Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 437 2015 NORTHEASTERN NATURALIST 22(2):437–450 Diet Composition and Feeding Behavior of Larval American Shad, Alosa sapidissima (Wilson), after the Introduction of the Invasive Zebra Mussel, Dreissena polymorpha (Pallas), in the Hudson River Estuary, NY Christopher C. Nack1,*, Karin E. Limburg1, and Robert E. Schmidt2 Abstract - The invasive Dreissena polymorpha (Zebra Mussel) has greatly altered the zooplankton community of the Hudson River by reducing the abundance of native zooplankton and inundating the system with its free-swimming veliger larvae. Since the invasion, there has been a reduction in pelagic fishes, including Alosa sapidissima (American Shad), which is thought to be, in part, a result of the decreases in zooplankton populations. To better understand the complex interaction between this mussel species and American Shad, it is important to describe the fish’s current larval diet. Although American Shad larvae readily consumed veligers and this food source may contribute to year-class strength, the importance of veligers as a diet item greatly depends on larval–veliger temporal overlap and yearly shifts in veliger abundance, digestibility, and nutrition. Introduction The Alosa sapidissima (Wilson) (American Shad) fishery on the Hudson River once ranked among the most important fisheries in North America, providing critical nourishment to native Americans and early European settlers and constituting a major activity through the mid-20th century (Limburg et al. 2006). The American Shad population in the Hudson River has declined since World War II and particularly since the mid-1980s; currently the stock is at an all-time low, resulting in a fishery closure in 2010 (ASMFC 2010). Population declines have been attributed to several factors including dredging and channelizing of the river, water pollution, overfishing, marine bycatch, and the introduction of invasive species. In this last regard, Dreissena polymorpha (Pallas) (Zebra Mussel) has been the cause of many changes in the food web of the Hudson River (MacIsaac 1996, Pace et al. 1998, Strayer et al. 2004); thus, it is important to describe the interactions between fishes and Zebra Mussels at different life stages. The establishment of Zebra Mussels in North America, which was first documented in Lake St. Claire, MI, in 1988 (Hebert et al. 1989) and later in Lake Erie starting in 1986 (Carlton 2008), is one of the most extensively documented and well-known species invasions. The presence of this freshwater exotic bivalve has caused alterations in phytoplankton (Smith et al. 1998), zooplankton (MacIsaac et al. 1995, Pace et al. 1998), vegetation (Skubinna et al. 1995), and zoobenthos 1State University of New York College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210. 2Bard College at Simon’s Rock, 84 Alford Road, Great Barrington, MA 01230. *Corresponding author - ccnack@syr.edu. Manuscript Editor: Trevor Avery Northeastern Naturalist 438 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 (Nalepa et al. 1998, Strayer and Smith 2001) communities, and has reduced abundances of many ecological communities throughout its range of invasion. However, studies of fish-community responses to exotic bivalve invasions have obtained inconsistent results (Paolucci et al. 2010b, Strayer et al. 2004), possibly due to the complex interaction between fish-habitat use (littoral versus pelagic feeding), spawning behavior (nest builders versus broadcast spawners), and the different life stages of Zebra Mussels. The abundance of young-of-year alosine herrings such as American Shad, A. aestivalis (Mitchell) (Blueback Herring), and A. pseudoharengus (Wilson) (Alewife) has decreased in the Hudson River since the discovery of Zebra Mussels there in 1992, while littoral fish abundances have increased (Strayer et al. 2004). Changes in the abundance of pelagic fishes have been attributed to decreases in native zooplankton in response to high grazing rates by adult Zebra Mussels. In an opposing interaction, the free-swimming veliger larvae contribute to the zooplankton community, often outnumbering other major taxonomic groups such as planktonic crustaceans and rotifers (Karatayev et al. 2007, Winkler et al. 2005). An invasion of Dreissena mussels does not always elicit a decrease in pelagic fishes. For example, 2 years after the discovery of D. bugensis Andrusov (Quagga Mussel) in Lake Mead, NV, there was no significant change in the pelagic Dorosoma petenese (Günther) (Threadfin Shad) population (Loomis et al. 201 1). The veligers of Zebra Mussels and other bivalves with similar life histories contribute to the diets of fry of several fish species. In Europe, at least 10 species prey on Zebra Mussel veligers (Molloy et al. 1997), which contributed 67% of the diet of Rutilus rutilus (L.) (Roach) larvae (Belyaev et al. 1970, reported in Molloy et al. 1997). Paolucci