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Density and Distribution of Amphipods in Oneida Lake, New York, after the Introduction of the Exotic Amphipod Echinogammarus ischnus
John E. Cooper, Elin Wallquist , Kristen T. Holeck, Catharine E. Hoffman, Edward L. Mills, and Christine M. Mayer

Northeastern Naturalist, Volume 19, Issue 2 (2012): 249–266

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2012 NORTHEASTERN NATURALIST 19(2):249–266 Density and Distribution of Amphipods in Oneida Lake, New York, after the Introduction of the Exotic Amphipod Echinogammarus ischnus John E. Cooper1,*, Elin Wallquist2, Kristen T. Holeck3, Catharine E. Hoffman3, Edward L. Mills3, and Christine M. Mayer4 Abstract - The exotic amphipod Echinogammarus ischnus, first reported in North America from western Lake Erie in 1995, was recorded in Oneida Lake, NY in 2001. Some North American studies have suggested that E. ischnus was replacing native amphipods, but other studies found no evidence for this. We sampled amphipods at six depths (<0.2, 0.6, 1.2, 1.8, 3.0, and >3.8 m) along six transects in Oneida Lake to quantify variation in densities of amphipod species as a function of depth, substrate (cobble with Dreissena and with or without macroalgae, sand with or without Dreissena, and macroalgae or submersed vascular plants) and density of Dreissena, and compared the present amphipod density to the historical record. Four species of amphipods, Gammarus fasciatus, Hyalella azteca, E. ischnus, and Crangonyx sp., were collected from Oneida Lake. Gammarus fasciatus was 9 to 90 times more abundant (mean = 0.09 individuals/ cm2) than other amphipod species and was collected on all substrates and at all depths, as was H. azteca. Statistical comparisons were made with non-parametric tests between mean ranks of density of amphipods and Dreissena and the other variables. Mean ranks of density of G. fasciatus were correlated with depth (Spearman rank = 0.28, P < 0.0001), but mean ranks of density of H. azteca were not, and neither species was correlated with mean ranks of density of Dreissena. Mean ranks of density of G. fasciatus were greater on sand with or without macroalgae or submersed vascular plants (SVP) or Dreissena than on cobble with macroalgae and Dreissena (H = 28.2, P < 0.0001). Mean ranks of density of H. azteca were greater on sand with SVP, with or without Dreissena, than on sand with Dreissena and without SVP (H = 21.8, P = 0.0013). Echinogammarus ischnus was collected only in water less than 1.8 m depth and always with Dreissena. Mean ranks of density of E. ischnus were correlated with depth (Spearman rank = -0.29, P < 0.0001) and with Dreissena mean ranks of density (Spearman rank = 0.14, P = 0.01). Mean ranks of density of E. ischnus was greater on cobble with Dreissena than on sand with Dreissena regardless of the presence or absence of macroalgae or SVP (H = 35.4, P < 0.0001). Although E. ischnus is established in the near-shore zone of Oneida Lake, we found no evidence that it will replace the native amphipods G. fasciatus and H. azteca. Introduction The exotic amphipod Echinogammarus ischnus Stebbing, native to the Ponto- Caspian region, was introduced into the North American Great Lakes through 1Cooper Environmental Research, 1444 County Route 23, Constantia, NY 13044. 2Faculty of Social and Life Sciences, Karlstad University, 651 88 Karlstad, Sweden. 3Cornell Biological Field Station, 900 Shackelton Point Road, Bridgeport, NY 13030. 4University of Toledo, Lake Erie Center, 6200 Bayshore Road, Oregon, OH 43618. *Corresponding author - cooperesearch@hughes.net. 250 Northeastern Naturalist Vol. 19, No. 2 ballast-water releases of commercial ships (Holeck et al. 2004) in the 1990s, and colonized the lower Great Lakes and the upper St. Lawrence River within three years (Dermott et al. 1998, Nalepa et al. 2001, Witt et al. 1997). Establishment of exotic species can have profound effects on the preexisting biological communities (Bailey et al. 2006, Mills et al. 1993, Pimentel 2005). For example, predatory behavior of the exotic amphipod Dikerogammarus villosus Sovinskij in Europe was implicated in the rapid decline of macroinvertebrate abundance (Krisp and Maier 2005), as well as the replacement of the native amphipod Gammarus duebeni Lilljeborg and an exotic North American amphipod Gammarus tigrinus Sexton (Dick and Platvoet 2000). Interspecific competition and predation have been hypothesized as causes for the observed displacement of Gammarus fasciatus Say (native to North American Great Lakes) by E. ischnus from hard substrates in the Great Lakes (Dermott et al. 1998, Van Overdijk et al. 2003). Several studies demonstrated that intensity of predator-prey interactions between native and exotic amphipods were dependant on specific conductivity (Dick and Platvoet 1996; Kestrup and Ricciardi 2009, 2010, 2011). Echinogammarus ischnus has been associated most often with hard substrate (cobble, concrete), Dreissena (Kang et al. 2007, Kohn and Waterstraat 1990), and shallow water (0.2–3.6 m; Kohn and Waterstraat 1990, Van Overdijk et al. 2003), but it has been collected at depths from 5 to 7 m in Lake Ontario (Haynes et al. 2005), and from 16 m to 94 m in Lake Michigan (Nalepa et al. 2001). Kang et al. (2007) found E. ischnus to be more abundant in high-energy shorelines than in the slower-moving water of Great Lakes wetlands. In the upper St. Lawrence River, Palmer and Ricciardi (2004) found positive correlations between E. ischnus, current velocity, and abundance of gravel-sized substrate. Gammarus fasciatus, more of a generalist in habitat preferences, has previously been associated with algae and rooted vegetation in the slow-moving water of lakes and large rivers from shoreline to 12 m depth (Beckett and Miller 1982, Bousfield 1958, Clemens 1950). In Lake Erie, G. fasciatus showed no preference for Dreissena over Cladophora but did prefer Cladophora over bare rock (Van Overdijk et al. 2003); G. fasciatus abundance increased in the Great Lakes after the introduction of Dreissena, which it utilized as habitat (Ricciardi et al. 1997). Abundance of G. fasciatus relative to E. ischnus in the St. Lawrence River has varied temporally and spatially: E. ischnus was not present at some sampling sites where it had been found previously (Palmer and Ricciardi 2004), and increased abundance of E. ischnus in one year was followed by a decline in abundance in the second year of an experimental study (Palmer and Ricciardi 2005). The authors noted that these results were in contrast to those found in the Great Lakes, where E. ischnus dominance progressed over time at several sites. Gammarus fasciatus is a major food resource for Perca flavescens (Mitchill) (Yellow Perch) (Keast 1977, Pothoven et al. 2000), which, in turn, is a major forage species for Sander vitreus (Mitchill) (Walleye) in Oneida Lake (Forney 1974, VanDeValk et al. 2005). If G. fasciatus is replaced by E. ischnus, 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 251 changes in abundance of near-shore amphipods might alter foraging success by young-of-the-year Yellow Perch. It is less likely that adult Yellow Perch would be affected since a greater proportion of young-of-the-year Yellow Perch occur at near-shore areas. The native amphipod Hyalella azteca de Saussure, considered by Bousfield (1958) to be the most widely distributed North American freshwater amphipod, has been associated with fine sand substrate and various forms of aquatic vegetation (Baker 1918, Beatty and Hooper 1958, Edwards and Cowell 1992). Hyalella azteca has been recorded at 13 m water depth (Dionne et al. 2011) but more often from water <5 m in depth (Hargrave 1970, Wood 1952). Four native amphipod species were reported from Oneida Lake in 1916 (Baker 1918): Hyalella knickerbockeri (Bate) (= Hyalella azteca), Gammarus fasciatus, Eucrangonyx gracilis (= Crangonyx gracilis Smith), and G. limnaeus S.I. Smith. The most abundant species was H. azteca, followed distantly by G. fasciatus, and both species were associated with a variety of substrates ranging from mud to cobble at depths of 0.5 to 4.5 m water depth. Crangonyx gracilis and G. limnaeus were relatively rare and were recorded from depths <1.2 m and 3 m, respectively. Our study site, Oneida Lake, forms part of the Erie Barge Canal (EBC) that links the Hudson River, and the Finger Lakes in central NY, with lakes Ontario and Erie (Fig. 1). The EBC has facilitated the introduction of more than 30 exotic species into Oneida Lake since the early 1900s (K. Holeck, Cornell University, Bridgeport, NY, pers. comm.). Two of the exotic species in Oneida Lake, Dreissena polymorpha Pallas (Zebra Mussel) and D. bugensis Andrusov (Quagga Mussel), introduced in 1991 and 2001, respectively, were considered as a suitable Figure 1. Location of Oneida Lake (a) and its position relative to the Erie Barge Canal system linking the Hudson River to lakes Ontario and Erie; and (b) transects (shown as lines) sampled for amphipods and Dreissena. 252 Northeastern Naturalist Vol. 19, No. 2 habitat for E. ischnus colonization due to the established association of Dreissena and this exotic amphipod (Kohn and Waterstraat 1990). Echinogammarus ischnus was first recorded in Oneida Lake in 2001 (at <1 m depth; C.M. Mayer, University of Toledo, Toledo, OH, unpubl. data). The objectives of this study were 1) to determine the relative density of native and exotic amphipods in relation to depth, substrate, and Dreissena in Oneida Lake and 2) to compare the present amphipod density to that in the historical record. Methods Study lake characterization Oneida Lake (43°10′N, 76°00′W) is a large, shallow, mesotrophic lake (surface area = 207 km2; mean depth = 6.8 m; Fig. 1), and is located northeast of Syracuse, NY. The shallow water substrate is predominately cobble or sand, becoming primarily sand and silt in deeper