear Dune was estimated as 1.65

Table 3F tests for equality of slopes from the body–otolith relationships for round gobies betweensexes for each area of LakeMichigan; refer to the Sex:ORmodel terms. OR denotes otolithradius and Sex:OR is the interaction term.

Location ModelTerm

Degrees offreedom

Sum ofsquares

Meansquare

F-value P-value

Sturgeon Bay Sex 1 0.01134 0.01134 6.7300 0.010⁎

OR 1 0.43226 0.43226 256.4584 b0.001⁎⁎⁎

Sex:OR 1 0.01307 0.01307 7.7532 0.006⁎⁎

Residuals 192 0.32362 0.00169Sleeping BearDunes

Sex 1 0.04596 0.04596 23.2452 b0.001⁎⁎⁎

OR 1 0.57815 0.57815 292.3898 b0.001⁎⁎⁎

Sex:OR 1 0.01149 0.01149 5.8085 0.017⁎

Residuals 195 0.38558 0.00198Waukegan Sex 1 0.00048 0.00048 0.2251 0.636

OR 1 0.86148 0.86148 402.2528 b0.001⁎⁎⁎

Sex:OR 1 0.00240 0.00240 1.1221 0.291Residuals 255 0.54612 0.00214

⁎ Denotes significance at α = 0.05.⁎⁎ Denotes significance at α = 0.01.⁎⁎⁎ denotes significance at α = 0.001.

Fig. 6. Fitted von Bertalanffy growth curves, by sex, for round gobies caught in three areasof Lake Michigan. Symbols represent back-calculated total lengths.

Table 5Growth variation tests for round gobies between sexes for each area in Lake Michigan.

Statistic Sturgeon Bay Sleeping Bear Dunes Waukegan

Male–female Male–female Male–female

Ln(LF) −2259.3778 −1984.2349 −1972.3807Ln(LR) −2235.2493 −1929.1988 −1986.7654χ2 48.2570 110.0722 28.7694Degrees of freedom 3 3 4P-value b0.001⁎⁎⁎ b0.001⁎⁎⁎, ⁎ b0.001⁎⁎⁎,⁎⁎

LF denotes maximum likelihood ratio for full model. LR denotes maximum likelihood ratiofor reduced model.⁎ Denotes significance at α = 0.05.⁎⁎ Denotes significance at α = 0.01.⁎⁎⁎ Denotes significance at α = 0.001.

717B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

(SE = 0.02); and thus the annual survival and annual mortality rateswere 0.19 and 0.81 (SE = 0.004), respectively (Fig. 7). The R2 valuefor the fitted regression line in Fig. 7 was 0.9998, and the slope of thefitted regression line was significantly less than zero (t test: t =−74.17; df= 1; P= 0.0086). The annual survival and annual mortalityrates at Waukegan were estimated to be 0.16 and 0.84 (SE = 0.03), re-spectively. Annual survival and annual mortality rates at Sturgeon Baywere estimated to be 0.21 and 0.79, respectively. Only two pointswere available on the descending limb of the catch curves forWaukeganand Sturgeon Bay round gobies. Variances could not be determined forthe survival and mortality estimates for Sturgeon Bay.

Discussion

We documented significant spatial variation in round goby growthwithin Lake Michigan. Round gobies at Sleeping Bear Dunes andWaukegan grew significantly faster than round gobies at SturgeonBay. One plausible explanation for these spatial differences in growthwas that diet composition of round gobies varied across areas of LakeMichigan, and these diet differences were responsible for the growthdifferences. Fish growth is dependent on both the quantity and qualityof the food (Wootton, 1990). Chironomids represented a substantialportion of the diet of round gobies at Sleeping Bear Dunes andWaukegan (Creque and Czesny, 2013; S. Farha, U. S. Geological Survey,Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI

Table 4Growth variation tests for round gobies among three areas for each sex in Lake Michigan.

Location Male

Ln(LF) Ln(LR) χ2 Degrees of freedom P-value

SB-SBD −1807.0094 −1730.733 152.5528 3 b0.0001⁎

SB-WA −1893.3884 −1868.227 50.3228 3 b0.0001⁎

SBD-WA −1919.3620 −1926.859 7.4970 4 0.8880

LR denotes maximum likelihood ratio for reduced model. SB denotes Sturgeon Bay. SBD denot⁎ Denotes significance at α = 0.0166.⁎⁎ Denotes significance at α = 0.0033.

⁎⁎⁎ Denotes significance at α = 0.00033.

