Burbot Growth and Diets in Lakes Michigan and Huron: an Ongoing Shift from Native Species to Round Gobies

Burbot Growth and Diets in Lakes Michigan and Huron: An Ongoing Shift from Native Species to Round Gobies

Stephen R. Hensler* and David J. Jude University of Michigan, School of Natural Resources and Environment 440 Church Street, Ann Arbor, Michigan 48109, USA

Ji He Michigan Department of Natural Resources 160 East Fletcher Street, Alpena, Michigan 49707, USA

Abstract.—Burbot Lota lota is a native species of cod (Gadidae) found in the coldwater regions of all five Laurentian Great Lakes. Burbot age-at-length data from along western Lake Huron showed that fish reached 18 years of age. Fish age 7 and younger grew more slowly in southern Lake Huron than in north-central and northern Lake Huron, while this trend was reversed for fish ≥ 8 years old. Burbot growth and diet data were recorded for fish collected near Leland, Fairport, and Bridgman (D. C. Cook nuclear power plant), Michigan and Washington Island, Wisconsin in Lake Michigan and Alpena, Michigan in northern Lake Huron to determine changes in growth and diet with the recent invasion of the nonindigenous round goby Neogobius melanostomus. We compared burbot growth at four length intervals (500–800 mm) among these locations and found significantly lower growth at Alpena compared with the other sites; burbot from Bridgman at 500 and 600 mm were the lightest among all sites. Burbot diets have changed substantially in some areas from native fish and invertebrate species to a diet that includes large proportions of the nonindigenous round goby (77% by wet weight in Lake Huron near Alpena, 53% in Lake Michigan near Fairport). Establishment of round gobies in the open waters of the Great Lakes is likely to change coldwater food webs, including replacement of sculpins (Cottus spp.) at depths up to 70 m, where round gobies have been found. Burbot, whose diets were composed of large amounts of round gobies, showed lower growth, and there is a potential for decreased bioaccumulation of toxic substances because round gobies consume zebra mussels Dreissena polymorpha and quagga mussels D. bugensis, which are lower in the food chain than organisms that native species eat.

