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Diet composition of age-0 fishes in created habitats of the Lower Missouri River.

Introduction

Degradation of freshwater habitats has prompted several large-scale restoration projects aimed at recovering lost ecosystem structure and function (Roni, 2005; Bernhardt et al, 2007). Restoration projects in large rivers have often been aimed at recovering losses of habitat complexity, biodiversity, and dynamic ecological processes at the river floodplain interface, which represents a species-rich environment that drives productivity and energy exchange at multiple trophic levels (Junk et al., 1989; Ward et al., 1999). Since 2003 there has been a large effort to construct shallow-water habitats (SWH) in the lower Missouri River that were lost during channelization for barge navigation (USFWS, 2003). However, difficulties with post monitoring make gauging the relative "success" of restoration problematic (Roni et al, 2005). A multitude of restoration metrics encompassing abiotic and biotic characteristics exist (Pess et al., 2005) and the responses by each may vary considerably.

Constructed SWH chutes in the lower Missouri River support more species of juvenile fishes than adjacent mainstem habitats, although there is no difference in effective number of species (Jost, 2006) between these habitats (Starks et al., 2015). Trophic responses by individual fish species may provide another means to assess the effectiveness of chute construction on fishes that rely on the natural environments of the river. Analysis of the diets of fishes collected from different habitat types is one method for assessing responses to these restoration activities (Jud et al, 2011; Jordan and Arrington, 2014). This approach helps identify predator-prey relationships, trophic linkages, and other aspects of ecosystem function (Jordan and Arrington, 2014).

In the current study, we assessed diet metrics of age-0 (those individuals born within the last year) freshwater drum (Aplodinotus grunniens [Rafinesque]) and goldeye and mooneye (Hiodon alosoides [Rafinesque], Hiodon tergisus [Lesueur]) to determine trophic responses by fishes to creation of chute shallow-water habitats on the lower Missouri River. We focused on these species because they were abundant in both habitats throughout the river (Starks et al., 2015) and to increase our understanding of the dietary needs of the early life stages of these fishes. Furthermore, there is a paucity of information on prey use by these two species at early life-history stages and results from this study would help fill this knowledge gap. Freshwater drum spawn in open water where buoyant eggs float for 1 to 2 d before hatching (Daiber, 1953). Diet studies of age-0 freshwater drum have been limited to lakes and reservoirs, where they have been described as consuming cladocerans, chironomid larvae, mayfly larvae, and occasionally larvae of other fishes (Swedburg and Walburg, 1970; Clark and Pearson, 1979; Bur, 1982). Both goldeye and mooneye are thought to spawn at midwater depths where semi-buoyant eggs and newly hatched larvae float freely (Battle and Sprules, 1960). Age-0 goldeye primarily consumed calanoid copepods and cladocerans in the Peace-Athabasca Delta, Alberta, Canada (Donald and Kooyman, 1976). Because feeding patterns can be attributed to habitat quality (e.g:, prey availability or habitat heterogeneity; Tews et al., 2004), we sought to quantify prey richness, numbers of empty stomachs, and proportional prey use by these two commonly abundant fish species in chute and mainstem habitats in the lower Missouri River.

Materials and Methods

SAMPLE COLLECTION

Age-0 freshwater drum, goldeye, and mooneye were collected by the U.S. Army Corps of Engineers (USACE) from early May to late July in 2012 at six sites in the Missouri River spanning the state of Missouri from Holt County (rkm 807) to St. Louis (rkm 17; Fig. 1). Each site consisted of paired mainstem and created chute SWH. Four chute habitats were constructed by the USACE (Rush Bottoms, 40.089633, -95.405367; Worthwine, 39.855141, -94.935116; Jameson, 39.085196, -92.923878; and Overton, 38.962589, -92.566414) whereas two were formed naturally (Lisbon, 39.113836, -92.930617 and Littles, 38.858144, -90.258695). However, all chutes were fitted with control structures at the upstream and downstream ends to maintain connection with the mainstem, which made them all "constructed" to varying degrees.

Paired sites were sampled bimonthly from May to July using dual bow-mounted ichthyoplankton nets (750 [micro]m mesh, 750 mm diameter) and a benthic sled (750 [micro]m mesh, 750 mm diameter; Yocum and Tesar, 1980), each fitted with General Oceanics (General Oceanics Inc., Miami, Florida) model 2030R mechanical flow meters. Nets were deployed stationary or pushed through areas that met the standard for SWH (depth <1.5 m and current velocity <0.6 m/s; USFWS 2000, 2003) until a minimum volume of 500 [m.sup.3] was sampled. The order in which chute or mainstem habitat was sampled at a given site was haphazardly chosen. Samples were preserved in 70% ethanol and identified using the larval fish key developed by Auer (1982). Goldeye (Hiodon alosoides) and mooneye (Hiodon tergisus) were grouped together as Hidon spp. because they could not be reliably identified to species at these early life stages, although they were most likely to be goldeye (Pflieger, 1997).