et al. (2007) found that larvae of 11 out of 15 fish taxa examined consumed veligers of the invasive Asian bivalve, Limnoperna fortunei (Dunker) (Golden Mussel) in the Paraná River, Argentina. Protolarvae and mesolarvae from the Paraná River (Paolucci et al. 2007) and of Prochilodus lineatus (Valenciennes) (Curimatidae) in the lab (Paolucci et al. 2010a) selected Golden Mussel veligers in natural planktonic conditions (0.06 individuals ml-1). When concentrations of veligers were reduced (0.02 individuals ml-1), only protolarvae selected for the veligers (Paolucci et al. 2010a). Little research has been conducted in North America to examine the contribution of Zebra Mussel veligers to the diets of fish. Veligers of Zebra Mussels and Quagga Mussels have been documented in the diets of some fishes including young-ofthe- year and adult Alewife and Osmerus mordax (Mitchell) (Rainbow Smelt) in Lake Ontario (Mills et al. 1995) and in the larvae of Blueback Herring, Morone americana (Gmelin) (White Perch), and M. saxatilis (Walbaum) (Striped Bass) in the Hudson River (Limburg and Arend 1994, Limburg et al. 1997). In these studies, veligers were a small proportion (less than 0.1%) of the overall diets. In the St. Lawrence River, a stable isotope analysis suggested that larval American Shad also fed on veligers, although no stomach contents were examined (Barnard et al. 2006). During a 2010 survey of larval American Shad habitat use in the Hudson River estuary, we noted the presence of Zebra Mussel veligers in the intestinal tracts Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 439 of American Shad larvae. Subsequently, we undertook a quantitative analysis to determine if veligers were an important component in the fish’s overall diet and if the contribution changed during different larval developmental stages. Field-site Description The Hudson River is the second largest drainage (36,260 km2) in New York State and extends 510 river kilometers (rkm) from Lake Tear of the Clouds located in the Adirondacks to the Battery in New York City (rkm 0). The Federal Dam (248 rkm) in Troy, NY, impedes the migration of anadromous fishes to the upper river. Below the dam, the river has ~1-m tides, and tidal flows there are much greater than the average freshwater flows of 577 m3s-1 (Cooper et al. 1988). A salt wedge fluctuates at ~100 rkm depending on freshwater flows and tidal cycles (Strayer et al. 2004). We made collections in the tidal–freshwater reach between Catskill, NY, at rkm 180 and Castleton, NY, at rkm 225. A wide channel with variable, vegetated, shallow habitats adjacent to the navigation channel in this section provided habitat for both post-larval American Shad and adult Zebra Mussels. Methods We collected post-yolk-sac larval American Shad using paired 1-m diameter, 505-μm-mesh ichthyoplankton nets (Hoffman et al. 2007, Wilhite et al. 2003). We conducted weekly tows at 16 sites for 5 weeks starting 21 May and ending 18 June 2010. A digital flowmeter placed inside the mouth of each ichthyoplankton net measured the speed of each tow, and we calculated volume sampled from the speed and duration of the tow. We collected samples in 4 shallow-water (depth < 3 m) habitats including vegetated main channel, open main channel, contiguous backwater, and secondary channel habitats. We sampled during the day when feeding activity for American Shad larvae was highest (Johnson and Dropkin 1996) and preserved specimens in 95% ethanol. We identified and sorted American Shad from other larvae (Wang and Kernehan 1979) in the lab and then calculated mean abundance (# of shad/100 m3) per week. We performed gut analysis on up to 20 post-yolk-sac larval American Shad from each of the 16 sites for all 5 sampling weeks. For sites with few larvae, we combined replicate tows to ensure robust sample sizes for statistical analysis. We chose American Shad individuals for analysis by stratifying each sample into 2 size groups based on length (≤15.0 mm and >15.0 mm) and then selecting specimens using proportional allocation so that the size range selected represented the size range of the sample. These size categories roughly corresponded to the onset of larval to juvenile metamorphosis (Savoy and Crecco 1988) and have been associated with ontogenetic changes in habitat suitability (Nack et al. 2014). We measured the fish with calipers and recorded total length to the nearest 0.1 mm. We identified gut contents to Order for copepods and to family for cladocerans and bivalves. We derived relative proportion of prey taxa using dry-weight estimates. To estimate the dry weight (μg) of cladocerans, copepods, chironomids, hydrachnids, and ostracods, Northeastern Naturalist 440 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 we collected specimens with a zooplankton net, removed 50 to 100 individuals of each taxon, dried the subsamples at 105 °C for 24 h, and weighed them. We obtained