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Evaluation of trophic niche overlap between native fishes and young-of-the-year common carp.

INTRODUCTION

Translocation of species outside of their native range often occurs without an adequate understanding of the implications of such introductions on native fauna. Introductions and invasions of nonnative species can have unintended consequences on invaded ecosystems and native species through the transformation of basic ecosystem structure and function (Parker et al., 1999). One of the most detrimental and widespread invasive species is common carp Cyprinus carpio (Lowe et al., 1994). Carp were widely distributed across much of the United States during the 1800s for recreational and food purposes (Panek, 1987). Historically, such introductions were perceived as beneficial but have since resulted in numerous negative effects within invaded ecosystems (Weber and Brown, 2009). Carp populations often shift shallow aquatic ecosystems from the clear- to turbid-water stable state by increasing turbidity, nutrient availability, and noxious algal blooms and reducing aquatic macrophytes and benthic invertebrates (Parkos et al., 2003; Koehn, 2004; Weber and Brown, 2009). Perturbations induced by carp on physicochemical variables and lower trophic levels may extend to higher trophic levels, resulting in reduced growth, survival, and abundance of native fishes (Wolfe et al., 2009; Jackson et al., 2010; Weber and Brown, 2011). Adult carp have been associated with declines in abundances of native fish populations under various abiotic conditions (Weber and Brown, 2011) but little is known about interactions with age-0 carp.

Invasive fishes often occupy ecological niches similar to native fishes, with the possibility for resource overlap and competitive interactions that may result in native fish population declines. Prey resource overlap may be particularly important during early life stages where prey availability can regulate foraging success, growth, and survival (Graeb et al., 2004). Early life stages of many native fishes initially rely on zooplankton prey (Mittelbach, 1984; Pope and Willis, 1998) before undergoing ontogenetic diet shifts to feed on larger invertebrates or fishes (Fisher and Willis, 1997; Graeb et al., 2004). High densities of some larval and juvenile omnivorous fish can greatly reduce prey resources, affecting growth and survival of co- occurring species (Stein et al., 1995). Carp are highly fecund (Sivakumaran et al., 2003; Weber and Brown, 2012b) with protracted spawning that can translate into a high juvenile abundance (Phelps et al., 2008; Weber and Brown, 2013b). Similar to native fishes, early life stages of carp are zooplanktivorous and later undergo an ontogenetic diet shift to benthic invertebrates (Britton et al., 2007; Rahman et al., 2009; Weber and Brown, 2013a). High densities of zooplanktivorous carp can reduce zooplankton densities (Meijer et al., 1990; Kahn et al., 2003) and thus may limit prey availability for other fishes, potentially resulting in interspecific competition (Tonkin et al., 2006).

Comparing how invasive and native species use resources can help predict the extent and potential consequences of their interactions. Biologists need a better understanding of carp resource utilization and niche overlap with native fishes (Carey and Wahl, 2010), specifically during early life stages, a critical period when fishes are most abundant and overlap is likely to occur. Our objectives were to evaluate fish abundance, prey resource use, and diet overlap between age-0 carp and native fish during mid to late summer. We first compared relative abundances of age-0 carp and four common native fishes: age-0 bluegill Lepomis macrochirus, black crappie Pomoxis nigromaculatus, and yellow perch Perea Jlavescens and adult orangespotted sunfish Lepomis humilis. These species were chosen because they are the most abundant species regionally that co- occur with carp populations (St. Sauver et al., 2009), they represent ecologically and economically important fishes for the region, and their populations may be negatively affected by carp (Weber and Brown, 2011). We then investigate prey resource overlap among these species in two lakes by quantifying fish diets using traditional diet analyses and stable isotopes.

METHODS

STUDY AREAS

Brant Lake is a 420 ha (3 m mean depth, 4.3 m maximum depth) glacial lake located in Lake County, South Dakota, U.S.A (43.9215[degrees]N, 96.9489[degrees]W). Lake Sinai is a 696 ha (5 m mean depth, 10 m maximum depth) glacial lake located approximately 53 km north of Brant Lake in Brookings County, South Dakota, U.S.A. (44.2678[degrees]N, 97.0693[degrees]W). Sparse beds of sago pondweed Potamogeton pectinatus exist throughout parts of both lakes and cattails Typha spp. are present in shallow marginal areas of embayments (St. Sauver et al., 2009). Fish communities in both lakes are composed of carp, black crappie, yellow perch, bluegill, orangespotted sunfish, smallmouth bass Micropterus dolomieu, walleye Sander vitreus, bigmouth buffalo Ictiobus cyprinellus, black bullhead Ameiurus melas, channel catfish Ictalurus punctatus, green sunfish Lepomis cyanellus, northern pike Esox lucius, spottail shiner Notropis hudsonius, white bass Morone chrysops, and white sucker Catostomus commersonii.