49759, personal communication, 5/23/2014); whereas round gobiesfrom Sturgeon Bay predominantly fed on dreissenid mussels(Mychek-Londer et al., 2013). Relatively high handling time and low en-ergy density may render dreissenid mussels of low energy return forround gobies compared with benthic soft-bodied invertebrates, suchas chironomids (Coulter et al., 2011; Diggins et al., 2002; Ruetz et al.,2009). Moreover, mussel shell material, which has a longer retentiontime through the digestive track, may result in artificial satiation thatwould reduce subsequent feeding and ultimately lead to reduced ener-gy intake and growth. In addition, higher energetic costs may be associ-ated with shell breakage and passage through the gut compared withsoft-bodiedmacroinvertebrates (Coulter et al., 2011). Another plausibleexplanation for these spatial differences in growth was that differencesin the water depths occupied by the round gobies between the threeareas led to differences in water temperatures experienced by theround gobies which, in turn, led to growth differences between areas.Round gobies from Sleeping Bear Dunes and Waukegan were caughtin relatively shallow water (3–20 m), whereas the round gobies fromSturgeon Bay were caught in deeper waters (46–91 m). Because LakeMichigan typically has a thermocline depth of about 30 m (Beletskyand Schwab, 2001), round gobies at Sleeping Bear Dunes andWaukeganwould be expected to experience primarily epilimnetic water tempera-tures, while round gobies from the Sturgeon Bay area would beexperiencing primarily hypolimnetic water temperatures, during thesummer. The energetic optimum temperature for round goby growthis 26 °C (Lee and Johnson, 2005), and therefore the round gobies atSleeping Bear Dunes andWaukeganwould be experiencing water tem-peratures closer to the optimal temperature for round goby growthcompared with water temperatures experienced by the Sturgeon Bayround gobies. Other factors, such as round goby population densityand social interactions, may also have contributed to the observed dif-ferences in growth between the three areas of Lake Michigan.

Our mortality estimates suggested that the Lake Michigan roundgoby population was under predatory control. We estimated that age-3 and older round gobies in Lake Michigan experienced annualmortality rates between 0.79 and 0.84. Madenjian et al. (2005) andTsehaye et al. (2014) estimated that age-3 and older alewives (Alosapseudoharengus) in Lake Michigan experienced annual mortality ratesin the same range that we estimated for Lake Michigan round gobies.

Female

Ln(LF) Ln(LR) χ2 Degrees of freedom P-value

⁎⁎ −2436.6033 −2382.0753 109.056 3 b0.0001⁎⁎⁎⁎⁎ −2338.3700 −2290.7170 95.306 3 b0.0001⁎⁎⁎

−2037.2537 −2040.4377 6.368 4 0.8270

es Sleeping Bear Dunes. WA denotes Waukegan.

Table 6Growth model parameters (±SE) for round gobies caught at three areas of Lake Michigan.

Parameter Sturgeon Bay Sleeping Bear Dunes Waukegan

Male Female Male Female Male Female

L∞ (mm) 184.47 ± 23.75 132.85 ± 9.43 142.70 ± 15.24 119.62 ± 7.18 146.54 ± 20.36 120.86 ± 14.48k (year−1) 0.162 ± 0.032 0.263 ± 0.037 0.324 ± 0.066 0.359 ± 0.050 0.295 ± 0.070 0.369 ± 0.091t0 −0.144 ± 0.086 −0.275 ± 0.087 0.075 ± 0.093 −0.144 ± 0.091 0.018 ± 0.089 −0.138 ± 0.125R2 0.907 0.898 0.843 0.856 0.853 0.810n 266 420 251 311 292 283

