A Comparison of Grass Carp Population Characteristics Upstream and Downstream of Lock and Dam 19 of the Upper Mississippi River

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A comparison of Grass Carp population characteristics upstream and downstream of Lock and Dam 19 of the Upper Mississippi River

Christopher J. Sullivan Iowa State University

Michael J. Weber Iowa State University, [email protected]

Clay L. Pierce U.S. Geological Survey, [email protected]

Carlos A. Camacho Iowa State University

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This Article is brought to you for free and open access by the Natural Resource Ecology and Management at Iowa State University Digital Repository. It has been accepted for inclusion in Natural Resource Ecology and Management Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. A comparison of Grass Carp population characteristics upstream and downstream of Lock and Dam 19 of the Upper Mississippi River

Abstract Grass Carp Ctenopharyngodon idella have been intentionally stocked for aquatic vegetation control across the Midwestern United States for several decades. During the 1970s, escapement of Grass Carp into the Missouri River facilitated their naturalization into much of the Mississippi River basin, including the Upper Mississippi River. Lock and Dam 19 (LD19) in Keokuk, Iowa, is a high-head dam that represents a focal point for naturalized Grass Carp management where populations may differ between upstream and downstream pools as result of limited upstream migration, but potential differences between populations have yet to be evaluated to the best of our knowledge. The objective of this study was to compare the relative abundance, size structure, condition, growth, and recruitment variability of Grass Carp collected upstream and downstream of LD19. We sampled Grass Carp monthly (April–October) during 2014 and 2015 from four locations in the Des Moines River (downstream of LD19) and five locations throughout the Skunk, Iowa, and Cedar rivers (upstream of LD19) using boat electrofishing and trammel net sets. We captured 29 Grass Carp upstream of LD19 compared with 179 individuals captured downstream. Trammel nets only captured Grass Carp downstream of LD19; trammel net catch per unit effort upstream of LD19 was low and ranged from 0.0 to 8.0 fish/net lift (mean 6 SE¼0.39 6 0.13). Electrofishing catch per unit effort ranged from 0.0 to 22.7 fish/h (1.49 6 0.30) and was higher downstream (2.42 6 0.30) of LD19 than upstream (0.57 6 0.07). Grass Carp downstream of LD19 tended to be smaller, younger, of lower body condition, had higher mortality rates, and were slower growing compared with those collected upstream and to populations documented in other systems. Understanding and monitoring adult Grass Carp population characteristics upstream and downstream of LD19 is necessary to determine how they may change in response to ongoing harvest efforts for invasive carps in these river reaches.

Keywords Grass Carp, population characteristics, dam, Mississippi River, invasive

Disciplines Animal Sciences | Ecology and Evolutionary Biology | Natural Resources Management and Policy

Comments This article is published as Sullivan, Christopher J., Michael J. Weber, Clay L. Pierce, and Carlos A. Camacho. "A comparison of Grass Carp population characteristics upstream and downstream of Lock and Dam 19 of the Upper Mississippi River." Journal of Fish and Wildlife Management 11, no. 1 (2020): 99-111. doi:10.3996/062019-JFWM-046.

This article is available at Iowa State University Digital Repository: https://lib.dr.iastate.edu/nrem_pubs/338 Articles A Comparison of Grass Carp Population Characteristics Upstream and Downstream of Lock and Dam 19 of the Upper Mississippi River

Christopher J. Sullivan,* Michael J. Weber, Clay L. Pierce, Carlos A. Camacho

C.J. Sullivan, M.J. Weber, C.A. Camacho Department of Natural Resource Ecology and Management, Iowa State University, 339 Science II, Ames, Iowa 50011

Present address of C.J. Sullivan: Department of Natural Resources and the Environment, University of Connecticut, 1376 Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 Storrs Road, Storrs, Connecticut 06269

C.L. Pierce U.S. Geological Survey, Iowa Cooperative Fish and Wildlife Research Unit, Department of Natural Resource Ecology and Management, Iowa State University, 339 Science II, Ames, Iowa 50011

Abstract Grass Carp Ctenopharyngodon idella have been intentionally stocked for aquatic vegetation control across the Midwestern United States for several decades. During the 1970s, escapement of Grass Carp into the Missouri River facilitated their naturalization into much of the Mississippi River basin, including the Upper Mississippi River. Lock and Dam 19 (LD19) in Keokuk, Iowa, is a high-head dam that represents a focal point for naturalized Grass Carp management where populations may differ between upstream and downstream pools as result of limited upstream migration, but potential differences between populations have yet to be evaluated to the best of our knowledge. The objective of this study was to compare the relative abundance, size structure, condition, growth, and recruitment variability of Grass Carp collected upstream and downstream of LD19. We sampled Grass Carp monthly (April–October) during 2014 and 2015 from four locations in the Des Moines River (downstream of LD19) and five locations throughout the Skunk, Iowa, and Cedar rivers (upstream of LD19) using boat electrofishing and trammel net sets. We captured 29 Grass Carp upstream of LD19 compared with 179 individuals captured downstream. Trammel nets only captured Grass Carp downstream of LD19; trammel net catch per unit effort upstream of LD19 was low and ranged from 0.0 to 8.0 fish/net lift (mean 6 SE ¼ 0.39 6 0.13). Electrofishing catch per unit effort ranged from 0.0 to 22.7 fish/h (1.49 6 0.30) and was higher downstream (2.42 6 0.30) of LD19 than upstream (0.57 6 0.07). Grass Carp downstream of LD19 tended to be smaller, younger, of lower body condition, had higher mortality rates, and were slower growing compared with those collected upstream and to populations documented in other systems. Understanding and monitoring adult Grass Carp population characteristics upstream and downstream of LD19 is necessary to determine how they may change in response to ongoing harvest efforts for invasive carps in these river reaches.

