Abundance, biomass, and macrophyte consumption by rudd in Buffalo Harbor and the Niagara River, and potential herbivory by grass carp

Journal of Great Lakes Research 41 (2015) 387–395

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Abundance, biomass, and macrophyte consumption by rudd in Buffalo Harbor and the Niagara River, and potential herbivory by grass carp Kevin L. Kapuscinski a,⁎, John M. Farrell b,1, Michael A. Wilkinson c,2 a b c

State University of New York, College of Environmental Science and Forestry, 304 Illick Hall, 1 Forestry Drive, Syracuse, NY 13210, USA State University of New York, College of Environmental Science and Forestry, 250 Illick Hall, 1 Forestry Drive, Syracuse, NY 13210, USA New York State Department of Environmental Conservation, 270 Michigan Avenue, Buffalo, NY 14203, USA

a r t i c l e

i n f o

Article history: Received 20 June 2014 Accepted 16 January 2015 Available online 18 March 2015 Communicated by Tom Stewart Index words: Rudd Abundance Grass carp Macrophyte consumption

a b s t r a c t The invasive rudd and grass carp consume aquatic macrophytes, thereby altering important habitat, creating novel trophic pathways, and adversely affecting indigenous species. We estimated the abundance and biomass of rudd and their consumption of macrophytes in Buffalo Harbor (northeastern Lake Erie) and the upper Niagara River during 2012–2013. We also estimated consumption of macrophytes by hypothetical populations of grass carp equal in biomass to rudd populations. Using mark-recapture methods, we estimated that 2571 (95% CI: 2362–2821) rudd were present in Buffalo Harbor and 142,957 (95% CI: 135,127–151,751) were present in the upper Niagara River. Biomass of rudd was estimated at 1.89 mt (95% CI: 1.73–2.07) in Buffalo Harbor and 100.21 mt (95% CI: 94.72–106.38) in the upper Niagara River. Using observed water temperatures and published consumption rates, we estimated that (1) rudd could have consumed 98 mt of macrophytes in Buffalo Harbor and 5210 mt in the upper Niagara River, and (2) hypothetical populations of grass carp equal in biomass to rudd could consume 96 mt of macrophytes in Buffalo Harbor and 4941 mt in the upper Niagara River. Rudd abundance and biomass are substantial in these two waters, and consumption of aquatic macrophytes by rudd may threaten existing aquatic habitat and restoration projects. Annual standardized surveys of fish and macrophyte assemblages would provide data necessary to monitor rudd populations, detect invasion and reproduction by grass carp, and assess habitat changes resulting from herbivory by these two invasive fishes. © 2015 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

Introduction The Laurentian Great Lakes (hereafter Great Lakes) have a welldocumented history of human-induced invasions by non-indigenous species, and the rate of invasion (one species per 28 weeks) is the highest recorded for any freshwater ecosystem (Ricciardi, 2006). Among the non-indigenous fishes present in the Great Lakes are several species of Eurasian cyprinids, such as goldfish (Carassius auratus; Mills et al., 1993), grass carp (Ctenopharyngodon idella; Chapman et al., 2013), and rudd (Scardinius erythrophthalmus; Klindt, 1991), all of which readily consume aquatic macrophytes (hereafter macrophytes). Consumption of macrophytes by fishes can be substantial in some ecosystems and lead to (1) reductions in macrophyte biomass and changes in assemblage structure (Van Dyke et al., 1984; Lodge, 1991; McKnight and Hepp, 1995), (2) shifts from clear-water macrophyte-dominance to turbid-water phytoplankton-dominance (Hansson et al., 1987; van

⁎ Corresponding author at: School of Biological Sciences, CRW225, Lake Superior State University, 650 W. Easterday Ave., Sault Ste. Marie, MI 49783, USA. Tel.: +1 906 635 2093. E-mail addresses: [email protected], [email protected] (K.L. Kapuscinski), [email protected] (J.M. Farrell), [email protected] (M.A. Wilkinson). 1 Tel.: +1 315 470 6990; fax: +1 315 470 6934. 2 Retired.

Donk and Gulati, 1995; van Donk and Otte, 1996), and (3) limited success or failure of actions aimed at restoration of macrophytes (Moore et al., 2010). Non-indigenous herbivores, especially selective generalists, facilitate invasions by non-indigenous macrophytes (Parker et al., 2006; Nuñez et al., 2010) and contribute to invasional meltdown (Simberloff and Von Holle, 1999). However, the invasional meltdown hypothesis has been challenged in the Great Lakes, at least with respect to the effects of dreissenid mussels (DeVanna et al., 2011). Herbivory can have cascading effects in aquatic ecosystems because macrophytes (1) provide refugia from predation for zooplankton, thereby indirectly affecting the assemblage structure and biovolume of phytoplankton (Schriver et al., 1995), (2) provide critical spawning and nursery habitat for fishes (Balon, 1975), (3) are an important food source for many invertebrates (Newman, 1991) and waterfowl (Baldassarre et al., 2006), and (4) increase sedimentation, reduce turbidity, and reduce phosphorus recycling from sediments and thereby reduce the likelihood of a shift to a turbid-water phytoplankton-dominated state (Madsen et al., 2001; Genkai-Kato and Carpenter, 2005). Despite the importance of macrophytes to the structure and function of aquatic ecosystems, information is extremely limited on the effects of macrophyte-consuming fishes in the Great Lakes. This knowledge gap exists even though the goldfish has been established in the basin since about 1878 (Mills et al., 1993), and the rudd has been established in

