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Distribution of Round Gobies in Coastal Areas of Lake Michigan: Are Wetlands Resistant to Invasion?
J. Great Lakes Res. 33:303–313 Internat. Assoc. Great Lakes Res., 2007
Distribution of Round Gobies in Coastal Areas of Lake Michigan: Are Wetlands Resistant to Invasion? Matthew J. Cooper1,*, Carl R. Ruetz III1, Donald G. Uzarski1, and Thomas M. Burton2 1Grand
Valley State University Annis Water Resources Institute 740 W. Shoreline Dr. Muskegon, Michigan 49441 2Michigan
State University Departments of Zoology and Fisheries and Wildlife 25B Natural Science East Lansing, Michigan 48824 ABSTRACT. Great Lakes coastal wetlands may be more resistant to invasion by certain nonindigenous species and thus serve as refuge habitats for native species. As a first step in testing this hypothesis, we investigated the distribution of round goby (Apollonia melanostomus, formerly Neogobius melanostomus) in the lower reaches of several Lake Michigan tributary systems that contain both wetland and lake habitats near their confluences with Lake Michigan. Using fyke nets, we sampled round gobies in lake and adjacent wetland habitats in four systems in 2004 and six systems in 2005. In each macrohabitat (lake or wetland), we sampled three microhabitats (mono-dominant stands of Nuphar, beds of submersed aquatic vegetation, and bare sediment). We found that round goby catch was generally lower in wetland macrohabitats than adjacent lake macrohabitats and that round gobies appeared to prefer beds of submersed aquatic vegetation in lakes among the three microhabitats. The majority of round gobies in all habitats were relatively small (< 7 cm standard length). We also found a significant negative correlation between round goby catch and distance of sampling points from the Lake Michigan shoreline in 2005, suggesting that 1) Lake Michigan nearshore waters (including the connecting navigation channels and pier areas) may be serving as round goby spawning and nursery habitats with subsequent dispersal into the tributary lake/wetland complexes, and 2) round gobies may still be invading these systems from Lake Michigan. Our results provide evidence that coastal wetland habitats are more resistant to invasion by round gobies than adjacent lake habitats. INDEX WORDS: Round goby, Apollonia, Neogobius melanostomus, exotic species, coastal wetland, drowned river mouth, refugia, nonindigenous.
INTRODUCTION The round goby (Apollonia melanostomus, formerly Neogobius melanostomus; see Stepien and Tumeo 2006) is a small, benthic fish native to the Ponto-Caspian region of Eastern Europe and is a recent invader of the Great Lakes. The first documented round goby capture in the Great Lakes basin occurred in the St. Clair River in 1990 (Jude et al. 1992). Since 1990, the species has rapidly spread to all five Great Lakes and by 1999 round gobies had been documented at many ports along *Corresponding
the eastern shore of Lake Michigan (Clapp et al. 2001). Round goby densities approaching 130 fish/m2 have been reported in some Lake Michigan habitats (Chotkowski and Marsden 1999) and recent estimates suggest that round gobies have become a major component of fish assemblages throughout much of the Great Lakes basin (Clapp et al. 2001, Balshine et al. 2005, Johnson et al. 2005). The proliferation of this nonindigenous species has raised concerns over its long-term impacts on native fish populations and ecosystem function (Jude 2001, Corkum et al. 2004). For example, round gobies have been implicated in the decline of native
author. E-mail: [email protected]
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FIG. 1. Map of study locations in six Lake Michigan drowned river mouth systems. Within each system, we sampled lily (l), SAV (s), and bare sediment (b) microhabitats in both the lakes and adjacent wetlands. The small arrows indicate microhabitat sampling locations. The shaded areas in each inset indicate herbaceous wetland. johnny darters (Etheostoma nigrum), mottled sculpins (Cottus bairdii), and logperch (Percina caprodes) at several locations in the basin (Dubs and Corkum 1996, French and Jude 2001, Janssen and Jude 2001, Lauer et al. 2004, Balshine et al. 2005). Carmen et al. (2006) also found that round gobies could occupy a niche similar to that of native stream fishes by consuming both drifting and benthic invertebrates in the Flint River of central Michigan.
Identification and conservation of habitats resistant to invasion would be a valuable strategy for maintaining the integrity of native fish populations given that round gobies are already established throughout much of the Great Lakes basin (with few efforts to control their dispersal). Coastal wetlands may be more resistant to invasion by certain nonindigenous species because of the unique abiotic conditions and high structural complexity of these habitats (Kålås 1995, Chapman et al. 1996,
Distribution of Round Gobies in Coastal Areas of Lake Michigan Brazner et al. 1998, Bowers and De Szalaya 2004, Jude et al. 2005). The potential resistance of coastal wetlands to invasion by round gobies seems especially promising because the benthic round goby favors rock and gravel substrates (Charlebois et al. 1997, Ray and Corkum 2001), which are relatively rare in most Great Lakes coastal wetlands (Minc and Albert 1998, Keough et al. 1999). Moreover, Uzarski et al. (2005) found few round gobies (22 of 15,263 fish) in 62 coastal wetlands located throughout all five Great Lakes using fyke nets, which Breen and Ruetz (2006) showed to be an effective technique for sampling round gobies in shallowwater habitats. Round gobies were thought to be abundant in many of the habitats adjacent to the coastal wetlands sampled by Uzarski et al. (2005). This apparent difference in round goby densities between lake habitats and adjacent coastal wetlands suggests that Great Lakes coastal wetlands may be resistant to invasion by round gobies. As a first step in testing this hypothesis, we examined round goby distributions in tributary systems of eastern Lake Michigan. The systems we studied are considered “drowned river mouths” because they occupy ancestral river valleys that were inundated when lake levels rose following deglaciation (Albert et al. 2005). Drowned river mouth systems found along this shoreline contain a broad wetland at their upstream end and a distinct lake at their downstream end with the entire complex connected to Lake Michigan by a navigable connecting channel (Fig. 1). The proximity of lake and wetland habitats in these systems made them ideal for comparing lake and wetland habitat use by round gobies. Our hypothesis was that wetland habitats would have lower round goby densities than adjoining coastal lakes. To control for the influence of habitat structure (which had the potential to confound the lake/wetland factor), we sampled the same microhabitats in each lake and wetland macrohabitat. We also explored the relationship between catch and distance of sampling sites from Lake Michigan into the drowned river mouth systems as well as round goby size distributions in these habitats. METHODS Study Sites We sampled four tributary systems (Kalamazoo, Muskegon, White, and Pentwater) in July 2004 and re-sampled these four plus two additional systems (Pigeon and Lincoln) in June 2005 (Fig. 1, Table 1). Study systems were selected to cover a continuum
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of anthropogenic disturbance using watershed land use and cover variables as proxies for anthropogenic disturbance (Uzarski et al. 2005). Pigeon Lake has a power generating plant on its northern shore. The plant has a cooling water intake canal connected to Pigeon Lake approximately 400 m northeast of our Pigeon Lake bare sediment sampling site. We delineated lake and wetland macrohabitats by identifying the confluence of the main stem of each tributary river with the drowned-river-mouth lake. All inundated wetland upstream of this point was considered the wetland macrohabitat. Within each macrohabitat (lake and wetland), we sampled three microhabitats: mono-dominant stands of Nuphar spp. (“lily”), beds of submersed aquatic vegetation (“SAV”), and bare sediment (“bare”). The majority of SAV in both the lakes and wetlands consisted of dense beds of Myriophyllum spicatum. Most SAV beds also contained Ceratophyllum demersum and several species of Potamogeton, especially Potamogeton crispus. However, these species were found in much lower densities than M. spicatum. Our criteria in choosing microhabitats to sample included: 1) sufficient depth for using fyke nets (0.2 to 1.0 m), 2) sufficient inundated area for sampling with fyke nets (approximately 200 m2), and 3) access by boat. One microhabitat of each type (lily, SAV, and bare) was chosen at random from the available habitats in each wetland and lake (Fig. 1). Wetland habitats were located in remnant channels, backwater areas, and along river margins with low flow. Lake habitats were sampled within 40 m of the lake edge. The location of each sampling point (i.e., microhabitat) was determined using a handheld global positioning system. The distance between each sampling point and Lake Michigan was measured using Arcview version 3.3 (ESRI Institute, Redlands, CA). Distances were measured from the Lake Michigan shoreline at the navigation channel to each sampling point by following the shortest route over water. Fish Sampling Fish sampling was conducted using three replicate fyke nets in each microhabitat (18 nets total per system). Fyke nets are effective for capturing round gobies in shallow littoral-zone habitats (Breen and Ruetz 2006) and have been used extensively for sampling fish in Great Lakes coastal wetlands (Brazner et al. 1998, Wilcox et al. 2002,
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TABLE 1. Site locations, distance of sampling sites from Lake Michigan, water depth, round goby catch, and mean standard lengths (±1 standard deviation) of round gobies. The Kalamazoo, Muskegon, White, and Pentwater were sampled in 2004. These four, plus the Pigeon and Lincoln, were sampled in 2005. Within each system, we sampled lake and wetland macrohabitats (“Macrohab.”). Within each macrohabitat, we sampled three microhabitats (“Microhab.”) including bare substrate, submersed aquatic vegetation (“SAV”), and lily. Distance from Lake Michigan was measured for each microhabitat as the shortest route over water. Round goby catch 2004 2005
Standard length (cm) 2004 2005
Microhab.