Keywords: Grass Carp; population characteristics; dam; Mississippi River; invasive Received: June 19, 2019; Accepted: December 19, 2019; Published Online Early: January 2020; Published: June 2020 Citation: Sullivan CJ, Weber MJ, Pierce CL, Camacho CA. 2020. A comparison of Grass Carp population characteristics upstream and downstream of Lock and Dam 19 of the Upper Mississippi River. Journal of Fish and Wildlife Management 11(1):99–111; e1944-687X. https://doi.org/10.3996/062019-JFWM-046 Copyright: All material appearing in the Journal of Fish and Wildlife Management is in the public domain and may be reproduced or copied without permission unless specifically noted with the copyright symbol &. Citation of the source, as given above, is requested.

* Corresponding author: e-mail: [email protected]

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Introduction and negative effects (e.g., Maceina et al. 1992) on invaded ecosystems. Native to the region between northern Vietnam and the Throughout the UMR, a series of 29 lock and dams Amur River basin in southern Siberia, Grass Carp Ctenophar- have been erected that regulate river discharge and form yngodon idella are now common throughout much of the a series of slow-moving pools that are more lentic than world (Cudmore and Mandrak 2004). Grass Carp ,200 mm the historical natural lotic discharge regime. Most in length typically feed on chironomidae larvae and larger notably, Lock and Dam 19 (LD19; Keokuk, Iowa) is a zooplankton (Cladocera and Copepoda; Opuszynski 1968; high-head dam that controls water levels at all flows, Watkins et al. 1981) but Grass Carp .270 mm in length are whereas most other UMR lock and dams (with the primarily herbivores, where micro- and macroflora material exception of Lock and Dam 1 near St. Paul, Minnesota) comprise the majority of diets (Michewicz et al. 1972; are tainter and roller gates or a series of tainter gates that Opuszynski 1972; Colle et al. 1978). Adult Grass Carp diets create a more free-flowing river when their gates are rarely deviate from plant material unless food resources open (Knights et al. 2002). Spillways at LD19 are unique become scarce (Bain 1993), which can significantly reduce in that they are elevated approximately 6 m above the

aquatic plant biomass (Bettoli et al. 1993; Schramm and downstream river surface (Wilcox et al. 2004), creating a Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 Brice 2000). Reductions of micro- and macroflora resulting semipermanent barrier, particularly when completely from Grass Carp herbivory can result in limnological open (i.e., velocity barrier), to upstream migration except changes, including increased nutrient and phytoplankton through the navigation lock chambers (Tripp et al. 2014). concentrations and algal biomass, and decreased water Lock and Dam 19 represents the farthest downstream clarity (Maceina et al. 1992). These limnological changes UMR dam where fish movement upstream is restricted to may also affect nativefishes through indirect pathways(e.g., the navigation locks, and invasive carp density is much reduction or elimination of micro- and macroflora) rather higher downstream of LD19 than upstream as a result than directly (e.g., competition or predation). For example, (Camacho et al. 2016; Maher 2016). In addition to limiting native fishes that use vegetated littoral areas as predator fish migration, the creation of slow-moving pools refuge, for foraging, or as nursery habitats have experienced between each dam greatly reduces the amount of decreased population biomass (Shireman and Smith 1983; quality spawning habitat available for many riverine Chilton and Muoneke 1992) as well as increased mortality species, including Grass Carp. During spawning periods via double-crested cormorant Phalacrocorax auritus preda- in the spring and summer when discharge is high, Grass tion (Hubert 1994) following Grass Carp introduction. Carp migrate upstream and often congregate in large Grass Carp show strong preference for aquatic numbers within turbulent, higher velocity river sections vegetation, and so were commonly stocked throughout to spawn (Kolar et al. 2007). In areas such as the dammed the United States from the 1960s to the early 1990s for UMR, these higher velocity river sections are more biological control of aquatic plants (Mitchell and Kelly common immediately downstream of dams, particularly 2006; Kelly et al. 2011). Early stocking efforts targeted LD19 where spawning of Grass Carp and other invasive lakes or reservoirs that were open to stream or river carp has been documented to occur (Camacho 2016). systems, particularly throughout Arkansas, USA, and by Thus, LD19 is considered a key choke point (i.e., limited the 1970s there were numerous reports of Grass Carp in movement upstream and quality spawning habitat the Missouri River (Courtenay et al. 1984). The ability of downstream where fish congregate) for invasive carp Grass Carp to migrate long distances (e.g., Gorbach and population management in the main stem UMR (e.g., Krykhtin 1988) and tolerate a wide range of environ- Larson et al. 2017; Whitledge et al. 2019). mental conditions (e.g., Opuszynski 1967; Bettoli et al. As a result of limited movement through LD19 into 1985; Trimm et al. 1989) has since facilitated their upstream UMR reaches, Grass Carp populations are introduction and naturalization into many large Midwest- hypothesized to differ upstream and downstream of ern rivers (Pflieger 1978), including the Upper Mississippi LD19. However, no studies have quantified these differ- River (UMR) watershed (Pflieger 1978; NAS 2019). ences beyond interpreting commercial fisheries catch data Naturalized populations of Grass Carp occur throughout (e.g., Maher 2016) to the best of our knowledge. much of the UMR watershed, particularly in river sections Therefore, the primary objective of this study was to bordering Missouri, Illinois, and Iowa (Camacho 2016; assess Grass Carp population characteristics (relative Larson et al. 2017; NAS 2019). However, Grass Carp abundance, size structure, condition, growth, and recruit- populations have yet to reach high densities, unlike ment variability) between populations upstream and other invasive carps inhabiting the UMR (e.g., Silver Carp downstream of LD19. Understanding Grass Carp popula- Hypophthalmichthys molitrix; Irons et al. 2007; Kolar et al. tion characteristics upstream and downstream of this key 2007; Sullivan et al. 2017). For example, fish community choke point is a necessary prerequisite for the develop- monitoring efforts from 1990 to 2017 in Mississippi River ment of effective control and preventative measures (e.g., Pools 8, 13, and 26 using pulsed-DC boat electrofishing MICRA 2017) and should provide the basis for a better captured only 260 Grass Carp (,0.001% of total catch in understanding of an elusive nonnative species. number; LTRM 2019). In addition to low densities, Grass Carp are difficult to capture (Wanner and Klumb 2009a; Study Area Sullivan et al. 2019). As a result, limited information exists on naturalized Grass Carp populations despite their We assessed Grass Carp populations in the four widespread distribution throughout the UMR watershed southernmost major tributaries of the UMR in Iowa

