Predation on Zebra Mussels by Freshwater Drum and Yellow Perch in Western Lake Erie

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1 J. Great Lakes Res. 23(2): Internat. Assoc. Great Lakes Res., 1997 Predation on Zebra Mussels by Freshwater Drum and Yellow Perch in Western Lake Erie T.W. Morrison, W.E. Lynch Jr. & K. Dabrowski School of Natural Resources The Ohio State University 2021 Coffey Rd. Columbus, Ohio Abstract. Although considerable research has been done regarding zebra mussel (Dreissena polymorpha) expansion in the Great Lakes, information on fish species preying on zebra mussels is lacking. We examined diets of freshwater drum (Aplodinotus grunniens) and yellow perch (Perca flavescens) collected in western Lake Erie, Stomach contents were quantified in May, July, and October to examine the importance of zebra mussels in the diets and to determine if either fish species exhibited size-selective feeding. Zebra mussels were consumed by freshwater drum and yellow perch once they reached 250 mm and 150 mm total length, respectively. Consumption by freshwater drum was highest in May and July and lowest in October. Most yellow perch consumption occurred in May. Chesson 's alpha indicated that freshwater drum less than 350 mm TL and yellow perch less than 200 mm TL selected small zebra mussels and generally rejected larger individuals. Larger fish exhibited less selectivity, consuming zebra mussels in proportion to their estimated availability in western Lake Erie. Small fish just beginning to prey on zebra mussels may be physically limited to small sizes or clumps by their pharyngeal gape and musculature. Larger freshwater drum and yellow perch are restricted more by the sizes of zebra mussels available on the surface of the substrate and possibly the size of clumps which they remove, rather than by their physical abilities to crush any one size. This may explain the strong selection for small zebra mussels by both species even though they are capable of eating larger sizes. INDEX WORDS: Zebra mussel, yellow perch, freshwater drum, Lake Erie.

2 Introduction Zebra mussels (Dreissena polymorpha) were first collected in the Great Lakes in Lake St. Clair, The introduction probably resulted from the discharge of freshwater ship ballast around 1986 (Hebert et al. 1989). This prolific spawner has colonized much of the Great Lakes, attaining densities of up to 341,000 individuals m -2 in western Lake Erie (MacIsaac et al. 1991). The ability of zebra mussels to form high-density colonies has led to a myriad of research efforts in recent years, ranging from their effects on ecosystems (Wu and Culver 1991) to methods for their control (Fisher et al. 1991). Consumption of zebra mussels by European fish species has been documented (Stein et al. 1975, Olszewski 1976, Prejs 1976, Martyniak et al. 1987), but few studies have examined the feeding ecology of fishes that eat zebra mussels in North America. French (1993) noted that at least six North American species are potential predators because they possess pharyngeal teeth and/or chewing pads for crushing mollusk shells. However, he also noted that zebra mussels are found in the diets of several Great Lakes species lacking teeth or pads. Exotic species such as the round goby (Neogobius melanostomus) have also made use of zebra mussels in their diets (Jude et al. 1995). In Lake Erie, freshwater drum (Aplodinotus grunniens) and yellow perch (Perca flavescens) consume zebra mussels although only freshwater drum have pharyngeal teeth (French and Bur 1993, French 1993). One of our objectives is to quantify seasonal diets of freshwater drum and yellow perch and qualitatively compare our 1992 results with diet information for freshwater drum from French and Bur's (1993) 1990 data. This comparison may provide insight into whether diets of these two important fish species changed in response to the continual progression of zebra mussel colonization. It is unknown whether North American fish species exhibit size-selective predation on zebra mussels similar to that exhibited by roach (Rutilus rutilis) in Europe (Olszewski 1976, Prejs et al. 1990). In the initial stages of the zebra mussel colonization of Lake Erie, French (1993) found that freshwater drum consumed zebra mussels less than 25 mm long. Continued colonization may result in increased availability of larger zebra mussels and allow molluscivores to selectively prey on these larger sizes and maximize energy return. Prejs et al. (1990) found that roach optimally foraged on zebra mussels, concentrating on numerous, easily accessible size classes. We examined whether freshwater drum and yellow perch selectively consumed specific sizes of zebra mussels and explored how mouth and throat morphology influenced their predation. Methods F i s h C o l l e c t i o n s Freshwater drum and yellow perch were collected in conjunction with Ohio Department of Natural Resources, Division of Wildlife's scheduled surveys in May, July, and October, Survey sites were randomly selected from grid squares in western Lake Erie. Each grid was a 2.5-by 2.5-min latitude x longitude section of Lake Erie. Grid sites were unevenly distributed across the following depth strata: < 3 m; 3-6 m; 6-9 m; and 9 m (Fig. 1). Neither fish species was evenly sampled at every site, therefore we were unable to evaluate diet across depths and sites. Rather, fish were kept as they were encountered. Fish were collected using a semi-balloon bottom trawl with a m headrope and 6.4-mm mesh in the cod end. All tows averaged 0.8 m s -1 and lasted 10 min. We kept a maximum of 25 fish each month from each of four size groups of yellow perch (50-mm intervals; mm) and five groups of freshwater drum (50-mm intervals; mm). All fish retained for stomach analysis were quickfrozen on dry ice to stop digestion.