Latitude
Longitude
Dist. (m)
Depth (cm)
Bare Lily SAV
43° 46.28′ 43° 45.84′ 43° 46.25′
86° 25.02′ 86° 25.34′ 86° 24.91′
2,684 3,081 3,077
50 70 70
19 4 18
23 30 44
6.6±1.7 5.5±0.8 4.2±2.5
5.8±0.2 5.4±0.7 6.2±1.9
Bare Lily SAV
43° 45.57′ 43° 45.74′ 43° 45.63′
86° 23.93′ 86° 24.44′ 86° 24.02′
5,148 3,081 4,860
50 65 30
0 0 13
3 5 0
— — 7.0±2.1
5.7±3.0 5.6±1.6 —
Lake
Bare Lily SAV
42° 38.98′ 42° 38.82′ 42° 38.91′
86° 12.59′ 86° 11.82′ 86° 12.07′
4,344 4,972 4,581
55 70 52
18 11 19
10 1 16
3.2±1.6 3.1±0.3 3.3±1.6
2.2±1.8 5.3 5.2±1.5
Wetland
Bare Lily SAV
42° 38.31′ 42° 38.26′ 42° 38.31′
86° 9.58′ 86° 9.71′ 86° 9.64′
9,257 8,734 9,026
40 67 40
35 16 4
1 4 1
2.8±0.4 2.6±0.4 2.2
5.2 5.5±1.4 2
Lake
Bare Lily SAV
43° 14.35′ 43° 15.55′ 43° 14.62′
86° 19.51′ 86° 15.22′ 86° 16.92′
1,731 8,775 5,490
80 42 98
0 0 93
0 0 67
— — 4.5±1.1
— — 5.1±0.4
Wetland
Bare Lily SAV
43° 15.91′ 43° 16.49′ 43° 15.99′
86° 11.70′ 86° 11.79′ 86° 12.08′
14,973 14,038 14,015
27 26 38
4 0 2
1 24 0
6.8±1.8 — 4.5±3.0
4.8 5.0±1.3 —
Lake
Bare Lily SAV
43° 23.28′ 43° 24.72′ 43° 24.61′
86° 22.60′ 86°21.13′ 86° 21.44′
4,767 8,216 7,715
58 55 70
1 1 1
1 0 1
4.6 6.0 5.6
4.8 — 6.3
Wetland
Bare Lily SAV
43° 25.54′ 43° 25.42′ 43° 25.56′
86° 19.56′ 86° 18.69′ 86° 19.57′
11,427 12,940 11,535
30 35 70
0 0 0
0 1 2
— — —
— 4.6 5.1±0.1
Lake
Bare Lily SAV
42° 54.00′ 42° 54.16′ 42° 54.09′
86° 12.51′ 86° 11.98′ 86° 11.99′
640 1,394 1,385
94 70 55
NA NA NA
278 22 399
— — —
4.2±1.1 4.5±1.0 4.5±1.0
Wetland
Bare Lily SAV
42° 53.98′ 42° 53.37′ 42° 53.91′
86° 11.72′ 86° 11.48′ 86° 11.63′
1,660 2,850 2,041
60 75 82
NA NA NA
39 5 24
— — —
4.9±0.7 6.4±1.0 5.2±0.8
Lake
Bare Lily SAV
43° 58.93′ 43° 58.65′ 43° 58.77′
86° 27.83′ 86° 27.04′ 86° 27.43′
973 2,329 1,590
80 60 98
NA NA NA
23 0 9
— — —
4.6±1.3 — 6.3±0.8
Wetland
Bare Lily SAV
43° 58.88′ 43° 58.89′ 43° 58.90′
86° 26.01′ 86° 26.22′ 86° 26.16′
3,879 3,686 3,390
50 45 60
NA NA NA
4 2 1
— — —
6.6±1.1 4.9±0.1 5.2
System Macrohab. Pentwater Lake
Wetland Kalamazoo
Muskegon
White
Pigeon
Lincoln
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Uzarski et al. 2005). Small fyke nets (mouth: 0.5 × 1 m) were fished at water depths of 0.2 to 0.5 m, whereas large fyke nets (mouth: 1 × 1 m) were fished at water depths of 0.5 to 1.0 m. Water depth dictated which size fyke net we used because the only difference between large and small nets was the height. Leads extended 7.3 m from the middle of the mouth, and wings extended 1.8 m from both sides of the mouth (45° angle to the lead). The mesh size was 4.8 mm (bar measurement). Two of the three nets fished in each microhabitat were set as a pair with openings facing one another and leads positioned end to end within the microhabitat of interest (Brazner 1997, Brazner et al. 1998). A third net was set nearby (approximately 25–75 m away) with the lead extending into the microhabitat (Uzarski et al. 2005). Nets were hauled after an approximate 24-hour soak time and round gobies were measured (standard length) and enumerated in the field. After measurement and enumeration, round gobies were euthanized and disposed of. All other fish were released alive. We report catch as the total number of round gobies captured in the three nets fished at each microhabitat. Statistical Analyses Data from 2004 were analyzed separately from 2005. A three-way split-plot analysis of variance (ANOVA) was used to test whether the catch of round gobies differed among macrohabitats (lake, wetland), microhabitats (lily, SAV, bare), and their interaction (Montgomery 1991). System served as a blocking variable, macrohabitat was the whole plot, and microhabitat was the subplot. When significant effects were found, Tukey’s HSD tests were conducted post-hoc to identify differences. Round goby catch was natural log-transformed [ln(n+1)] prior to analysis to homogenize variance based on residual plots. Differences in round goby standard length (each observation was a mean of all round gobies caught at a microhabitat) between macrohabitats were analyzed using paired t-tests (lake vs. wetland sites paired by microhabitat type). We used paired t-tests for the length comparisons because round gobies were not collected at a number of microhabitats, which prevented us from using a split-plot ANOVA approach. We used pair-wise deletion for cases when at least one of the microhabitats in a pair did not have round gobies. We ran split-plot ANOVA, Tukey’s HSD, and paired t-tests in SAS version 8.0 (Cary, North Carolina). To investigate the relationship between round goby catch and dis-
FIG. 2. Round goby catch (±1 standard error) showing differences due to macrohabitat (lake vs. wetland) in four Lake Michigan drowned river mouth systems sampled in 2004 and six systems sampled in 2005. tance from Lake Michigan, we used Pearson correlations. Both variables were natural log-transformed [ln(n+1) for catch data]. RESULTS Round Goby Distributions Round gobies were caught at 67% of the sites in 2004 and 81% in 2005 (Table 1). The largest collections of round gobies were made in SAV microhabitats of lakes in both years (Fig. 2). Catch of round
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Cooper et al. TABLE 2. Split-plot analysis of variance results for the effects of macrohabitat (lake, wetland), microhabitat (bare substrate, lily, submersed aquatic vegetation), and the interaction of macrohabitat and microhabitat on round goby catch in Lake Michigan drowned river mouth systems. System (four in 2004, six in 2005) was the blocking variable. Source of variation
df
MS
System Macrohabitat Whole plot errora Microhabitat Microhabitat x Macrohabitat Subplot errorb
3 1 3 2 2 12
5.96 3.55 0.59 2.48 0.72 1.40
F
P
5.97
0.092
1.78 0.52
0.211 0.610
2004
2005 System 5 8.01 Macrohabitat 1 9.21 5.88 0.060 Whole plot errora 5 1.57 Microhabitat 2 1.44 1.36 0.279 Microhabitat x Macrohabitat 2 6.14 5.82 0.010 Subplot errorb 20 1.05 a The whole plot error term was the system x macrohabitat effect b The subplot error term was the system x macrohabitat x microhabitat effect
gobies was greatest in Muskegon Lake in 2004 and Pigeon Lake in 2005 (Table 1). We captured the fewest round gobies in White Lake in both years (Table 1). Round goby catch tended to be greater in lake macrohabitats than wetland macrohabitats in both years (Fig. 2). The effect of macrohabitat (lake vs. wetland) was marginally significant in 2004 and 2005 (Table 2). The interaction between macrohabitat and microhabitat was significant in 2005 (Table 2). Catch of round gobies was significantly greater at lake-SAV sites than lake-lily, wetland-bare, and wetland-SAV sites (Table 3). The effect of microhabitat alone was not significant in either year (Table 2). Excluding White Lake and wetland from our analysis, because few round gobies were caught
in this system (Table 1), weakened the effect of macrohabitat in 2004 and strengthened the effect of macrohabitat in 2005. Macrohabitat (F1,2 = 3.20, p = 0.215), microhabitat (F 2,8 = 1.81, p = 0.224), and the interaction (F2,8 = 0.53, p = 0.610) were not significant in 2004, whereas microhabitat (F 2,16 = 1.20, p = 0.328) was not significant and macrohabitat (F 1,4 = 8.44, p = 0.044) and the interaction (F2,16 = 6.12, p = 0.011) were significant in 2005 when White Lake and wetland were excluded. The majority of round gobies that we caught were smaller than 7 cm standard length (Table 1, Fig. 3). The dominant size class in both macrohabitats during both years was 3-7 cm (Fig. 3). No reproductive male round gobies, with their characteristic dark color (Jude 1997), were ob-
TABLE 3. Tukey’s HSD p-values for pair-wise comparisons of round goby catch per net-night per microhabitat in 2005. Catch data were natural log-transformed [ln(n+1)]. Lake SAV Lake lily Lake bare Wetland SAV Wetland lily
Lake lily 0.022
Lake bare 0.760 0.282
Wetland SAV 0.008 0.998 0.134
Wetland lily 0.117 0.959 0.743 0.800
Wetland bare 0.035 0.999 0.392 0.984 0.990