718 B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

Because modeling studies have shown that alewives in Lake Michiganare under top-down control by salmonines (Madenjian et al., 2002,2005; Stewart et al., 1981; Tsehaye et al., 2014), this similarity betweenour round goby mortality estimates and mortality estimates for LakeMichigan alewives indicated that round gobies may also be under top-down control by piscivores in Lake Michigan. Alewives have been theprimary prey of salmonines in Lake Michigan since the 1960s (Jacobset al., 2013; Madenjian et al., 2005; Tsehaye et al., 2014). Round gobiesin Lake Michigan are preyed upon by a wide variety of piscivores, in-cluding smallmouth bass (Micropterus dolomieu) (T. Galarowicz, CentralMichigan University, personal communication), yellow perch (Percaflavescens) (Truemper et al., 2006), burbot (Lota lota) (Jacobs et al.,2010), and lake trout (Salvelinus namaycush) (McKenna, 2014). More-over, round gobies have recently become an important component ofthe diet of lake whitefish (Coregonus clupeaformis) in Lake Huron(Pothoven and Madenjian, 2013) as well as in Lake Michigan (Lehrer-Brey and Kornis, 2014; S. Hansen,Wisconsin Department of Natural Re-sources, personal communication, 3/13/2014). Undoubtedly, the roundgoby has become an integral part of the Lake Michigan food web. Wealso hypothesize that certain harbors may serve as a refuge from preda-tion for round gobies invading aquatic ecosystems. The relatively lowmortality rates experienced by roundgobies inDuluthHarbor andHam-ilton Harbour can be explained by a low degree of predation on roundgobies in these harbor areas. In contrast, round gobies suffered relativelyhigh mortality in the non-harbor waters of Lake Erie’s central basin, asreported by Bunnell et al. (2005), and in the non-harbor waters ofLake Michigan’s main basin, as documented by our study, and thesehighmortality rates are likely attributable to a high degree of predation.Further, round gobies in the offshore waters of eastern Lake Erie ap-peared to be under predatory control (Madenjian et al., 2011), andthis predatory control was probably accompanied by relatively highmortalities suffered by these round gobies as well. We still must ac-knowledge that, although unlikely, factors other than predation, suchas disease, may have been primarily responsible for these relatively

Fig. 7. Catch curve for round gobies from Sleeping Bear Dunes in Lake Michigan. Roundgobies were caught during August–September, 2012. The fit to catch observations, ages4–6, by simple linear regression analysis yielded an estimate of the instantaneousmortal-ity rate Z. The procedure recommended by Van Den Avyle and Hayward (1999) was usedto fit this regression line to the log-transformed catch data.

highmortality rates observed for round gobies in the non-harborwatersof the main basins of the Laurentian Great Lakes.

Results from our study, in conjunction with results from previousstudies, indicate that the Laurentian Great Lakes round gobies grewslower than Baltic Sea and Ponto-Caspian round gobies (Table 7). Inter-estingly, round gobies from the Ponto-Caspian region, where the roundgoby is native, exhibited slower growth than individuals from the BalticSea, where the round goby has invaded. This slower growth by individ-uals of the native population may be partially due to anthropogenic in-tervention, including commercial exploitation and industrial activities(Sokołowska and Fey, 2011).

The maximum estimated age from our study was 7 years, whichappears to be the oldest age recorded for round gobies (Table 7). This re-cord for the oldest age may be related to our aging method differingfrom previous aging methods. Beamish and McFarlane (1987) notedthat greater longevity is generally recorded with sectioned otoliths,the technique that we used, compared with other techniques to agefish. Comparative studies of scales and otoliths as aging structures inother species demonstrated that scales of old fishes might underesti-mate age relative to otoliths (Beamish and McFarlane, 1987; RochaOlivares, 1998). This is caused by different growth patterns for bothstructures in relation to somatic growth,whichmay influence their abil-ity to reflect annual growth as age increases (Beamish and McFarlane,1987; Casselman, 1990). Besides the aging methods, other factors mayinfluence the estimated longevity. The exploitation history of fish popu-lations affects their demography, and sustained heavy exploitation re-sults in truncated age distributions by eliminating the largestindividuals (Goñi, 1998). Alternatively, environmental conditions andavailability and type of food resources could affect fish growth ratesand thus lengths at age (Wootton, 1990), but not longevity.

We acknowledge that three different gear were deployed to catchthe round gobies used in our study, and that each gear has its own sam-pling bias. Very large (N160 mm in total length) round gobies may nothave been vulnerable to capture in the small-mesh gill nets and min-now traps used in our study. However, at present, these very largeround gobies appear to be in very low abundance in the non-harborwa-ters of the main basin of Lake Michigan, based on data from bottomtrawl survey work (C. P. Madenjian, unpublished data). In addition,the ranges in total lengths of round gobies used for agingwere very sim-ilar across the three gear. Further, the round goby length–frequency dis-tributions were similar across the three gear. Thus, sampling bias withregard to round goby size did not appear to drastically differ betweenthe three gear.

The theory of alternative ontogenies and invasive potential is basedon the assumption that successful invaders benefit from their develop-mental plasticity (Kováč, 2010). A life history that is advantageous atthe beginning of the invasionmay turn into a disadvantage once the in-vading population has become established and achieved a relativelyhigh density. Thus, ontogenies and life histories may eventually trendto more specialized trajectories over time when stable environmentalcondition prevail; whereas, ontogenies may shift towardmore general-ized trajectories when conditions are unpredictable (Geist, 1978; Gruľaet al., 2012). Results from our study indicated that round goby subpop-ulations exist in LakeMichigan because round goby growth showed sig-nificant spatial variation within the lake. These different life history

Table 7Maximum total length (MTL) and total length at age of round gobies from different locations.