dry-weights for copepod nauplii and rotifers from Pace et al. (1992). We estimated mean dry weight of Zebra Mussel veligers using the regression proposed by Mackie (1991): Total dry weight (μg) = 0.051(Length)2.996 We measured veligers to the nearest 0.01 mm under a calibrated compound microscope at 10x magnification. We calculated diet composition as percent-by-biomass of each prey item for each American Shad specimen and derived averages for all American Shad and each size category, ≤15.0 mm (protolarvae) and >15.0 mm (mesolarvae and metalarvae). Five other nonnative bivalve species were present in the freshwater tidal reach of the Hudson River. The most abundant of these was the Quagga Mussel, which constituted a small fraction of the Dreissena population (Strayer and Malcom 2013). We also calculated the percent of empty stomachs. To determine if Zebra Mussel veligers were a constant source of food for larval American Shad, we compared diets among the 5 sampling weeks. We employed a one-way analysis of variance (ANOVA) to compare the biomass of dreissenid veligers, copepods, and cladocerans among weeks. Significant homogeneous groups were identified using a Tukey’s HSD all-pairwise comparison test. We set a significance level of 0.01 (alpha-value) for all ANOVA and Tukey’s HSD comparisons. To determine the feeding behavior of American Shad from different size categories, we used a graphical analysis following a modified Costello (1990) method (Amundsen et al. 1996). This method is used to determine the niche-width contribution (between- versus within-phenotype components), feeding strategy (specialization versus generalization), and prey importance (rare versus dominant) of each prey item using the prey-specific occurrence (%) and abundance (%). By phenotype, we refer to the composite of the observed behavioral traits of larval American Shad examined, which was most likely a result of environmental influences such as differences in water velocity and turbidity. A population where different individuals specialize on different prey items is considered to have a high between-phenotype component to the niche breadth. High within-phenotype niche width refers to a high proportion of the individuals having consumed many different prey items (Amundsen et al. 1996, Giller 1984, Pianka 1988, Wooton 1990). Finally, we calculated the Levin’s measure of niche breadth (B) and standardized measure (BA) for each size category using the equations: B = 1 / Σ pj 2 BA = (B – 1) / (n – 1) where pj is the proportion of the diet composed of prey species j and n is the total number of prey species (Levins 1968, Marshall and Elliott 1997). Levins’ B is used to indicate if a diet is considered diverse (high B value, >4) or specialized (low B value, ≤4). The standardized measure BA indicates if a diet is dependent on a limited prey group (Marshall and Elliot 1997). Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 441 Results Of all American Shad sampled, 24.5% (± 1.5 SE) had empty stomachs (Table 1). American Shad ≤15.0 mm (39.6 % ± 3.5) were more likely to have an empty stomach than American Shad >15.0 mm (11.5% ± 1.4). Bosmina (a common genus of freshwater cladoceran, probably B. freyi De Melo and Hebert in the Hudson River), cyclopoid copepods, and Zebra Mussel veligers accounted for at least 96% of the diet biomass for both size categories (Table 2). Zebra Mussel veligers made up an average of 68.3% (± 6.0) of the diet by individual counts and 24.8 % (± 3.4) of the diet by dry weight. Our analyses indicated no difference in the contribution of Zebra Mussel veligers to the overall diet biomass (%) between American Shad ≤15.0 Table 2. Average percent biomass of each prey taxon consumed and the corresponding Levins’ niche breadth (B) with standardized niche breadth (BA; in parenthesis) for all larvae, larvae ≤15.0 mm, and larvae >15.0 mm of American Shad sampled from the Hudson River estuary, NY in 2010. Percent biomass is shown. Biomass was estimated using dry-weight data for each prey taxon. Prey taxon All larvae Larvae ≤15.0 mm Larvae >15.0 mm Diatoms 0.9 2.2 0.2 Rotifer less than 0.1 less than 0.1 less than 0.1 Cladocera Bosmina 28.1 31.4 26.2 Chydoridae 1.1 0.1 1.7 Daphnia less than 0.1 less than 0.1 0.0 Copepoda Cyclopoida 42.3 39.8 43.8 Calanoidea 0.1 less than 0.1 0.1 Copepoda nauplii 0.7 1.3 0.4 Bivalvia Dreissena veliger 26.2 24.8 27.1 Gastropoda Gyraulus less than 0.1 less than 0.1 less than 0.1 Ostracoda 0.1 0.1 0.1 Diptera Chironomidae 0.3 0.0 0.4 Arachnida Hydrachnidiae 0.1 0.2 less than 0.1 Levins’ B (BA) 1.95 (0.13) 2.04 (0.18) 1.98 (0.13) Table 1. Larval American Shad sample size, average diet biomass (μg), and the percent of empty stomachs for all larvae sampled , ≤15.0 mm larvae, and >15.0 mm larvae from the Hudson River, NY. Size category Number of larvae Average diet biomass (μg) % empty stomachs All larvae 1371 9.5 24.5 Larvae ≤15.0 mm 634 3.2 39.6 Larvae >15.0 mm 