Juvenile fishes were measured for total length (mm) and dissected to remove entire digestive tracts. Specimens that had not begun exogenous feeding (full or partial sac yolk) were not included in analysis, which resulted in 21 Hiodon spp. being excluded. Items found in the digestive tract were removed, quantified, and identified to the lowest practical taxonomic unit using the aquatic insect key developed by Merritt et al. (1996). Prey items that made up less than 1% of all diet items were grouped into a "rare" prey category and analyzed as a single prey type.

STATISTICAL ANALYSIS

Prey richness, number of empty stomachs, and proportion of each prey type consumed were quantified and analyzed for each group separately (freshwater drum and Hiodon spp.) to assess differences in habitat types. Paired f-tests were used to determine size differences of each species between habitat type.

Feeding patterns for each species were assessed using a graphical method to characterize feeding strategy (specialization vs. generalization), relative prey importance (rare or dominant), and niche variation (within or between individual variation; Costello, 1990; Amundsen et al., 1996). The modified graphical method by Amundsen et al. (1996) was used by plotting prey specific abundance ([P.sub.i]) against frequency of occurrence ([O.sub.i]). Prey specific abundance was calculated as [P.sub.i] = ([summation]; [S.sub.i]/[S.sub.ti]) where [P.sub.i] represents prey specific abundance of prey i, [S.sub.i] is the abundance of prey i, in diets, and [S.sub.ti] is the total abundance of prey in predators that contain prey i. Frequency of occurrence ([0.sub.i]) was calculated by dividing the number of fish containing prey i by the total number of conspecifics with food in their stomachs (Chipps and Garvey, 2007). Both metrics were calculated from all specimens collected from each habitat type for each species. Differences in numbers of empty stomachs between habitat types for each species were assessed using contingency tables. These analyses were performed using the "vegan" package (Oksanen et aL, 2005) in Program R 3.0.2 (R Core Team, 2013) and results were considered significant at P < 0.05.

Differences in the proportions of each prey consumed by habitat and prey type were assessed using the generalized linear mixed-model procedure for each species (PROC GLIMMIX, SAS, 2014). These models contained the effects of habitat type (chute or mainstem), prey, and the interaction between habitat type and prey type. These models used a logit link and a binary distribution (prey type eaten = 1, prey type not eaten = 0) with site (Littles, Lisbon, Rush Bottoms, etc.) as a random effect. Subsequent testing of main effect differences in significant interaction terms were assessed using a SLICE statement within the generalized linear mixed-model procedure (SAS, 2014) and all results were considered significant at P < 0.05.

Results

A total of 350 freshwater drum and 145 Hiodon spp. were collected in constructed chute SWH compared to 262 freshwater drum and 78 Hiodon spp. in mainstem SWH. In chutes drum and Hiodon spp. composed 6% and 2.6% of total catch, whereas in mainstem they composed 12.5% and 3.7%, respectively. Freshwater drum total lengths ranged from 3 mm to 18 mm, while Hiodon total lengths ranged from 4 mm to 38 mm. Mean total length of fishes did not differ between habitat types (freshwater drum, paired-t(16) = 0.33, P = 0.79; Hiodon spp., paired-t(5) = 0.97, P = 0.38), although Hiodon spp. (12.5 mm TL) were roughly twice as large as freshwater drum (5.7 mm TL; Table 1).

Most freshwater drum (82%) and Hiodon spp. (87%) had food in their stomachs. The number of empty stomachs was significantly greater in chute SWH for freshwater drum (contingency analysis, [chi square] = 54.99, P = 0.03) but not Hiodon spp (contingency analysis, [chi square] = 1.62, P = 0.20). In chute habitat 63 freshwater drum and 20 Hiodon spp. had empty stomachs, whereas 30 freshwater drum and six Hiodon spp. collected in mainstem habitat had empty stomachs.