Introduction namaycush as the two most important top predators in these coldwater lakes (Ward et Burbot Lota lota, a top predator with a cir- al. 2000). Lake trout were extirpated in all cumpolar distribution, inhabit the coldwa- the Great Lakes except Lake Superior, while ter regions of the Great Lakes. Historically, burbot populations were greatly depressed in they coevolved with lake trout Salvelinus Lake Michigan and other Great Lakes during the 1950s (Wells and McLain 1973), fol- * Corresponding author: [email protected] lowing colonization by the invasive sea lam- 91 92 hensler et al. prey Petromyzon marinus (Lavis et al. 2003). tario (McCrimmon and Devitt 1954). How- Burbot are particularly susceptible to sea ever, diets of burbot in Lake Michigan shift- lamprey predation (Swink 2003), and their ed in the late 1980s to more nonindigenous larvae are also preyed on by alewives Alosa species, since Fratt et al. (1997) found that pseudoharengus (Eshenroder and Burnham- alewife and rainbow smelt Osmerus mordax Curtis 1999), which delayed burbot recovery composed 56% of the diet. In contrast, Fratt in Lake Michigan until the 1980s (Madenjian et al. (1997) also found that diets of burbot et al. 2002). Burbot were likely able to sur- from Green Bay waters of Lake Michigan vive and rebound from sea lamprey predation more than 40 m deep changed little from the in the Great Lakes due to their high fecundity 1930s and were similar to that found in Lake (up to 1 million eggs/female [Bailey 1972]), Superior fish in the 1960s (Bailey 1972). early age at maturity (Swink and Fredericks Burbot may compete with important sport 2000), and spawning in tributaries (Mansfield fish because burbot inhabit sensitive rocky et al. 1983) and on reefs in lakes. areas, which are prime feeding and spawning Burbot is a coldwater, benthic species with sites for lake trout and lake whitefishCorego - a varied diet. Its main food items are other fish nus clupeaformis, with implications for pre- and invertebrates, with the proportion of fish dation on their eggs, newly hatched fry, and in the diet increasing with size (Guthruf et al. stocked yearlings. Burbot also might compete 1990; Rudstam et al. 1995). Large burbot are with lake trout for food (Edsall et al. 1993; comparable to northern pike Esox lucius in Jones et al. 1995). Janssen et al. (2006a) have their loss of swimming stamina to increasing recently reported natural reproduction of lake velocities (Jones et al. 1974), but they are vo- trout on Lake Michigan’s mid-lake reef com- racious feeders, adapted to stalking (Hackney plex, where burbot may be implicated in their 1973) and hunting from ambush (Boyer et al. currently low survival rates. Slimy sculpin 1989) and taking advantage of the absence of Cottus cognatus and burbot also prey on lake light (Scott and Crossman 1973; Jones et al. trout eggs (Janssen et al. 2006a) and probably 1974). On soft substrates, they often inhabit fry; hence, removal of slimy sculpins by bur- trenches that they excavate (Boyer et al. 1989; bot may indirectly affect lake trout survival. Edsall et al. 1993). Because of their docu- The burbot as a keystone predator is also mented feeding on emerald shiners Notropis involved in recent dramatic changes in food atherinoides, a pelagic species, burbot some- webs induced by the nonindigenous round goby times forage in the water column and migrate Neogobius melanostomus, which entered the long distances, including to shallow water, in Great Lakes during 1990 with a ballast water search of food (Clemens 1951; McCrimmon deposit (Jude et al. 1992). Round gobies have and Devitt 1954). since spread to all the Great Lakes and the Mis- Historically, native cottids and corego- sissippi River watershed. Round gobies eat ze- nines were eaten by burbot in Lake Michigan bra mussels Dreissena polymorpha and quagga (Van Oosten and Deason 1938). Food habits of mussels D. bugensis (French and Jude 2001; D. burbot in other waters included yellow perch J. Jude, unpublished data), an abundant food Perca flavescens in Mille Lacs Lake, Minne- supply and potential source of contaminants, sota (Bonde and Maloney 1960) and Heming and have been responsible for extirpation of Lake, Manitoba (Lawler 1963), while yel- mottled sculpin C. bairdii (Janssen and Jude low perch, cisco (also known as lake herring) 2001) and greenside darter Etheostoma blen- Coregonus arteii, and emerald shiners were nioides (Jude 2001) in areas of habitat overlap. eaten in river mouths of Lake Simcoe, On- Hence, how the appearance of round gobies burbot growth and diets in lakes michigan and huron 93 in burbot diets will affect burbot growth and Resources (MDNR) surveys and commercial perhaps ameliorate the negative interactions fisherman in Michigan and Wisconsin at five between round gobies and native species is a locations (Table 1; Figure 1). Fish were col- critical information gap in the Great Lakes. lected from Lake Michigan at Leland, Michi- There have been two recent ecosystem gan (n = 25), Fairport, Michigan (n = 118), level changes, which have changed energy and Washington Island, Wisconsin (n = 120) flow to top predators and caused shifts of fish- and from Lake Huron at Alpena, Michigan (n es to deeper waters (O’Gorman et al. 2000). = 97). Trap nets used were large Great Lakes The first was the introduction of quagga mus- commercial trap nets set at depths between sels, which have replaced zebra mussels and 20 and 39 m. Most were deployed near rocky extended their range over much of the deep- reefs. At Alpena, Michigan, surveys were con- water abyss and reefs of Lake Michigan (and ducted in northern Lake Huron reefs by the other Great Lakes). The second was expan- MDNR on November 18, 2004. Commercial sion of round gobies to deeper water in lakes gill nets (several gangs of 300-m-long, 50- Michigan (Jude, unpublished data), Huron mm-bar, multifilament, nylon mesh) were (Schaeffer et al. 2005), and Ontario (Walsh deployed near Washington Island, Wiscon- et al. 2007), where they inhabited rocky reefs sin, in Lake Michigan. Similar gill nets were and became prey for many predators (Jude set through the ice in Big Bay de Noc, Lake 2001; Schaeffer et al. 2005) and even lake Michigan near Fairport, Michigan during Feb- whitefish (Jude, unpublished data). Adult ruary 2005. Commercial fishermen also col- dreissenids filter about l L of water per day, lected burbot for us using trap nets and gill removing phytoplankton and detritus from nets in northern Lake Michigan off Leland, the water column (Vanderploeg et al. 2002), Michigan. sometimes resulting in uptake of toxic substances by round gobies (Kwon et al. 2006; Fish and Diet Processing Jude, unpublished data), which can then be After field collections were made, burbot bioaccumulated in food chains. Since burbot were kept on ice until total length (mm) and are sometimes eaten, there are important im- weight (g) could be measured and diets de- plications for public health. termined by dissection. All stomach contents In this paper, we present diet and growth were weighed in mass (nearest 0.1 g); then, information to document shifts in burbot di- individual prey items were weighed and ets from native species to round gobies; this identified to the lowest practicable taxonom- shift is occurring on many rocky reefs and ic unit. Total length of fish eaten was mea- elsewhere in the Great Lakes. These changes sured to the nearest millimeter or estimated may negatively affect burbot growth, depress from skeletal remains. Burbot collected other native species, and modify bioaccumu- were analyzed within 2 d of collection. For lation pathways in coldwater food webs in the diet analysis, burbot were divided into the Great Lakes. three groups (400–499 mm, 500–599 mm, and >599 mm) representing natural breaks in Methods amount and types of prey eaten. These data Gear Deployment were compared with earlier burbot diet data from 1986 to 1988 (Fratt et al. 1997), col- Adult burbot analyzed for diets during this lected at similar depths (20–39 m) and habi- study were collected by a variety of sources, tats to elucidate changes in burbot diet after including the Michigan Department of Natural round gobies were introduced to the Great 94 hensler et al.

Table 1. Date, location (see Figure 1), and gear type used to collect burbot for diet analyses from several sites on Lake Michigan (LM) and Lake Huron (LH) during 2004-2006. TN = trap net, GN = gill net, MDNR and WDNR = Michigan and Wisconsin Departments of Natural Resources, CF = commercial fisherman, MSU= Michigan State University. Gear Date Location City deployed Project 23 Jun 04 LM:eastern shoreline Leland, MI GN, TN CF 18 Nov 04 LH:Thunder Bay Alpena, MI TN MDNR/CF 3 Dec 04 LM:Green Bay Washington Island, WI GN.TN CF 3 Feb 05 LM:Big Bay de Noc Fairport, MI GN MSU/CF 8 Jun 06 LM:eastern shoreline Leland, MI GN,TN CF 15 Jun 06 LM:Green Bay Washington Island, WI GN,TN CF 6 Dec 06 LM:Green Bay Washington Island, WI GN,TN CF