Region MTL (mm) TL at age (mm) Source

0 1 2 3 4 5 6 7 Max

Gulf of Gdańsk⁎ 235/187 \ \ 119/94 136/125 146/133 155/144 209/175 \ 6 Sokołowska and Fey (2011)Gulf of Gdańsk⁎ 246/209 \ \ 152 182 212 × \ \ 5 Skóra and Stolarski (1996)Gulf of Gdańsk⁎ 233/220 \ 107/96 144/132 179/157 204/177 \/195 \ \ 4/5 Wandzel (2000, 2003)Gulf of Gdańsk⁎ 250/190 \ 53/54 105/108 158/144 173/159 \ \ \ 4 Sapota (2004)Slovak stretch, Danube River⁎ 143/141 45/45 66/68 84/78 103/94 129/112 \ \ \ 4/4 Gruľa et al. (2012)St Clair River, Michigan⁎ 118 × × × × × × × × × Jude et al. (1992)St Clair River, Canada⁎ 115 × × × × × × × × × Crossman et al. (1992)Upper Detroit River⁎ 124/112 × × × × × × × × 3 MacInnis and Corkum (2000b)Pennsylvania tributary streams, Lake Erie⁎ 112 44 68 80 94 × × × × 4 Phillips et al. (2003)Western Lake Erie⁎ 141 × × × × × × × × × Johnson et al. (2005)Lake Michigan⁎ 131/119 \ \ 70/71 84/80 94/91 108/99 \/111 131/\ 7/6 Present studyCaspian Sea⁎ 190/160 \ 69/63 88/67 111/81 138/85 \ \ \ 4 Nikolski (1956)Azov Sea⁎ 130/140 \ 93/84 102/88 \/95 \ \ \ \ 3 Apanasenko (1973)Black Sea⁎ 130/150 \ 47/54 88/78 104/88 116/114 \ \ \ 4

Data for males and females are separated (/). Lengths reported in the literature as standard length (SL) were converted to total length (TL) using the following equation:TL = 1.1977*SL + 0.4586 (R2 = 0.9932, n = 193) (Kornis et al., 2012). ⁎ denotes that observed length at age was reported. denotes that standard length was converted to total lengthusing the equation in this table heading. × denotes that TL at age was not reported. \ denotes that no data were available.

719B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

characteristics (e.g., growth rates) in the Lake Michigan round gobysubpopulations, as well as in subpopulations of other invaders, reflectresponses of the subpopulations to different selection pressures relatedto length of time since the start of the invasions.

Our study represented an important step in better understandingthe role of the invasive roundgobywithin the LakeMichigan ecosystem.Estimates of growth and mortality are essential in developing fish pop-ulation models (Quinn and Deriso, 1999), and our results providedthese estimates. Further, we envision the eventual development of acoupling of a round goby population model with population modelsfor the predators of round gobies, using an approach similar to that ofTsehaye et al. (2014) for alewives and salmonines in Lake Michigan, toquantify this predator–prey interaction in the LakeMichigan ecosystem.Such a computer simulation model would not only be invaluable in de-fining the contribution of round gobies to energy flow within the LakeMichigan ecosystem, but it may also provide insights into improvingcontrol of round goby abundance in Lake Michigan. Any invasion pro-cess can be broken down into four phases: entry, establishment, spread,and impact (Andersen et al., 2004). Moreover, the impact phase can befurther characterized as either low impact (persistence and integrationinto the food web without significant alteration of the food web struc-ture) or high impact (significant alteration of the food web structure).The difference between low and high impacts in the LakeMichigan eco-system may depend on the amount of energy flowing between theround goby population and populations of predators on round gobies,and this amount of energy flow can be estimated from application of apredator–prey simulation model similar to the one used by Tsehayeet al. (2014). Our results indicated that the round goby invasion ofLake Michigan is in the impact phase, as round gobies appear to beunder predatory control in Lake Michigan. Campbell et al. (2009)contended that round gobies have a high impact on energy flowwithinthe eastern Lake Erie littoral food web. Further assessment of the pred-ator–prey trophic linkbetween predators of round gobies and the roundgoby population could possibly show a high degree of impact of roundgobies on the Lake Michigan ecosystem.