737 14.9 11.5 Northeastern Naturalist 442 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 mm (24.8 % ± 3.4) and >15.0 mm (27.1 % ± 4.2). It was common for larval American Shad to have eaten over 200 veligers, and one larva (17.4 mm) had consumed 423 individuals. We observed both open and closed Zebra Mussel veligers in the larval American Shad stomachs examined (Fig. 1). Biomass of Zebra Mussel veligers in American Shad diets was negligible in the first 2 weeks of sampling (less than 0.0006 μg, less than 0.1%) but was the most abundant prey item consumed by 11 June 2010 (0.72 μg, 37.8%) and 18 June 2010 (1.14 μg, 51.6%) (Fig. 2) We observed a similar pattern for the presence of Bosmina in the diet—very few individuals were consumed in the first 2 weeks. Cyclopoid copepods were consistently consumed by American Shad larvae over the 5-week sampling period (Table 3). Larvae ≤15.0 mm exhibited a high between-phenotype feeding behavior (Fig. 3) and larvae >15.0 mm were found to have a more mixed feeding behavior with different levels of specialization and generalization of prey. Overall larval niche breadth (Levins’ B) was 1.95 (± 0.23) and was similar for larvae >15.0 mm (1.98 ± 0.27) and ≤15.0 mm (2.04 ± 0.27). Overall standardized B A was 0.13 (± 0.05). Discussion Our results show that the free-swimming veligers of Zebra Mussels were actively consumed by larval American Shad and accounted for a large portion of the diet Figure 1. Larval American Shad gut containing Zebra Mussel veligers. Note that some veligers appear to be open while others are still closed. Bottom right quadrant shows pigmented myomeres of the larva. Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 443 of samples collected during our study. We observed no difference in Zebra Mussel veliger biomass (%) in the diets of the ≤15.0-mm and >15.0-mm size classes, although feeding behavior was different. The high between-phenotype feeding behavior of larval American Shad ≤15.0 mm, where individual larvae specialized on different prey and each prey type was consumed by a small fraction of the larvae, suggest that the importance of veligers in the diet of the smaller size class was greater than for the larger one. An underdeveloped swimming ability (Miller et al. 1988) and low prey-abundance in nursery areas (Crecco and Savoy 1985, 1987; Johnson and Dropkin 1995; Limburg 1996) have been associated with an increase in the susceptibility of larvae to starvation. The presence of Zebra Mussel Figure 2. Mean biomass (μg) of Zebra Mussel veligers consumed by American Shad larvae and larval abundance for larvae >15.0 mm and ≤15.0 mm in 2010 b y sample date. Table 3. Mean weekly biomass of Bosmina freyi cladocerans, cyclopoid copopods, and Zebra Mussel veligers found in the stomachs of all American Shad sampled from the Hudson River in 2010. Mean biomass values (± standard error) within a column not followed by a similar superscript letter were significantly different (P-value = 0.01). Sample date Bosmina (μg) Cyclopoid (μg) Veliger (μg) 18 June 0.46A ± 0.04 0.10A ± 0.01 1.14A ± 0.12 11 June 0.36A ± 0.04 0.41B ± 0.05 0.72B ± 0.08 4 June 0.35A ± 0.05 0.18C ± 0.02 0.08C ± 0.02 28 May 0.01B ± 0.01 0.23C ± 0.02 0.0006D ± 0.0004 21 May 0.07B ± 0.01 0.10A ± 0.02 0.0003D ± 0.0002 Northeastern Naturalist 444 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 veligers in the Hudson River may help offset decreases in the overall abundance of zooplankton by providing a new food resource for larval American Shad, especially for larvae ≤15.0 mm with the poorest swimming ability . Overall, larval American Shad from the Hudson River fed heavily on relatively large prey items (Bosmina and copepods) and very few small prey items (rotifers and copepod nauplii). This pattern may have been due to the size of the larvae at hatch and their relatively large mouth-gape-to-length ratio (Binion 2011, Crecco and Blake 1983), which allowed them to feed on larger prey earlier in their developmental stage than other larval alosines found in the Hudson River. Johnson and Dropkin (1996, 1997) found that larval American Shad diets were composed primarily of copepods (37.7%) and cladocerans (37.4%) in small release ponds in the upper Susquehanna River basin and of chironomid pupae (50–96%) after being stocked in the Susquehanna River itself. Crecco and Blake (1983) similarly found that American Shad selected for the larger cyclopoids and chironomid larvae. It has also been shown that American Shad select for and consume the larger zooplankton in the upstream reaches of the Connecticut River, leaving only smaller zooplankton for American Shad farther downriver (Rosen 1981). The fact that larval American Shad are able to consume large zooplankton and select for them suggests that American Shad larvae have not been affected by the decrease in zooplankton in response to the introduction of Zebra Mussels as greatly as other pelagic species such as Alewife and Blueback Herring. Initially after the Zebra Mussel invasion, abundances of cladocerans and copepods were not reduced as dramatically as small zooplankton, and their seasonal patterns were unaltered (Pace et al. 1998). However, reduced abundances of rotifers and copepod nauplii, putatively caused by the introduction of Zebra Mussels (Pace et al. Figure 3. Graphical analysis of feeding behavior and the importance of each prey item determined according to Amundsen et al. (1995). Graphs are shown for larvae (A) >15.0 mm and (B) ≤15.0 mm. Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 445 1998), have also reduced the amount of small-prey items available to larval American Shad. Even accounting for the faster digestion of small-prey items (Fossum 1983, Sutela and Huusko 2000), rotifers and copepod nauplii still made up a small proportion of the overall diet. Eventually, Pace and colleagues did find significant declines in Bosmina. However, variability in adult Zebra Mussel abundances in the last 5+ years has led to a partial recovery of the pelagic food web (Pace et al 2010, Strayer et al 2011). Zebra Mussel veliger abundances in the Hudson River may not always be sufficient to contribute a large portion of the larval American Shad diet. In years of high abundances, veligers may contribute to year-class strength by increasing prey availability during the critical period of first feeding (Hjort 1926), which can have a profound effect on year-class size (May 1974). The benefits of veligers may also be limited over time due to the sequential spawning behavior of Zebra Mussels, which produce larvae over a period of 6–8 weeks (Nichols 1996). Zebra Mussel veliger presence in the stomachs of larval American Shad changed over the sampling period, making up only a negligible portion of the diet of the first 2 sampling periods. Wiktor (1958, reported in Molloy 1997) similarly found that feeding on Zebra Mussel veligers by larvae lasted ~2–4 weeks. The Levins’ B and standardized measure BA was very low for larval American Shad in the Hudson River, indicating a diet that was highly specialized and skewed (greatly dependent on a limited prey group). We found that niche breadth for larval American Shad was lower by half than all estuarine fishes from the Humber estuary described by Marshall (1995). When compared to other larval American Shad studies, the niche-breadth range we found in the Hudson River (Levins’ B = 1.95–2.04, BA = 0.13–0.18) was similar to the niche breadth of larval American Shad diets found in the literature (Levins’ B = 1.3–2.7, BA = 0.06–0.34). The highly specialized diet of larval American Shad suggests that mortality rates and cohort strength are highly dependent on the availability of Bosmina, cyclopoid copepods, and Zebra Mussel veligers. The nutritional value (protein and lipid content) of Zebra Mussel veligers and the ability of American Shad to digest them is still unknown. Some larval fishes have been found to feed substantially on veligers of other species, which provided nutritional benefits. Specifically, Gobiosoma bosc (Lacepède) (Naked Goby) and Hypsoblennius hentz (Lesueur) (Feather Blenny) larvae preferentially selected veligers of Crassostrea virginica (Gmelin) (Eastern Oyster) or Mercenaria mercenaria (L.) (Northern Quahog) even if the veligers were only 12% of the available food items (Harding 1999). Engraulis mordax Girard (North Pacific Anchovy) larvae grew in the laboratory on a diet of rotifers, Gymnodinium, and veligers (Lasker et al. 1970, Theilacker and McMaster 1971) although they very rarely eat veligers in nature (Arthur 1976). Govoni et al. (1986) reported that Leiostomus xanthurus Lacepède (Spot) larvae selectively feed on veligers in the Gulf of Mexico; these authors did not comment on digestibility. Paolucci et al. (2007) found veligers of the invasive Golden Mussel in the guts of 11 fishes in the Paraná River, Argentina. The larvae of 1 of these fishes, Prochilodus lineatus (Curimatidae), showed increased growth rates Northeastern Naturalist 446 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 when supplied with veligers or veliger-enhanced zooplankton mixtures (Paolucci et al. 2010a). Veligers of Golden Mussel had 3–5 times the proportion of lipids per body weight than Cladocera or Copepoda (Paolucci et al. 2010a). Other research has shown that for some fishes, veligers have little or no nutritional value. Scophthalmus maximus (L.) (Turbot) larvae pass lamellibranch bivalve veligers through the digestive system apparently unaltered (Conroy et al. 1993). Kane (1984) omitted bivalve veligers from his analysis of gadid larval foods because they “were found intact throughout the digestive tract”. In clupeids, Lebour (1924) documented that larval Clupea harengus L. (Atlantic Herring) selected veligers when available. In laboratory studies, small Atlantic Herring larvae ingested veligers but they showed