Lakes. Diet item categories were organized to could be related to the addition of round goby be comparable with those used by Fratt et al. to the diets. First, MDNR collected burbot (1997), which included alewife, rainbow smelt, from 1996 to 2006 using gill nets as part of bloater Coregonus hoyi, Cottus spp., deepwa- routine sampling in Michigan waters of Lake ter sculpin Myoxocephalus thompsonii, yellow Huron in statistical districts MH-1 (northern, perch, other fish, invertebrates (not including n = 144), MH-2 (north-central, n = 194), and crayfish), unidentified fish, and miscellaneous MH-3–5 (southern, n = 229), which are locat- (including crayfish). The other fish category ed along the western side of Lake Huron (Fig- included gizzard shad Dorosoma cepedianum, ure 1; Smith et al. 1961). Burbot were mea- lake whitefish, ninespine stickleback Pungitius sured to the nearest mm and otoliths removed pungitius, and spottail shiner Notropis hud- from fish. Otoliths were prepared using the sonius. Unidentified fish were too digested to crack-and-burn method (Nielsen and John- promote further identification. Miscellaneous son 1983), and age was estimated by count- food items included crayfish, deepwater sculpin ing annuli. Asymptotic length and growth and lake whitefish eggs, and quagga and zebra coefficients were determined using the von mussels. Mean food weight consumed per fish Bertalanffy growth function (von Bertalanffy was compared among our sites using analysis 1938; Ricker 1975), and their 95% confi- of variance (ANOVA; α = 0.05). Statistical dence intervals were used to compare growth comparisons between our 2004–2006 data and differences among sites (α = 0.05). the 1986–1988 data of Fratt et al. (1997) were Second, length and weight data on 357 not possible due to lack of available raw data. burbot from the fish we collected for diet However, mean food volume (mL) consumed analyses (Table 1) and 73 fish collected dur- per fish derived from Fratt et al. (1997) was ing 1973–1977 at Bridgman, Michigan (D. determined to be similar enough to our mean C. Cook nuclear power plant) on Lake Michi- wet-weight diet data for comparative purposes. gan were analyzed to determine if there were growth differences at given lengths (500, 600, Age and Growth 700, and 800 mm) for burbot among sites. There were two different growth analyses The Cook plant is located in southeastern performed to determine if there were changes Lake Michigan (see Figure 1). Burbot from in burbot growth and whether these changes 1973 to 1977 were collected in gill nets and burbot growth and diets in lakes michigan and huron 95

Figure 1. Map of lakes Michigan and Huron showing statistical districts MH-1 to MH-6, our sampling stations, including Muskegon, Alpena, Leland, Fairport, Bridgman (the D. C. Cook nuclear power plant), Michigan; Washington Island, Wisconsin; and East Reef in southern Lake Michigan.

trawls deployed monthly from April through collected near Bridgman, Michigan during November in water 6–9 m deep (Jude et al. the 1970s. 1986; Tesar et al. 1986). Length and weight data were log-transformed, and a linear, Results fixed-effects model (Lai and Helser 1994) Burbot Age and Growth was used to test for significant length–weight differences among burbot from the four We analyzed two data sets to determine if 2004–2006 study sites (Table 1) and burbot there have been changes in growth of bur- 96 hensler et al. bot in the early 2000s that may be related districts. The central tendency for fish from to changes in diet with the addition of the the north was lower than the confidence in- round goby. First, we used age-at-length data terval for fish from the north-central district, from burbot collected from western Lake and the central tendency for fish from north- Huron from 1996 to 2006. Fish generally central was larger than the confidence inter- grew about 40 mm/year to about age 6, after val for fish from the north. Thus, asymptotic which growth slowed substantially (Figure length was significantly longer in the south 2). The oldest burbot was 18 years old. As- and smallest in the north. Growth coefficient ymptotic total length (SD) showed a gradi- K (SD) was 0.271 (0.041), 0.284 (0.065), and ent from north to south of 577 (10), 619 (14), 0.143 (0.024) for northern, north-central, and and 750 (29) mm for northern (MH1), north- southern Lake Huron, respectively. Based on central (MH2), and southern (MH3–5) Lake confidence-interval comparisons similar to Huron, respectively. The confidence interval those for asymptotic lengths, growth coef- of asymptotic length (693–807 mm) for fish ficients were similar between the north and from the south had no overlap with the con- north-central districts, while it was signifi- fidence intervals for fish from the north-cen- cantly smaller for fish from the south. Thus, tral (592–646 mm) and north (557–597 mm) lengths of fish less than age 8 were smaller

700 1 650 2 600 3 (mm)

550 ng th 500

450 To ta l le

400

350

300 0510 15 20 Age (year)