FIELD SAMPLING

Orangespotted sunfish and age-0 carp, black crappie, yellow perch, and bluegill were sampled on Jul. 14 and Aug. 19, 2008 in Brant Lake to estimate relative abundance and a subsample of collected fish were subsequently used for diet analysis (Table 1). Additional fish were collected on Aug. 26-27 and Sep. 19-20, 2009 from lakes Brant and Sinai for stable isotope analyses, providing additional spatiotemporal insights into juvenile feeding patterns. All fish collections were done using daytime, pulsed direct-current electrofishing (5-8 A, 180-220 V) at four transects with 15 min of effort each in a single embayment that was sampled each year. Because our goal was to observe spatiotemporal overlap in age-0 fishes, we only used electrofishing to estimate the relative abundance of each species in shallow littoral habitats where this method was effective and where we expected our target species to cohabitate for foraging and predator avoidance. Orangespotted sunfish used for relative abundance and diet analyses in Jul. 2008 were likely [greater than or equal to] age-1 whereas those used for relative abundance and diet analyses in Aug. 2008 were age-0. Upon collection in 2008, specimens were immediately preserved in 90% ethanol for diet analysis whereas those collected in 2009 for stable isotope analysis were sorted by species, placed on ice in the field, and frozen in the laboratory. Within each lake, month, year, and species, fish catch per unit effort (CPUE) was calculated as the mean number of fish captured per hour of electrofishing. Catch per unit effort data were transformed ([log.sub.10]-CPUE+1) and compared across species and months with repeated-measures analysis of variance (ANOVA), as CPUE from one date was not independent from samples collected on previous dates. When significant differences were detected ([alpha] = 0.05) for either main factor (species and months) or their interaction, LSD mean separation tests adjusted for multiple comparisons were used to compare CPUE of carp to each native fish species.

To evaluate zooplankton availability concurrent with fish sampling in Brant Lake during 2008, triplicate zooplankton subsamples were collected with an integrated tube sampler at three locations within the same embayment where fish were sampled. Water was filtered through 64 [micro]m mesh and preserved with Lugol's solution in the field. In the laboratory zooplankton samples were adjusted to 60 mL volumes, sub-sampled with three 1 mL aliquots, and identified to suborder or family. Counts were extrapolated to estimate density (number/ L). In 2009 both zooplankton and benthic invertebrates were collected for stable isotope analysis but not invertebrate density estimates, in the same embayments where fish were collected. Zooplankton were collected using similar methods as in 2008 whereas benthic invertebrates were collected from three sites using triplicate Eckman dredge subsamples that were filtered through 500 [micro]m mesh. To purge digestive tracts, zooplankton and benthic invertebrate samples were placed in separate containers, soaked in distilled water for 4 h, and then frozen. Zooplankton used for stable isotope analysis were subsampled from combined samples of all zooplankton collected, whereas benthic macroinvertebrates were identified as Trichoptera, Chironomids, Chydorus, and Corixidae before being combined into a singular homogenous sample for stable isotope analysis. Separation of data into these two major invertebrate prey groups allowed us to identify fish reliance on pelagic (zooplankton) versus littoral (benthic invertebrates) energy pathways (France 1995).

DIET COMPOSITION

No age-0 bluegills were captured in Jul., and we only included fish with prey in their stomachs in the diet analysis. The esophagus, stomach, and intestines were removed and examined under magnification using a dissecting microscope; prey items were identified to genus (zooplankton) or order (benthic invertebrates), enumerated, and when possible, total length (TL) was measured along the longest axis using a micrometer. Dry mass was estimated for each prey type (zooplankton genus or benthic invertebrate order) based on established length-weight equations (Culver et al., 1985; Benke et al., 1999). Using estimated dry mass values, we calculated mean percent dry mass (PDM,) for each prey type by fish species and month as

[PDM.sub.i] = 1/P [P.summation over (j = 1)] ([W.sub.ij]/[[summation].sup.q.sub.(i=1)] [W.sub.ij])

where [W.sub.ij] is the dry weight of prey type i in the diet of fish j, q is the number of prey types, and P is the number of fish for a given species and month that contained that prey item (Chipps and Garvey, 2007).