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Figure 1. Locations of the nine sites sampled from April to October 2014 and 2015 used to assess differences in Grass Carp Ctenopharyngodon idella population characteristics upstream (white circle) and downstream (black circle) of Lock and Dam 19 (LD19), a semi-permanent barrier to upstream movement located near Keokuk, Iowa, USA. located both upstream and downstream of LD19: Des believed to pass upstream under most river conditions Moines, Skunk, Iowa, and Cedar rivers (Figure 1). We except during low-discharge periods (J. Euchner, Iowa limited our study to these rivers because they represent Department of Natural Resources, personal communica- most of the farthest upstream UMR pools (Pools 17–20) tion). Starting in either southern Minnesota or central where natural reproduction by Grass Carp has been Iowa, these tributaries drain a substantial portion of documented (Larson et al. 2017), limiting differences north-central to southeastern Iowa. Catchment areas attributable to recruitment. The Des Moines and range between 11,222 km2 (Skunk River) and 37,296 km2 Mississippi river confluence is approximately 6 river (Des Moines River; USGS 2019). In contrast, the Iowa kilometers (km) downstream from LD19 (Pool 20). The River catchment is composed mainly (62%) of the Cedar Skunk and Iowa river confluences with the Mississippi River catchment (20,279 km2; USGS 2019). River are approximately 32 and 69 river km upstream (Pools 18–19), respectively. These rivers have an array of wing dikes and levees and have been channelized to Methods manipulate river discharge. Both the Ottumwa Dam (near Ottumwa, Iowa) on the Des Moines River and Field and laboratory methods Oakland Mills Dam (near Oakland Mills, Iowa) on the We sampled Grass Carp monthly from April to October Skunk River operate to mitigate flooding but fish are 2014 and 2015 at four sites downstream of LD19 in the