Figure 2. Growth (length-at-age) of burbot from northern (MH1), north-central (MH2), and southern (MH3–5) Lake Huron. See Figure 1 and Smith et al. (1961) for details of the statistical districts. Fish samples were from 1996 to 2006. Age was estimated using otoliths. Sample sizes were 144, 194, and 229 for the three areas, respectively. burbot growth and diets in lakes michigan and huron 97 in southern Lake Huron than in the other two ied by location. No round gobies were pres- northern areas, while burbot reached a much ent in diets of burbot of any size from Le- larger size at age 7 in north-central Lake Hu- land, Michigan, where medium-sized burbot ron (Figure 2). ate alewives (89%), Cottus spp. (8%), and Our second analysis focused on the fish rainbow smelt (4%). At the other three sites, we collected at various sites in lakes Michigan round gobies composed 32–84% of the diet and Huron (Table 1), for which we have diet of medium-sized burbot, with the Lake Hu- information. Growth of burbot, as reflected ron Alpena site having the highest percent- in length–weight relationships, showed sig- age. Medium-sized burbot from the Wash- nificant differences in the mean weight for a ington Island Green Bay site consumed 32% given length when compared with the overall round gobies and had the most diverse diet, mean weight for two sites: Alpena and Bridg- with alewives, rainbow smelt, Cottus spp., man (Cook plant) (Table 2). Mean weight of and other fish making up from 5% to 35% fish from Alpena was always significantly of the non-round goby diet. Invertebrates lighter than the mean for all sizes (500, 600, (excluding crayfish) and miscellaneous food 700, 800 mm) tested. These fish were col- items composed 3% of medium-sized burbot lected in November and had not spawned diets at Washington Island. yet, which was true for several of the other Large burbot (>599 mm) ate round gobies collections, some of which included fish that in high percentages (38–77) at all sites except had spawned. Leland, Michigan, where no round gobies were consumed. At Leland, large burbot ate Burbot Diets Cottus spp. (25%), unidentified fish (25%), Burbot diets have changed dramatically in alewife (21%), miscellaneous food (11%), some areas following establishment of the rainbow smelt (8%), bloater (5%), and other nonindigenous round goby in the Great Lakes fish (4%). The average percent composition (first found in 1990, Jude et al. 1992). Where of round gobies in the burbot diet at the three alewives, rainbow smelt, sculpins, and some- sites where round gobies were present was times bloaters once composed a substantial 93% for small burbot, 58% for medium bur- portion of burbot diets, they are now being bot, and 58% for large burbot (Figure 4). replaced with round gobies in areas where The average amount of food eaten per round gobies are present (Figures 3 and 4). fish for small burbot at Fairport, Michigan Round gobies composed 62% of the diet by (30 g/fish, n = 2) and Washington Island, wet-weight of burbot collected among all sites Wisconsin (35 g/fish, n = 7) was higher than combined, while traditionally important prey, the average amounts of food eaten by small such as alewife, lake whitefish, and crayfish, burbot in Green Bay, Wisconsin (Fratt et al. composed only 8%, 6%, and 5% of the diet, 1997: 3.9–26.4 mL/fish, n = 147) prior to the respectively (n = 299 burbot). The only small round goby introduction (Figure 5). For me- (<500 mm total length; n = 9) burbot col- dium-sized burbot, however, 51.8 g/fish was lected during 2004–2006 were caught in Lake eaten at the Lake Huron Alpena, Michigan Michigan off Fairport, Michigan in Big Bay site, which was at least twice as high as the de Noc and at Washington Island, Wisconsin, quantity eaten at any of the other seven sites and these fish consumed 100% and 85% round for which data were calculated. Round gobies gobies, respectively. composed 84% of the fish eaten by these bur- Dominance of round gobies in the diets bot. The trend of high consumption of round of medium-sized burbot (500–599 mm) var- gobies by burbot was even stronger for large 98 hensler et al.

Table 2. Mean weight-at-length derived from a linear fixed-effects model calculated for burbot collected from various locations in the Great Lakes: Lake Michigan: Leland, MI (n = 22); Fairport, Michi- gan (n = 118); Bridgman (D. C. Cook Nuclear Power Plant), Michigan (n = 73); Washington Island (Wash. Isl.), Wisconsin (n = 120); and Lake Huron: Alpena, Michigan (n = 97). * = significant at the 0.05 level. SD = standard deviation. Confidence interval Sites Mean weight (g) SD 2.5% 97.5% 500 mm Alpena *1067 19 1030 1105 Bridgman *970 21 930 1011 Fairport 1172 15 1142 1202 Leland 1164 34 1098 1231 Wash. Isl. 1168 14 1140 1196 Mean 1176 21 1135 1216

600 mm Alpena *1588 26 1538 1638 Bridgman *1649 41 1569 1729 Fairport 1823 16 1792 1854 Leland 1863 33 1798 1928 Wash. Isl. 1810 17 1776 1843 Mean 1853 32 1790 1915

700 mm Alpena *2222 40 2143 2302 Bridgman 2582 80 2425 2740 Fairport 2648 43 2563 2733 Leland 2773 61 2653 2892 Wash. Isl. 2620 46 2531 2710 Mean 2721 72 2579 2863

800 mm Alpena *2973 65 2846 3101 Bridgman 3808 145 3523 4093 Fairport 3660 92 3479 3841 Leland 3912 129 3660 4165 Wash. Isl. 3611 94 3426 3796 Mean 3796 140 3522 4071 burbot, which consumed 55.6 g/fish at the Al- station A 5. Consumption at our other three pena, Michigan, Lake Huron site (Figure 5). study sites (Washington Island, Fairport, Le- However, a higher amount was recorded for land, Figure 5) was significantly lower than large burbot diets prior to round goby colo- the quantity (less than 10 g/fish) eaten by bur- nization, when more than 60 mL/fish were bot at Alpena (ANOVA df = 3, F = 51.334, P eaten by fish from Green Bay, Wisconsin at < 0.001) and was far below prey consumption burbot growth and diets in lakes michigan and huron 99

Figure 3. Percent composition by weight of the diet of burbot collected from lakes Michigan and Huron at depths of 20–39 m during 2004–2006 (n = 299). Study locations (see Figure 1) include Leland, Fairport, and Alpena, Michigan and Washington Island (W. Isl.), Wisconsin. Burbot prey codes are RG = round goby, AL = alewife, UF = unidentified fish, LW = lake whitefish, CR = crayfish, and MC = miscellaneous.

at the other Green Bay sites prior to round since the very productive Saginaw Bay is goby appearance there. in the southern district. Interestingly, burbot length–weight relationships indicated that Discussion burbot consuming the most round gobies (at Alpena in Lake Huron) were actually lighter Small burbot from southern Lake Huron grew at a particular length than those consuming slower than those farther north, but once they fewer or no round gobies at other sites. This reached age 7, they grew significantly faster suggests that burbot have not eaten round go- than burbot from the north. Since burbot pre- bies long enough to effect increases in growth fer water temperatures of 10–12°C (Hackney or that native prey fishes at the sites we sam- 1973), it is unlikely that these growth differ- pled provided for better burbot growth than ences were related to thermal characteris- round gobies. Our growth results contradict tics, but rather to prey availability changes, those of Johnson et al. (2005), who found that 100 hensler et al. while round gobies had a lower energy den- in areas without round gobies. The largest sity than native prey organisms in Lake Erie, burbot we collected came from near Alpena, mean length-at-age of Lake Erie burbot in- Michigan, in Lake Huron, where diet of large creased, suggesting that enough round gobies burbot was composed of the highest percent- were eaten to increase burbot growth. John- age of round gobies (77%). We found up to son et al. (2005) believed that one advantage 46 round gobies in one of these fish. Burbot of round gobies over native prey was due to collected in southeastern Lake Michigan near the ability of round gobies to transfer energy Bridgman, Michigan, near the D. C. Cook from zebra and quagga mussels to top preda- nuclear power plant in the 1970s were the tors, which native prey organisms cannot do. smallest in maximum length and were sig- Burbot collected in areas where round gobies nificantly lighter than fish from other sites. were present tended to be longer than those Reasons for this could be a combination of