http://dx.doi.org/10.1016/j.jglr.2015.02.006 0380-1330/© 2015 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

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K.L. Kapuscinski et al. / Journal of Great Lakes Research 41 (2015) 387–395

the St. Lawrence River since 1989 (Klindt, 1991) and Buffalo Harbor (eastern Lake Erie) and the upper Niagara River at least since 1991 (Kapuscinski et al., 2012a). More recently, a diploid grass carp was captured in Lake Erie off Sandusky, OH (USGS, 2014a). Chapman et al. (2013) documented wild-hatched grass carp in the Sandusky River, Ohio, and four grass carp of unknown origin were captured from New York waters of the Great Lakes, including one each from Scajaquada Creek at the confluence with Black Rock Canal in Buffalo, NY, (17 May 2007; USGS, 2014b), Buffalo Harbor (14 May 2005; M.A. Wilkinson, unpublished data), the lower Niagara River (15 August 2008; M.A. Wilkinson, unpublished data), and Cayuga Creek, a tributary to the Buffalo River (11 April 2010; M.A. Wilkinson, unpublished data). These latter four grass carp were not tested for ploidy, which may have helped determine if they originated from legally authorized introductions of triploid grass carp. Herbivory by invasive fishes may pose a substantial risk to existing aquatic habitat and restoration efforts, especially in nearshore areas and connecting channels of the Great Lakes, which have received increased attention in recent years from researchers, resource managers, and restoration practitioners (Roseman et al., 2014). For example, 1117 of the 2127 projects supported by the Great Lakes Research Initiative fall under the focal areas of “promoting nearshore health” or “restoring wetlands and other habitats” (see http://greatlakesrestoration.us/). Failing to account for the effects of herbivory by invasive fishes will likely jeopardize efforts to protect and restore aquatic habitats where these fishes are established. Therefore, in this paper we use information from the scientific literature and our data collected on wild populations of rudd to estimate consumption of macrophytes. We also extrapolate our findings to hypothetical populations of grass carp at similar levels of biomass to compare the potential consumption of macrophytes by these two invasive fishes. The rudd is a European cyprinid that now has a nearly global longitudinal distribution due to anthropogenic translocations; the rudd ranges from New Zealand to the Midwestern USA and is established on five continents (L. Nico et al., 2014; Froese and Pauly, 2014). The rudd was intentionally introduced into the USA during the late 19th or early 20th century (Burkhead and Williams, 1991; Mills et al., 1993) and has been spread to the waters of at least 21 states, largely due to its popularity in the bait fish industry during the 1980s (L. Nico et al., 2014). Although widespread in the USA, most rudd populations occur at relatively low densities. The populations in Buffalo Harbor and the upper Niagara River are apparent exceptions, based on catch rates of rudd relative to other fishes (Kapuscinski et al., 2012a). The grass carp is indigenous to eastern Asia, but has been introduced into over 50 countries due to its popularity as a food fish and use as a biological control of macrophytes (Shireman and Smith, 1983). The first introduction of grass carp into the USA occurred in 1963 (Stevenson, 1965; Guillory and Gasaway, 1978), and they have subsequently been introduced or spread to at least 46 states and Ontario, Canada (L.G. Nico et al., 2014). However, reproduction by grass carp has only been documented in the Mississippi River Basin, the Texas Gulf Coast drainage, and the Lake Erie Basin (Baerwaldt et al., 2013; Chapman et al., 2013). The rudd is omnivorous, but larger individuals (N about 150 mm) are often herbivorous and consume mostly macrophytes during the growing season (Prejs and Jackowska, 1978; Prejs, 1984; Hicks, 2003; Kapuscinski et al., 2012b). Grass carp ≥ age 1 are herbivorous and apparently consume trace quantities of animal matter incidentally while feeding on plants (Colle et al., 1978; Chilton and Muoneke, 1992). Thus, rudd and grass carp exploit food resources not typically utilized by indigenous fishes in north temperate regions of North America and create novel trophic pathways in the ecosystems they invade. Consumption of macrophytes by rudd in Buffalo Harbor and the upper Niagara River is of particular interest because substantial effort and funding has been dedicated to habitat restoration (USAFERC, 2007). Rudd and grass carp may reduce total macrophyte biomass through consumption, and may alter macrophyte assemblages by feeding