Acknowledgments

We thank Brian Maitland, Kelley Smith, Ryan Darnton, and SteveFarha for providing round gobies from Sleeping Bear Dunes; SaraThomas andWilliam Stacy for providing round gobies fromWaukegan;Tim Desorcie and Melissa Kostich for providing round gobies fromSturgeon Bay; Margret Chriscinske and Pat Hudson for assisting withthe use of the microscope-camera system; Jason Ross for preparingthe map; and Brian Weidel for reviewing a draft of the manuscript

and providing comments for its improvement. This study was funded,in part, by the Chinese Scholarship Council. Use of trade, product, orfirm names does not imply endorsement by the U. S. Government.This article is Contribution 1865 of the U. S. Geological Survey GreatLakes Science Center.

References

Andersen, M.C., Adams, H., Hope, B., Powel, M., 2004. Risk assessment of invasive species.Risk Anal. 24, 787–793.

Apanasenko, M.N., 1973. Age and size of round goby Neogobius melanostomus (Pallas)from different regions of the Azov and Black seas. Biol. Moria. 31, 98–106.

Beamish, R.J., McFarlane, G.A., 1987. Current trends in age determination methodology.In: Summerfelt, R.C., Hall, G.E. (Eds.), Age and Growth of Fish. Iowa State UniversityPress, Ames, pp. 15–42.

Beletsky, D., Schwab, D.J., 2001. Modeling circulation and thermal structure in LakeMichigan: annual cycle and interannual variability. J. Geophys. Res. 106, 19745–19771.

Bronnenhuber, J.E., Dufour, B.A., Higgs, D.M., Heath, D.D., 2011. Dispersal strategies, sec-ondary range expansion and invasion genetics of the nonindigenous round goby,Neogobius melanostomus, in Great Lakes tributaries. Mol. Ecol. 20, 1845–1859.

Brown, J.E., Stepien, C.A., 2009. Invasion genetics of the Eurasian round goby in NorthAmerica: tracing sources and spread patterns. Mol. Ecol. 18, 64–79.

Bunnell, D.B., Johnson, T.B., Knight, C.T., 2005. The impact of introduced round gobies(Neogobius melanostomus) on phosphorus cycling in central Lake Erie. Can. J. Fish.Aquat. Sci. 62, 15–29.

Campbell, L.M., Thacker, R., Barton, D., Muir, D.C.G., Greenwood, D., Hecky, R.E., 2009. Re-engineering the eastern Lake Erie littoral food web: the trophic function of non-indigenous Ponto-Caspian species. J. Great Lakes Res. 35, 224–231.

Casselman, J.N., 1990. Growth and relative size of calcified structures of fish. Trans. Am.Fish. Soc. 119, 673–688.

Charlebois, P.M., Corkum, L.D., Jude, D.J., Knight, C., 2001. The round goby (Neogobiusmelanostomus) invasion: current research and future needs. J. Great Lakes Res. 27,263–266.

Chotkowski, M.A., Marsden, J.E., 1999. Round goby and mottled sculpin predation on laketrout eggs and fry: field predictions from laboratory experiments. J. Great Lakes Res.25, 26–35.

Claudi, R., Ravishankar, T., 2006. Quantification of risks of alien species introductions as-sociated with ballast water discharge in the Gulf of St. Lawrence. Biol. Invasions 8,25–44.

Corkum, L.D., MacInnis, A.J., Wickett, R.G., 1998. Reproductive habits of round gobies.Great Lakes Res. Rev. 3, 13–20.

Coulter, D.P., Murry, B.A., Webster, W.C., Uzarski, D.G., 2011. Effects of dreissenid mussels,chironomids, fishes, and zooplankton on growth of round goby in experimentalaquaria. J. Freshw. Ecol. 26, 155–162.

Creque, S.M., Czesny, S.J., 2013. Growth and survival rate of nearshore fishes in LakeMichigan. Illinois Natural History Survey Tech. Rep., 24 (Champaign).

Crossman, E.J., Holm, E., Cholmondeley, R., Tuininga, K., 1992. First record for Canada ofthe rudd, Scardinius erythrophthalmus, and the round goby, Neogobius melanostomus.Can. Field Nat. 106, 206–209.

Diggins, T.P., Kaur, J., Chakraborti, R.K., DePinto, J.V., 2002. Diet choice by the exotic roundgoby (Neogobius melanostomus) as influenced by prey motility and environmentalcomplexity. J. Great Lakes Res. 28, 411–420.

Francis, R.I.C.C., 1990. Back-calculation of fish length: a critical review. J. Fish Biol. 36,883–902.