Figure 4. Percent composition by weight of the diet for (A) small (400–499 mm total length [TL]), (B) medium (500–599 mm TL), and (C) large (at least 600 mm TL) burbot collected from lakes Michigan and Huron at depths of 20–39 m during 1986–1988 (Fratt et al. 1997) before round gobies were introduced to the Great Lakes, and during 2004–2006 (this study). Sites A 2–5 were selected from Fratt et al. (1997) as being comparable to locations where burbot were recently collected, with sample sizes of 17, 128, 2, and 6, respectively. Recent study locations included Leland, Fairport, and Alpena, Michigan and Washington Island (W. Isl.), Wisconsin, where burbot sample sizes were 22, 118, 48, and 111, respectively. Burbot prey codes are RG = round goby, AL = alewife, RS = rainbow smelt, BL = bloater, CT = Cottus spp., DS = deepwater sculpin, YP = yellow perch, OF = other fish, IV = invertebrates (not including crayfish), UF = unidentified fish, and MC = miscellaneous (including crayfish). burbot growth and diets in lakes michigan and huron 101 B

Figure 4. Continued. 102 hensler et al.

Figure 5. Mean food weight (g) present in burbot stomachs for small (400–499 mm TL, n = 9), medium (500–599 mm TL, n = 159), and large (at least 600 mm TL, n = 145) burbot collected in Lake Michigan near Leland and Fairport, Michigan and Washington Island, Wisconsin and in Lake Huron off of Al- pena, Michigan, during 2004–2006. Error bars represent ±2 SD of the mean. gear bias, warmer temperatures, or a function mussels have shifted energy flow from the of the fish being collected near shore (9 m) in pelagic to the benthic zone, altered bioaccu- the 1970s, away from prime rocky habitat for mulation pathways (Vanderploeg et al. 2002; burbot, where they may grow larger. Madenjian et al. 2002), and provided an op- Near shore, rocky bottom is optimal hab- timal food source for round gobies (French itat for round gobies (Jude and DeBoe 1996), and Jude 2001). Introduction of dreissenids and round gobies have heavily colonized has allowed round gobies to expand their many of these sites, providing burbot and populations from their initial dumping sites other top predators with a new, abundant prey at harbors from freighters (Hensler and Jude fish. A major ecosystem shift has occurred in 2007) to adjacent Great Lakes deep water many of the Great Lakes as zebra and quagga sites, including critical rocky reefs, which burbot growth and diets in lakes michigan and huron 103 act as important nursery, feeding, and spawn- Second, burbot are apparently not im- ing sites (Janssen et al. 2006b). Hence, the pacting salmonines through predation, as we impact of round gobies on burbot diets will found no juvenile salmonines in any stom- be confined to the near shore zone when suf- achs we examined (some lake whitefish were ficiently cold temperatures allow overlap. eaten at Alpena and Fairport, Michigan). Round gobies appear to be distributed in wa- This was similar to what Fratt et al. (1997) ter about 70 m or less in lakes Huron, Ontario, concluded from their Green Bay, Wisconsin and Michigan (Schaeffer et al. 2005; Walsh burbot studies. While overall competition for et al. 2007; Jude, unpublished data); hence, forage between burbot and salmonines (see we expect that burbot residing deeper than Jude et al. 1987 for salmonine diets) in the 70 m will not encounter any round gobies to Great Lakes may be reduced due to habitat eat. Burbot have not been found eating any differences (benthic versus pelagic), there is round gobies on the mid-lake reefs (50 m) in still substantial diet overlap, which may cre- offshore southern Lake Michigan (P. McKee, ate an important bottleneck during specific Wisconsin Department of Natural Resources, ontogenies of certain salmonines. For ex- Sturgeon Bay, personal communication). ample, a considerable amount of sculpins is There are several implications of the new eaten by lake trout (Madenjian et al. 1998) colonization by round gobies of these rocky and brown trout Salmo trutta juveniles (Jude sites. First, once round gobies colonize these et al. 1987) in Lake Michigan. sites, we expect mottled and slimy sculpins to Third, burbot can also impact various be extirpated (Janssen and Jude 2001) and di- species through consumption of eggs. They ets of top predators to begin to include round ate lake whitefish eggs at Alpena, Michigan gobies (Jude 2001). For example, burbot diets in Lake Huron and deepwater sculpin eggs at now include large percentages of round go- Leland, Michigan in Lake Michigan. Burbot bies, when historically they ate a wide range also ate lake trout eggs in the fall (Claramunt of native species in the Great Lakes (Van et al. 2005) as do slimy sculpins, one of their Oosten and Deason 1938; Clemens 1951; Bai- prey (Janssen et al. 2006a). Therefore, preda- ley 1972; Bohr and Liston 1981; Rudstam et tion by burbot on slimy sculpins and the cur- al. 1995; Fratt et al. 1997). This scenario oc- rent switch to the new invasive round goby, curred at three of our four sites where we col- which also is known to eat lake trout eggs