selectively among macrophyte species (Lake et al., 2002; Kapuscinski et al., 2014a; Colle et al., 1978; Wiley et al., 1986; Bowers et al., 1987; Pine and Anderson, 1991). Indigenous macrophytes are less likely to possess anti-herbivore adaptations (e.g., defensive structures or chemical compounds) and may be preferentially consumed by rudd and grass carp over non-indigenous macrophytes, such as Potamogeton crispus, Myriophyllum spicatum, and Butomus umbellatus, which are established in the upper Niagara River (Kapuscinski, unpublished data) and share an indigenous range and evolutionary history with rudd and grass carp. Knowledge about the abundance and biomass of invasive herbivorous fishes, and the biomass of macrophytes they may consume, is critical to the conservation, management, and restoration of indigenous species. Therefore, our objectives were to: (1) estimate the abundance and biomass (wet-weight) of rudd in Buffalo Harbor and the upper Niagara River, (2) estimate the biomass (wet-weight) of macrophytes consumed by rudd, and (3) estimate the biomass (wetweight) of macrophytes consumed by hypothetical populations of grass carp at biomass levels equivalent to those estimated for rudd. There is no evidence to suggest that grass carp, if established, would achieve biomasses less than, equal to, or greater than that estimated for rudd in Buffalo Harbor and the upper Niagara River; therefore, our estimates are only provided for the purpose of comparison. Material and methods We estimated the abundance of rudd using mark-recapture methods. Rudd were captured in Oneida (1.8–2.4 m high with 6.1-m wings, 15.2–121.9-m leaders, and 2.54-cm bar measure mesh) and hoop (0.9–1.2 m high with 6.1-m wings, 15.2–30.5-m leads, and 2.54cm bar measure mesh) style trap-nets during two sample periods (29 May–15 June 2012 and 3–14 June 2013). All trap-nets consisted of a single trap and a single lead, except for one net in the Niagara River that had two traps attached to one lead. During 2012, trap-nets were set at four locations in Buffalo Harbor on 29 May, seven locations in the upper Niagara River during 30–31 May, and emptied on 10 subsequent dates. All nets were removed on 15 June, except for two nets in the upper Niagara River, one of which was removed on 2 June and the other on 8 June. During 2013, Oneida style trap-nets were set at two locations in Buffalo Harbor and three locations in the upper Niagara River on 3 June, emptied on eight subsequent dates, and removed on 14 June. One trap-net in the upper Niagara River was relocated on 11 June 2013, so a total of six locations were sampled in 2013. When nets were emptied, all fish were identified and counted prior to release, and a subsample were measured for total length (TL) and weight. All rudd were examined for marks (fin clips) upon capture, and a fin was removed prior to release if a rudd was unmarked (2012: Buffalo Harbor = right pelvic fin, upper Niagara River = left pelvic fin; 2013: Buffalo Harbor = right pectoral fin, upper Niagara River = left pectoral fin). Rudd were also captured via boat electrofishing (Smith-Root boom shocking boat, pulsed DC, 500–1000 V, 6–12 amps) on 10 dates in 2012 and 11 dates in 2013. Electrofishing runs were conducted along shorelines of Buffalo Harbor and the upper Niagara River by moving in a downstream direction from predetermined starting points. In total, about 23 km of shoreline was surveyed in Buffalo Harbor and 100 km in the upper Niagara River. All rudd captured while electrofishing were examined for marks, and both pelvic fins (2012) or both pectoral fins (2013) were removed, if present, to avoid counting rudd as recaptured more than once. Field examinations of recaptured, finclipped rudd suggested very few instances of any appreciable regrowth of fin tissue. We estimated the abundance of rudd and 95% confidence intervals (CIs) using Schnabel's multiple-census, mark-recapture abundance estimate (Van Den Avyle et al., 1999), with each date that trap-nets were emptied and each electrofishing run serving as a sample period. Only 17 of 1634 recaptured rudd (1%) had both paired fins previously removed and could not be assigned to an original capture location, so

K.L. Kapuscinski et al. / Journal of Great Lakes Research 41 (2015) 387–395

we assumed zero net movement between Buffalo Harbor and the upper Niagara River. We estimated the number of rudd per ha of Buffalo Harbor by dividing our abundance estimate by 443 ha (measured in Google Earth [version7.1.2.2041, Google Inc.] to include all water east of (inside) the breakwalls, excluding the Buffalo River; Fig. 1). We estimated the number of rudd per river km of the upper Niagara River by dividing the abundance estimate by 50 km, which represents the length of the river from the Peace Bridge to Niagara Falls (including both channels around Grand Island; Fig. 1). We estimated the number of rudd per ha of the upper Niagara River by dividing the abundance estimate by 4532 ha, which represents the area of the river from the Peace Bridge to just upstream of Niagara Falls and includes Ontario waters (Wilkinson, 1993). We estimated the biomass (wet-weight) of rudd using the observed length-frequency distribution of rudd captured in trap-nets and a previously published weight-length model (Kapuscinski et al., 2012b). First, we determined the proportion of rudd in 10 mm length-classes that were captured in trap-nets and multiplied these proportions by the