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Des Moines River and five sites upstream in the Skunk, surface of the fin ray cross-section to improve clarity. We Iowa, and Cedar rivers (Figure 1). We selected sampling wetted cross-sections with immersion oil to further sites within rivers based on the location of river access improve clarity, and viewed annuli under a dissecting points, logistical constraints, and agency interests. Grass microscope with transmitted light. Each fin ray cross- Carp have been effectively captured using both boat section was independently aged by two experienced electrofishing (Cumming et al. 1975; Wanner and Klumb readers with no knowledge of fish length, estimated age 2009a; Clemens et al. 2016) and stationary trammel nets of other structure, or location. If the readers disagreed, (George and Chapman 2015). Consequently, we used then they jointly decided a common age to ensure both boat electrofishing surveys and trammel net sets confidence in annulus identification. concurrently. At each of the nine sites, we surveyed three fixed sampling locations separated by approximately 1.5 Data analysis river km once per month. Sampling occurred in areas ,4 We grouped Grass Carp population characteristics as m deep (DeGrandchamp et al. 2008) within areas of low either downstream (Des Moines River sites) or upstream velocity (,1.0 m/s; e.g., eddies, dike pools, inside river (Skunk, Iowa, and Cedar river sites) of LD19 for analyses. Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 bends, etc.). Within each fixed sampling location, we first We limited comparisons of Grass Carp population deployed a stationary, multifilament trammel net (2.4-m- characteristics on account of small sample sizes; there- deep inner wall, 1.8-m-deep outer wall, 38.1-m-long, 10- fore, we combined data collected from both 2014 and cm-bar inner mesh) by anchoring one end of the net on 2015 to evaluate location (upstream or downstream of shore and stretching the remaining net toward deeper LD19) differences. Sampling gears represented a combi- water or an opposite shore, restricting fish movement nation of a passive and an active technique and thus out of low-velocity areas. We only deployed trammel catch per unit effort (CPUE) is not directly comparable; nets when current velocity was low enough to avoid therefore, we expressed Grass Carp relative abundance hazardous conditions and decrease the likelihood of net as mean CPUE separately for boat electrofishing and entanglement. Next, we conducted a 15-min daytime trammel net sets and analyzed separately. We calculated boat electrofishing (DC; 4-13 A, 100–500 V, 25% duty boat electrofishing CPUE as average number of Grass cycle, 25 Hz frequency, 60 pulses/s with two netters) Carp captured per hour (fish/hour), whereas we calcu- survey using a ‘‘standardizing by power’’ approach lated trammel net CPUE as average number of Grass (Miranda 2009) parallel to the shoreline. We then Carp captured per net lift (fish/net lift). Preliminary collected the trammel net immediately after each analysis indicated that the CPUE data were zero-inflated electrofishing transect (net set duration ranged between (i.e., many surveys where Grass Carp were not captured), 20 and 30 min). We measured thalweg water tempera- overdispersed, and the number of fish captured per ture (Yellow Springs Instruments 550A; Celsius) and survey was generally low. In these situations, the mean conductivity (EC400 ExStik 2 Conductivity Meter; ls/cm) and variance are often correlated and modeling using a during each monthly sampling event at each site and negative-binomial distribution can rectify these issues obtained mean daily discharge values (cubic meters per (Gardner et al. 1995). Thus, we used a negative-binomial second [m3/s]) on the day of sampling from U.S. generalized linear model to assess differences in monthly Geological Survey gauging stations upstream from each mean Grass Carp CPUE upstream and downstream of sampling location (Table S1, Supplemental Material). LD19. We modeled Grass Carp CPUE data as a count (i.e., We weighed (nearest 1 g) and measured for total number of Grass Carp captured) for a given amount of length (TL; nearest 1 mm) all Grass Carp captured during effort both years of the study. During 2015, we removed the y ~negativebinomialðk 3 u Þ; ð1Þ first pectoral fin ray on each side for age and growth ijk ij ijk analysis. We used pectoral fin rays because the assigned where i represents the month, j represents the location age agreement 61 y is relatively high between pectoral (upstream or downstream of LD19), and k represents the fin ray and otolith age estimates in other closely related individual trammel net or electrofishing survey. The kij carps (e.g., Silver Carp; Seibert and Phelps 2013) and term is the Grass Carp CPUE for month i and location j, have been previously used to age Grass Carp (Wieringa while /ijk is the effort (offset) for month i, location j, and et al. 2017). Furthermore, otoliths collected from a subset trammel net or electrofishing survey k. We used pairwise of Grass Carp throughout this study revealed that annuli comparisons of monthly Grass Carp CPUE ratios (pro- were not easily discernable (CJ Sullivan, unpublished portional changes between months) to compare CPUE data). We air-dried pectoral fin rays (fin ray hereafter) at among months upstream and downstream of LD19. We room temperature for 4 wk following collection before used a post hoc Tukey’s honestly significant difference we processed them. We cut a 1-mm-thick cross-section test using Bonferroni corrections to determine which at the base of the fin ray using a Buehler Isomet low- location (upstream or downstream of LD19) and months speed saw (Isomet Corporation, Springfield, VA). We differed at a significance level a of 0.05. mounted each cross-section to a glass microscope slide We constructed total length (TL) frequency histograms using Crystalbond 509 (Electron Microscopy Sciences). and used a nonparametric Kolmogorov–Smirnov (K–S) We used wetted, 2,000-grit sandpaper to polish the two-sample test to test the null hypothesis that

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cumulative frequency of Grass Carp TL distributions did Kðtt0Þ L ¼ L‘ 1 e þ e ; ð4Þ not differ between gears. Using Grass Carp captured t i downstream of LD19, TL frequency distributions were not significantly different between gears (D ¼ 0.16, P ¼ where Lt is the TL at time t, L‘ is the average asymptotic 0.23), suggesting that both gears captured similar sizes maximum TL, K is the Brody–Bertalanffy growth coeffi- of Grass Carp. Therefore, we used a K–S two-sample test cient, t0 is the x-intercept, and ei is an additive error term. Preliminary growth analysis yield nonsensical results for to test the null hypothesis that cumulative frequency of t due to low numbers of Grass Carp ,3 y of age Grass Carp TL distributions did not differ upstream and 0 captured. The t parameter was fixed at 0 when deriving downstream of LD19 using data combined across gears 0 K and L‘ from the von Bertalanffy model, which can help and years. We set statistical significance at a of 0.05, reduce biases when using sampling gears that are which we Bonferroni-corrected to maintain family-wise selective for large individuals (Gwinn et al. 2010). We error rates of 0.05. We evaluated Grass Carp condition conducted all statistical analyses in Program R Version using a length–weight relationship (Ricker 1975) and 3.2.0 (R Core Team 2016) or SAS Version 9.2 (SAS