lected burbot diet information, as no or very (Chotkowski and Marsden 1999), could af- few Cottus spp. were eaten at sites where the fect lake trout survival by reducing egg con- most prominent diet item for burbot was round sumption. gobies. Additionally, where round gobies are The switch in burbot diets from native spe- present, burbot now prey more heavily on cies to round gobies could have implications strongly benthic forage, as round gobies now for toxic substance uptake. Round gobies, be- compose 67% of the diet of burbot collected cause they eat dreissenids, which filter large at depths of 20–39 m, while Fratt et al. (1997) quantities of water, bioaccumlate polychlori- found burbot from similar habitats to consume nated biphenyls (PCBs), which can be passed more alewife, bloater, and rainbow smelt. In to top predators (Kwon et al. 2006; Jude, un- some cases, availability of round gobies as published data). Jude’s studies showed that in prey has enhanced survival of juvenile small- highly contaminated Areas of Concern, such mouth bass Micropterus dolomieu (Steinhart as the River Raisin, a tributary to Lake Erie, et al. 2004), while in others they caused local round gobies accumulated up to 5 mg/kg of extirpation of native species (Jude 2001). PCBs, while smallmouth bass there had lev- 104 hensler et al. els up to 2 mg/kg. At a control site upriver, Acknowledgments concentrations were at trace levels. In con- We thank the National Marine Fisheries Ser- trast, because round gobies are feeding at vice, whose support through Saltonstall-Ken- lower levels in the food chain by eating dreis- nedy Program funds enabled sample collec- senids, we expect that in uncontaminated ar- tion for this analysis. We also are grateful eas of the Great Lakes, burbot-eating native for the sampling assistance provided by Jim species may accumulate more contaminants Johnson and Randy Claramunt, Michigan than those eating round gobies. Department of Natural Resources in Alpena This change in burbot diets may also and Charlevoix, Michigan; Mark Ebener, In- compromise their ability to be used commer- ter-Tribal fisheries and Assessment Program, cially (Lindsay et al. 1981; Krivchenia and Chippewa Ottawa Resource Authority, Sault Fennema 1988). Pääkkönen et al. (2005) fed Ste. Marie, Michigan; commercial fishermen PCBs to burbot and found that (1) 65–81% Ken Koyen, Washington Island, Wisconsin, of the PCBs were retained with highest doses William Fowler, Leland, Michigan, and Bill found in the liver, and (2) levels of PCBs in Peterson, Fairport, Michigan. William Carl- burbot collected in 2005 were no different son, Leland, Michigan provided advice and from levels observed in the 1970s, despite specimens. Sample analysis space was gra- banning PCBs. While fillets are probably go- ciously provided by Michigan Department of ing to be considered safe, liver oils may be- Natural Resources (DNR), Alpena, Michigan; come more highly contaminated, particularly the Mackinac Straits Fish Company, St. Ig- with PCBs, as a result of the high propor- nace, Michigan; and Ken Koyen, Washington tion of round gobies in diets from the early Island, Wisconsin. Patrick McKee, Wiscon- 2000s. The liver is a major source of revenue sin DNR is thanked for providing diet data on in oceanic cod fisheries, and this may make some burbot from the mid-lake reefs in Lake commercial fishing for burbot a less lucrative Michigan. We thank Vaughn Paragamian for venture for commercial fishers in the Great encouragement and he, David Bennett, and Lakes. Tony Lamansky for substantive, constructive Several recent papers have documented critiques of the manuscript. changes in burbot populations in the Great Lakes (Schram et al. 2006; Stapanian et al. References 2006; Stapanian and Madenjian 2007), show- Bailey, M. M. 1972. Age, growth, reproduction, ing recent population upsurges due to sea lam- and food of the burbot, Lota lota (Linnaeus), prey control and reduction of alewife predation in southwestern Lake Superior. Transactions on burbot larvae. Burbot compete with other of the American Fisheries Society 101:667– top predators for similar fish prey but may en- 674. hance successful lake trout reproduction by re- Bohr, J., and C. Liston. 1981. Relative abundance ducing lake trout egg predators, such as slimy and feeding relationships of sculpin (Cottus sculpin and round gobies. Because of these spp.), johnny darter (Etheostoma nigrum) fluctuations in their population levels and their and trout-perch (Percopsis omiscomaycus) recent switch to invasive round gobies with its in the Ludington pumped storage reservoir on Lake Michigan. Michigan Academician implications for toxic substance bioaccumula- 13:111–123. tion, it is important to monitor their popula- Bonde, T., and J. Maloney. 1960. Food habits of tion abundances so managers can implement burbot. Transactions of the American Fisher- changes that might favor other competing spe- ies Society 89:374–376. cies, such as lake trout. Boyer, L., R. Cooper, D. Long, and T. Askew. burbot growth and diets in lakes michigan and huron 105