389

estimated abundance. Next, we used the midpoint of each length-class to estimate the weight of rudd in that length-class using the weightlength model of Kapuscinski et al. (2012b). We then summed the weight of rudd from all length-classes to obtain the total biomass estimate. Finally, we calculated 95% CIs for the biomass estimate by substituting the lower and upper 95% CIs of our abundance estimate in the first step described above. We divided the biomass estimate by 443 ha to determine the biomass of rudd per ha in Buffalo Harbor, and divided the biomass estimate by 50 km and 4532 ha to determine the biomass of rudd per river km and per ha of the Niagara River. We estimated the amount of macrophytes (wet-weight) that rudd could have consumed if they were entirely herbivorous using the rudd biomass estimate described above, 2013 daily water temperatures, and consumption rates from a previously published study (Hofer and Niederholzer, 1980). Daily water temperatures were measured at the Buffalo Water Treatment Plant located on Lake Erie at the entrance to the Niagara River (data available from http://www.erh.noaa.gov/buf/ laketemps/laketemps.php). Fig. 1 of Hofer and Niederholzer (1980)

Grand Island

Niagara River

Canada

Peace Bridge

USA

Black Rock Canal

Buffalo Harbor Lake Erie

Fig. 1. Map of Buffalo Harbor (northeastern Lake Erie) and the upper Niagara River indicating trap-net locations used in 2012 (circles), 2013 (triangles), and both years (stars).

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indicates that daily consumption of Zannichellia palustris by rudd was about 9% of body weight at 12 °C, 19% at 16 °C, 36% at 20 °C, and 40.5% at 24 °C. We used these consumption rates because, of the few studies that quantified consumption rates of macrophytes by rudd, Hofer and Niederholzer (1980) used (1) a relatively long acclimation period (two weeks) to laboratory conditions, (2) four different temperatures that were similar to those experienced by rudd in Buffalo Harbor and the upper Niagara River during spring, summer, and fall, and (3) a macrophyte species (Z. palustris) that is structurally similar to two common species in Buffalo Harbor and the upper Niagara River (Najas flexilis and Stuckenia pectinata) that are readily consumed by rudd (Kapuscinski et al., 2012b; Kapuscinski et al., 2014a). Using the consumption rate data of Hofer and Niederholzer (1980), we conducted a logistic regression (SAS Institute Inc., Cary, North Carolina, NLIN Procedure, Gauss– Newton least-squares method) to predict daily consumption (% of body weight), C, based on water temperature, WT, as: C¼

∝ 1 þ β  e−γWT ;

ð1Þ

where α represents the maximum asymptote (starting value = 45), β is a constant (starting value = 20), and γ is the rate of change (starting value = 0.1). The resulting model was: C¼

44:0256 1 þ 319:3  e−0:3523WT ;

ð2Þ

and had a pseudo R2 value (1 − SSE / SST) of 0.989. This equation predicts that rudd would consume a small amount (0.1% of body weight) of macrophytes even at 0 °C. However, we assumed that rudd did not consume macrophytes during January–April and December because live macrophytes were probably rare or absent, and water temperatures (0–6.7 °C) were not conducive for digesting macrophytes (Hofer and Niederholzer, 1980; Prejs, 1984). For the May–November 2013 time period, we estimated daily consumption rates of macrophytes by rudd based on the equation above and observed daily water temperatures. Then, we multiplied these daily consumption rates by our biomass estimate for rudd and summed the values to estimate the total biomass of macrophytes consumed by rudd for each month. Because rudd are often omnivorous, we adjusted monthly consumption estimates downward by multiplying the potential biomass of macrophytes consumed by the mean proportion by weight of macrophytes observed in the stomachs of rudd reported by Kapuscinski et al. (2012b) for May (0.36), June (0.94), July (0.77), and November (0.65). For August, we assumed rudd were completely herbivorous because Kapuscinski et al. (2012b) reported observing macrophytes in each of the 36 rudd they examined that month and a single, small leech (Hirudinea). For September and October, we used the average mean proportion by weight for June–August and November (0.84) to adjust our consumption estimates downward. We estimated the amount of macrophytes (wet-weight) that hypothetical populations of grass carp could consume, should they achieve biomass levels equal to those estimated for rudd, using the daily water temperatures described above and the relative consumption rate equation of Wiley and Wike (1986): C r ¼ ð−2:4596 þ 1:07480  ln WT Þ