French III, J.R.P., Black, M.G., 2009. Maximum length and age of round gobies (Apolloniamelanostomus) in Lake Huron. J. Freshw. Ecol. 24, 173–175.

720 B. Huo et al. / Journal of Great Lakes Research 40 (2014) 712–720

Geist, V., 1978. Life Strategies, Human Evolution, Environmental Design: Toward a Biolog-ical Theory of Health. Springer Verlag, New York.

Goñi, R., 1998. Ecosystem effects of marine fisheries: an overview. Ocean Coast. Manag.40, 37–64.

Gruľa, D., Balážová, M., Copp, G.H., Kováč, V., 2012. Age and growth of invasive roundgoby Neogobius melanostomus from middle Danube. Cent. Eur. J. Biol. 7, 448–459.

Gümüs, A., Kurt, A., 2009. Age structure and growth by otolith interpretation of Neogobiusmelanostomus (Gobiidae) from Southern Black Sea. Cybium 33, 29–37.

Jacobs, G.R., Madenjian, C.P., Bunnell, D.B., Holuszko, J.D., 2010. Diet of lake trout andburbot in northern Lake Michigan during spring: evidence of ecological interaction.J. Great Lakes Res. 36, 312–317.

Jacobs, G.R., Madenjian, C.P., Bunnell, D.B., Warner, D.M., Claramunt, R.M., 2013. Chinooksalmon foraging patterns in a changing Lake Michigan. Trans. Am. Fish. Soc. 142,362–372.

Janssen, J., Jude, D.J., 2001. Recruitment failure of mottled sculpin Cottus bairdi in CalumetHarbor, southern Lake Michigan, induced by the newly introduced round gobyNeogobius melanostomus. J. Great Lakes Res. 27, 319–328.

Johnson, T.B., Allen, M., Corkum, L.D., Lee, V.A., 2005. Comparison of methods needed toestimate population size of round gobies (Neogobius melanostomus) in westernLake Erie. J. Great Lakes Res. 31, 78–86.

Jude, D.J., Reider, R.H., Smith, G.R., 1992. Establishment of Gobiidae in the Great Lakesbasin. Can. J. Fish. Aquat. Sci. 49, 416–421.

Jude, D.J., Janssen, J., Crawford, G., 1995. Ecology, distribution, and impact of the newlyintroduced round and tubenose gobies on the biota of the St. Clair & Detroit Rivers.In: Munawar, M., Edsall, T., Leach, J. (Eds.), The Lake Huron Ecosystem: Ecology,Fisheries, and Management. SPB Academic Publishing, Amsterdam, pp. 447–460.

Kolar, C.S., Lodge, D.M., 2001. Progress in invasion biology: predicting invaders. TrendsEcol. Evol. 16, 199–204.

Kornis, M.S., Vander Zanden, M.J., 2010. Forecasting the distribution of the invasive roundgoby (Neogobius melanostomus) in Wisconsin tributaries to Lake Michigan. Can. J.Fish. Aquat. Sci. 67, 553–562.

Kornis, M.S., Mercado-Silva, N., Vander Zanden, M.J., 2012. Twenty years of invasion: areview of round goby Neogobius melanostomus biology, spread and ecological impli-cations. J. Fish Biol. 80, 235–285.

Kováč, V., 2010. Developmental plasticity and successful fish invasions. Proceedings of17th International Conference on Aquatic Invasive Species (29 August–2 September2010, San Diego, California, USA).

Krakowiak, P.J., Pennuto, C.M., 2008. Fish and macroinvertebrate communities in tribu-tary streams of eastern Lake Erie with and without round gobies (Neogobiusmelanostomus, Pallas 1814). J. Great Lakes Res. 34, 675–689.

Kuhns, L.A., Berg, M.B., 1999. Benthic invertebrate community responses to round goby(Neogobius melanostomus) and zebra mussel (Dreissena polymorpha) invasion insouthern Lake Michigan. J. Great Lakes Res. 25, 910–917.

LaRue, E., Ruetz, C., Stacey, M., Thum, R., 2011. Population genetic structure of the roundgoby in Lake Michigan: implications for dispersal of invasive species. Hydrobiol 663,71–82.

Lauer, T.E., Allen, P.J., McComish, T.S., 2004. Changes in mottled sculpin and johnny dartertrawl catches after the appearance of round gobies in the Indiana waters of LakeMichigan. Trans. Am. Fish. Soc. 133, 185–189.

Lee, V.A., Johnson, T.B., 2005. Development of a bioenergetics model for the round goby(Neogobius melanostomus). J. Great Lakes Res. 31, 125–134.