1989. Burbot (Lota lota) biogenic sedimen- Lakes. Journal of Great Lakes Research tary structures in Lake Superior. Journal of 33:295–302. Great Lakes Research 15:174–185. Janssen, J., and D. J. Jude. 2001. Recruitment Chotkowski, M. A., and J. E. Marsden. 1999. failure of mottled sculpin Cottus bairdi in Round goby and mottled sculpin predation southern Lake Michigan induced by the new- on lake trout eggs: field predictions from lab- ly introduced round goby Neogobius mela- oratory experiments. Journal of Great Lakes nostomus. Journal of Great Lakes Research Research 25:26–35. 27:319–328. Claramunt, R. M., J. L. Jonas, J. D. Fitzsimons, Janssen, J., D. Jude, T. Edsall, M. Paddock, N. and J. E. Marsden. 2005. Influences of Wattrus, M. Toneys, and P. McKee. 2006a. spawning habitat characteristics and inter- Evidence of lake trout reproduction at Lake stitial predators on lake trout egg deposition Michigan’s Mid-lake Reef Complex: hy- and mortality. Transactions of the American potheses regarding the indigenous fish and Fisheries Society 134:1048–1057. implications for restoration. Journal of Great Clemens, H. P. 1951. The food of the burbot, Lakes Research 32:749–763. Lota lota maculosa (LeSueur), in Lake Erie. Janssen, J., M. Berg, and S. Lozano. 2006b. Sub- Transactions of the American Fisheries Soci- merged terra incognita: the abundant but un- ety 80:56–66. known rocky zones. Pages 439–477 in M. Edsall, T., G. Kennedy, and W. Horns. 1993. Dis- Munawar and T. Edsall, editor. The state of tribution, abundance, and resting microhabi- Lake Michigan. S. P. B. Academic Publish- tat of burbot on Julian’s Reef, southwestern ing, Ecovision World Monograph Series, The Lake Michigan. Transactions of the Ameri- Netherlands. can Fisheries Society 122:560–574. Johnson, T. B., D. B. Bunnell, and C. T. Knight. Eshenroder, R. L., and M. K. Burnham-Curtis. 2005. A potential new energy pathway in cen- 1999. Species succession and sustainability tral Lake Erie: the round goby connection. of the Great Lakes fish community. Pages Journal of Great Lakes Research 31(Supple- 145–184 in W. W. Taylor and C. P. Ferreri, ment 2):238–251. editors. Great Lakes fisheries and policy man- Jones, D., J. Kiceniuk, and O. Bamford. 1974. agement: a binational perspective. Michigan Evaluation of the swimming performance of State University Press, East Lansing. several fish species from the Mackenzie Riv- Fratt, T. W., D. W. Coble, F. Copes, and R. E. er. Journal of the Fisheries Research Board of Bruesewitz. 1997. Diet of burbot in Green Canada 31:1641–1647. Bay and western Lake Michigan with com- Jones, M. L. K., G. W. Eck, D. O. Evans, M. C. parison to other waters. Journal of Great Fabrizio, M. H. Hoff, P. Hudson, J. Janssen, Lakes Research 23:1–10. D. Jude, R. O’Gorman, and J. F. Savino. French, J. R., III, and D. Jude. 2001. Diets and 1995. Limitations to lake trout (Salvelinus diet overlap of nonindigenous gobies and namaycush) rehabilitation in the Great Lakes small benthic native fishes co-inhabiting the imposed by biotic interactions occurring at St. Clair River, Michigan. Journal of Great early life stages. Journal of Great Lakes Re- Lakes Research 27:300–311. search 21(Supplement 1):505–517. Guthruf, J., S. Gerster, and P.-A. Tschumi. 1990. Jude, D. J., and S. DeBoe. 1996. Possible impact The diet of burbot (Lota lota) in Lake Biel, of gobies and other introduced species on Switzerland. Archiv für Hydrobiologie habitat restoration efforts. Canadian Journal 199:103–114. of Fisheries and Aquatic Sciences 53(Supple- Hackney, P. 1973. Ecology of the burbot Lota lota ment 1):136–141. with special reference to its role in the Lake Jude, D. J. 2001. Round and tubenose gobies: 10 Openogo fish community. Doctoral disserta- years with the latest Great Lakes phantom tion. University of Toronto, Toronto. menace. Dreissena 11:1–14. Hensler, S. R., and D. Jude. 2007. Diel vertical Jude, D. J., F. J. Tesar, S. DeBoe, and T. Miller. migration of round goby larvae in the Great 1987. Forage fish selection by Lake Michigan 106 hensler et al.

salmonines, 1973–1982. Transactions of the Madenjian, C. P., T. J. DeSorcie, and R. M. Sted- American Fisheries Society 116:677–691. man. 1998. Ontogenic and spatial patterns in Jude, D. J., R. H. Reider, and G. R. Smith. 1992. diet and growth of lake trout in Lake Michi- Establishment of Gobiidae in the Great Lakes gan. Transactions of the American Fisheries basin. Canadian Journal of Fisheries and Society 127:236–252. Aquatic Sciences 49:416–421. Mansfield, P., D. Jude, D. Michaud, D. Brazo, and Jude, D., D. Bimber, N. Thurber, F. Tesar, L. J. Gulvas. 1983. Distribution and abundance Noguchi, P. Mansfield, H. Tin, and P. Rago. of larval burbot, Lota lota, and deepwater 1986. Impact of the D. C. Cook plant on fish. sculpin, Myoxocephalus thompsoni, in Lake In R. Rossmann, editor. Southeastern Lake Michigan. Transactions of the American Michigan: the impact of the D. C. Cook Fisheries Society 112:162–172. nuclear plant. University of Michigan, Great McCrimmon, H., and O. Devitt. 1954. Winter Lakes Research Division, Publication Num- studies on the burbot, Lota lota lacustris, of ber 22, Ann Arbor. Lake Simcoe, Ontario. Canadian Fish Cultur- Krivchenia, M., and O. Fennema. 1988. Effect of ist 16:35–41. cryoprotectants on frozen burbot fillets and a Nielsen, L., and D. Johnson, editors. 1983. Fish- comparison with whitefish fillets. Journal of eries techniques. American Fisheries Society, Food Science 53:1004–1008. Bethesda, Maryland. Kwon, T-D., S. Fisher, G. Kim, H. Hwan, and J-E. O’Gorman, R., J. H. Elrod, R. W. Owens, C. P. Kim. 2006. Trophic transfer and biotransfor- Schneider, T. E. Eckert, and B. F. Lantry. mation of polychlorinated biphenyls in zebra 2000. Shifts in depth distributions of ale- mussel, round goby, and smallmouth bass in wives, rainbow smelt, and age-2 lake trout Lake Erie, USA. Environmental Toxicology in southern Lake Ontario following estab- and Chemistry 25(4):1068–1078, 2006. lishment of dreissenids. Transactions of Lai, H., and T. Helser. 1994. Linear mixed-effects the American Fisheries Society 129:1096– models for weight-length relationships. Fish- 1106. eries Research 70:377–387. Pääkkönen, J.-P., A. L. Rantalainen, A. Karels, Lavis, D. S., M. P. Henson, D. A. Johnson, E. M. A. Nikkilak, and J. Karjalainen. 2005. Bio- Koon, and D. J. Ollila. 2003. A case history accumulation of PCBs in burbot (Lota lota) of sea lamprey control on Lake Michigan: after delivery in natural food. Archives of 1979 to 1999. Journal of Great Lakes Re- Environmental Contamination and Toxicol- search 29(Supplement 1):584–598. ogy 49:223–231. Lawler, G. 1963. The biology and taxonomy of Ricker, W. E. 1975. Computation and interpre- the burbot, Lota lota, in Heming Lake, Mani- tation of biological statistics of fish popula- toba. Journal of the Fisheries Research Board tions. Fisheries Research Board of Canada of Canada 20:417–433. Bulletin 191. Lindsay, R., D. Stuiber, B. Stewart, and V. Carl- Rudstam, L. G., P. E. Peppard, T. W. Fratt, R. E. son. 1981. Evaluation of burbot (Lota lota) Bruesewitz, D. W. Coble, F. A. Copes, and acceptability for processing. Canadian Insti- J. F. Kitchell. 1995. Prey consumption by tute of Food Science and Technology Journal the burbot (Lota lota) population in Green 14:196–202. Bay, Lake Michigan, based on a bioenerget- Madenjian, C. P., G. L. Fahnenstiel, T. H. Johen- ics model. Canadian Journal of Fisheries and gen, T. F. Nalepa, H. A. Vanderploeg, G. W. Aquatic Sciences 52:1074–1082. Fleischer, P. J. Schneeberger, D. M. Benja- Schaeffer, J. S., A. Bowen, M. Thomas, J. R. P. min, E. B. Smith, J. R. Bence, E. S. Ruth- French, III, and G. L. Curtis. 2005. Invasion erford, D. S. Lavis, D. M. Robertson, D. J. history, proliferation, and offshore diet of Jude, and M. P. Ebener. 2002. Dynamics of the round goby Neogobius melanostomus in the Lake Michigan food web, 1970–2000. western Lake Huron, USA. Journal of Great Canadian Journal of Fisheries and Aquatic Lakes Research 31:414–425. Sciences 59:736–753. Schram, S. T., T. B. Johnson, and M. J. Seider. burbot growth and diets in lakes michigan and huron 107