used an analysis of covariance (ANCOVA) of weight to Institute, Cary, NC) with a significance level of a ¼ 0.05. Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 assess potential differences in condition between populations located both upstream and downstream of LD19 Results using log10length as a covariate. Using age-frequency distributions, we evaluated loca- Data collected for this project are available in tion-specific (upstream or downstream of LD19) interan- electronic format (Data S1, Supplemental Material). We nual recruitment variability using the recruitment conducted 95.7 electrofishing hours and 198 trammel variability index (RVI; Guy and Willis 1995) calculated as net sets throughout rivers in southeastern Iowa from April to October 2014 and 2015. We captured 179 Grass RVI ¼ ½ðSN=ðNM þ NPÞ NM=NPÞ; ð2Þ Carp at the Des Moines River (downstream of LD19) and captured 29 Grass Carp upstream of LD19 at the Skunk, where S is the sum of the cumulative relative N Iowa, and Cedar rivers (Tables 1, 2). Boat electrofishing frequencies across year-classes in the sample, NM is the captured 144 Grass Carp (Table 1) while trammel nets number of missing year-classes from the sample (year- captured 64 Grass Carp (Table 2). Electrofishing CPUE classes beyond the oldest year-class in the sample are ranged from 0 to 22.7 fish/h (mean 6 SE ¼ 1.49 6 0.3) excluded), NP is the total number of year-classes present while trammel net CPUE ranged from 0 to 8.0 fish/net in the sample, and only included age-5 and older Grass lift (0.46 6 0.15). Mean electrofishing CPUE varied Carp. We estimated instantaneous total mortality rates between locations upstream and downstream of LD19 (Z) for Grass Carp populations upstream and down- (P , 0.001); electrofishing CPUE was higher downstream of LD19 using a weighted, age-based catch-curve stream of LD19 (2.42 fish/h 6 0.30) than upstream (0.57 analysis with age as the independent variable and fish/h 6 0.07). Downstream of LD19, mean electrofish- ln(frequency of catch) as the dependent variable, where ing CPUE varied among months (P , 0.001), where the each data point was weighted by the ln(total catch) of pairwise comparisons of monthly CPUE ratios revealed that age class. The descending limb of age-frequency that catch rates were highest during May and October histograms suggests a full recruitment to the sampling and lowest in July (pairwise comparisons P , 0.001; gears at ages 5 to 6 for Grass Carp. Then, we estimated Figure 2). Grass Carp mean electrofishing CPUE did not vary among months upstream of LD19 (all pairwise total annual mortality rates (A), comparisons P . 0.05). We did not capture Grass Carp A ¼ 1 eZ ; ð3Þ upstream of LD19 using trammel nets, precluding comparisons upstream and downstream of LD19. Mean where Z is the instantaneous total mortality rate. Estimates trammel net CPUE was similar among months (P ¼ 0.06; of A were considered significantly different among sites if all pairwise comparisons P . 0.14), with consistently 95% confidence intervals did not overlap. Differences in lower capture rates from May through September mortality rates could be attributed to both natural and (Figure 2). fishing-induced mortality because variable amounts of Using data combined across gears, Grass Carp TL commercial harvest occurs across sites (e.g., Maher 2016) frequency distributions differed between populations and rates herein likely reflect both sources of mortality. located at sites upstream and downstream of LD19 (D ¼ , We used a weighted, two-way ANOVA to test for site 0.56, P 0.001; Figure 3). Grass Carp TL ranged from 421 to 964 mm (787 mm 6 29) and 0.9 to 11.6 kg (6.4 and age differences in Grass Carp length. If we detected kg 6 0.5) upstream of LD19 and 574 to 996 mm (725 significant differences, we used pairwise t-tests with mm 6 6) and 2.0 to 9.4 kg (4.2 kg 6 0.1) downstream Bonferroni corrections to determine which groups (Tables 1, 2). Grass Carp ,900 mm in length comprised differed. In addition, we estimated growth trajectories 76% of total catches upstream of LD19 and 95% of total of Grass Carp upstream and downstream of LD19 using catches downstream; however, Grass Carp ,500 mm von Bertalanffy models fit to individual length at were only captured upstream of LD19 (n ¼ 4fish).Grass estimated age data using nonlinear least-squares regres- Carp weight-at-length relationships were significantly sion (von Bertalanffy 1938): different between populations located upstream and

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Table 1. Total number (N), mean (61 SE), minimum, and maximum total length (mm) and weight (kg) of Grass Carp Ctenopharyngodon idella captured upstream and downstream of Lock and Dam 19 (LD19) from April to October 2014 and 2015 using boat electrofishing. Located near Keokuk, Iowa, USA, LD19 represents the farthest downstream lock and dam where fish movement upstream is restricted to the navigation locks, creating a semipermanent barrier to upstream movement. Mean Grass Carp length and weight represent mean values across both 2014 and 2015.

Total length (mm) Weight (kg) Location Site N Mean Minimum Maximum Mean Minimum Maximum Downstream LD19 Des Moines River Eddyville 2 743 (627) 716 770 4.9 4.9 4.9 Cliffland 35 711 (613) 615 996 3.9 (60.2) 2.4 9.3 Keosauqua 45 734 (69) 619 892 4.3 (60.1) 2.7 6.3 Keokuk 33 741 (613) 603 986 4.5 (60.2) 3.0 8.2 Upstream LD19 Skunk River Cedar Creek 0 — — — — — —

Blackhawk Bottoms 5 875 (624) 826 941 8.5 (60.9) 6.7 11.6 Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 Iowa River English River 15 744 (644) 428 964 5.5 (60.7) 0.9 10.1 New Boston 2 793 (629) 764 821 6.7 (60.7) 6.0 7.4 Cedar River Conesville 7 812 (669) 421 964 6.6 (61.1) 0.9 10.0