little evidence of digestion (Checkley 1982). Herein, Zebra Mussel veligers did show signs of digestion in American Shad larvae in the Hudson River, although many were found still intact. Barnard et al. (2006) found that American Shad and Alewife had carbon-isotope signatures similar to and nitrogen-isotope signatures 1 trophic level above Zebra Mussel veligers, but did not report gut contents. Zebra Mussel veligers, cyclopoid copepods, and Bosmina cladocerans were the 3 major prey items consumed by larval American Shad in our study. American Shad larvae exhibited a narrow niche breadth making them vulnerable to high mortality in years of poor food availability. The presence of Zebra Mussel veligers could help reduce mortality, especially for American Shad ≤15.0 mm, by increasing prey availability. This benefit is limited to years with high veliger abundances and specific times of the year when veliger presence overlaps with larval presence. Although American Shad larvae are able to consume veligers, this does not mean that they are able to efficiently digest veligers or that veligers are a nutritious food source. Further studies need to be conducted to determine prey electivity by American Shad and if their feeding behavior changes depending on the abundance of Zebra Mussel veligers. Literature Cited Amundsen, P.-A., H.-M. Gabler, and F.J. Staldvik. 1996. A new approach to graphical analysis of feeding strategy from stomach-contents data: Modification of the Costello (1990) method. Journal of Fish Biology 48:607–614. Arthur, D.K. 1976. Food and feeding of larvae of three fishes occurring in the California Current, Sardinops sagax, Engraulis mordax, and Trachurus symmetricus. Fishery Bulletin 74:517–530. Atlantic Stated Marine Fisheries Commission (ASMFC). 2010. Amendment 3 to the Interstate Fishery Management Plan for Shad and River Herring (American Shad Management). Washington, DC. Barnard, C., C. Martineau, J. Frenette, J.J. Dodson, and W.F. Vincent. 2006. Trophic position of Zebra Mussel veligers and their use of dissolved organic carbon. Limnology and Oceanography 51(3):1473–1484. Belyaev, L.D., V.L. Galinsky, V.F. Nikitin, and M.A. Fatovenko. 1970. Fry in the Dniprodzerzhynsk water-storage and its feed base. Biological Processes in Sea and Continental Water Reservoirs. Pp. 42–43. Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 447 Binion, S.M. 2011. Evaluating spatial and temporal overlap between larval alosines and potential zooplankton prey in lower Roanoke River and Albemarle Sound, North Carolina. M.Sc. Thesis. East Carolina State University, Greenville, NC. Carlton, J.T. 2008. The Zebra Mussel, Dreissena polymorpha, found in North America in 1986 and 1987. Journal of Great Lakes Research 34:770–773. Checkley, D.M., Jr. 1982. Selective feeding by Atlantic Herring (Clupea harengus) larvae on zooplankton in natural assemblages. Marine Ecology Progress Series 9:245–253. Conroy, D.V.P., P.R.G. Trantor, and S.H. Coombs. 1993. Digestion of natural food by larval and post-larval Turbot Scophthalmus maximus. Marine Ecology Progress Series 100:221–231. Cooper, J.C., F.R. Cantelmo, and C.E. Newton. 1988. Overview of the Hudson River estuary. Pp. 11–24, In L.W. Barnthouse, R.J. Klauda, D.S. Vaughan, and R.L. Kendall (Eds.). Science, Law, and Hudson River Power Plants: A Case Study in Environmental Impact Assessment. American Fisheries Society, Monograph 4, Bethesda, MD. [# PP.?] Costello, M.J. 1990. Predator-feeding strategy and prey importance: A graphical analysis. Journal of Fish Biology 36:261–263. Crecco, V.A., and M.M. Blake. 1983. Feeding ecology of coexisting larvae of American Shad and Blueback Herring in the Connecticut River. Transactions of the American Fisheries Society 112:498–507. Crecco, V.A., and T.F. Savoy. 1985. Effects of biotic and abiotic factors on growth and relative survival of young American Shad (Alosa sapidissima) in the Connecticut River. Canadian Journal of Fisheries and Aquatic Sciences 42:1640–1648. Crecco, V.A., and T.F. Savoy. 1987. Review of recruitment mechanisms of the American Shad: The critical period and match–mismatch hypotheses reexamined. American Fisheries Society Symposium 1:455–468. Fossum, P. 1983. Digestion rate of food particles in the gut of larval Herring (Clupea harengus L.). Fiskeridirektoratets Skrifter. Serie Havundersoekelser 17:347–357. Giller, P.S. 1984. Community Structure and the Niche. Chapman and Hall, London, UK. Govoni, J.J., P.B. Ortner, F. Al-Yamani, and L.C. Hill. 1986. Selective feeding of Spot, Leiostomus xanthurus, and Atlantic Croaker, Micropogonias undulates, larvae in the northern Gulf of Mexico. Marine Ecology Progress Series 28:175– 183. Harding, J.M. 1999. Selective feeding behavior of larval Naked Gobies Gobiosoma bosc and Blennies Chasmodes bosquianus and Hypsoblennius hentzi: Preferences for bivalve veligers. Marine Ecology Progress Series 179:145–153. Hebert, P.D.N., B.W. Muncaster, and G.L. Mackie. 