For each fish species and month, we calculated prey-specific abundance ([PSA.sub.i]), as

[MATHEMATICAL EXPRESSION NOT REPRODUCIBLE IN ASCII]

where [S.sub.i] is the total dry mass of prey type i consumed and [S.sub.ti] is the dry mass of all prey consumed by those fish with prey type i in the diet (Amundsen et al., 1996; Chipps and Garvey, 2007). Percent occurrence was calculated for each species by month as

[PO.sub.i] = ([N.sub.i]/N) x 100

where [PO.sub.i] is the percent occurrence of species i, [N.sub.i] is the number of fish with prey type i in their diet composition, and A is the total number of fish with stomach contents (Amundsen et al., 1996).

[PSA.sub.i] was plotted on the y-axis and [PO.sub.i] on the x-axis in a bivariate scatter plot for each species by month to interpret prey use in relation to feeding strategy, relative prey importance, and homogeneity of diets within the species (Fig. 1; Amundsen et al., 1996; Chipps and Garvey, 2007). The complexity of factors affecting prey utilization by individual fish precludes assigning semiquantitative terms to values for each axis (e.g., less than 40% PSA and less than 40% PO means a prey type is rare), which is likely why Amundsen et al. (1996) did not attempt to assign such values, rather relying on interpretation using graphical methods. A prey type was considered dominant if it was consumed in high abundance by a large percentage of the sample population (high PSA, and high PO,; Fig. 1, bottom left panel; Amundsen et al., 1996). Feeding strategy was represented along the vertical axis (Fig. 1, bottom left panel; Amundsen et al., 1996). A population niche pattern was characterized as a large percentage of the sample population consuming low abundances of many prey types (Fig. 1, bottom left panel; Amundsen et al., 1996).

DIET OVERLAP

Morisita's index of diet overlap was used to compare among prey items consumed by species pairs in each month in 2008 because it minimizes sample size biases (Wolda, 1981; Krebs, 1989). Morisita's index was calculated as

C = 2 [[summation].sup.n.sub.i] [P.sub.ij][P.sub.ik]/ [[summation].sup.n.sub.i] [P.sub.ij][([n.sub.ij] - 1)/([N.sub.j] - 1] + [[summation].sup.n.sub.i] [P.sub.ik][([n.sub.ik] - 1)/([N.sub.k] - 1]

where C is Morisita's index of niche overlap between species j and k; [P.sub.ij] is proportion resource i of the total resources used by species j; [P.sub.ik] is proportion resource i of the total resources used by k; [n.sub.ij] is number of individuals of species j that use resource i; [n.sub.ik] is number of individuals of species k that use resource i; [N.sub.j] and [N.sub.k] are total number of individuals of each species in sample (the sum of [n.sub.ij] = [N.sub.j] the sum of [n.sub.ik] = [N.sub.k]). A value of 1 indicates complete overlap, a value of 0 indicates no overlap, and a value of 0.6 or greater is considered biologically significant, suggesting a potential for prey resource competition (Morisita, 1959). Percent diet overlap was calculated by multiplying Morisita's value (C) by 100.

STABLE ISOTOPES

In the laboratory fish samples were thawed, heads and digestive tracts were removed, and bodies were rinsed in distilled water. Zooplankton samples were thawed, centrifuged to separate zooplankton from phytoplankton, and rinsed with disdlled water. Benthic invertebrate samples were rinsed with distilled water. Samples were dried at 60 C for 72 h, ground into a fine powder using a mortar and pestle, and weighed out into 2.5 mg samples ([+ or -] 0.1 mg). Samples were sent to the South Dakota State University Mass Spectrometry Laboratory to determine [[delta].sup.13]C and [[delta].sup.15]N ratios using a continuous flow, stable isotope mass spectrometer coupled to an elemental analyzer. Stable isotope units were expressed in delta ([delta]) notation, as parts per thousand ([per thousand]) relative to the international standard for that isotope,

[[delta].sup.15]N or [[delta].sup.13]C([per thousand]) = ([R.sub.sample] - [R.sub.standard]/[R.sub.standard]) x 1000

where R is the ratio of the heavier isotope to the lighter isotope, or for this experiment, R = N[sup.15]/ N[sup.14] and R = C[sup.13]/ C[sup.12] for [delta][sup.13]N ([per thousand]) and [delta][sup.13]C ([per thousand]), respectively (Peterson and Fry, 1987). Nitrogen was standardized against atmospheric nitrogen gas and carbon was standardized against the Pee Dee limestone deposit (Peterson and Fry, 1987). Precision for nitrogen was [+ or -] .3 [per thousand] and precision for carbon was [+ or -] 0.2 [per thousand] based on laboratory flour and fish standards.