downstream of LD19 (F2, 197 ¼ 21.3, P , 0.001; Figure 4) Discussion with fish captured downstream weighing less at a given length compared with those captured upstream. Difficulties related to capture and low Grass Carp Age-frequency distributions and recruitment variabil- densities offer limited opportunities to formally evaluate ity index scores suggest that Grass Carp recruitment was populations unless substantial effort is allocated toward moderately consistent downstream of LD19 (RVI ¼ 0.53; the collection of Grass Carp (Sullivan et al. 2019). Figure 5) despite missing age classes. Upstream of LD19, Assessments of adult Grass Carp populations have often limited samples (n ¼ 27) precluded the comparison of focused on stocked or introduced populations in the age-frequency distributions between sites; however, the southeastern or eastern United States (Shireman et al. recruitment variability index indicated relatively consis- 1980; Morrow et al. 1997; Stich et al. 2013) with few assessments conducted within the Mississippi River tent recruitment (RVI ¼ 0.41; Figure 5). The Grass Carp watershed (but see Wanner and Klumb 2009a). Lock annual mortality rate (A) for populations captured and Dam 19, a key focal point for naturalized Grass Carp downstream was 0.40 (95% confidence interval: 0.31, management because limited upstream migration oc- 0.49) whereas the mortality rate upstream of LD19, based curs, creates a semipermanent barrier between Grass on a small sample of 27 fish, was 0.10 (95% confidence Carp populations that exhibited different population interval: 0.04, 0.16). Lastly, Grass Carp length-at-age characteristics throughout our study. Grass Carp down- varied by location and age (F1, 107 ¼ 4.98, P ¼ 0.027); fish stream of LD19 tended to be smaller, younger, of lower were consistently longer at a given age upstream body condition, had a higher mortality rate, and were compared with downstream of LD19, with the exception slower growing compared with fish collected upstream. of age 8 and 9 Grass Carp (Figure 6). The von Bertalanffy For an open system like the UMR, it may be possible to growth-parameter estimates for Grass Carp captured reduce propagule pressure by targeting key manage- downstream of LD19 were L‘ ¼ 810 mm and K ¼ 0.42 and ment areas for control like LD19. Commercial fishing L‘ ¼ 916 mm and K ¼ 0.38 for Grass Carp captured efforts already occur upstream and downstream of LD19 upstream. but focus on decreasing abundance and understanding

Table 2. Total number (N), mean (61 SE), minimum, and maximum total length (mm) and weight (kg) of Grass Carp Ctenopharyngodon idella captured upstream and downstream of Lock and Dam 19 (LD19) from April to October 2014 and 2015 using trammel nets. Located near Keokuk, Iowa, USA. LD19 represents the farthest downstream lock and dam where fish movement upstream is restricted to the navigation locks, creating a semipermanent barrier to upstream movement. We did not capture Grass Carp upstream of LD19. Mean Grass Carp length and weight represent mean values across both 2014 and 2015.

Total length (mm) Weight (kg) Des Moines River site N Mean Minimum Maximum Mean Minimum Maximum Eddyville 4 790 (660) 673 950 5.4 (60.9) 3.5 7.6 Cliffland 27 683 (612) 574 856 3.4 (60.2) 2.0 5.7 Keosauqua 0 — — — — — — Keokuk 27a 739 (615) 638 960 4.5 (60.3) 2.8 9.4 a We captured 33 Grass Carp but did not measure or weigh 6 fish.

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(mean CPUE ,0.05 fish/100 m net lift; Wanner and Klumb 2009a) compared with catch rates in the Des Moines River downstream of LD19, but was higher than catch rates in the Skunk, Iowa, and Cedar rivers upstream of LD19 (zero captures). However, those sampling methodologies were designed for the capture of Pallid Sturgeon Scaphirhynchus albus (Wanner and Klumb 2009a), potentially excluding habitats commonly used by Grass Carp (e.g., backwater; Shireman and Smith 1983). In this study, Grass Carp electrofishing CPUE was higher (up to 22.7 fish/h) than values reported throughout literature and at least one Grass Carp was captured in 17.8% of electrofishing surveys (382 total surveys), whereas trammel net CPUE was lower (up to 8.0 fish/

net lift) and Grass Carp were captured in 13.1% of Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 trammel net sets (198 total net sets). Differences in capture rates may be due in part to the active sampling in shallow-water habitats that would not be effectively sampled using trammel nets or the short duration of net sets (20–30 min/set used herein versus overnight sets) that may have limited Grass Carp captures. Additionally, Grass Carp electrofishing CPUE varied intra-annually where catches were highest during May and October compared with other months, especially July. Grass Carp are a highly migratory species (Gorbach and Krykhtin 1988; Bain et al. 1990) and spring spawning migrations or autumn movement patterns could result in seasonal changes in local abundances that would result in higher catch rates (e.g., congregating below a dam). Our results indicate that Grass Carp recruitment was moderately consistent (indicated by RVI values) both upstream and downstream of LD19. Grass Carp are broadcast spawners that release semibuoyant eggs into Figure 2. Mean catch per unit effort (CPUE 6 1 SE) of Grass turbulent flowing water (Verigin et al. 1978; Kolar et al. Carp Ctenopharyngodon idella using both boat electrofishing (top; fish per hour) and trammel nets (bottom; fish per net lift) 2007). Eggs must remain suspended in the water column from April to October 2014 and 2015 downstream (black circle) for 24 to 48 h for successful hatching, which equates to a and upstream (white circle) of Lock and Dam 19, a semiper- drift distance of roughly 15 to 80 river km (Krykhtin and manent barrier to upstream movement located near Keokuk, Gorbach 1981; Garcia et al. 2015). Previous studies have Iowa, USA. Estimates with similar letters represent monthly found that invasive carp reproduction is highest during electrofishing or trammel net catch per unit effort estimates high discharge events (DeGrandchamp et al. 2007; that were not significantly different (a ¼ 0.05). Lohmeyer and Garvey 2009; Sullivan et al. 2018) and have speculated that the impounded UMR may only trends in Silver and Bighead Carp demographics; these offer high-quality spawning conditions during those efforts also capture and remove Grass Carp but do not periods. However, large tributaries of the UMR, such as focus on determining population demographics and the Des Moines, Skunk, Iowa, and Cedar rivers, offer long stretches of free-flowing river where Grass Carp repro- monitoring changes through time (MICRA 2017). For duction has occurred (Camacho 2016), likely leading to removal efforts to work for Grass Carp, it is important to the more consistent recruitment patterns in our study. In understand population status upstream and down- addition, the migratory abilities of Grass Carp (Gorbach stream of these areas to determine appropriate man- and Krykhtin 1988) indicate that migrants from more agement strategies. consistently recruiting populations downstream of LD19 Little information is available documenting Grass Carp (e.g., Larson et al. 2017) could supply a few recruits capture rates throughout their native or introduced periodically, similar to other invasive carp (e.g., Whit- range. Methods such as bow fishing (Morrow et al. 1997; ledge et al. 2019). Placement of deterrents within the Stich et al. 2013) and commercial harvests (Pflieger 1978) navigation locks at LD19 are being considered to reduce have been used to obtain individuals but cannot be used migration of invasive carps and propagule pressures to infer patterns in relative abundance estimates. Within upstream (e.g., Donaldson et al. 2016). We did not the Missouri River basin, standardized sampling surveys determine the natal origin of Grass Carp captured (e.g., trammel, gill, mini-fyke, and hoop nets) have been upstream of LD19; however, further research could be used to estimate Grass Carp relative abundance. conducted to determine if adult Grass Carp upstream of Trammel net CPUE in that system was relatively low LD19 are born upstream of LD19, migrated through