2006. Burbot consumption and relative abun- Tesar, F., D. Jude, H. Tin, and P. Mansfield. 1986. dance in the Apostle Islands region of Lake Ecology of fish in nearshore southeastern Superior. Journal of Great Lakes Research Lake Michigan, 1973–1982. In R. Rossman, 32:798–805. editor. The impact of the D. C. Cook nuclear Scott, W. B., and E. J. Crossman. 1973. Fresh- plant on southeastern Lake Michigan. Uni- water fishes of Canada. Fisheries Research versity of Michigan, Great Lakes Research Board of Canada Bulletin 184. Division, Publication Number 22, Ann Ar- Smith, S. H., H. J. Buettner, and R. Hile. 1961. bor. Fishery statistical districts of the Great Lakes. Van Oosten, J., and H. Deason. 1938. The food of Great Lakes Fishery Commission, Technical lake trout (Cristivomer namaycush namaycu- Report 2, Ann Arbor, Michigan. sh) and of the lawyer (Lota maculous) of Stapanian, M. A., and C. P. Madenjian. 2007. Lake Michigan. Transactions of the Ameri- Evidence that lake trout served as a buffer can Fisheries Society 67:155–177. against sea lamprey predation on burbot in Vanderploeg, H. A., T. F. Nalepa, D. J. Jude, Ed- Lake Erie. North American Journal of Fish- ward L. Mills, Kristen T. Holeck, J. R. Li- eries Management 27(1):238–245. ebig, I. A. Grigorovich, and H. Ojaveer. 2002. Stapanian, M. A., C. P. Madenjian, and L. D. Wit- Dispersal and emerging ecological impacts zel. 2006. Evidence that sea lamprey control of Ponto-Caspian species in the Laurentian led to recovery of the burbot population in Great Lakes. Canadian Journal of Fisheries Lake Erie. Transactions of the American and Aquatic Sciences 59:1209–1228. Fisheries Society 135:1033–1043. von Bertalanffy, L. 1938. A quantitative theory of Steinhart, G. B., E. A. Marschall, and R. A. Stein. organic growth (inquiries on growth laws II). 2004. High growth rate of young-of-the-year Human Biology 10:181–213. smallmouth bass in Lake Erie: a result of the Walsh, M., D. Dittman, and R. O’Gorman. 2007. round goby invasion? Journal of Great Lakes Occurrence and food habits of round goby Research 30:381–389. in the profundal zone of southwestern Lake Swink, W. D. 2003. Host selection and lethality Ontario. Journal of Great Lakes Research of attacks by sea lampreys (Petromyzon ma- 33:83–92. rinus) in laboratory studies. Journal of Great Ward, C., R. L. Eshenroder, and J. R. Bence. Lakes Research 29(Supplement 1):307–319. 2000. Relative abundance of lake trout and Swink, W. D., and K. T. Fredericks. 2000. Mortality burbot in the main basin of Lake Michigan in of burbot from sea lamprey attack, and initial the early 1930s. Transactions of the Ameri- analyses of burbot blood. Pages 147–154 in V. can Fisheries Society 129:282–295. L. Paragamian and D. Willis, editors. Burbot Wells, L., and A. L. McLain. 1973. Lake Michi- biology, ecology and management. American gan - man’s effects on native fish stocks and Fisheries Society, Fisheries Management Sec- other biota. Great Lakes Fishery Commission tion Publication 1, Bethesda, Maryland. Technical Report 20, Ann Arbor, Michigan.