ð3Þ

where Cr is the proportion of the daily consumption rate (% of body weight) observed at 25 °C, and WT is the water temperature. Multiplying Cr by 42, the maximum consumption rate at 25 °C observed by Wiley and Wike (1986), yielded a temperature-dependent daily consumption rate. This equation predicts zero consumption at ≤ 9.86 °C, so we assumed that consumption by grass carp would not have occurred during January–April or 12 November–31 December 2013. We multiplied the daily, temperature–dependent consumption rates by our biomass estimates for rudd and summed daily values to estimate total biomass of

macrophytes consumed by a hypothetical population of grass carp on a monthly basis. We used the methods described above to estimate the biomass of macrophytes consumed by rudd and hypothetical populations of grass carp for each year during 2009–2013, in order to understand how annual variability in water temperatures may affect consumption. Consumption was assumed to be zero for rudd during January–April and December of each year, and zero for grass carp when daily water temperatures were ≤ 9.86 °C (generally January through mid-May and mid-November through December). Results We captured, marked, and released 1376 rudd in Buffalo Harbor from 31 May 2012 to 11 July 2013 and 18,883 rudd in the upper Niagara River from 31 May 2012 to 15 October 2013. Rudd comprised 43% of all fishes captured in trap-nets in Buffalo Harbor in 2012 and 59% in 2013, and 93% of all fishes captured in the upper Niagara River in 2012 and 96% in 2013 (Fig. 2). We measured 136 rudd from Buffalo Harbor that averaged 356 mm TL (SE = 3.16, range = 220–441), and 279 rudd from the upper Niagara River that averaged 349 mm TL (SE = 2.76, range = 173–434). The mean length of rudd did not differ between Buffalo Harbor and the upper Niagara River (t-test assuming unequal variances, df = 327, P = 0.056). The length-frequency distributions of rudd from both locations were similar, with the majority of captured fish in the 320–400 mm length classes (Fig. 3). We recaptured a total of 490 rudd in Buffalo Harbor and 1144 in the upper Niagara River during 2012–2013. Based on Schnabel's multiple-census mark-recapture abundance estimate, we estimated that 2571 (95% CI: 2362–2821) rudd were present in Buffalo Harbor (6/ha, 95% CI: 5–6), and 142,957 (95% CI: 135,127–151,751) were present in the upper Niagara River (32/ha, 95% CI: 30–33; 2859 per river km, 95% CI: 2703–3035) during the period sampled (Table 1). We estimated the biomass of rudd in Buffalo Harbor at 1.89 mt (95% CI: 1.73–2.07; 0.004 mt/ha, 95% CI: 0.004–0.005) and 100.21 mt (95% CI: 94.72–106.38) in the upper Niagara River (0.022 mt/ha, 95% CI: 0.021–0.023; 2.00 mt per river km, 95% CI: 1.89–2.13). We estimated that rudd could have consumed about 98 mt of macrophytes in Buffalo Harbor in 2013 and about 5210 mt in the upper Niagara River (Table 2). After adjusting rates of macrophyte consumption by rudd downward to account for omnivory, we estimated that rudd would have consumed about 84 mt of macrophytes in Buffalo Harbor and about 4451 mt in the upper Niagara River (Table 2). A hypothetical population of grass carp, equal in biomass to that estimated for rudd, could consume about 96 mt of macrophytes in Buffalo Harbor and about 4941 mt in the upper Niagara River (Table 3). Mean annual water temperatures differed by as much as 2.0 °C during 2009–2013, and subsequently, the estimated biomass of macrophytes consumed by rudd differed by about 15 mt in Buffalo Harbor and 814 mt in the upper Niagara River (Table 4). Similarly, the estimated biomass of macrophytes consumed by grass carp differed by about 16 mt in Buffalo Harbor and 849 mt in the upper Niagara River. Discussion Our results indicate that the abundance and biomass of invasive rudd are substantial, and the ability of rudd to consume N110 mt of macrophytes annually in Buffalo Harbor and N5900 mt in the upper Niagara River likely threatens existing aquatic habitat. Furthermore, herbivory by rudd may jeopardize the many planned, ongoing, or recently completed projects in Buffalo Harbor and the upper Niagara River that include actions to restore macrophytes (USAFERC, 2007). Both rudd (Lake et al., 2002; Dorenbosch and Bakker, 2011; Kapuscinski et al., 2014a) and grass carp (Edwards, 1974; Wiley et al., 1986; Pine and Anderson, 1991) have been shown to feed selectively, adversely affect macrophyte assemblages, and have cascading effects