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Figure 3. Total length frequency distributions of Grass Carp Ctenopharyngodon idella captured using both electrofishing (left) and trammel nets (right) during 2014 (black) and 2015 (grey) from upstream (top) and downstream (bottom) of Lock and Dam 19, a semipermanent barrier to upstream movement located near Keokuk, Iowa, USA. n ¼ number of Grass Carp captured.

LD19, or are of hatchery origin (i.e., escapement) to help 1997), Florida, USA (Shireman et al. 1980), and Virginia, inform management decisions. USA (Stich et al. 2013). Grass Carp collected downstream Grass Carp population characteristics described herein of LD19 were of lesser body condition than those varied from those reported for both stocked populations collected from the Missouri River (Wanner and Klumb in lakes and naturalized populations in other Mississippi 2009b) and a Virginia lake (Stich et al. 2013), but Grass River tributaries. Grass Carp captured both downstream Carp upstream of LD19 were of greater body condition. and upstream of LD19 were smaller compared with Grass Carp populations upstream and downstream of populations captured using similar gears from the LD19 are generally smaller, composed younger fish, and Missouri River (mean TL 6 SE ¼ 803 mm 6 6.8; Wanner in lower condition than Grass Carp captured from other and Klumb 2009a) and age structure was younger and lotic and lentic systems, potentially in response to highly represented a more restricted age structure than variable river environments (e.g., Gutreuter et al. 1999) populations in a Virginia lake (Stich et al. 2013). and the greater energetic demands of lotic systems (e.g., Additionally, the mean length-at-age and von Bertalanffy Glebe and Leggett 1981) or due to commercial harvest of parameter estimates for Grass Carp captured both adult Grass Carp through time (Klein et al. 2018). upstream and downstream of LD19 suggests that Grass Grass Carp ,420 mm TL were not captured upstream Carp are smaller, reach the asymptotic length quicker, or downstream of LD19. Currently, Grass Carp reproduc- and reach a smaller maximum size compared with Grass tion is known to occur as far upstream as Pool 12 (Larson Carp captured in South Carolina, USA (Morrow et al. et al. 2017) and did occur within the tributaries sampled

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Figure 4. Weight–length relationship of Grass Carp Ctenophar- yngodon idella captured during 2014 and 2015 using both electrofishing and trammel nets from both upstream (solid line; white circles) and downstream (dashed line; black circles) of Lock and Dam 19, a semipermanent barrier to upstream movement located near Keokuk, Iowa, USA. herein during 2014 and 2015 (Camacho 2016). Thus, smaller sized Grass Carp may be present throughout our sites but went undetected, suggesting that boat electrofishing and trammel nets select for larger sized Grass Carp. Wanner and Klumb (2009a) employed boat electrofishing, trammel nets, hoop nets, gill nets, and mini-fyke nets throughout the Missouri River to collect invasive carp, and mini-fyke nets were the only gear to Figure 5. Age frequency and recruitment variability index (RVI) capture multiple Grass Carp 300 mm TL, although scores of Grass Carp Ctenopharyngodon idella captured during captures were relatively low (,20 captures over 5 y). 2015 from upstream (top, white) and downstream (bottom, Most commonly used sampling gears (e.g., electrofishing black) of Lock and Dam 19, a semipermanent barrier to and trammel nets) require depths of approximately 1.0– upstream movement located near Keokuk, Iowa, USA. Grass 2.0 m and shorelines that are generally free of Carp pectoral fins were aged only during 2015. n ¼ number of obstructions. Smaller sized Grass Carp tend to use areas Grass Carp aged. with a higher density of submerged vegetation (Bain et al. 1990) in currents ,0.05 m/s (Raibley et al. 1995). In the aim to reduce population density and potential up- impounded UMR, fine sediments are trapped in shallow, stream migrants to decrease propagule pressures in low-flow areas, and water turbidity is high, resulting in upstream reaches of the UMR (MICRA 2017). Generally, absent or sparse patches of aquatic vegetation that may commercial fishers employ trammel nets or gill nets to be only available seasonally in shallow habitats (Moore et capture invasive carp (Maher 2016) that select for larger al. 2010). Smaller sized Grass Carp may be locally sized Grass Carp (e.g., Wanner and Klumb 2009a). Grass abundant in these vegetation patches that are generally Carp populations upstream and downstream of LD19 difficult to sample with most sampling gears, but this were generally smaller and slower growing compared remains unknown. Since 2013, Western Illinois University with many other populations; therefore, shifting com- has routinely conducted surveys targeting juvenile mercial harvest efforts to use gears that capture smaller invasive carps in these habitat types throughout the sized Grass Carp may be required, particularly down- UMR, but with few captures reported (JT Lamer, Illinois stream of LD19. Targeting smaller sized invasive carp for Natural History Survey, personal communication). Iden- removal has been suggested as an effective manage- tifying effective gears and capturing smaller sized Grass ment strategy in other UMR rivers (Tsehaye et al. 2013) Carp will allow managers to describe the dynamics of and could lead to a more successful reduction in Grass early life stages across the UMR, knowledge of which is Carp density through time. Further, the lack of historical currently lacking. demographic information about Grass Carp populations The Grass Carp is a widely dispersed nonnative species limits our capacity to determine how populations have throughout the UMR and our study provides important changed since their first detection near LD19 in the insight for management. Lock and Dam 19 represents a 1970s (NAS 2019). However, our study represents the first focal point for management where contract commercial evaluation of Grass Carp population characteristics fishing efforts immediately downstream and upstream within the UMR, establishing a baseline for future