Lehrer-Brey, G., Kornis, M.S., 2014. Winter distributional overlap facilitates lake whitefish(Coregonus clupeaformis) piscivory on invasive round gobies (Neogobiusmelanostomus) in Green Bay, Lake Michigan. J. Freshw. Ecol. 29, 153–156.

Lynch, M.P., Mensinger, A.F., 2013. Temporal patterns in growth and survival of the roundgoby Neogobius melanostomus. J. Fish Biol. 82, 111–124.

MacInnis, A.J., Corkum, L.D., 2000a. Fecundity and reproductive season of the round gobyNeogobius melanostomus in the upper Detroit River. Trans. Am. Fish. Soc. 129,136–144.

MacInnis, A.J., Corkum, L.D., 2000b. Age and growth of round goby, Neogobiusmelanostomus in the Upper Detroit River. Trans. Am. Fish. Soc. 129, 852–858.

Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M., Bazzaz, F.A., 2000. Biotic in-vasions: causes, epidemiology, global consequences, and control. Ecol. Appl. 10,689–710.

Madenjian, C.P., Fahnenstiel, G.L., Johengen, T.H., Nalepa, T.F., Vanderploeg, H.A., Fleischer,G.W., Schneeberger, P.J., Benjamin, D.M., Smith, E.B., Bence, J.R., Rutherford, E.S., Lavis,D.S., Robertson, D.M., Jude, D.J., Ebener, M.P., 2002. Dynamics of the Lake Michiganfood web, 1970–2000. Can. J. Fish. Aquat. Sci. 59, 736–753.

Madenjian, C.P., Höök, T.O., Rutherford, E.S., Mason, D.M., Croley, T.E. III., Szalai, E.B.,Bence, J.R., 2005. Recruitment variability of alewives in Lake Michigan. Trans. Am.Fish. Soc. 134, 218–230.

Madenjian, C.P., Stapanian, M.A., Witzel, L.D., Einhouse, D.W., Pothoven, S.A., Whitford, H.L., 2011. Evidence for predatory control of the invasive round goby. Biol. Invasions 13,987–1002.

McKenna, P.R., 2014. Use of Stomach Contents, Fatty Acids, and Stable Isotopes to DetectSpatial Variability in Lake Trout Diets Throughout the Laurentian Great Lakes. Univer-sity of Illinois (Thesis).

Mychek-Londer, J.G., Bunnell, D.B., Stott, W., Diana, J.S., French, J.R.P. III., Chriscinske, M.A.,2013. Using diets to reveal overlap and egg predation among benthivorous fishes inLake Michigan. Trans. Am. Fish. Soc. 142, 492–504.

Nikolski, G., 1956. Detailed Ichthyology. Państwowe Wydawnictwo Rolniczei Lesne,Warsaw.

Phillips, E.C., Washek, M.E., Hertel, A.W., Niebel, B.M., 2003. The round goby (Neogobiusmelanostomus) in Pennsylvania tributary streams of Lake Erie. J. Great Lakes Res.29, 34–40.

Pimentel, D., Zuniga, R., Morrison, D., 2005. Update on the environmental and economiccosts associated with alien-invasive species in the United States. Ecol. Econ. 52,273–288.

Pothoven, S.A., Madenjian, C.P., 2013. Increased piscivory by lake whitefish in Lake Huron.N. Am. J. Fish Manag. 33, 1194–1202.

Quinn, T.J. II., Deriso, R.B., 1999. Quantitative Fish Dynamics. Oxford University Press, NewYork.

Ricciardi, A., MacIsaac, H.J., 2000. Recent mass invasion of the North American Great Lakesby Ponto-Caspian species. Trends Ecol. Evol. 15, 62–65.

Ricker, W.E., 1975. Computation and interpretation of biological statistics of fish popula-tions. Bull Fish. Res. Board Can. 191.

Rocha Olivares, A., 1998. Age, growth, mortality and population characteristics of the Pa-cific red snapper, Lutjanus peru, off the southeast coast of Baja California, Mexico. Fish.Bull. 96, 562–574.

Ruetz III, C.R., Strouse, D.L., Pothoven, S.A., 2009. Energy density of introduced round gobycompared with four native fishes in a Lake Michigan tributary. Trans. Am. Fish. Soc.138, 938–947.

Sakai, A.K., Allendorf, F.W., Holt, J.S., Lodge, D.M., Molofsky, J., With, K.A., Baughman, S.,Cabin, R.J., Cohen, J.E., Ellstrand, N.C., McCauley, D.E., O’Neil, P., Parker, I.M.,Thompson, T.N., Weller, S.G., 2001. The population biology of invasive species.Annu. Rev. Ecol. Syst. 32, 305–332.