1989. Ecological and genetic studies on Dreissena polymorpha (Pallas): A new mollusc in the Great Lakes. Canadian Journal of Fisheries and Aquatic Science 46:1587–1591. Hjort, J. 1926. Fluctuations in the year classes of important food fishes. Journal du Conseil/ Conseil Permanent International pour l’Exploration de la Mer 1: 5–38. Hoffman, J.C., D.A. Bronk, and J.E. Olney. 2007. Contribution of allochthonous carbon to American Shad production in the Mattaponi River, Virginia, using stable isotopes. Estuaries and Coasts 30:1034–1048. Johnson, J.H., and D.S. Dropkin. 1995. Effects of prey density and short-term food deprivation on the growth and survival of American Shad larvae. Journal of Fish Biology 46:872–879. Johnson, J.H., and D.S. Dropkin. 1996. Feeding ecology of larval and juvenile American Shad (Alosa sapidissima) in a small pond. Journal of Applied Ichthyology 12(1):9–13. Johnson, J.H., and D.S. Dropkin. 1997. Food and prey selection of recently released American Shad (Alosa sapidissima) larvae. Journal of Freshwater Ecology 12(3):355–358. Northeastern Naturalist 448 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 Loomis, E.M., J.C. Sjoberg, W.H. Wong, and S. Gerstenberger. 2011. Abundance and stomach-content analysis of Threadfin Shad in Lake Mead, Nevada: Do invasive Quagga Mussels affect this prey species?. Aquatic Invasions 6:157. Kane, J. 1984. Feeding habitats of co-occurring cod and Haddock larvae from Georges Banks. Marine Ecology Progress Series 16:9–21. Karatayev, A.Y., D. Boltovskoy, D.K. Padilla, and L.E. Burlakova. 2007. The invasive bivalves Dreissena polymorpha and Limnoperna fortunei: Parallels, contrasts, potential spread, and invasion impacts. Journal of Shellfish Research 26:2 05–213. Lasker, R., H.M. Feder, G.H. Theilacker, and R.C. May. 1970. Feeding, growth, and survival of Engraulis mordax larvae reared in the laboratory. Marine Biology 5:345–353. Lebour, M.V. 1924. The food of young herring. Journal of the Marine Biological Association of the United Kingdom 13:325–330. Levins, R. 1968. Evolution in changing environments: Some theoretical explorations. Princeton University Press, Princeton, NJ. 120 pp. Limburg, K.E. 1996. Growth and migration of 0-year American Shad (Alosa sapidissima) in the Hudson River estuary: Otolith microstructural analysis. Canadian Journal of Fisheries and Aquatic Sciences 53:220–238. Limburg, K.E., and K. Arend. 1994. Zebra Mussel veligers observed in larval fish guts. Dreissena! 5:4. Limburg, K.E., M.L. Pace, D. Fischer, and K.K. Arend. 1997. Consumption, selectivity, and use of zooplankton by larval Striped Bass and White Perch in a seasonally pulsed estuary. Transactions of the American Fisheries Society 126:607–621. Limburg, K.E., K.A. Hattala, A.W. Kahnle, and J.R. Waldman. 2006. Fisheries of the Hudson River Estuary. Pp. 189–204, In J.S. Levinton and J.R. Waldman (Eds.). The Hudson River Estuary. Cambridge University Press, New York, NY. 471 pp. MacIsaac, H.J. 1996. Potential abiotic and biotic impacts of Zebra Mussels on the inland waters of North America. American Zoology 36:287–299. MacIsaac, H.J., C.J. Lonee, and J.H. Leach. 1995. Suppression of microzooplankton by Zebra Mussels: Importance of mussel size. Freshwater Biology 34:379–387. Mackie, G.L. 1991. Biology of the exotic Zebra Mussel, Dreissena polymorpha, in relation to native bivalves and its potential impact in Lake St. Clair. Hydrobiologia 219:251–268. Marshall, S. 1995. The structure and functioning of the fish assemblage of the Humber Estuary, UK. Unpublished Ph.D. Dissertation. University of Hull, Yorkshire, UK. Marshall, S., and M. Elliott. 1997. A comparison of univariate and multivariate numerical and graphical techniques for determining inter- and intraspecific feeding relationships in estuarine fish. Journal of Fish Biology 51:526–545. May, R.C. 1974. Larval mortality in marine fishes and critical period concept, Pp. 3–19, In J.H.S. Blaxter (Ed.). The Early Life History of Fish. Springer-Verlag, Heidelberg, Germany. 768 pp. Miller, T.J., L.B. Crowder, J.A. Rice, and E.A. Marschall. 1988. Larval size and recruitment mechanisms in fishes: Toward a conceptual framework. Canadian Journal of Fisheries and Aquatic Sciences 45:1657–1670. Mills, E.L., R. O’Gorman, E.F. Roseman, C. Adams, and R.W. Owens. 1995. Planktivory by Alewife (Alosa pseudoharengus) and Rainbow Smelt (Osmerus mordax) on microcrustacean zooplankton and dreissenid (Bivalvia: Dreissenidae) veligers in southern Lake Ontario. Canadian Journal of Fisheries and Aquatic Science 52:925–935. Molloy, D.P., A.Y. Karatayev, L.E. Burlakova, D.P. Kurandina, and F. Laruelle. 1997. Natural enemies of Zebra Mussels: Predators, parasites, and ecological competitors. Reviews in Fisheries Science 527–97. Northeastern Naturalist Vol. 22, No. 2 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 449 Nack, C.C., K.E. Limburg, and D. Miller. 