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391

Buffalo Harbor 100%

Percent of total catch

80%

60%

Other invasive spp. Native spp. Rudd

40%

20%

0% 2007

2008

2012

2013

Year

Upper Niagara River 100%

Percent of total catch

80%

60%

Other invasive spp. Native spp. Rudd

40%

20%

0% 2007

2008

2012

2013

Year Fig. 2. Percent of total catch of rudd, native species, and other invasive species captured in trap-nets set in Buffalo Harbor and the upper Niagara River. Note: 2007 and 2008 data are from Kapuscinski et al. (2012a).

in aquatic ecosystems (Hansson et al., 1987; van Donk and Gulati, 1995; van Donk and Otte, 1996; Pípalová, 2006; Dibble and Kovalenko, 2009). Selective herbivory by these generalist fishes may cause shifts in biomass and species composition of macrophyte assemblages towards dominance by unpalatable species with greater structural and chemical defenses, such as Ceratophyllum demersum and non-indigenous Butomus umbellatus, Myriophyllum spicatum and Potamogeton crispus. If grass carp establish populations in the Great Lakes, the resulting effects on aquatic habitat will be counter to the goals of restoration projects. Projects aiming to restore macrophytes should include both actions that mitigate herbivory and rigorous evaluations of restoration actions. Rudd and grass carp are likely to spread further within the Great Lakes basin to areas with (1) suitable macrophyte food resources, (2) temperatures conducive to digestion of macrophytes,

(3) macrophytes that can support the phytophilic reproductive requirement of rudd (Schofield et al., 2005), and (4) adequate flow regimes and turbulence to support the riverine reproductive strategy of grass carp (Murphy and Jackson, 2013; Garcia et al., 2013). The populations of rudd in Buffalo Harbor and the upper Niagara River appear to be the most abundant in North America and may serve as a source for invasion into other areas of the Great Lakes. For example, rudd were captured in Long Point Bay, Ontario, and apparently are colonizing Ontario waters of Lake Erie from the east (Gislason et al., 2010). The six-fold difference between our estimates of the density of rudd in the upper Niagara River (32/ha) and Buffalo Harbor (6/ha) shows that rudd populations can thrive in lotic environments, contrary to previous descriptions of the rudd being a lentic species (Johansson, 1987; Lake et al., 2002). Buffalo Harbor is highly industrialized and contains much less vegetated littoral area than the upper Niagara River, so rudd may become more abundant

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35

30 BH UNR

Frequency

25

20

15

10

5

0

Length class (mm) Fig. 3. Length-frequency histograms of rudd populations from Buffalo Harbor (BH; n = 136) and the upper Niagara River (UNR; n = 280) captured in trap-nets during May and June 2012–2013.

in less altered nearshore lentic habitats of the Great Lakes. However, rudd have not become abundant in the Thousand Islands Region of the St. Lawrence River since their first detection there in 1989 (Klindt, 1991), despite the presence of suitable habitat (macrophytes) for spawning and feeding in both lotic and lentic areas. Reducing the abundance of rudd in Buffalo Harbor and the upper Niagara River may reduce emigration rates to other areas of the Great Lakes and to inland waters in New York that are linked to the upper Niagara River via the New York State Canal System. The apparent lack of density-dependent feedbacks on population characteristics of rudd in Buffalo Harbor and the upper Niagara River indicates that abundance may increase and will probably remain high due to low intraspecific competition for food resources and a lack of predation pressure that results from the rudd's rapid growth, large size compared to indigenous piscivores, and laterally-compressed body (Kapuscinski et al., 2012b). Our abundance and biomass estimates for rudd can serve as points of reference for reduction efforts should resource managers determine that reducing rudd populations would be ecologically beneficial. We have shown that rudd are highly susceptible to capture in trap-nets during late spring, and rudd may also be vulnerable to capture during winter via the Judas technique (Bajer et al., 2011), so reducing the abundance of adult rudd seems feasible. Concentrations of contaminants in rudd from the upper Niagara River appear low (Kapuscinski et al., 2014b),

so targeted harvest by commercial or recreational fisheries may not pose a health risk to human consumers. The accuracy of our abundance and biomass estimates for rudd depends, in part, on meeting assumptions associated with markrecapture estimates. For example, mortality, emigration, and immigration rates must be similar among sample periods for marked and unmarked rudd. Conducting abundance estimates using mark-recapture methods in large, open systems like Buffalo Harbor and the upper Niagara River makes assessing adherence to these assumptions difficult. However, our estimates seem reasonable, at least when compared to abundance estimates for other invasive freshwater cyprinids in North America. For example, we marked 53.5% of the estimated population of rudd in Buffalo Harbor and 13.2% of the estimated population in the upper Niagara River. In contrast, Sass et al. (2010) marked about 1.4% of the estimated population of silver carp (Hypophthalmichthys molitrix) in the La Grange Reach of the Illinois River, and Bajer and Sorensen (2012) marked 1.3–11.7% of the estimated number of common carp