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FIG. 3. Length frequency distributions for round gobies caught in Lake Michigan drowned river mouth lakes and wetlands in 2004 and 2005. served in our catch. Mean lengths of round gobies (Table 1) did not differ significantly between macrohabitats in either year (2004: t = 0.23, d.f. = 4, p = 0.84; 2005: t = 0.54, d.f. = 10, p = 0.60). Round goby catch tended to decrease the farther a site was located from Lake Michigan. Correlations between round goby catch and distance from Lake Michigan were negative in both years but only significant in 2005, which may be due in part to the lower sample size in 2004 (i.e., four systems were sampled in 2004 and six in 2005). In 2004, the correlations were not significant for lake sites (r = –0.161, d.f. = 11, p = 0.618), wetland sites (r = –0.093, d.f. = 11, p = 0.775), or all sites (r = –0.273, d.f. = 23, p = 0.197). In 2005, significant negative correlations were found for lake sites (r = –0.570, d.f. = 17, p = 0.013), wetland sites
(r = –0.527, d.f. = 17, p = 0.025), and all sites (r = –0.599, d.f. = 35, p = 0.003). DISCUSSION We caught round gobies in lake and wetland habitats of all six study systems, indicating that this nonindigenous fish has successfully colonized coastal habitats in this portion of Lake Michigan. Lake macrohabitats tended to have more round gobies than wetland macrohabitats in both years though the effect was stronger in 2005. Excluding White Lake and wetland from habitat comparisons weakened the effect of macrohabitat in 2004 and strengthened this effect in 2005, highlighting the potential for temporal variation in habitat selection by round gobies. However, this difference between years was likely a consequence of reduced statisti-
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cal power (Lenth 2001) rather than an ecologically meaningful difference between years because more round gobies were caught in White Lake than White wetland in 2004 while the opposite trend was observed in 2005 (Table 1). Our hypothesis was based on the fact that Uzarski et al. (2005) captured few round gobies in coastal wetlands, yet round gobies were thought to inhabit adjacent habitats. Therefore, if we exclude systems with low numbers of round gobies, then we are biasing our analysis toward finding an effect. For example, if all the systems had few round gobies, then this observation would not support our hypothesis and, therefore, has bearing on whether coastal wetlands are resistant to invasion. Nevertheless, if our focus had been purely on habitat selection by round gobies, then excluding the White system is justified given that few round gobies were captured in that system. The apparent preference for lake habitats by round gobies supported our working hypothesis that coastal wetlands are resistant to invasion by round gobies. However, this trend was not consistent across the three microhabitat types. Catch of round gobies at lake-SAV sites was greater than two of the three wetland microhabitats. This suggests that while coastal wetlands may provide refuge from round gobies, the effect could be more pronounced for native species that utilize SAV microhabitats. Also, lily appeared to be the least preferred of the three lake microhabitats, which further supports our hypothesis that wetlands are resistant to invasion by round gobies because the lily microhabitat in lakes was more similar to a wetland than the other lake microhabitats. Plausible explanations for the difference in round goby catch between drowned river mouth lakes and wetlands may be related to time since invasion and availability of hard benthic substrate. First, invading round gobies most likely entered drowned river mouth systems either from Lake Michigan or by secondary dispersal via ship ballast water exchange (Mills et al. 1993, Clapp et al. 2001). The duration necessary for round goby populations to colonize upstream wetlands is not clear. However, distances between adjacent lake and wetland macrohabitats in our study were typically less than distances between drowned river mouth systems along the eastern shore of Lake Michigan (Fig. 1). Given that round gobies spread naturally to drowned river mouth systems that do not have shipping traffic (Clapp et al. 2001), it seems unlikely that the difference in round goby catch between macrohabitats was merely a result of insufficient time for round
gobies to invade the upstream wetlands. Secondly, hard substrates were rarely observed in the wetlands compared to the lakes where seawalls, concrete riprap, docks, and pilings were common. We did not sample a hard-substrate microhabitat because of their low occurrence in wetlands. We preferred a conservative approach where we maintained consistent microhabitats between lakes and wetlands to ensure that the macrohabitat factor was not confounded by sampling different microhabitats in each macrohabitat. Since round gobies prefer habitats containing cobble, boulders, and/or artificial riprap (Jude and DeBoe 1996, Charlebois et al. 1997, Ray and Corkum 2001, Johnson et al. 2005), differences in substrate may explain the difference in round goby catch between the lakes and wetlands. We predict that including rock and gravel microhabitats in the lakes would have magnified differences in round goby catch between macrohabitats. The majority of round gobies we caught most likely consumed benthic insects and crustaceans because they were less than 7 cm standard length, the size that round gobies begin to include bivalves in their diet (Jude et al. 1995, Ghedotti et al. 1995, Ray and Corkum 1997). Furthermore, in benthic dipnet samples taken in the same microhabitats as this study (2004 only), bivalves (including dreissenids and spaeriid clams) were rare, comprising less than 1% of the benthic macroinvertebrate fauna (unpublished data). This suggests that bivalves are probably not an important food resource for round gobies in the three microhabitats we sampled. Carmen et al. (2005) found that round gobies primarily ate chironomid larvae and pupae, heptageniid nymphs, and Daphnia in a river that did not contain dreissenid mussels, indicating that round goby populations can persist in the absence of dreissenids. Future studies should address the diet of round gobies in coastal habitats with low bivalve densities, such as Great Lakes coastal wetlands, to determine the extent round gobies are consuming non-mussel prey. The negative relationship we found between round goby catch and distance from Lake Michigan may suggest that round gobies are still invading these systems. However, an alternative explanation is that Lake Michigan nearshore habitats (including the pier areas) function as round goby spawning and nursery habitats that are a continual source of round gobies to the drowned river mouth lake/wetland complexes. This explanation seems plausible given that round gobies prefer habitats containing
Distribution of Round Gobies in Coastal Areas of Lake Michigan cobble, boulders, and/or artificial riprap (Jude and DeBoe 1996, Charlebois et al. 1997, Ray and Corkum 2001, Johnson et al. 2005) and most of the channels that connect drowned river mouth lakes to Lake Michigan were lined with boulders and/or riprap in our study systems. Furthermore, Ray and Corkum (2001) found that in the St. Clair RiverLake St. Clair-Detroit River corridor, round gobies tended to be smaller in recently invaded habitats. The round gobies that we caught also tended to be small with the majority being between 2 and 6 cm standard length (Fig. 3). Though we did not determine ages, we speculate that the majority of round gobies we caught were between age 0+ and 2+ based on length-at-age data from other studies in the Great Lakes basin (Phillips et al. 2003, MacInnis and Corkum 2000). This suggests that round gobies in drowned river mouth lakes and wetlands tend to be young immigrants from other habitats. We also found pronounced differences in round goby catch among the six study systems. While this was not a focus of the study, we found that Pigeon Lake had much higher catches of round gobies than any of the other systems. Pigeon Lake’s small size and proximity to Lake Michigan (Fig. 1) likely facilitated movement and spread of round gobies throughout the system. However, explanations for the low catches of round gobies in White Lake and wetland are unknown. Our results are consistent with our working hypothesis that Lake Michigan drowned river mouth wetlands are more resistant to invasion by round gobies than adjacent lake habitats. This contributes to a growing body of evidence suggesting that Great Lakes coastal wetlands are resistant to invasion by certain nonindigenous species. For example, native unionid populations were found to utilize coastal wetlands for refugia from nonindigenous zebra mussels (Nichols and Amberg 1999, Bowers and De Szalaya 2004) and wetland habitats in Lake Superior were found to be resistant to invasion by nonindigenous ruffe (Gymnocephalus cernuus) (Brazner et al. 1998). However, we observed nonindigenous plants (M. spicatum and P. crispus) at our study sites, and common carp (Cyprinus carpio) inhabit many Great Lakes coastal wetlands (Lougheed et al. 1998), indicating that coastal wetlands are not resistant to all nonindigenous species and the potential for coastal wetlands to serve as true refugia for native species is likely species specific. While we generally found fewer round gobies in wetland habitats, the questions remain: 1) will