3 To estimate the size distribution of zebra mussels available to fish, we used SCUBA in May-July to randomly collect rocks with zebra mussels in the Marblehead (mainland) and Green Island (offshore) areas of western Lake Erie. All zebra mussels were removed from the rocks and separated from each other, measured with calipers, and assigned to 1-mm size classes. L a b o r a t o r y A n a l y s i s Morphology Fish were thawed and measured (mm total length, TL). Pharyngeal gape was measured (mm) for all freshwater drum (N = 66) and yellow perch (N = 61) collected in May using wood/plastic dowels, a method described by Wainwright (1987). Dowel diameters ranged from 3.2 to 25.4 mm with intervals of 1.6 mm. Dowels were inserted into the pharyngeal gape until we encountered a dowel that would not fit. The diameter of the largest dowel that fit was the pharyngeal gape measurement. The zebra mussel's anterior abductor muscle attaches to two internal septa, which are usually undamaged when ingested by fish (Prejs et al. 1990). We measured right septa and corresponding shell length, width, and height from 100 Lake Erie zebra mussels ranging in length from 3 to 35 mm. Measurements of septa were made using a dissecting microscope at 40X magnification; length, width, and height measurements of whole zebra mussels were made using calipers. We generated regression equations of septa length versus shell length, width, and height and used them to calculate dimensions of zebra mussels ingested by fish.

4 Diet The entire gastrointestinal tracts were removed and preserved in 95% alcohol. Stomach contents were identified under a dissecting microscope (up to 40X). Fish were identified to species, mollusks to genus, and other invertebrates to order when possible. High abundance of zooplankton in July samples necessitated subsampling, using methods described by Edmondson (1974). Random 2-mL subsamples were analyzed until either 50 Leptodora sp. or 75 cladocerans of the most abundant genus were counted and measured. Except for fish, a reference body part (usually head capsule or total length) was measured with an ocular micrometer for each ingested prey item. Prey TL was calculated using equations provided in Appendix 1. These TLs were then used to calculate individual dry weight of prey items eaten (Appendix 2). For fish, standard or backbone lengths were recorded when possible and converted to total length using equations from Knight (1983). Wet weight of individual fish was calculated from TL with equations developed by Hartman and Margraf (1992). Dry weight of fish was 23% of wet weight (Dabrowski 1979). Because stomachs often yielded few zebra mussels for assessing size-selective feeding, we also used mussels in the intestines, calculating their size from the zebra mussel septa length equation. No attempt was made to identify other material in the intestine, thus intestinal contents were not used for assessing diet composition. A n a l y t i c a l M e t h o d s To compare zebra mussel populations between our two collection sites, we used Kolomogorov-Smirnov's two-sample test (Hollander and Wolfe 1973). Similar frequencies would allow us to combine sites for use in evaluating size-selective predation by fish. To evaluate size-selective predation, diets of freshwater drum and yellow perch were analyzed using Chesson's alpha (Chesson 1978, 1983), treating individual fish within a length group as replicates. Chesson's alpha is calculated as follows: p i is the proportion of zebra mussel size class i from our estimated zebra mussel size distribution, and r i is the proportion of zebra mussel size class i in the fish's diet. Preference for various 1-mm mussel size classes was determined by comparing mean (± 1 SE) alpha values for a size class with the alpha expected had that size class been eaten in proportion to that size's availability. Expected alphas are the reciprocal of the number of size classes (N = 35) we estimated to be in the western Lake Erie zebra mussel size distribution (sites combined). Alpha values greater than the reciprocal indicate positive selection for a particular mussel size class. Mean alphas (all months combined) were calculated for three freshwater drum length groups ( , , 350+ mm TL) and two length groups of yellow perch (<200, 200 mm TL). Results M u s s e l - S e p t a R e l a t i o n s Significant positive linear relations were found between septa length and total length (y = 0.263x , r 2 = 0.958, P 0.001), width (y = 0.124x , r 2 = 0.917, P 0.001), and height (y = 0.130х , r 2 = 0.928, Р 0.001) of zebra mussels collected from western Lake Erie. Our zebra mussel shell length/septa length relation was similar to that reported by Prejs et al. (1990) for populations in Poland.