Isotope biplots allowed interpretation of the diet source (813C on the x-axis) and relative trophic position ([delta][sup.15]N on the y-axis) of fishes (see Table 1 for numbers of each species used in stable isotope analysis). An increase of approximately 3.4 [per thousand] in [[delta].sup.15]N corresponds to an increase of one trophic level (Peterson and Fry, 1987). The [delta][sup.13]C values indicate energy pathways that distinguish between pelagic (more negative) and benthic sources (more positive) in freshwater systems (France, 1995). To test for changes though time, we used independent t-tests (assuming unequal variance) to detect shifts in [delta][sup.13]C and [delta][sup.15]N signatures from Aug. to Sep. for each species within each lake ([alpha] = 0.05). Independent t-tests (assuming unequal variance) were conducted within each lake and month combination to test for differences ([alpha] = 0.05) in [delta][sup.13]C and [delta][sup.15]N signatures between each native species and carp and tablewise Bonferonni adjustments were made for multiple comparisons.

RESULTS

RELATIVE ABUNDANCE

We collected between 0 (bluegill during Jul.) and 702 (bluegill in Aug.) individuals per species and month from Brant Lake during 2008 (Table 1). Differences in CPUE of juvenile fishes among species in Brant Lake during 2008 depended on month ([F.sub.4,10] = 29.41, P < 0.0001). In Jul. carp were more abundant than yellow perch (t = 2.87, P = 0.04) and bluegill (t = 3.01, P = 0.03) and marginally more abundant than orangespotted sunfish (t = 2.20, P = 0.08; Fig. 2A). In Aug. carp were more abundant than black crappie (t = 4.11, P = 0.001) and orangespotted sunfish (t = 4.41, P = 0.007) and marginally more abundant than yellow perch (t = 2.08, P = 0.09; Fig. 2A).

In 2009 we collected between 2 (black crappie in Sinai during Sep.) and 655 (bluegills in Brant during Aug.) individuals per species, month, and lake. Relative abundance of juvenile fishes in Brant Lake differed among species ([F.sub.4,10] = 23.59, P < 0.0001) but not between months ([F.sub.1,10] = 0.30, P = 0.59) or among combinations of species and month ([F.sub.4,10] = 0.78, P = 0.56). Carp were more abundant than black crappie (t = 3.32, P = 0.008), yellow perch (t = 4.52, P = 0.001), and orangespotted sunfish (t = 5.99, P = 0.0001; Fig. 2B) in Brant Lake but relative abundance was similar among species ([F.sub.3.6] = 0.47, P = 0.71) and between months ([F.sub.1.6] = 1.07, P = 0.34) in Lake Sinai.

DIET COMPOSITION

A total of 201 fish were processed from collections in Jul. (88) and Aug. (113) of 2008 for diet analysis (Table 1). Between 14 and 30 individuals were used per species and month. With the exception of bluegill when no individuals were collected during Jul., the mean difference in number of fish per species processed for diet analysis between months was 1.3 [+ or -] 0.6 se. Of these fish, only three had empty stomachs and were not used in diet analysis. Bluegill were not collected because larvae were likely still pelagic (Werner and Hall, 1988). Carp, bluegill, black crappie, and yellow perch (but not orangespotted sunfish) typically exhibited a mixed feeding strategy, generalizing on a large number of prey types, whereas individuals or populations (within a lake and month) displayed specialization on particular prey. In Brant Lake during Jul. 2008, Daphnia was a prominent prey item for all fishes, occurring in 93% of all fish diets (78-100% by species) and representing 39-56% of prey specific abundance (Fig. 1). Total zooplankton density in Jul. samples was 419.4 ([+ or -] 159.2 SE) individuals/L and Daphnia density was 104.9 ([+ or -] 27.4 SE) individuals/L. In Jul. carp were generalists and Daphnia composed 51% of 78% of Brant Lake carp diets (Fig. 1). Most prey items were rare in carp or consumed in low abundances, but some individual carp (22%) specialized on Trichoptera (Fig. 1). Black crappie displayed a consistent feeding pattern, where Daphnia was the predominant prey item (41% of the diet), some individuals (10%) appeared to specialize on Ostracods, and other prey taxa were consumed in low relative abundance or were rare (Fig. 1). Yellow perch also displayed a feeding pattern where Daphnia were important (39% of the diets) and most other taxa were consumed in low to moderate relative abundance (Fig. 1). Orangespotted sunfish consumed a large proportion (56% of the diets of 90% of the sample population) of Daphnia (Fig. 1) while other prey items were consumed in low relative abundance by the Brant Lake sample population (<21% of diets) or by a few individuals (Trichoptera, 15% of the population; Fig. 1).