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round goby densities in Lake Michigan drowned river mouth wetlands increase in future years once adjacent lakes are saturated (assuming the lakes are not currently saturated), 2) do round goby populations in other types of Great Lakes coastal wetland have similar distribution patterns, and 3) are round goby distributions determined by community-level drivers such as predation pressure or prey availability? Numerous studies have identified deleterious effects of the round goby invasion on native species including displacement by aggressive interactions (Dubs and Corkum 1996, Janssen and Jude 2001, Balshine et al. 2005) and predation of eggs and fry (Chotkowski and Marsden 1999, Nichols et al. 2003, Steinhart et al. 2004). Therefore, restoration and protection of Great Lakes coastal wetlands may help control the spread of round gobies as well as provide critical habitat for native fishes (Jude and Pappas 1992, Uzarski et al. 2005), birds (Prince et al. 1992), reptiles, and amphibians (Weeber and Vallianatos 2000). ACKNOWLEDGMENTS We thank the Great Lakes Coastal Program of the U.S. Fish and Wildlife Service, especially Ted Koehler, as well as the Michigan Department of Environmental Quality, especially Peg Bostwick and Dave Kenaga, for funding this research. We thank Matthew Breen, Adam Bosch, Aaron Parker, Keto Gyekis, Michael Shoemaker, Pam Parker, Nicholas Fiore, Eric Nemeth, Dana VanHaitsma, Melissa Reneski, Nathan Coady, Kenneth Davenport, Rebecca E. Kolar, Jamie M. Zbytowski, and Mary Ogdahl for assistance in the field and laboratory. Comments by Drs. J. Brazner, J. Janssen, T. Phillips, and an anonymous reviewer contributed substantially to an earlier version of this manuscript. REFERENCES Albert, D.A., Wilcox, D.A., Ingram, J.W., and Thompson, T.A. 2005. Hydrogeomorphic classification for Great Lakes coastal wetlands. J. Great Lakes Res. 31 (Supplement 1):126–146. Balshine, S., Verma, A., Chant, V., and Theysmeyer, T. 2005. Competitive interactions between round gobies and logperch. J. Great Lakes Res. 31:68–77. Bowers, R., and De Szalaya, F.A. 2004. Effects of hydrology on unionids (Unionidae) and zebra mussels (Dreissenidae) in a Lake Erie coastal wetland. Am. Mid. Nat. 151:286–300. Brazner, J.C. 1997. Regional, habitat, and human devel-
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opment influences on coastal wetland and beach fish assemblages in Green Bay, Lake Michigan. J. Great Lakes Res. 23:36–51. ——— , Tanner, D.K., Jensen, D.A., and Lemke, A. 1998. Relative abundance and distribution of Ruffe (Gymnocephalus cernus) in a Lake Superior coastal wetland fish assemblage. J. Great Lakes Res. 24:293–303. Breen, M.J., and Ruetz, C.R. 2006. Gear bias in fyke netting: evaluating soak time, fish density, and predators. N. Am. J. Fish. Manage. 26:32–41. Carman, S.M., Janssen, J., Jude, D.J., and Berg, M.B. 2006. Diel interactions between prey behavior and feeding in an invasive fish, the round goby, in a North American river. Freshwater Biology 51:742–755. Chapman, L.J., Chapman, M., and Chandler, M. 1996. Wetland ecotones as refugia for endangered fishes. Biol. Conserv. 78:263–270. Charlebois, P.M., Marsken, J.E., Goettel, R.G., Wolfe, R.K., Jude, D.J., and Rudnicka, S. 1997. The round goby, Neogobius melanostomus (Pallas), a review of European and North American literature. IllinoisIndiana Sea Grant Program and Illinois Natural History Survey. INHS Special Publication No. 20. Chotkowski, M.A., and Marsden, J.E. 1999. Round goby and mottled sculpin predation on lake trout eggs and fry: field predictions from laboratory experiments. J. Great Lakes Res. 25:26–35. Clapp, D.F., Schneeberger, P.J., Jude, D.J., Madison, G., and Pistis, C. 2001. Monitoring round goby (Neogobius melanostomus) population expansion in eastern and northern Lake Michigan. J. Great Lakes Res. 27:335–341. Corkum, L.D., Sapota, M.R., and Skora, K.E. 2004. The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biol. Invasions 6:173–181. Dubs, D.O.L., and Corkum, L.D. 1996. Behavioral interactions between round gobies (Neobobius melanostomus) and mottled sculpin (Cottus baridi). J. Great Lakes Res. 22:838–844. French, III, J.R.P., and Jude, D.J. 2001. Diets and diet overlap of nonindigenous gobies and small benthic fishes co-inhabiting the St. Clair River, Michigan. J. Great Lakes Res. 27:300–311. Ghedotti, M.J., Smihula, J.C., and Smith, G.R. 1995. Zebra mussel predation by round gobies in the laboratory. J. Great Lakes Res. 21:665–669. Janssen, J., and Jude, D.J. 2001. Recruitment failure of mottled sculpin Cottus bairdi in Calumet Harbor, southern Lake Michigan, induced by the newly introduced round goby Neogobius melanostomus. J. Great Lakes Res. 27:319–328. Johnson, T.B., Allen, M., Corkum, L.D., and Lee, V.A. 2005. Comparison of methods needed to estimate population size of round gobies (Neogobius melanos-
tomus) in western Lake Erie. J. Great Lakes Res. 31:78–86. Jude, D.G. 1997. Round gobies: Cyberfish of the third millennium. Great Lakes Research Review 3:27–34. ——— . 2001. Round and tubenose gobies: 10 years with the latest Great Lakes phantom menace. Dreissena! 11:1–14. ——— , and DeBoe, S.F. 1996. Possible impact of gobies and other introduced species on habitat restoration efforts. Can. J. Fish. Aquat. Sci. 53(Suppl. 1):136–141. ——— , and Pappas, J. 1992. Fish utilization of Great Lakes wetlands. J. Great Lakes Res. 18:651–672. ——— , Reider, R.H., and Smith, G.R. 1992. Establishment of Gobiidae in the Great Lakes basin. Can. J. Fish. Aquat. Sci. 49:416–421. ——— , Janssen, J., and Crawford, G. 1995. Ecology, distribution, and imapct of the newly introduced round and tubenose gobies on the biota of the St. Clair and Detroit Rivers. In The Lake Huron ecosystem: ecology, fisheries, and management, M. Munawar, T. Edsall, and J. Leach, eds., Ecovision World Monograph Series, pp. 447–460. Amsterdam, The Netherlands: Academic Publishing. ——— , Albert, D., Uzarski, D.G., and Brazner, J. 2005. Lake Michigan’s Coastal Wetlands: Distribution, Biological Components and Threats. In The State of Lake Michigan, M. Munawar and T. Edsall, eds. Ecovision World Monograph Series. Aquatic Ecosystem Health and Management Society. Kålås, S. 1995. The ecology of ruffe, Gymnocephalus cernus (Pisces: Percidae), introduced to Mildevatn, western Norway. Environ. Biol. Fish. 42:219–232. Keough, J.R., Thompson, T.A., Guntenspergen, G.R., and Wilcox, D.A. 1999. Hydrogeomorphic factors and ecosystem responses in coastal wetlands of the Great Lakes. Wetlands 19:821–834. Lauer, T.E., Allen, P.J., and McComish, T.S. 2004. Changes in mottled sculpin and johnny darter trawl catches after the appearance of round gobies in the Indiana waters of Lake Michigan. Trans. Am. Fish. Soc. 133:185–189. Lenth, R.V. 2001. Some practical guidelines for effective sample size determination. Am. Stat. 55:187–193 Lougheed, V.L., Crosbie, B., and Chow-Fraser, P. 1998. Predictions on the effect of common carp (Cyprinus carpio) exclusion on water quality, zooplankton, and submergent macrophytes in a Great Lakes wetland. Can. J. Fish. Aquat. Sci. 55:1189–1197. MacInnis, A.J., and Corkum, L.D. 2000. Fecundity and reproductive season of the round goby Neogobius melanostomus in the upper Detroit River. Trans. Am. Fish. Soc. 129:136–144. Mills, E.L., Leach, J.H., Carlton, J.T., and Secor, C.L. 1993. Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J. Great Lakes Res. 19:1–54.