Table 2 Estimated biomass (wet-weight, mt) of macrophytes consumed by rudd in Buffalo Harbor and the upper Niagara River in 2013. “Maximum” amounts of macrophytes consumed represent completely herbivorous rudd, whereas “adjusted” amounts account for omnivory as observed by Kapuscinski et al. (2012b). Month

Table 1 Estimated abundance (N), biomass (wet-weight in mt), and associated lower (LCL) and upper (UCL) 95% confidence limits for rudd in Buffalo Harbor and the upper Niagara River in 2012–2013. Note: Rkm = river km. Estimate Buffalo Harbor

Upper Niagara River

N N/ha Biomass (mt) Biomass/ha (mt) N N/Rkm N/ha Biomass (mt) Biomass/Rkm (mt) Biomass/ha (mt)

LCL

UCL

2571 2362 2821 6 5 6 1.89 1.73 2.07 0.004 0.004 0.005 142957 135127 151751 2859 2703 3035 32 30 33 100.21 94.72 106.38 2.00 1.89 2.13 0.02

0.02

0.02

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Maximum amount of macrophytes consumed

Adjusted amount of macrophytes consumed

Buffalo Harbor

Upper Niagara River

Buffalo Harbor

Upper Niagara River

0 0 0 0 3.4 13.6 23.1 22.9 20.0 13.2 2.0 0 98.1

0 0 0 0 179.4 722.5 1224.8 1215.0 1063.3 700.8 104.2 0 5209.9

0 0 0 0 1.2 12.8 17.8 22.9 16.8 11.1 1.3 0 83.8

0 0 0 0 64.6 679.1 943.1 1215.0 893.2 588.7 67.7 0 4451.4

K.L. Kapuscinski et al. / Journal of Great Lakes Research 41 (2015) 387–395 Table 3 Estimated biomass (wet-weight, mt) of macrophytes consumed by hypothetical populations of grass carp equal in biomass to estimates for rudd in Buffalo Harbor and the upper Niagara River. Month

Buffalo Harbor

Upper Niagara River

Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

0 0 0 0 2.6 13.8 22.1 21.5 21.5 13.2 1.1 0 95.8

0 0 0 0 139.0 730.5 1174.9 1142.8 997.0 699.1 58.0 0 4941.3

(Cyprinus carpio) in seven small (33.2–152.0 ha) Minnesota lakes, but 79.5% in Lake Lucy (34.6 ha), Minnesota. In our study, we recaptured 19.1% of marked rudd in Buffalo Harbor and 6.1% in the upper Niagara River. Sass et al. (2010) recaptured b0.7% of marked silver carp in the La Grange Reach of the Illinois River, and Bajer and Sorensen (2012) recaptured 4.6–78.2% of marked common carp in small Minnesota lakes. Lastly, the width of our 95% CIs were 17.8% of the estimated number of rudd in Buffalo Harbor and 11.6% of the estimated number of rudd in the upper Niagara River. In contrast, the width of the 95% CI reported by Sass et al. (2010) was 77.2% of the estimated abundance of silver carp in the La Grange Reach of the Illinois River, and the 95% CIs reported by Bajer and Sorensen (2012) ranged from 8.9 to 147.7% of the estimated abundance of common carp in eight small Minnesota Lakes. Only 1% of our recaptured rudd had both paired fins previously removed and could not be assigned to a capture location. It is unlikely that our assumption of zero net movement by rudd between Buffalo Harbor and the upper Niagara River appreciably affected our abundance estimates. However, quantifying movement rates between the two locations would help resource managers predict the likelihood of rudd emigrating from these areas to invade new habitats, predict the response of these rudd populations to reduction efforts, and understand gene flow between these two locations. Our estimates of the abundance and biomass of rudd, and consumption of macrophytes by rudd and grass carp, are probably biased low for four reasons. First, small (b330 mm), relatively young (ages 0–5) rudd would have been underrepresented in our sampling gears (trap-nets and boat electrofishing). Rudd up to age 15 have been captured in the upper Niagara River (Kapuscinski et al., 2012b), so although our study included the majority of age classes present, we certainly underestimated the total number of rudd. Rudd as small as 138 mm (age-1 in November) consume macrophytes in the upper Niagara River (Kapuscinski, unpublished data), so our estimates of macrophyte consumption are also low. Second, our sampling gears were restricted

Table 4 Estimated biomass (wet-weight, mt) of macrophytes consumed by populations of rudd and grass carp (hypothetical) in Buffalo Harbor and the upper Niagara River during 2009–2013, with associated mean (standard error) annual water temperatures (WT) calculated from daily measurements. Year

2009 2010 2011 2012 2013

Mean (SE) WT

Rudd Buffalo Harbor

Upper Niagara River

Grass carp Buffalo Harbor

Upper Niagara River

10.1 (0.4) 10.9 (0.5) 10.7 (0.5) 12.1 (0.4) 10.6 (0.5)