Sapota, M.R., 2004. The round goby (Neogobius melanostomus) in the Gulf of Gdańsk – aspecies introduction into the Baltic Sea. Hydrobiol 514, 219–224.

Schaeffer, J.S., Bowen, A., Thomas, M., French, J.R.P. III., Curtis, G.L., 2005. Invasion history,proliferation, and offshore diet of the round gobyNeogobius melanostomus in westernLake Huron, USA. J. Great Lakes Res. 31, 414–425.

Seber, G.A.F., 1982. The Estimation of Animal Abundance, Second ed. Griffin, London.Secor, D.H., Dean, J.M., Laban, E.H., 1991. Manual for Otolith Removal and Preparation for

Microstructural Examination, Vol. 1. Electric Power Research Institute, Palo Alto.Skóra, K.E., Stolarski, J., 1996. Neogobius melanostomus (Pallas 1811) a new immigrant

species in Baltic Sea. In: Styczyńska-Jurewicz, E. (Ed.), Proceedings of the Second In-ternational Estuary Symposium, Vol. 1. Crangon Issue, Gdynia, pp. 101–108.

Sokołowska, E., Fey, D.P., 2011. Age and growth of the round goby Neogobiusmelanostomus in the Gulf of Gdańsk several years after invasion. Is the Baltic Sea anew Promised Land? J. Fish Biol. 78, 1993–2009.

Steingraeber, M.T., Thiel, P.A., 2000. The round goby (Neogobius melanostomus): anotherunwelcome invader in the Mississippi River basin. Trans. N. Am. Wildl. Nat. Res.Conf. 65, 328–344.

Steinhart, G.B., Marschall, E.A., Stein, R.A., 2004. Round goby predation on smallmouthbass offspring in nests during simulated catch-and-release angling. Trans. Am. Fish.Soc. 133, 121–131.

Stewart, D.J., Kitchell, J.F., Crowder, L.B., 1981. Forage fishes and their salmonid predatorsin Lake Michigan. Trans. Am. Fish. Soc. 110, 751–763.

Taraborelli, A.C., Fox, M.G., Johnson, T.B., Schaner, T., 2010. Round goby (Neogobiusmelanostomus) population structure, biomass, prey consumption and mortalityfrom predation in the Bay of Quinte, Lake Ontario. J. Great Lakes Res. 36, 625–632.

Truemper, H.A., Lauer, T.E., McComish, T.S., Edgell, R.A., 2006. Response of yellow perchdiet to a changing forage base in southern Lake Michigan, 1984–2002. J. GreatLakes Res. 32, 806–816.

Tsehaye, I., Jones, M.L., Bence, J.R., Brenden, T.O., Madenjian, C.P., Warner, D.M., 2014. Amultispecies statistical age-structured model to assess predator–prey balance: appli-cation to an intensively managed Lake Michigan pelagic fish community. Can. J. Fish.Aquat. Sci. 71, 627–644.

Van Den Avyle, M.J., Hayward, R.S., 1999. Dynamics of exploited fish populations, In:Kohler, C.C., Hubert, W.A. (Eds.), Inland Fisheries Management in North America,2nd editionAmerican Fisheries Society, Bethesda, Maryland, pp. 127–166.

Veitch, C.R., Clout, M.N., 2002. Turning the tide: the eradication of invasive species: Proceed-ings of the International Conference on Eradication of Island Invasives, No. 27, IUCN.

Vélez-Espino, L.A., Koops, M.A., Balshine, S., 2010. Invasion dynamics of round goby(Neogobius melanostomus) in Hamilton Harbour, Lake Ontario. Biol. Invasions 12,3861–3875.

Walsh, M.G., Dittman, D.E., O’Gorman, R., 2007. Occurrence and food habits of the roundgoby in the profundal zone of southwestern Lake Ontario. J. Great Lakes Res. 33, 83–92.

Wandzel, T., 2000. The fecundity and reproduction of round goby Neogobiusmelanostomus (Pallas, 1811) in the Puck Bay (Baltic Sea). Bull. Sea. Fish. Inst. 2, 43–51.

Wandzel, T., 2003. The round goby Neogobius melanostomus (Pallas, 1811) — a new com-ponent of the southern Baltic ichthyocenosis. Its roles in ecosystem and fisheries. Sea.Fish. Inst. Gdynia. Monograph.

Wootton, R.J., 1990. Ecology of Teleost Fishes. Chapman & Hall, New York.