Over 13 prey types were found in dissected digestive tracts. Eight prey types made up less than 1% of total prey consumed in each species and were treated as one prey category ("rare prey") for analysis (Table 2). Prey types that contributed at least 1% of the diet of freshwater drum included Diptera larvae, Diptera pupae, Trichoptera larvae, copepods, and Ephemeroptera larvae. Prey types that contributed at least 1% of the diet of Hiodon spp. were Diptera larvae, Diptera pupae, Trichoptera larvae, Ephemeroptera larvae, and Odonata larvae. Rare prey types included Plecoptera larvae, amphipods, Coleopteran larvae, Hemipteran larvae, ostracods, and two terrestrial invertebrates. Use of specific prey types differed by habitat type for freshwater drum ([F.sub.5,3061] = 3.29, P < 0.01) but not Hiodon spp. ([F.sub.5,1155] = 0.67, P = 0.65). Of the prey consumed by freshwater drum, Diptera larvae were consumed more often in mainstem SWH than chute SWH (Fig. 2), whereas all comparisons for Hiodon spp. were not significantly different (Fig. 3). Graphical analysis indicates that freshwater drum specialized on Diptera larvae, which were also the dominant prey found in guts overall (Fig. 4). Graphs for Hiodon spp. indicate some specialization ([0.sub.i] = 0.67, [P.sub.i]= 0.53) on Diptera pupae and Diptera larvae, whereas all other prey items were less consumed (Fig. 5).

Discussion

Fishes, especially during their early life stages, are important indicators of the ecological integrity of river because they are responsive to changes in flow regime, water quality, habitat composition, and prey availability (Karr, 1991; Schiemer, 2003). In the current study, few differences in prey use by age-0 freshwater drum and Hiodon spp. were found between habitat types. However, the number of freshwater drum without food items in their stomachs found in chute habitats could indicate differences in habitat quality, with number of empty stomachs indicating relatively lower productivity levels (Knowlton and Jones, 2000; Bunn et al., 2003; O'Neill and Thorp, 2011). The proportion of empty stomachs for invertivores is considered "high" at about 10% (Arrington et al., 2003) and 18% of freshwater drum stomachs were empty' in chute habitats (compared to 13% in mainstem habitats). However, these effects are also dependent on site-specific factors. For instance the frequency and duration of flood pulses have very strong influences on the timing of emergence and abundance of many aquatic invertebrate species that are important food sources for age-0 fishes (Boulton and Lloyd, 1992; Lemke et al, 2003). The Lisbon and Overton chute SWH sites in particular were not connected with the mainstem Missouri River during periods of low flow in the summer of 2012, creating lentic conditions (Gosch et al, 2015). This reduced flow likely affected the resident invertebrate assemblage and increased competition among fishes for limited food resources (Garvey and Stein, 1998; Gosch et al., 2014). In the current study, 32% of freshwater drum and 55% of Hiodon spp. with empty stomachs came from Lisbon and Overton chutes alone.

The higher proportion of Diptera larvae consumed by freshwater drum in mainstem SWH is likely linked with hydrologic conditions. Significant differences in macroinvertebrate community structures were found between lentic and lotic habitat types in the lower Missouri River (Sampson and Hall, 2011). Given that Diptera larvae, predominately chironomid larvae, tend to numerically dominate invertebrate communities in newly inundated (<1 mo) lotic habitats, one would expect higher abundances of this prey source in mainstem SWHs as they maintain greater hydrological connection than some chutes (Galat et al., 1998; Gosch et al., 2014), From our findings it appears freshwater drum actively select for chironomid larvae, whereas Hiodon spp. were more opportunistic feeders. Additional research on these feeding relationships could help gauge predator-prey dynamics in created habitats, as well as indicate if SWHs are providing greater abundances of prey.

In conclusion created chute SWH does not appear to provide better quality foraging habitats than unrestored mainstem habitats for age-0 freshwater drum, goldeye, and mooneye. The prevalence of specimens with empty stomachs in chute habitats may even point to a lack of foraging opportunities for these two species; however, the effect of hydrology on habitat structure and prey availability needs further investigation. Of the few studies done on these species, the habitat type in question seems to be the overall driving factor for foraging patterns. Habitat type seems to be a driving factor for foraging patterns of the age-0 fishes we studied, although more research is needed to gain a more holistic perspective of how habitat characteristics structure juvenile fish dynamics.