Distribution of Round Gobies in Coastal Areas of Lake Michigan Minc, L.D., and Albert, D.A. 1998. Great Lakes Coastal Wetlands: Abiotic and Floristic Characterization. Michigan Natural Features Inventory. Montgomery, D.C. 1991. Design and Analysis of Experiments (3rd ed.), New York: John Wiley and Sons, Inc. Nichols, S.J., and Amberg, J. 1999. Co-existence of zebra mussels and freshwater unionids: population dynamics of Leptodea fragilis in a coastal wetland infested with zebra mussels. Can. J. Zool. 77:423–432. ——— , Kennedy, G., Crawford, E., Allan, J., French, J., Black, G., Blouin, M., Hickey, J., Chernyak, S., Haas, R.C., and Thomas, M.V. 2003. Assessment of lake sturgeon (Acipenser fulvescens) spawning effort in the lower St. Clair River, Michigan. J. Great Lakes Res. 29:383–391. Phillips, E.C., Washek, M.E., Hertel, A.W., and Niebel, B.M. 2003. The round goby (Neogobius melanostomus) in Pennsylvania tributary streams of Lake Erie. J. Great Lakes Res. 29:34–40. Prince, H.H., Padding, P.I., and Knapton, R.W. 1992. Waterfowl use of the Laurentian Great Lakes. J. Great Lakes Res. 18:673–99. Ray, W.J., and Corkum, L.D. 1997. Predation of zebra mussels by round gobies, Neogobius melanostomus. Environ. Biol. Fish. 50:267–273. ——— , and Corkum, L.D. 2001. Habitat and site affinity of the round goby. J. Great Lakes Res. 27:329–334.
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Steinhart, G.B., Marschall, E.A., and Stein, R.A. 2004. Round goby predation on smallmouth bass offspring in nests during simulated catch-and-release angling. Trans. Am. Fish. Soc. 133:121–131. Stepien, C.A., and Tumeo, M.A. 2006. Invasion of Ponto-Caspian gobies in the Great Lakes: a “cryptic” species, absence of founder effects, and comparative risk analysis. Biological Invasions 8:61–78. Uzarski, D.G., Burton, T.M., Cooper, M.J., Ingram, J.W., and Timmermans, S. 2005. Fish habitat use within and across wetland classes in coastal wetlands of the five Great Lakes: Development of a fish-based index of biotic integrity. J. Great Lakes Res. 31 (Supplement 1):171–196. Weeber, R.C., and Vallianatos, M. 2000. The Marsh Monitoring Program 1995–1999: Monitoring Great Lakes wetlands and their amphibian and bird inhabitants. Bird Studies Canada, Port Rowan, Ontario. Wilcox, D.A., Meeker, J.E., Hudson, P.L., Armitage, B.J., Black, M.G., and Uzarski, D.G. 2002. Hydrologic variability and the application of index of biotic integrity metrics to wetlands: a Great Lakes evaluation. Wetlands 22:588–615. Submitted: 24 February 2006 Accepted: 9 January 2007 Editorial handling: John Janssen
Distribution of Round Gobies in Coastal Areas of Lake Michigan: Are Wetlands Resistant to Invasion? Matthew J. Cooper1,*, Carl R. Ruetz III1, Donald G. Uzarski1, and Thomas M. Burton2 1Grand
Valley State University Annis Water Resources Institute 740 W. Shoreline Dr. Muskegon, Michigan 49441 2Michigan
State University Departments of Zoology and Fisheries and Wildlife 25B Natural Science East Lansing, Michigan 48824 ABSTRACT. Great Lakes coastal wetlands may be more resistant to invasion by certain nonindigenous species and thus serve as refuge habitats for native species. As a first step in testing this hypothesis, we investigated the distribution of round goby (Apollonia melanostomus, formerly Neogobius melanostomus) in the lower reaches of several Lake Michigan tributary systems that contain both wetland and lake habitats near their confluences with Lake Michigan. Using fyke nets, we sampled round gobies in lake and adjacent wetland habitats in four systems in 2004 and six systems in 2005. In each macrohabitat (lake or wetland), we sampled three microhabitats (mono-dominant stands of Nuphar, beds of submersed aquatic vegetation, and bare sediment). We found that round goby catch was generally lower in wetland macrohabitats than adjacent lake macrohabitats and that round gobies appeared to prefer beds of submersed aquatic vegetation in lakes among the three microhabitats. The majority of round gobies in all habitats were relatively small (< 7 cm standard length). We also found a significant negative correlation between round goby catch and distance of sampling points from the Lake Michigan shoreline in 2005, suggesting that 1) Lake Michigan nearshore waters (including the connecting navigation channels and pier areas) may be serving as round goby spawning and nursery habitats with subsequent dispersal into the tributary lake/wetland complexes, and 2) round gobies may still be invading these systems from Lake Michigan. Our results provide evidence that coastal wetland habitats are more resistant to invasion by round gobies than adjacent lake habitats. INDEX WORDS: Round goby, Apollonia, Neogobius melanostomus, exotic species, coastal wetland, drowned river mouth, refugia, nonindigenous.
INTRODUCTION The round goby (Apollonia melanostomus, formerly Neogobius melanostomus; see Stepien and Tumeo 2006) is a small, benthic fish native to the Ponto-Caspian region of Eastern Europe and is a recent invader of the Great Lakes. The first documented round goby capture in the Great Lakes basin occurred in the St. Clair River in 1990 (Jude et al. 1992). Since 1990, the species has rapidly spread to all five Great Lakes and by 1999 round gobies had been documented at many ports along *Corresponding
the eastern shore of Lake Michigan (Clapp et al. 2001). Round goby densities approaching 130 fish/m2 have been reported in some Lake Michigan habitats (Chotkowski and Marsden 1999) and recent estimates suggest that round gobies have become a major component of fish assemblages throughout much of the Great Lakes basin (Clapp et al. 2001, Balshine et al. 2005, Johnson et al. 2005). The proliferation of this nonindigenous species has raised concerns over its long-term impacts on native fish populations and ecosystem function (Jude 2001, Corkum et al. 2004). For example, round gobies have been implicated in the decline of native
author. E-mail: [email protected]
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FIG. 1. Map of study locations in six Lake Michigan drowned river mouth systems. Within each system, we sampled lily (l), SAV (s), and bare sediment (b) microhabitats in both the lakes and adjacent wetlands. The small arrows indicate microhabitat sampling locations. The shaded areas in each inset indicate herbaceous wetland. johnny darters (Etheostoma nigrum), mottled sculpins (Cottus bairdii), and logperch (Percina caprodes) at several locations in the basin (Dubs and Corkum 1996, French and Jude 2001, Janssen and Jude 2001, Lauer et al. 2004, Balshine et al. 2005). Carmen et al. (2006) also found that round gobies could occupy a niche similar to that of native stream fishes by consuming both drifting and benthic invertebrates in the Flint River of central Michigan.