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6 Freshwater Drum D i e t C o m p o s i t i o n Diets varied by month and fish size (Table 1). Zebra mussels were present in May and July stomachs from freshwater drum larger than 250 mm TL. Highest consumption occurred in the largest (350+ mm) size group, up to 33% of estimated dry weight volume in May and 21% in July. Often, we found several septa attached to shell fragments from other zebra mussels indicating fish were eating "clumps" of zebra mussels. Zebra mussels were absent from the diets of all freshwater drum in October. Chironomids were important in the diets of all freshwater drum in May, for mm fish in July, and unimportant for all sizes during October. Zooplankton were absent from most stomachs in May and October; however, all sizes of freshwater drum, except the largest group, consumed zooplankton in July, although dry weight contributions were small. Fish were an important diet component for freshwater drum larger than 250 mm TL in July and more so in October ( 93% of estimated dry weight volume), but not in May. Gizzard shad (Dorosoma cepedianum) and shiners (Notropis spp.) were the primary prey fish eaten. Yellow Perch Diets also varied considerably among months and fish sizes (Table 2). Zebra mussels were found in all sizes of yellow perch in May, but were most common in fish larger than 200 mm TL. Zebra mussels were only occasionally eaten in July and October. Like freshwater drum, yellow perch apparently ate clumps of zebra mussels. Chironomids were very important prey in May, less so in July, and generally were absent in October. Trichoptera and zooplankton were prevalent for all sizes of yellow perch in July, but were rarely eaten in May and October. Amphipods were eaten in all 3 months. Fish were eaten by all sizes of yellow perch in July but only by yellow perch larger than 150 mm TL in October. Similar to freshwater drum, gizzard shad and shiners were the primary fish species eaten. S i z e - S e l e c t i v e P r e d a t i o n o n M u s s e l s Pharyngeal Gape Considerations Most zebra mussels eaten by freshwater drum and yellow perch were smaller than the pharyngeal gape of the fish eating them (Figs. 2 and 3). However, the largest zebra mussels eaten did exceed (in length) the estimated pharyngeal gape. Widths and heights of ingested zebra mussels were considerably less than the gape. Because zebra mussel height is roughly equal to width, we only show data on width's of mussels eaten. As lengths of freshwater drum and yellow perch increased, lengths, widths, and heights of consumed zebra mussels changed little. Nearly horizontal slopes of the following relations confirm this: freshwater drum length versus zebra mussel length (у = О.ООЗх ; r 2 = 0.017; p ) and width (y = 0.007x ; r 2 = 0.017; p ); yellow perch length versus zebra mussels length (y = 0.016x ; r 2 = 0.082; p ) and width (y = 0.034x ; r 2 = 0.082; p < ). Mussel Availability Length distributions of zebra mussels collected from two Lake Erie locations had modes of 7 mm with few individuals larger than 20 mm (Fig. 4). Distributions were skewed toward the smaller sizes of 5-12 mm at both locations. Larger (> 12 mm) zebra mussels were more prevalent at Green Island. The Kolomogorov-Smirnov twosample test confirmed that the zebra mussels sampled at these locations can be considered to be from the same population (p = 0.14).

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12 Fish Size Selectivity Freshwater drum feeding selectively on various zebra mussel sizes was affected by fish size (Fig. 5). Freshwater drum less than 350 mm selected strongly for zebra mussels 4-6 mm long; indices less than 0.03 for zebra mussels larger than 11 mm indicate they were not eaten in proportion to their estimated abundance in Lake Erie. Zebra