Acknowledgments.--Financial support for this publication was provided by the U.S. Army Corps of Engineers and the U.S. Geological Survey through Cooperative Agreement G12AC20430. YVe thank A. George for constructive comments that improved the paper. This study was performed under the auspices of a protocol approved bv the U.S. Army Corps of Engineers. The Oklahoma Cooperative Fish and Wildlife Research Unit is supported by Oklahoma State University, Oklahoma Department of Wildlife Conservation, U.S. Geological Survey, U.S. Fish and Wildlife Service, and Wildlife Management Institute. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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Submitted 8 December 2016

Accepted 23 January 2017

TREVOR A. STARKS (1)

Department of Natural Resources Ecology and Management, Oklahoma Stale University, Stillwater 74078

AND

JAMES M. LONG

US. Geological Survey, Oklahoma Cooperative Fish anil Wildlife Research Unit, Department of Natural Resources Ecology and Management, Oklahoma State University, Stillwater 74078

(1) Present address: Oklahoma Department of Wildlife Conservation, 9097 N 34th St W, Porter, Oklahoma 74454: e-mail: tstarksl990@gmail.com

Caption: Fig. 1.--Paired chute and mainstem sites on the lower Missouri River sampled where juvenile freshwater drum and Hindon spp. were captured in 2012 for prey use analysis

Caption: Fig. 2.--Proportions of each individual prey type consumed by larval freshwater drum caught in created chute and adjacent mainstem habitats in the summer of 2012. Error bars represent [+ or -] 1 standard error. * Indicates a significant difference between mainstem and chute habitats for the prey type

Caption: Fig. 3.--Proportions of each individual prey type consumed by larval Hiodon spp. caught in created chute and adjacent mainstem habitats in the summer of 2012. (Error bars represent [+ or -] 1 SE)

Caption: Fig. 4.--Amundsen index graph (along with key) indicating feeding strategy, prey importance, and niche width contribution or prey categories for freshwater drum sampled from the lower Missouri Riser in the summer of 2012

Caption: Fig. 5.--Amundsen index graph (along with key) indicating feeding strategy, prey importance, and niche width contribution or prey categories for Hiodpn spp. sampled from the lower Missouri Riser in the summer of 2012
Table 1.--Mean total length (milt) of freshwater drum and Hiodon spp.
collected at each site and habitat type (chute and mainstem shallow
water habitat) in the summer of 2012. Parentheses denote standard
deviation

Site               Freshwater drum             Hiodon spp.

               Chute SWH   Mainstem SWH   Chute SWH   Mainstem SWH

Rush Bottoms   7.5(2.2)      7.2(2.6)        NA            NA
Worthwine      6.2(1.6)      8.4(1.9)     9.3(2.3)         NA
Lisbon         8.2(3.4)      6.9(3.4)     11.4(2.2)    11.1(0.8)
Jameson        5.3(2.3)      4.6(0.8)     11.7(2.3)    12.0(0.7)
Overton        4.6(0.6)      4.8(1.6)     15.2(3.8)    12.2(2.2)
Littles        4.9(0.8)      5.0(0.8)     18.1(1.8)    19.1(7.8)

Table 2.--Frequency of occurrence of prey types in age-0 freshwater
drum and Hiodon spp. Collected from created chute and nearby mainstem
habitats in the lower Missouri River in the summer of 2012. Sample
sizes are ill parentheses. NA indicates prey item was not consumed
by that species

                          Freshwater drum

                       Chute SWH   Mainstem SWH
      Pre type         (n = 287)    (n = 232)

Diptera larvae           30.4%        35.7%
Diptera pupae            10.2%         6.3%
Trichoptera larvae       5.1%          5.1%
Copepoda                 0.7%          2.5%
Ephemeroptera larvae     1.1%          1.9%
Cladocera                0.6%           NA
Amphipoda                0.4%           NA
Odonata larvae            NA           0.1%
Coleoptera larvae         NA            NA
Terrestrial               NA            NA
invertebrates
Hemiptera insects         NA            NA
Ostracoda                 NA            NA
Plecoptera larvae         NA            NA

                             Hiodon spp.

                       Chute SWH   Mainstem SWH
      Pre type         (n = 130)     (n = 72)

Diptera larvae           27.0%        11.0%
Diptera pupae            30.3%        1 1.8%
Trichoptera larvae       6.4%          4.6%
Copepoda                 0.2%          0.4%
Ephemeroptera larvae     3.9%          1.1%
Cladocera                0.2%          0.4%
Amphipoda                 NA            NA
Odonata larvae           1.1%          0.6%
Coleoptera larvae        0.4%          0.2%
Terrestrial              0.2%          0.4%
invertebrates
Hemiptera insects        0.2%           NA
Ostracoda                 NA           0.2%
Plecoptera larvae        0.2%           NA
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Publication:The American Midland Naturalist
Date:Jul 1, 2017
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