In Aug. Daphnia became a less important dietary component for many fishes, whereas Cyclops occurred in 94% of all diets (57-100% by species) and represented 2-87% of prey-specific abundance. Total zooplankton density in Aug. was 333.8 ([+ or -] 47.5 SE) individuals/L and Daphnia density declined nearly fourfold from Jul. densities to 24.2 ([+ or -] 5.9 SE) individuals/L. Carp specialized on Trichoptera, which was a dominant prey item, whereas Cyclops and Chydorus were consumed in lower abundances (Fig. 1). Black crappie displayed a population feeding pattern in which Diaptomus and Cyclops each represented nearly 50% of the prey consumed by the sample population and Daphnia was consumed in low abundance (Fig. 1). Yellow perch exhibited an individual feeding pattern where individuals consumed a wide variety of prey (Fig. 1). Corixidae was the dominant prey type for approximately 60% of yellow perch, while one individual (7% of perch evaluated) specialized on fish (species unknown; Fig. 1). Orangespotted sunfish specialized in Cyclops, which was the dominant prey type and accounted for 87% of the diet for the sample population (Fig. 1). Bluegills also specialized on Cyclops (65% of the diet for the population) as the dominant prey type (Fig. 1).

DIET OVERLAP

High diet overlap occurred in Brant Lake in Jul. when Daphnia was the most prevalent prey type but decreased in Aug. as carp and yellow perch progressed through ontogenetic diet shifts toward more varied diets. In Jul. a high degree of diet overlap existed among all species, ranging from 87% to 98%, with carp diet overlap with other species ranging from 87% to 95% (Table 2). In Aug. carp and native fishes tended to partition prey resources. Diet overlap between carp and native fishes decreased to 3% to 15% in Aug. (Table 2). Yellow perch diet overlap with Centrarchids also decreased in Aug., ranging from 9% to 16% (Table 2). Dietary overlap among Centrarchids remained high in Aug., ranging from 67% to 97% (Table 2).

STABLE ISOTOPES

During Aug. 2009 a total of 99 fish were processed for stable isotope analysis (49 from Brant Lake and 50 from Lake Sinai); during Sep., a total of 66 fish were processed (34 from Brant Lake and 32 from Lake Sinai; Table 1). In Brant Lake [[delta].sup.15] N signatures of carp, yellow perch, and black crappie did not change from Aug. to Sep. (Table 3), indicating they were feeding at a similar trophic level during each month. However, bluegill [[delta].sup.15] N signatures became more positive, though the differences were not indicative of a full trophic level shift (Fig. 3; difference <3.4 [per thousand]). In contrast 61' C signatures of all species became less negative from Aug. to Sep. (Table 3; Fig. 3). In Aug. [[delta].sup.13] C signatures were similar between carp and bluegill and between common carp and yellow perch (Table 4), indicating all three species used similar prey resources in Brant Lake in Aug. (Fig. 3). The only significant differences in [[delta].sup.15] N signatures in Brant Lake occurred between bluegill and carp and yellow perch and carp (Table 4), though the differences were not indicative of a full trophic level shift (difference <3.4 [per thousand]). In Sep. there were no significant differences in either [[delta].sup.13] C or [[delta].sup.15] N signatures between native species and carp (Table 4).

In Lake Sinai [[delta].sup.13] C signatures were significantly higher in Sep. for bluegill and carp (Table 3; Fig. 3), indicating a higher reliance on benthic invertebrates. There were no significant changes in [[delta].sup.13] C signatures for black crappie or yellow perch between months, but bluegill and yellow perch both exhibited decreased [[delta].sup.15] N values in Sep. (Table 3; Fig. 3). During Aug. in Lake Sinai, [delta][sup.13]C signatures of black crappie and bluegill were different compared to carp, whereas yellow perch and carp [delta][sup.13]C signatures were similar (Table 4; Fig. 3). Carp exhibited statistically significant differences in [delta][sup.15]N signatures when compared to each of black crappie, bluegill, and yellow perch (Table 4), but the changes were not large enough to indicate a difference in trophic level (Fig. 3). In Sep. there were differences in carp [[delta].sup.13] C signatures compared to bluegill and yellow perch but not compared to black crappie (Table 4). There were no significant differences in [delta][sup.15]N between native species and carp (Table 4; Fig. 3).

DISCUSSION

Juvenile fishes (introduced and native) often occupy similar niches and consume similar prey items, which may result in interspecific competition (Matthews et al., 1992; Sutton and Ney, 2002). Comparisons of resource use between native and introduced species can help predict potential interactions among species and mechanisms of biotic resistance (Carey and Wahl, 2010). However, despite their utility, food web approaches are rarely used to inform and guide efforts to understand, manage, and restore invaded aquatic ecosystems (Vander Zanden et al., 2003). Here, we outline potential food web effects of juvenile carp on native fishes.