13 mussels larger than 14 mm were rarely found in the gastrointestinal tracts. Larger freshwater drum ( 350 mm) selected for 3-10 mm zebra mussels and against zebra mussels greater than 13 mm. Thus, larger freshwater drum exhibited a greater willingness to consume longer (1-4 mm) zebra mussels than did their smaller conspecifics. Differences in selective predation on zebra mussels by two sizes of yellow perch were also evident (Fig. 6). Small (< 200 mm) yellow perch showed selection for zebra mussels smaller than 6 mm long although variability among fish was high. In general, these fish rarely ate zebra mussels greater than 10 mm. Larger (> 200 mm) yellow perch selected against the largest zebra mussels (> 20 mm) and consumed 1-15 mm zebra mussels in percentages either greater than or equal to their proportion in the lake. Discussion The recent invasion of Lake Erie by zebra mussels presents a new prey for freshwater drum, a fish long known to be molluscivorous (Forbes 1890). Freshwater drum have used this new food source but not to the exclusion of other prey. Our data corroborate past studies in Lake Erie that found Diptera (primarily chironomids), Trichoptera, Cladocera, and fish to be seasonal components in freshwater drum diets (Griswold and Tubb 1977, Bur 1982, Cunningham 1989). Seasonal shifts in the diet suggest freshwater drum are opportunistic feeders. Stomach contents reflect seasonal changes in abundances of potential prey. From a recent study (French and Bur 1993), we can compare the importance of zebra mussels to the diets of freshwater drum in 1990 with that in In both years, freshwater drum ate zebra mussels in May and July, consumption being greatest for larger fish. Smaller fish also consumed zebra mussels but Diptera were more prevalent in their diets. Neither study showed a high frequency of occurrence of zebra mussels in fish smaller than 375 mm, up to 28% in 1990 and 43% in French and Bur (1993) did find zebra mussels to be prevalent in fish larger than 375 mm; we sampled few fish this large. Another similarity was the increased importance of prey fish in fall: about 50% of biomass in 1990 and nearly 100% in The major discrepancy between the two studies is that zebra mussels were consumed in fall 1990 compared with their total absence in our fall 1992 stomach samples. Reasons for this are not clear, but we do know that prey fish abundance was not a factor. Prey fish abundances in summer-fall 1992, as determined from Ohio Division of Wildlife trawl samples, were generally lower than in 1990 (Knight and Turner 1993), yet nearly 100% of the 1992 diets consisted of fish. If prey abundances had been greater in 1992, then higher fish consumption may have been expected. Adult yellow perch are largely piscivorous but will also eat a wide variety of prey types when fish are not abundant. Shifts in diets from benthic invertebrates (mainly Diptera) in early spring to prey fish in the summer and fall are well documented for Lake Erie (Knight et al. 1984, Schaeffer and Margraf 1986, Parrish 1988). In early spring, prey fish are less abundant than in summer and fall months; consequently, yellow perch need to use other food sources. Zebra mussels are abundant year-round and consequently, they have the potential to be an additional food source when other prey are in short supply. This appears to have occurred, particularly for adult yellow perch. Although zebra mussels were found in stomachs in each of the 3 months, use was considerably greater in May when prey fish were not abundant. In July and October, yellow perch diets shifted to fish. The presence of abundant zebra mussel populations did not change the seasonal diet shifts of yellow perch; rather, they provided an additional benthic prey resource that appeared to be more important in spring. Predation by freshwater drum and yellow perch on zebra mussels may reflect changes in seasonal energy content of these mussels. The highest predation on zebra mussels

14 coincides with the period when energy content of zebra mussels may be highest. Dry organic biomass and lipid levels are higher in late May and June, these levels decline throughout summer reaching their lowest levels in October and November (Dorgelo and Kraak 1993, Nalepa et al. 1993). Garton and Haag (1993), working in Lake Erie, attributed these declines in weight and lipid content to reductions in phytoplankton populations in late spring and culmination of spawning in late summer. Fish are known to alter their feeding behavior to increase energy intake (Ringler 1979, Weisberg and Lotrich 1982). The sense of taste is often associated with lipid concentrations within the prey item and can be the basis for acceptance or rejection (McBride et al. 1962). If fish sensed a lower lipid content, this could explain the absence of zebra mussels in fall diets even though this prey is abundant throughout Lake Erie. Our study indicates that the threshold size at which freshwater drum and yellow perch begin to prey on zebra mussels appears to be about 250 mm TL and 150 mm, respectively. French and Bur (1993) found similar results, reporting that freshwater drum smaller than 250 mm fed rarely on zebra mussels. We found zebra mussels in freshwater drum as small as 200 mm. However, these zebra mussels were small (< 5 mm) and unfragmented. These mussels were always accompanied by other benthic prey suggesting they may have been inadvertently swallowed while grasping and eating other prey items. Similarly, yellow perch smaller than 150 mm swallowed small zebra mussels whole and probably not intentionally. Typically, these small (< 3 mm) mussels in the stomachs were found with amphipods that often inhabit zebra mussel colonies. Mouth measurements, when compared with zebra mussel width and height measurements, suggest that smaller fish should be able to eat zebra mussels less than 6 mm, sizes that were abundant in Lake Erie. Similarly, Prejs et al. (1990) found that roach less than 160 mm did not eat small zebra mussels even though they were an abundant prey. They provided convincing evidence that these small roach would only be able to take small zebra mussels at a very high cost/benefit ratio. It is possible that the same argument applies for small freshwater drum and yellow perch. Both Gatz (1970) and Zaret (1980) showed that mouth morphology and pharyngeal cavity are important in determining prey choices among fishes. Morphological features such as strength of crushing musculature, the musculature needed to remove zebra mussels off rocks, pharyngeal cavity size, and calcification or maturation of teeth could influence a predator's ability to eat zebra mussels. Mouth measurements indicate yellow perch and freshwater drum are both capable of handling larger zebra mussels than are usually consumed. We found occasional crushed mussels up to 21 mm in stomachs or intestines. French (1993) found individuals up to 25 mm in larger freshwater drum. However, neither species preys substantially on large zebra mussels. Rather, freshwater drum and yellow perch consume small (< 6 mm) zebra mussels, sizes that are considerably smaller than they are capable of handling. Two types of musculature strength are required to prey on zebra mussels: 1) strength to remove zebra mussels from the substrate and 2) strength to crash the removed mussels prior to ingestion. Strengths to accomplish these tasks are affected both by the development of the fish predator and the zebra mussels. Additional factors such as substrate type, area of shell exposed, and colony size all affect the required strengths. Although these factors certainly should limit the maximum edible size and probably influence when fish can become molluscivorous, we doubt this accounts for the positive selection for small zebra mussels. All sizes of freshwater drum and yellow perch successfully crushed adequate numbers of larger mussels to convince us that sufficient musculature strength was available to prey on larger zebra mussels should the fish elect to do so. The ability of freshwater drum and yellow perch to prey on zebra mussels may be influenced by the zebra mussel's ability to form large, dense colonies. Studies indicate that up to 90% of the Lake Erie zebra mussel population is less than 11 mm in length (Griffiths et al. 1991, Bunt et al. 1993, Fig. 3). Prejs et al. (1990) estimated that 80-