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differences in Grass Carp Ctenopharyngodon idella population characteristics. Found at DOI: https://doi.org/10.3996/062019-JFWM- 046.S2 (24 KB DOCX).

Reference S1. Camacho CA, Sullivan CJ, Weber MJ, Pierce CL. 2016. Distribution and population dynamics of Asian Carp in Iowa rivers. Des Moines: Iowa Department of Natural Resources. Annual Progress Report. Found at DOI: https://doi.org/10.3996/062019-JFWM- 046.S3 (5.22 MB PDF).

Acknowledgments

We thank the numerous undergraduate research techni- Downloaded from http://meridian.allenpress.com/jfwm/article-pdf/11/1/99/2511819/i1944-687x-11-1-99.pdf by guest on 25 May 2021 cians from Iowa State University that helped complete Figure 6. Mean length-at-age estimates of Grass Carp field work, and J. Euchner and K. Bogenschutz (Iowa Ctenopharyngodon idella captured during 2014 and 2015 from Department of Natural Resources) for providing helpful upstream (white circles) and downstream (black circles) of Lock insights about Grass Carp. We thank D. Stich, the and Dam 19, a semipermanent barrier to upstream movement located near Keokuk, Iowa, USA. Error bars represent 95% journal’s anonymous reviewers, and the Associate Editor confidence intervals. See Figure 5 for the number of Grass Carp for their time and comments on earlier drafts of this per estimated age upstream and downstream of Lock and Dam manuscript. This study was funded by the Iowa 19. Department of Natural Resources through contract 14CRDFBGSCHO-0001. This study was performed under evaluations. In the future, managers will be able to track the auspices of Iowa State University Institutional Animal population characteristics through time and can set Care and Use Committee (IACUC) protocol permit 7-13- benchmarks for the success of various management 7599-I, and animals were collected under state permit efforts (e.g., harvest, barriers, etc.). We suggest that SC1037. improved monitoring (e.g., expansion of sampling Any use of trade, product, website, or firm names is for locations, use of gears that are effective in shallow descriptive purposes only and does not imply endorse- vegetated habitats) across several generations, robust ment by the U.S. Government. population abundance estimates, and a better understanding of movement patterns (e.g., frequency of Grass References Carp movement through LD19) enable refining of the management goals for Grass Carp in the UMR and at Bain MB. 1993. Assessing impacts of introduced aquatic LD19. species: Grass Carp in large systems. Environmental Management 17:211–224. Supplemental Material Bain MB, Webb DH, Tangedal MD, Mangum LN. 1990. Movements and habitat use by Grass Carp in a large Please note: The Journal of Fish and Wildlife Management mainstream reservoir. Transactions of the American is not responsible for the content or functionality of any Fisheries Society 119:553–561. supplemental material. Queries should be directed to the Bettoli PW, Maceina MJ, Noble RL, Betsill RK. 1993. corresponding author for the article. Response of a reservoir fish community to aquatic vegetation removal. North American Journal of Data S1. Grass Carp Ctenopharyngodon idella captures Fisheries Management 13:110–124. (e.g., site and date) and individual data (e.g., total length, Bettoli PW, Neill WH, Kelsch WL. 1985. Temperature weight, sex, age) upstream and downstream of Lock and preferences and heat resistance of Grass Carp, Dam 19. Ctenopharyngodon idella (Valenciennes), Bighead Carp, Found at DOI: https://doi.org/10.3996/062019-JFWM- Hypophthalmichthys nobilis (Gray), and their F1 hybrid. 046.S1 (51 KB XLSX). Journal of Fish Biology 27:239–247. Camacho CA. 2016. Asian Carp reproductive ecology Table S1. Mean, maximum (Max), and minimum (Min) along the Upper Mississippi River invasion front. daily river discharge (m3/s; estimates obtained from U.S. Master’s thesis. Ames: Iowa State University. Geological Survey [USGS] gauging stations), water Camacho CA, Sullivan CJ, Weber MJ, Pierce CL. 2016. temperature (8C), and conductivity (lS/cm) measured Distribution and population dynamics of Asian Carp in during sampling occasions from April to October 2014 Iowa rivers. Des Moines: Iowa Department of Natural and 2015 at the nine sampling sites upstream and Resources. Annual Progress Report (see Supplemental downstream of Lock and Dam 19 used to assess Material, Reference S1).

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