Juvenile carp were as or more abundant than native fishes in Jul. and Aug. and initially relied extensively on zooplankton. High dietary overlap (87-93%) existed between carp and native fishes during Jul. when carp and native species relied primarily on Daphnia. Although diet analyses were conducted on different numbers of individuals across species and months, a relatively large ([greater than or equal to] 14) number of individuals per species were evaluated in both Jul. and Aug. 2008. Thus, our are results are likely reflective of these fish populations at large. Age-0 individuals of carp (Tonkin et al., 2006), yellow perch (Mills et al., 1984), and black crappie (Pope and Willis, 1998) often prefer Daphnia to other zooplankton when gape size permits and, as a result, may compete for this prey resource. In addition to diet overlap, juvenile carp, yellow perch, bluegill, and black crappie use similar habitats in shallow lakes (Weber and Brown, 2012a) and in this study were collected in similar habitats, thus increasing the likelihood of competitive interactions. Prey availability is often an important determinant of growth, survival, and recruitment during early life stages (Cushing, 1990; Weber et al., 2011). Fishes foraging on Daphnia may experience higher growth and survival during early life stages compared to those foraging on alternative, smaller zooplankton (Graeb et al., 2004). However, Daphnia are highly vulnerable to predation and their densities may be greatly reduced by larval and juvenile fishes (Mills et al., 1987; Khan et al., 2003), forcing fishes to switch to alternative prey.

Daphnia density declined nearly fourfold from Jul. to Aug. in Brant Lake in 2008, coinciding with the time period when most age-0 fishes switched to consuming either alternative zooplankton taxa or benthic invertebrates. Carp generally exhibit an ontogenetic diet shift to benthic taxa at 100 mm fork length (Britton et al., 2007) to 150 mm TL (Kahn, 2003). However, in Brant Lake, carp diets shifted from Daphnia in Jul. to Trichoptera in Aug., when individual fish ranged between 30 and 58 mm TL. Similarly in Aug. 70 mm TL yellow perch switched their dominant prey type from zooplankton to benthic invertebrates (Corixidae). Such ontogenetic diet shifts are typically beneficial because energy return is higher for macroinvertebrates and often increases growth rates of juvenile fishes (Graeb et al., 2005). We did not evaluate benthic invertebrate densities in Brant Lake during 2008, but the timing of the ontogenetic shifts may have coincided with increases in availability of this prey type. In contrast to diet shifts by carp and yellow perch, Centrarchids (black crappies, bluegills, and orangespotted sunfish) remained primarily zooplanktivorus in Aug., consuming Diaptomus and Cyclops as their dominant prey types. Because the three Centrarchids continued to consume similar zooplankton prey during Aug., diet overlap among these fishes remained relatively high. Other studies have indicated that juvenile sunfishes share similar prey resources and may experience competition (Werner and Hall, 1977; Collingsworth and Kohler, 2010). In contrast the increased diversity of prey types consumed by carp and native fishes in Aug. resulted in decreased diet overlap. Transitions between developmental stages, as mouth gape increases and individuals are able to diversify their diets, may lead to decreased dietary overlap among some species (Matthews et al., 1992; Sutton and Ney, 2002; Probst and Eckmann, 2009). Although diet overlap between carp and native fishes was very low in Aug., consumption rates increase as juvenile fishes become larger (Tonkin et al., 2006). Thus, even species having low diet overlap may compete for increasingly limited resources (Persson, 1987; Deus and Petrere-Junior, 2003).

Because we collected diet analysis and stable isotope samples in different years, direct comparisons between the two approaches were not possible. However, stable isotope analysis provided a time-integrated perspective, showing greater spatial and temporal diversity of prey use by juvenile fishes in 2009, which indicated that juvenile fishes came to rely more on benthic invertebrates later in the year. In Brant Lake in 2009, isotopic signatures for juvenile fishes showed a more distinct transition from zooplankton to benthic invertebrates as compared to Lake Sinai, where less pronounced shifts were due to high variation in isotopic signatures among fishes. Shifts less than a full trophic level were likely biologically insignificant. Rapid shifts in isotopic signatures, reflecting ontogenetic diet shifts, are common in age-0 fishes due to high turnover rates of tissues in young individuals (typically 8-18 d; Weidel et al., 2011). Similarity among [[delta].sup.13] C signatures of all fishes in Brant Lake during both Aug. and Sep. suggests that all fishes were using similar prey resources. In comparison carp in Lake Sinai had less negative [[delta].sup.13] C signatures than did native fishes during both months, suggesting carp consistently relied more on benthic invertebrate prey. Differences in isotopic signatures reflecting differences in consumption patterns for juvenile fishes between lakes Brant and Sinai may also reflect differences in prey resource availability, habitat types, or foraging conditions. Although we collected zooplankton and benthic invertebrates for isotopic analysis, we did not evaluate densities of either prey group in either lake to test this hypothesis. However, regardless of the mechanism, extant lake differences in resource use by juvenile fishes are likely an important predictor for interactions between carp and native species.