15 95% of all zebra mussels smaller than 12 mm are exposed to predation because they settle on the shells of others building colonies, and these upper layers almost always contain the least firmly attached individuals. If fish randomly graze on individual zebra mussels only on the surface, the majority of mussels eaten would be between 2 and 11 mm. Our data suggest this to be a plausible explanation for why small zebra mussels dominate the diets of freshwater drum and yellow perch. Zebra mussel colony patterns may promote an alternative feeding strategy that explains the size frequencies of zebra mussels found in stomachs. We suspect freshwater drum and yellow perch quite often remove clumps of zebra mussels for consumption rather than eating individual mollusks. Although our study did not allow for direct viewing of fish feeding, the common occurrence of septa from several individuals still being attached to shell pieces from another zebra mussel in fish stomachs supports this possibility. If all sizes of freshwater drum and yellow perch were removing clumps from the tops of the colonies, zebra mussel size frequencies consumed (and mean length) should be similar across fish sizes. We found this to be the case. In this scenario, size of the clumps that could be removed may have been the limiting factor, not size of individual zebra mussels. Eating clumps of zebra mussels may also provide energetic benefits and allow these fish species to optimally forage. Traditional optimal foraging theory was based on a predator searching, chasing, and consuming individual prey. In molluscivores preying on zebra mussels, we suggest that maximum energy return results from eating mouthfuls or clumps rather than individual mussels. Large zebra mussels might be energetically preferable to a fish predator, but may not be available to fish because they are buried under smaller individuals in a typical zebra mussel colony. The costs of removing and crushing individual 2-6-mm zebra mussels would be high given that these small mussels have energy values less than 50 joules per mussel (Draulans and Wouters 1988). Removing clumps of zebra mussels not only allows these fish to maximize energy return from small mussels but, also allows for the occasional consumption of larger, anchoring individuals which would provide greater energy return. It is interesting to consider why zebra mussels are not more prevalent in the diets of these two species, particularly freshwater drum, given its molluscivorous reputation and the finding that individual stomachs occasionally contained hundreds of these mussels. In addition, zebra mussels are a sedentary prey and the sizes selected are extremely abundant, essentially providing an unlimited food resource. Clearly there are factors underlying the predation patterns exhibited by these two species. Handling costs, seasonal energy content fluctuations in zebra mussels, energy gained from zebra mussels versus other prey, and evolution toward other food resources could all be important factors. Additional research is needed to further explore the mechanisms causing these predation patterns by freshwater drum and yellow perch, two important Lake Erie fishes. Acknowledgments This study was conducted for and funded by the United States Environmental Protection Agency, Project CR Additional salaries and research support were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. We thank the Sandusky Research Station of the Ohio Department of Natural Resources, Division of Wildlife for graciously allowing us to make our collections as they conducted their standardized sampling schedule. We thank Mike Bur, Roger Knight, and Jennifer Tomsen for their critical reviews of drafts of this manuscript.

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