Identification and conservation of habitats resistant to invasion would be a valuable strategy for maintaining the integrity of native fish populations given that round gobies are already established throughout much of the Great Lakes basin (with few efforts to control their dispersal). Coastal wetlands may be more resistant to invasion by certain nonindigenous species because of the unique abiotic conditions and high structural complexity of these habitats (Kålås 1995, Chapman et al. 1996,
Distribution of Round Gobies in Coastal Areas of Lake Michigan Brazner et al. 1998, Bowers and De Szalaya 2004, Jude et al. 2005). The potential resistance of coastal wetlands to invasion by round gobies seems especially promising because the benthic round goby favors rock and gravel substrates (Charlebois et al. 1997, Ray and Corkum 2001), which are relatively rare in most Great Lakes coastal wetlands (Minc and Albert 1998, Keough et al. 1999). Moreover, Uzarski et al. (2005) found few round gobies (22 of 15,263 fish) in 62 coastal wetlands located throughout all five Great Lakes using fyke nets, which Breen and Ruetz (2006) showed to be an effective technique for sampling round gobies in shallowwater habitats. Round gobies were thought to be abundant in many of the habitats adjacent to the coastal wetlands sampled by Uzarski et al. (2005). This apparent difference in round goby densities between lake habitats and adjacent coastal wetlands suggests that Great Lakes coastal wetlands may be resistant to invasion by round gobies. As a first step in testing this hypothesis, we examined round goby distributions in tributary systems of eastern Lake Michigan. The systems we studied are considered “drowned river mouths” because they occupy ancestral river valleys that were inundated when lake levels rose following deglaciation (Albert et al. 2005). Drowned river mouth systems found along this shoreline contain a broad wetland at their upstream end and a distinct lake at their downstream end with the entire complex connected to Lake Michigan by a navigable connecting channel (Fig. 1). The proximity of lake and wetland habitats in these systems made them ideal for comparing lake and wetland habitat use by round gobies. Our hypothesis was that wetland habitats would have lower round goby densities than adjoining coastal lakes. To control for the influence of habitat structure (which had the potential to confound the lake/wetland factor), we sampled the same microhabitats in each lake and wetland macrohabitat. We also explored the relationship between catch and distance of sampling sites from Lake Michigan into the drowned river mouth systems as well as round goby size distributions in these habitats. METHODS Study Sites We sampled four tributary systems (Kalamazoo, Muskegon, White, and Pentwater) in July 2004 and re-sampled these four plus two additional systems (Pigeon and Lincoln) in June 2005 (Fig. 1, Table 1). Study systems were selected to cover a continuum
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of anthropogenic disturbance using watershed land use and cover variables as proxies for anthropogenic disturbance (Uzarski et al. 2005). Pigeon Lake has a power generating plant on its northern shore. The plant has a cooling water intake canal connected to Pigeon Lake approximately 400 m northeast of our Pigeon Lake bare sediment sampling site. We delineated lake and wetland macrohabitats by identifying the confluence of the main stem of each tributary river with the drowned-river-mouth lake. All inundated wetland upstream of this point was considered the wetland macrohabitat. Within each macrohabitat (lake and wetland), we sampled three microhabitats: mono-dominant stands of Nuphar spp. (“lily”), beds of submersed aquatic vegetation (“SAV”), and bare sediment (“bare”). The majority of SAV in both the lakes and wetlands consisted of dense beds of Myriophyllum spicatum. Most SAV beds also contained Ceratophyllum demersum and several species of Potamogeton, especially Potamogeton crispus. However, these species were found in much lower densities than M. spicatum. Our criteria in choosing microhabitats to sample included: 1) sufficient depth for using fyke nets (0.2 to 1.0 m), 2) sufficient inundated area for sampling with fyke nets (approximately 200 m2), and 3) access by boat. One microhabitat of each type (lily, SAV, and bare) was chosen at random from the available habitats in each wetland and lake (Fig. 1). Wetland habitats were located in remnant channels, backwater areas, and along river margins with low flow. Lake habitats were sampled within 40 m of the lake edge. The location of each sampling point (i.e., microhabitat) was determined using a handheld global positioning system. The distance between each sampling point and Lake Michigan was measured using Arcview version 3.3 (ESRI Institute, Redlands, CA). Distances were measured from the Lake Michigan shoreline at the navigation channel to each sampling point by following the shortest route over water. Fish Sampling Fish sampling was conducted using three replicate fyke nets in each microhabitat (18 nets total per system). Fyke nets are effective for capturing round gobies in shallow littoral-zone habitats (Breen and Ruetz 2006) and have been used extensively for sampling fish in Great Lakes coastal wetlands (Brazner et al. 1998, Wilcox et al. 2002,
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TABLE 1. Site locations, distance of sampling sites from Lake Michigan, water depth, round goby catch, and mean standard lengths (±1 standard deviation) of round gobies. The Kalamazoo, Muskegon, White, and Pentwater were sampled in 2004. These four, plus the Pigeon and Lincoln, were sampled in 2005. Within each system, we sampled lake and wetland macrohabitats (“Macrohab.”). Within each macrohabitat, we sampled three microhabitats (“Microhab.”) including bare substrate, submersed aquatic vegetation (“SAV”), and lily. Distance from Lake Michigan was measured for each microhabitat as the shortest route over water. Round goby catch 2004 2005
Standard length (cm) 2004 2005
Microhab.
Latitude
Longitude
Dist. (m)
Depth (cm)
Bare Lily SAV
43° 46.28′ 43° 45.84′ 43° 46.25′
86° 25.02′ 86° 25.34′ 86° 24.91′
2,684 3,081 3,077
50 70 70
19 4 18
23 30 44
6.6±1.7 5.5±0.8 4.2±2.5
5.8±0.2 5.4±0.7 6.2±1.9
Bare Lily SAV
43° 45.57′ 43° 45.74′ 43° 45.63′
86° 23.93′ 86° 24.44′ 86° 24.02′
5,148 3,081 4,860
50 65 30
0 0 13
3 5 0
— — 7.0±2.1
5.7±3.0 5.6±1.6 —
Lake
Bare Lily SAV
42° 38.98′ 42° 38.82′ 42° 38.91′
86° 12.59′ 86° 11.82′ 86° 12.07′
4,344 4,972 4,581
55 70 52
18 11 19
10 1 16
3.2±1.6 3.1±0.3 3.3±1.6
2.2±1.8 5.3 5.2±1.5
Wetland
Bare Lily SAV
42° 38.31′ 42° 38.26′ 42° 38.31′
86° 9.58′ 86° 9.71′ 86° 9.64′
9,257 8,734 9,026
40 67 40
35 16 4
1 4 1
2.8±0.4 2.6±0.4 2.2
5.2 5.5±1.4 2
Lake
Bare Lily SAV
43° 14.35′ 43° 15.55′ 43° 14.62′
86° 19.51′ 86° 15.22′ 86° 16.92′
1,731 8,775 5,490
80 42 98
0 0 93
0 0 67
— — 4.5±1.1
— — 5.1±0.4
Wetland
Bare Lily SAV
43° 15.91′ 43° 16.49′ 43° 15.99′
86° 11.70′ 86° 11.79′ 86° 12.08′
14,973 14,038 14,015
27 26 38
4 0 2
1 24 0
6.8±1.8 — 4.5±3.0
4.8 5.0±1.3 —
Lake
Bare Lily SAV
43° 23.28′ 43° 24.72′ 43° 24.61′
86° 22.60′ 86°21.13′ 86° 21.44′
4,767 8,216 7,715
58 55 70
1 1 1
1 0 1
4.6 6.0 5.6
4.8 — 6.3
Wetland
Bare Lily SAV
43° 25.54′ 43° 25.42′ 43° 25.56′
86° 19.56′ 86° 18.69′ 86° 19.57′
11,427 12,940 11,535
30 35 70
0 0 0
0 1 2
— — —
— 4.6 5.1±0.1
Lake
Bare Lily SAV
42° 54.00′ 42° 54.16′ 42° 54.09′
86° 12.51′ 86° 11.98′ 86° 11.99′
640 1,394 1,385
94 70 55
NA NA NA
278 22 399
— — —
4.2±1.1 4.5±1.0 4.5±1.0
Wetland
Bare Lily SAV
42° 53.98′ 42° 53.37′ 42° 53.91′
86° 11.72′ 86° 11.48′ 86° 11.63′
1,660 2,850 2,041
60 75 82
NA NA NA
39 5 24
— — —
4.9±0.7 6.4±1.0 5.2±0.8
Lake
Bare Lily SAV
43° 58.93′ 43° 58.65′ 43° 58.77′
86° 27.83′ 86° 27.04′ 86° 27.43′
973 2,329 1,590
80 60 98
NA NA NA
23 0 9
— — —
4.6±1.3 — 6.3±0.8
Wetland
Bare Lily SAV
43° 58.88′ 43° 58.89′ 43° 58.90′
86° 26.01′ 86° 26.22′ 86° 26.16′
3,879 3,686 3,390
50 45 60
NA NA NA
4 2 1
— — —
6.6±1.1 4.9±0.1 5.2
System Macrohab. Pentwater Lake
Wetland Kalamazoo
Muskegon
White
Pigeon
Lincoln
Distribution of Round Gobies in Coastal Areas of Lake Michigan