Invasive species can have multiple, complex effects on ecosystems and native fishes (Weber and Brown, 2009). Characterization of food webs can engender a more complete understanding of food web linkages between native and invasive species and have implications for restoration of native species and invaded ecosystems. Diet data provided a detailed snapshot of juvenile fish diets whereas stable isotopes revealed what resources were assimilated over longer temporal periods (8-18 d; Weidel et al., 2011). Diet overlap indicated that shared resources between carp and native fishes can be high, but change temporally, whereas stable isotopes indicated that shared resources among these species can fluctuate monthly and among lake populations. Although resource overlap provides an approach to quantify commonalities of prey among fishes (Schoener, 1971; Schleuter and Eckmann, 2007), high resource overlap does not provide direct evidence that carp compete with native fishes for those resources (Pianka, 1974; Porter and Dueser, 1982), as competition can only occur when resources are limiting (Wiens, 1977). Thus, future research should explore ecological conditions that are likely to result in competition among these species.

Acknowledgements.-We thank S. Chipps for diet analysis insights and M. Hennen, K. Rounds, B. Johnson, C. Funk, A. Wiering and C. Mortensen for assistance in the field and laboratory. We thank D. Clay, S. Hansen, and the SDSU Soils Laboratory for assistance with stable isotope samples and analysis. Partial funding for this project was provided by the Griffith Undergraduate Research Award through the Agricultural Experiment Station at South Dakota State University and through the Federal Aid in Sport Fish Restoration Act Study 1513 (Project F-15-R-42) administered by the South Dakota Department of Game, Fish, and Parks.

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SUBMITTED 24 MAY 2012

ACCEPTED 21 FEBRUARY 2014

JESSICA M. HOWELL, (1) MICHAEL J. WEBER (2) and MICHAEL L. BROWN

South Dakota State University, Department of Natural Resource Management, Box 2MOB, Brookings 57007

(1) Corresponding author present address: Kansas Department of Wildlife, Parks, and Tourism, Emporia Research and Survey Office, PO Box 1525, Emporia, KS 66801; Telephone: (620) 342-0658; FAX: (620) 342-6248; e-mail: jessica.howell@ksoutdoors.com

(2) Present address: Iowa State University, Department of Natural Resource Ecology and Management, 339 Science Hall II, Ames, Iowa 50011

TABLE 1.--Summary describing the total number (N) and size
distribution of fish sampled in lakes Brant and Sinai used to
calculate relative abundance and the number used for diet analysis in
2008 and for stable isotope analyses in 2009. Orangespotted sunfish in
Jul. 2008 were likely > age-1 based on sizes, whereas those in Aug.
2008 were likely age-0 (Miller 1963)

Lake     Year    Month           Species            N       Length
                                                          range (mm)

Brant    2008     Jul.    Common carp               23      21-50
                          Bluegill                  0         NA
                          Black crappie             92      26-37
                          Yellow perch              15      45-53
                          Orangespotted sunfish     33      41-59

         2008     Aug.    Common carp               28      30-59
                          Bluegill                 702      30-48
                          Black crappie             29      46-68
                          Yellow perch              14      65-79
                          Orangespotted sunfish     20      30-44

         2009     Aug.    Common carp               42      61-100
                          Bluegill                 655      29-46
                          Black crappie             9       44-65
                          Yellow perch              67      65-96

         2009     Sep.    Common carp               7       60-88
                          Bluegill                 498      36-49
                          Black crappie             10      62-74
                          Yellow perch              7       52-96

Sinai    2009     Aug.    Common carp               65      38-88
                          Bluegill                 297      28-34
                          Black crappie             57      25-46
                          Yellow perch              95      58-70

         2009     Sep.    Common carp               28      57-89
                          Bluegill                 127      27-46
                          Black crappie             2       68-102
                          Yellow perch              12      69-82

Lake     Year    Month           Species             Diet      Stable
                                                   analysis   isotopes