89.1 100.3 97.8 104.6 94.7

4738.5 5328.8 5187.7 5552.4 5209.9

84.5 95.2 94.1 100.5 93.0

4490.0 5056.7 4995.1 5338.7 4941.3

393

to relatively shallow waters (≤3 m) of Buffalo Harbor and the upper Niagara River. The rudd is typically described as a littoral species (Johansson, 1987; Lake et al., 2002), and García-Berthou and MorenoAmich (2000) reported only capturing rudd in trammel nets set at 0–2 m in Lake Banyoles, Spain, despite sampling to depths of 20 m. Although we sampled optimal habitats, our estimates may have been too low if we failed to sample rudd in deeper waters. Third, the temperature-dependent consumption rates that we acquired from the literature were derived from fish held in experimental systems. Wild rudd and grass carp would likely be more active, and therefore have higher consumption rates to meet energetic demands. Last, we estimated weight of rudd based on the mid-point of each 10 mm length class, which would underestimate biomass because the weight of fish increases by about the cube of length. Because of these four biases, our estimates of rudd abundance and biomass should be considered representative of only the adult spawning stocks in Buffalo Harbor and the upper Niagara River, and our estimates of macrophyte consumption by rudd should be viewed as conservative. It should also be noted that our estimates of macrophyte consumption by grass carp are based on consumption rates quantified for relatively small fish (0.08–2.5 kg, with only one fish N 2 kg; Wiley and Wike, 1986). Although Wiley and Wike (1986) did not observe a difference in consumption rates among grass carp of different sizes, the size range examined did not include large fish, which would be expected to have lower consumption rates per g of body weight than small grass carp (Osborne and Riddle, 1999). Therefore, our estimates of macrophyte consumption by grass carp would only apply to populations composed of fish ≤ 2 kg; populations dominated by large fish would need to attain higher biomass to achieve the same level of consumption. Our estimates of macrophyte consumption by rudd did not account for the effect of fish size on consumption rates, and therefore may be inaccurate. Our estimates are based on daily consumption rates reported by Hofer and Niederholzer (1980), which were quantified for rudd much smaller (mean weight among four groups ranged from 16 to 21 g, estimated mean TL 120–129 mm using weight-length equation of Kapuscinski et al., 2012b) than those observed in Buffalo Harbor (mean 356 mm TL) and the upper Niagara River (mean 349 mm TL). Unfortunately, it is unclear if consumption rates of macrophytes by rudd increase (e.g., see Table 1 in Lake et al., 2002) or decrease (Prejs, 1978) with rudd length. It should be noted that the consumption rate reported by Hofer and Niederholzer (1980) of 40.5% of body weight d− 1 at 24 °C is very similar to the rate of consumption (42% of body weight d− 1) reported by Wiley et al. (1986) for age-4 grass carp fed Elodea canadensis at 24 °C. In addition to size and temperature effects, consumption rates may be influenced by macrophyte palatability, structural complexity, and rigidity, which can affect digestion time. Laboratory experiments quantifying consumption rates of common macrophyte species by rudd of various sizes at various water temperatures are needed to estimate consumption of macrophytes by wild populations with more certainty. Similar research is needed on goldfish, which have long been established in the Great Lakes Basin (Mills et al., 1993), and grass carp, which are now likely reproducing in the Sandusky River, Ohio (Chapman et al., 2013), to aid resource managers in understanding threats to macrophytes and approaches for protecting and restoring this important habitat component. Currently, there is no standardized, annual monitoring of fish assemblages and macrophytes in Buffalo Harbor or New York waters of the Niagara River. Our trap-net data indicate that rudd populations are stable or increasing, but these data are inadequate for a statistically valid analysis of population trends. Furthermore, data do not exist to determine if herbivory by rudd has changed macrophyte biomass, distribution, or species composition. A rigorous, standardized survey of fish assemblages and macrophytes in Buffalo Harbor and the Niagara River would provide the information necessary to track changes in rudd populations, detect invasion and reproduction by grass carp, and assess

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changes in macrophyte assemblages that may be caused by these two herbivorous fishes. Acknowledgments Personnel of the New York State Department of Environmental Conservation's Lake Erie and Region 9 Fisheries Units provided critical field assistance and access to sampling gear. The authors thank Derek Crane, Michael Guinan, Matthew Gunderson, Christina Killourhy, Trevor Oakley, Andrew Panczykowski, Timothy Schnaufer, and Justin Zimmerman (State University of New York College of Environmental Science and Forestry) for their extensive sampling efforts. The authors are grateful to Alexander Karatayev and Mark Clapsadl for providing access to the State University of New York Buffalo State Great Lakes Center, which facilitated our sampling efforts. The authors thank Scott Schlueter (US Fish and Wildlife Service) for providing access to an electrofishing boat and assistance in the field. Gillian AvRuskin assisted with figure creation. 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