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Uzarski et al. 2005). Small fyke nets (mouth: 0.5 × 1 m) were fished at water depths of 0.2 to 0.5 m, whereas large fyke nets (mouth: 1 × 1 m) were fished at water depths of 0.5 to 1.0 m. Water depth dictated which size fyke net we used because the only difference between large and small nets was the height. Leads extended 7.3 m from the middle of the mouth, and wings extended 1.8 m from both sides of the mouth (45° angle to the lead). The mesh size was 4.8 mm (bar measurement). Two of the three nets fished in each microhabitat were set as a pair with openings facing one another and leads positioned end to end within the microhabitat of interest (Brazner 1997, Brazner et al. 1998). A third net was set nearby (approximately 25–75 m away) with the lead extending into the microhabitat (Uzarski et al. 2005). Nets were hauled after an approximate 24-hour soak time and round gobies were measured (standard length) and enumerated in the field. After measurement and enumeration, round gobies were euthanized and disposed of. All other fish were released alive. We report catch as the total number of round gobies captured in the three nets fished at each microhabitat. Statistical Analyses Data from 2004 were analyzed separately from 2005. A three-way split-plot analysis of variance (ANOVA) was used to test whether the catch of round gobies differed among macrohabitats (lake, wetland), microhabitats (lily, SAV, bare), and their interaction (Montgomery 1991). System served as a blocking variable, macrohabitat was the whole plot, and microhabitat was the subplot. When significant effects were found, Tukey’s HSD tests were conducted post-hoc to identify differences. Round goby catch was natural log-transformed [ln(n+1)] prior to analysis to homogenize variance based on residual plots. Differences in round goby standard length (each observation was a mean of all round gobies caught at a microhabitat) between macrohabitats were analyzed using paired t-tests (lake vs. wetland sites paired by microhabitat type). We used paired t-tests for the length comparisons because round gobies were not collected at a number of microhabitats, which prevented us from using a split-plot ANOVA approach. We used pair-wise deletion for cases when at least one of the microhabitats in a pair did not have round gobies. We ran split-plot ANOVA, Tukey’s HSD, and paired t-tests in SAS version 8.0 (Cary, North Carolina). To investigate the relationship between round goby catch and dis-
FIG. 2. Round goby catch (±1 standard error) showing differences due to macrohabitat (lake vs. wetland) in four Lake Michigan drowned river mouth systems sampled in 2004 and six systems sampled in 2005. tance from Lake Michigan, we used Pearson correlations. Both variables were natural log-transformed [ln(n+1) for catch data]. RESULTS Round Goby Distributions Round gobies were caught at 67% of the sites in 2004 and 81% in 2005 (Table 1). The largest collections of round gobies were made in SAV microhabitats of lakes in both years (Fig. 2). Catch of round
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Cooper et al. TABLE 2. Split-plot analysis of variance results for the effects of macrohabitat (lake, wetland), microhabitat (bare substrate, lily, submersed aquatic vegetation), and the interaction of macrohabitat and microhabitat on round goby catch in Lake Michigan drowned river mouth systems. System (four in 2004, six in 2005) was the blocking variable. Source of variation
df
MS
System Macrohabitat Whole plot errora Microhabitat Microhabitat x Macrohabitat Subplot errorb
3 1 3 2 2 12
5.96 3.55 0.59 2.48 0.72 1.40
F
P
5.97
0.092
1.78 0.52
0.211 0.610
2004
2005 System 5 8.01 Macrohabitat 1 9.21 5.88 0.060 Whole plot errora 5 1.57 Microhabitat 2 1.44 1.36 0.279 Microhabitat x Macrohabitat 2 6.14 5.82 0.010 Subplot errorb 20 1.05 a The whole plot error term was the system x macrohabitat effect b The subplot error term was the system x macrohabitat x microhabitat effect
gobies was greatest in Muskegon Lake in 2004 and Pigeon Lake in 2005 (Table 1). We captured the fewest round gobies in White Lake in both years (Table 1). Round goby catch tended to be greater in lake macrohabitats than wetland macrohabitats in both years (Fig. 2). The effect of macrohabitat (lake vs. wetland) was marginally significant in 2004 and 2005 (Table 2). The interaction between macrohabitat and microhabitat was significant in 2005 (Table 2). Catch of round gobies was significantly greater at lake-SAV sites than lake-lily, wetland-bare, and wetland-SAV sites (Table 3). The effect of microhabitat alone was not significant in either year (Table 2). Excluding White Lake and wetland from our analysis, because few round gobies were caught
in this system (Table 1), weakened the effect of macrohabitat in 2004 and strengthened the effect of macrohabitat in 2005. Macrohabitat (F1,2 = 3.20, p = 0.215), microhabitat (F 2,8 = 1.81, p = 0.224), and the interaction (F2,8 = 0.53, p = 0.610) were not significant in 2004, whereas microhabitat (F 2,16 = 1.20, p = 0.328) was not significant and macrohabitat (F 1,4 = 8.44, p = 0.044) and the interaction (F2,16 = 6.12, p = 0.011) were significant in 2005 when White Lake and wetland were excluded. The majority of round gobies that we caught were smaller than 7 cm standard length (Table 1, Fig. 3). The dominant size class in both macrohabitats during both years was 3-7 cm (Fig. 3). No reproductive male round gobies, with their characteristic dark color (Jude 1997), were ob-
TABLE 3. Tukey’s HSD p-values for pair-wise comparisons of round goby catch per net-night per microhabitat in 2005. Catch data were natural log-transformed [ln(n+1)]. Lake SAV Lake lily Lake bare Wetland SAV Wetland lily
Lake lily 0.022
Lake bare 0.760 0.282
Wetland SAV 0.008 0.998 0.134
Wetland lily 0.117 0.959 0.743 0.800
Wetland bare 0.035 0.999 0.392 0.984 0.990
Distribution of Round Gobies in Coastal Areas of Lake Michigan
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FIG. 3. Length frequency distributions for round gobies caught in Lake Michigan drowned river mouth lakes and wetlands in 2004 and 2005. served in our catch. Mean lengths of round gobies (Table 1) did not differ significantly between macrohabitats in either year (2004: t = 0.23, d.f. = 4, p = 0.84; 2005: t = 0.54, d.f. = 10, p = 0.60). Round goby catch tended to decrease the farther a site was located from Lake Michigan. Correlations between round goby catch and distance from Lake Michigan were negative in both years but only significant in 2005, which may be due in part to the lower sample size in 2004 (i.e., four systems were sampled in 2004 and six in 2005). In 2004, the correlations were not significant for lake sites (r = –0.161, d.f. = 11, p = 0.618), wetland sites (r = –0.093, d.f. = 11, p = 0.775), or all sites (r = –0.273, d.f. = 23, p = 0.197). In 2005, significant negative correlations were found for lake sites (r = –0.570, d.f. = 17, p = 0.013), wetland sites
(r = –0.527, d.f. = 17, p = 0.025), and all sites (r = –0.599, d.f. = 35, p = 0.003). DISCUSSION We caught round gobies in lake and wetland habitats of all six study systems, indicating that this nonindigenous fish has successfully colonized coastal habitats in this portion of Lake Michigan. Lake macrohabitats tended to have more round gobies than wetland macrohabitats in both years though the effect was stronger in 2005. Excluding White Lake and wetland from habitat comparisons weakened the effect of macrohabitat in 2004 and strengthened this effect in 2005, highlighting the potential for temporal variation in habitat selection by round gobies. However, this difference between years was likely a consequence of reduced statisti-
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cal power (Lenth 2001) rather than an ecologically meaningful difference between years because more round gobies were caught in White Lake than White wetland in 2004 while the opposite trend was observed in 2005 (Table 1). Our hypothesis was based on the fact that Uzarski et al. (2005) captured few round gobies in coastal wetlands, yet round gobies were thought to inhabit adjacent habitats. Therefore, if we exclude systems with low numbers of round gobies, then we are biasing our analysis toward finding an effect. For example, if all the systems had few round gobies, then this observation would not support our hypothesis and, therefore, has bearing on whether coastal wetlands are resistant to invasion. Nevertheless, if our focus had been purely on habitat selection by round gobies, then excluding the White system is justified given that few round gobies were captured in that system. The apparent preference for lake habitats by round gobies supported our working hypothesis that coastal wetlands are resistant to invasion by round gobies. However, this trend was not consistent across the three microhabitat types. Catch of round gobies at lake-SAV sites was greater than two of the three wetland microhabitats. This suggests that while coastal wetlands may provide refuge from round gobies, the effect could be more pronounced for native species that utilize SAV microhabitats. Also, lily appeared to be the least preferred of the three lake microhabitats, which further supports our hypothesis that wetlands are resistant to invasion by round gobies because the lily microhabitat in lakes was more similar to a wetland than the other lake microhabitats. Plausible explanations for the difference in round goby catch between drowned river mouth lakes and wetlands may be related to time since invasion and availability of hard benthic substrate. First, invading round gobies most likely entered drowned river mouth systems either from Lake Michigan or by secondary dispersal via ship ballast water exchange (Mills et al. 1993, Clapp et al. 2001). The duration necessary for round goby populations to colonize upstream wetlands is not clear. However, distances between adjacent lake and wetland macrohabitats in our study were typically less than distances between drowned river mouth systems along the eastern shore of Lake Michigan (Fig. 1). Given that round gobies spread naturally to drowned river mouth systems that do not have shipping traffic (Clapp et al. 2001), it seems unlikely that the difference in round goby catch between macrohabitats was merely a result of insufficient time for round