Brant    2008     Jul.    Common carp                 23         0
                          Bluegill                    0          0
                          Black crappie               30         0
                          Yellow perch                15         0
                          Orangespotted sunfish       20         0

         2008     Aug.    Common carp                 20         0
                          Bluegill                    30         0
                          Black crappie               29         0
                          Yellow perch                14         0
                          Orangespotted sunfish       20         0

         2009     Aug.    Common carp                 0          10
                          Bluegill                    0          20
                          Black crappie               0          9
                          Yellow perch                0          10

         2009     Sep.    Common carp                 0          7
                          Bluegill                    0          10
                          Black crappie               0          10
                          Yellow perch                0          7

Sinai    2009     Aug.    Common carp                 0          10
                          Bluegill                    0          10
                          Black crappie               0          10
                          Yellow perch                0          10

         2009     Sep.    Common carp                 0          10
                          Bluegill                    0          10
                          Black crappie               0          2
                          Yellow perch                0          10

TABLE 2.--Percent diet overlap (Morisita's C values x 100) for Brant
Lake Fishes collected in Jul. and Aug. 2008. COC = common carp, BLC =
black crappie, BLG = bluegill, OSP = orangespotted sunfish, and YEP =
yellow perch. NA = not available

Fish combination       Percent
                     diet overlap

                    Jul.    Aug.

COC X BLC            95       9
COC X BLG            NA      15
COC X OSP            87      15
COC X YEP            93       3
BLC X BLG            NA      80
BLC X OSP            95      67
BLC X YEP            98      16
BLG X OSP            NA      97
BLG X YEP            NA       9
OSP X YEP            96       9

TABLE 3.--Two-tailed independent t-test results comparing
[delta][sup.13] C and [delta][sup.15] N isotopic signatures between
Aug. and Sep. of 2009 for each species within each lake. Significant
P-values are indicated by an * ([alpha] = 0.05). BLC = black crappie,
BLG = bluegill, COC = common carp, and YEP = yellow perch

                    Species             Brant lake

                               t-statistic    P-value

[delta][sup.13]C      BLC         -5.44        0.00 *
([per thousand])      BLG         -5.46        0.00 *
                      COC         -2.54        0.02 *
                      YEP         -5.97        0.00 *

[[delta].sup.13]N     BLC         -0.54         0.60
([per thousand])      BLG         -2.27        0.03 *
                      COC         -2.04         0.06
                      YEP         -0.72         0.48

                    Species           Lake sinai

                               t-statistic    P-value

[delta][sup.13]C      BLC         -2.24         0.27
([per thousand])      BLG         -7.70        0.00 *
                      COC         -2.52        0.02 *
                      YEP          0.07         0.95

[[delta].sup.13]N     BLC          0.22         0.86
([per thousand])      BLG          5.55        0.00 *
                      COC         -1.36         0.19
                      YEP          2.58        0.02 *

TABLE 4.--Two-tailed independent t-test results comparing
[delta][sup.13]C and [delta][sup.15]N signatures of native species to
common carp [delta][sup.13]C and [delta][sup.15]N signatures,
respectively, in each lake each month. An * indicates a significant
difference in [delta][sup.13]C or [delta][sup.15]N signatures ([alpha]
= 0.017)

                                               Brant lake

                             Species     t-statistic    P-value

[[delta].sup.13]C   Aug.    BLC X COC        1.12         0.28
([per thousand])            BLG X COC        3.73        0.00*
                            YEP X COC        4.12        0.00*
                    Sep.    BLC X COC       -1.32         0.24
                            BLG X COC        1.92         0.09
                            YEP X COC        1.23         0.25

[[delta].sup.15]N   Aug.    BLC X COC        0.9          0.39
([per thousand])            BLG X COC        0.72         0.49
                            YEP X COC        -0.5         0.62
                    Sep.    BLC X COC        0.01         1.00
                            BLG X COC        1.57         0.14
                            YEP X COC       -0.66         0.52

                                               Lake sinai

                             Species     t-statistic    P-value

[[delta].sup.13]C   Aug.    BLC X COC        2.45         0.03
([per thousand])            BLG X COC        3.68        0.00 *
                            YEP X COC        4.12        0.00 *
                    Sep.    BLC X COC        0.01         1.00
                            BLG X COC       -0.97         0.35
                            YEP X COC        0.89         0.39

[[delta].sup.15]N   Aug.    BLC X COC       -4.52        0.00 *
([per thousand])            BLG X COC       -4.48        0.00 *
                            YEP X COC       -1.47         0.17
                    Sep.    BLC X COC       -7.85        0.00 *
                            BLG X COC       -7.73        0.00 *
                            YEP X COC       -5.69        0.00 *
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