2014. Assessing the quality of four inshore habitats used by post-yolk-sac Alosa sapidissima (Wilson 1811) in the Hudson River: A Prelude to Restoration. Restoration Ecology 23(1):57–64. Nalepa, T.F., D.J. Hartson, D.L. Fanslow, G.A. Lang, and S.J. Lozano. 1998. Declines in benthic macroinvertabrate populations in southern Lake Michigan, 1980–1993. Canadian Journal of Fisheries and Aquatic Sciences 55:2402–2413. Nichols, S.J. 1996. Variations in the reproductive cycle of Dreissena polymorpha in Europe, Russia, and North America. American Zoology 36:3111–325. Pace, M.L., S.E.G. Findlay, and D. Lints. 1992. Zooplankton in advective environments: The Hudson River community and a comparative analysis. Canadian Journal of Fisheries and Aquatic Sciences 14:1060–1069. Pace, M.L., S.E.G. Findlay, and D.T. Fischer. 1998. Effects of an invasive bivalve on the zooplankton community of the Hudson River. Freshwater Biology 39:103–116. Pace, M.L., D.L. Strayer, D.T. Fischer, and H.M. Malcom, 2010. Recovery of native zooplankton associated with increased mortality of an invasive mussel. Ecosphere 1:W07415. Paolucci, E.M., D.H. Cataldo, C.M. Fuentes, and D. Boltovskoy. 2007. Larvae of the invasive species Limnoperna fortunei (Bivalvia) in the diet of fish larvae in the Paraná River, Argentina. Hydrobiologia 589:219–233. Paolucci, E.M., D.H. Cataldo, and D. Boltovskoy. 2010a. Prey selection by larvae of Prochilodus lineatus (Pisces: Curimatidae): Indigenous zooplankton versus veligers of the introduced bivalve Limnoperna fortunei (Bivalvia: Mitilidae). Aquatic Ecology 44:255–267. Paolucci, E.M., E.V. Thuesen, D.H. Cataldo, and D. Boltovskoy. 2010b. Veligers of an introduced bivalve, Limnoperna fortunei, are a new food resource that enhances growth of larval fish in the Paranά River (South America). Freshwater Biology 55:1831–1844. Pianka, E.R. 1988. Evolutionary Ecology, 4th Edition. Harper Collins, New York, NY. Rosen, R.A. 1981. Seasonal cycles, distribution, and biomass of crustacean zooplankton and feeding and growth of young American Shad (Alosa sapidissima) in the Holyoke Pool, Connecticut River. Ph.D. Dissertation. University of Massachusetts Amherst, Amherst, MA. Savoy, T.F., and V.A. Crecco. 1988. The timing and significance of density-dependent and density-independent mortality of American Shad, Alosa sapidissima. Fisheries Bulletin 86:467–482. Skubunna, J.P., T.G. Coon, and T.R. Batterson. 1995. Increased abundance and depth of submersed macrophytes in response to decreased turbidity in Saginaw Bay, Lake Huron. Journal of Great Lakes Research 21:476–488. Smith, T.E., R.J. Stevenson, N.F. Caraco, and J.J. Cole. 1998. Changes in phytoplanktoncommunity structure during the Zebra Mussel (Dreissina polymorpha) invasion of the Hudson River, New York. Journal of Plankton Research 20:1567–1579. Strayer, D.L., and H.M. Malcom. 2013. Long-term changes in the Hudson River’s bivalve population: A history of multiple invasions (and recovery?). Pp. 71–81, In T.F. Nalepa and D.W. Schloesser (Eds.). Quagga and Zebra Mussels: Biology, Impacts, and Controls, 2nd Edition. CRC Press, Boca Raton, FL. 815 pp. Strayer, D.L., and L.C. Smith. 2001. The zoobenthos of the freshwater–tidal Hudson River and its response to the Zebra Mussel (Dreissena polymorpha) invasion. Archiv für Hydrobiologie Supplement (Monographic Studies) 131:1–52. Northeastern Naturalist 450 C.C. Nack, K.E. Limburg, and R.E. Schmidt 2015 Vol. 22, No. 2 Strayer, D.L., K.A. Hattala, and AW. Kahnle. 2004. Effects of an invasive bivalve (Dreissena polymorpha) on fish in the Hudson River estuary. Canadian Journal of Fisheries and Aquatic Science 61:924–941. Strayer, D.L., N. Cid, and H.M. Malcom. 2011. Long-term changes in a population of an invasive bivalve and its effects. Oecologia 165:1063–1072. Sutela, T., and A. Huusko. 2000. Varying resistance of zooplankton prey to digestion: Implications for quantifying larval fish diets. Transactions of the American Fisheries Society 129:545–551. Theilacker, G.H., and M.F. McMaster. 1971. Mass culture of the rotifer Brachionus plicatilis and its evaluation as a food for larval Anchovies. Marine Biology 10:183–188. Wang, J.C.S., and R.J. Kernehan. 1979. Fishes of the Delaware Estuaries: A Guide to the Early Life Histories. Ecological Analysts, Inc., Towson, MD. Wiktor, K. 1958. Larvae of Dreissena polymorpha Pallas, as a food for fish spawn. Pneglad Zoology 2:182–184. (in Polish). Wilhite, M.L., K.L. Maki, J.M. Hoenig, and J.E. Olney. 2003. Toward validation of a juvenile index of abundance for American Shad in the York River, Virginia. American Fisheries Society Symposium 35:285–294. Winkler, G., P. Sirois, L.E Johnson, and J.J Dodson. 2005. Invasion of an estuarine transition zone Dreissena polymorpha had no detectable effect on zooplankton-community structure. Canadian Journal of Fisheries and Aquatic Science 62:578–592. Wooton, R.J. 1990. Ecology of Teleost Fishes. Chapman and Hall, London, UK. 292 pp.