gobies to invade the upstream wetlands. Secondly, hard substrates were rarely observed in the wetlands compared to the lakes where seawalls, concrete riprap, docks, and pilings were common. We did not sample a hard-substrate microhabitat because of their low occurrence in wetlands. We preferred a conservative approach where we maintained consistent microhabitats between lakes and wetlands to ensure that the macrohabitat factor was not confounded by sampling different microhabitats in each macrohabitat. Since round gobies prefer habitats containing cobble, boulders, and/or artificial riprap (Jude and DeBoe 1996, Charlebois et al. 1997, Ray and Corkum 2001, Johnson et al. 2005), differences in substrate may explain the difference in round goby catch between the lakes and wetlands. We predict that including rock and gravel microhabitats in the lakes would have magnified differences in round goby catch between macrohabitats. The majority of round gobies we caught most likely consumed benthic insects and crustaceans because they were less than 7 cm standard length, the size that round gobies begin to include bivalves in their diet (Jude et al. 1995, Ghedotti et al. 1995, Ray and Corkum 1997). Furthermore, in benthic dipnet samples taken in the same microhabitats as this study (2004 only), bivalves (including dreissenids and spaeriid clams) were rare, comprising less than 1% of the benthic macroinvertebrate fauna (unpublished data). This suggests that bivalves are probably not an important food resource for round gobies in the three microhabitats we sampled. Carmen et al. (2005) found that round gobies primarily ate chironomid larvae and pupae, heptageniid nymphs, and Daphnia in a river that did not contain dreissenid mussels, indicating that round goby populations can persist in the absence of dreissenids. Future studies should address the diet of round gobies in coastal habitats with low bivalve densities, such as Great Lakes coastal wetlands, to determine the extent round gobies are consuming non-mussel prey. The negative relationship we found between round goby catch and distance from Lake Michigan may suggest that round gobies are still invading these systems. However, an alternative explanation is that Lake Michigan nearshore habitats (including the pier areas) function as round goby spawning and nursery habitats that are a continual source of round gobies to the drowned river mouth lake/wetland complexes. This explanation seems plausible given that round gobies prefer habitats containing
Distribution of Round Gobies in Coastal Areas of Lake Michigan cobble, boulders, and/or artificial riprap (Jude and DeBoe 1996, Charlebois et al. 1997, Ray and Corkum 2001, Johnson et al. 2005) and most of the channels that connect drowned river mouth lakes to Lake Michigan were lined with boulders and/or riprap in our study systems. Furthermore, Ray and Corkum (2001) found that in the St. Clair RiverLake St. Clair-Detroit River corridor, round gobies tended to be smaller in recently invaded habitats. The round gobies that we caught also tended to be small with the majority being between 2 and 6 cm standard length (Fig. 3). Though we did not determine ages, we speculate that the majority of round gobies we caught were between age 0+ and 2+ based on length-at-age data from other studies in the Great Lakes basin (Phillips et al. 2003, MacInnis and Corkum 2000). This suggests that round gobies in drowned river mouth lakes and wetlands tend to be young immigrants from other habitats. We also found pronounced differences in round goby catch among the six study systems. While this was not a focus of the study, we found that Pigeon Lake had much higher catches of round gobies than any of the other systems. Pigeon Lake’s small size and proximity to Lake Michigan (Fig. 1) likely facilitated movement and spread of round gobies throughout the system. However, explanations for the low catches of round gobies in White Lake and wetland are unknown. Our results are consistent with our working hypothesis that Lake Michigan drowned river mouth wetlands are more resistant to invasion by round gobies than adjacent lake habitats. This contributes to a growing body of evidence suggesting that Great Lakes coastal wetlands are resistant to invasion by certain nonindigenous species. For example, native unionid populations were found to utilize coastal wetlands for refugia from nonindigenous zebra mussels (Nichols and Amberg 1999, Bowers and De Szalaya 2004) and wetland habitats in Lake Superior were found to be resistant to invasion by nonindigenous ruffe (Gymnocephalus cernuus) (Brazner et al. 1998). However, we observed nonindigenous plants (M. spicatum and P. crispus) at our study sites, and common carp (Cyprinus carpio) inhabit many Great Lakes coastal wetlands (Lougheed et al. 1998), indicating that coastal wetlands are not resistant to all nonindigenous species and the potential for coastal wetlands to serve as true refugia for native species is likely species specific. While we generally found fewer round gobies in wetland habitats, the questions remain: 1) will
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round goby densities in Lake Michigan drowned river mouth wetlands increase in future years once adjacent lakes are saturated (assuming the lakes are not currently saturated), 2) do round goby populations in other types of Great Lakes coastal wetland have similar distribution patterns, and 3) are round goby distributions determined by community-level drivers such as predation pressure or prey availability? Numerous studies have identified deleterious effects of the round goby invasion on native species including displacement by aggressive interactions (Dubs and Corkum 1996, Janssen and Jude 2001, Balshine et al. 2005) and predation of eggs and fry (Chotkowski and Marsden 1999, Nichols et al. 2003, Steinhart et al. 2004). Therefore, restoration and protection of Great Lakes coastal wetlands may help control the spread of round gobies as well as provide critical habitat for native fishes (Jude and Pappas 1992, Uzarski et al. 2005), birds (Prince et al. 1992), reptiles, and amphibians (Weeber and Vallianatos 2000). ACKNOWLEDGMENTS We thank the Great Lakes Coastal Program of the U.S. Fish and Wildlife Service, especially Ted Koehler, as well as the Michigan Department of Environmental Quality, especially Peg Bostwick and Dave Kenaga, for funding this research. We thank Matthew Breen, Adam Bosch, Aaron Parker, Keto Gyekis, Michael Shoemaker, Pam Parker, Nicholas Fiore, Eric Nemeth, Dana VanHaitsma, Melissa Reneski, Nathan Coady, Kenneth Davenport, Rebecca E. Kolar, Jamie M. Zbytowski, and Mary Ogdahl for assistance in the field and laboratory. Comments by Drs. J. Brazner, J. Janssen, T. Phillips, and an anonymous reviewer contributed substantially to an earlier version of this manuscript. REFERENCES Albert, D.A., Wilcox, D.A., Ingram, J.W., and Thompson, T.A. 2005. Hydrogeomorphic classification for Great Lakes coastal wetlands. J. Great Lakes Res. 31 (Supplement 1):126–146. Balshine, S., Verma, A., Chant, V., and Theysmeyer, T. 2005. Competitive interactions between round gobies and logperch. J. Great Lakes Res. 31:68–77. Bowers, R., and De Szalaya, F.A. 2004. Effects of hydrology on unionids (Unionidae) and zebra mussels (Dreissenidae) in a Lake Erie coastal wetland. Am. Mid. Nat. 151:286–300. Brazner, J.C. 1997. Regional, habitat, and human devel-
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