water, and there are extensive cobble shoals offshore. The two species of Dreissena have formed aggregated colonies on cobble substrates, and filamentous benthic macroalgae cover many cobble substrates and the submersed vascular plants (SVP) in deeper water. The New York State Canal Corporation lowers the lake water level by 1 m in winter to accommodate spring snowmelt. Amphipod sampling and identification Six permanent transects were established (Fig. 1); we expected that five of these represented suitable habitat for E. ischnus (presence of cobble and Dreissena) and that one transect (Oneida Bay Marina) would not (fine sand, no Dreissena in water <1.8 m depth). Oneida Bay Marina was included because the same area had been sampled in the past (Baker 1918, Clady 1975, Mayer et al. 2002), which would enable comparisons to the present study. Paired quantitative samples (each sample was either a single cobble-sized rock or a sand grab, 12 samples per transect) were taken at each of six depths starting at the shoreline (<0.2 m, 0.6 m, 1.2 m, 1.8 m, 3.0 m, and >3.8 m) along each transect (Table 1). Samples were taken within a 15-m diameter circle at the appropriate depth. All transects were set perpendicular to shore, with the length of each transect determined by the distance required to reach >3.8 m depth. Lengths of transects were: Short Point, 1250 m; Oneida Bay Marina, 800 m; Jewell, 600 m; and 400 m each for Constantia, Dutchman Island, and Shackelton Point. The end point of each transect was referenced to latitude and longitude using a handheld global positioning device. Conductivity, water temperature, and dissolved oxygen were measured at the water surface and bottom at the deepest point of each transect; the latter two parameters were used to calculate percent oxygen saturation. Conductivity was considered to be intermediate between 121–215 μS/cm and high at >276 μS/cm (Kestrup and Ricciardi 2010). Conductivity values taken in 2005 and 2006 were compared to data from a long-term data set (1975 to 2006) measured at five open-water 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 253 Table 1. Substrate characteristics at six sampling depths along six transects in Oneida Lake. Echinogammarus ischnus was collected on the substrates shown in bold. SVP = submersed vascular plants. Transects Depth (m) Short Point Oneida Bay Marina Dutchman Island Shackelton Point Constantia Jewell < 0.2 Cobble Fine sand Cobble Cobble Cobble Cobble Dreissena No Dreissena Dreissena Dreissena Dreissena Dreissena No macroalgae SVP Macroalgae Macroalgae Macroalgae No macroalgae 0.6 Cobble Fine sand Fine sand Cobble Cobble Cobble Dreissena No Dreissena Dreissena Dreissena Dreissena Dreissena No macroalgae SVP Macroalgae Macroalgae Macroalgae No macroalgae 1.2 Cobble Fine sand Fine sand Coarse sand Fine sand Coarse sand Dreissena No Dreissena Dreissena Dreissena Dreissena Dreissena No macroalgae SVP SVP Macroalgae SVP No vegetation 1.8 Cobble Fine sand Fine sand Coarse sand Fine sand Coarse sand Dreissena Dreissena Dreissena Dreissena Dreissena Dreissena No macroalgae SVP SVP SVP SVP No vegetation 3 Fine sand Fine sand Fine sand Fine sand Fine sand Fine sand Dreissena Dreissena Dreissena Dreissena Dreissena Dreissena SVP SVP SVP SVP SVP No vegetation > 3.8 Fine sand Fine sand Fine sand Fine sand Fine sand Fine sand Dreissena No Dreissena No Dreissena No Dreissena Dreissena Dreissena No vegetation No vegetation No vegetation No vegetation No vegetation No vegetation 254 Northeastern Naturalist Vol. 19, No. 2 stations (Cornell Biological Field Station). Calcium values were obtained from several sources: from 1960 to 1990 (US Geological Survey, http://waterdata. usgs.gov/nwis/qwdata), for 2001 (Limburg and Siegel 2006), and recent determinations (2011) by the first author. Transects at Short Point, Oneida Bay Marina, and Dutchman Island were sampled in August 2005. Shackelton Point, Constantia, and Jewell were sampled in October 2005, and all transects were sampled in May, June, and July 2006. Single rocks were retrieved in cobble-dominated areas by hand or with an Ekman dredge and placed quickly into a bucket after being transported to the water surface. Rocks were then scraped to remove amphipods and Dreissena. Sand samples were sampled by dredge. Scraped material from rocks and entire sand samples were washed through a 500–μm screen, and the collected material was preserved in 70% ethanol. Colonizable surface area of collected rocks was estimated by measuring length, width, and height (mm) to the point of burial, and sand sample area was quantified as the flat benthic area of the dredge (225 cm2/sample). Dreissena density in 2005 was estimated from colonizable rock surface area, and, for sand samples, from the area sampled by the dredge. Abundance of SVP, macroalgae, and Dreissena were not quantified in 2006; however, their presence or absence from a plot was recorded. Gammarus fasciatus and Echinogammarus ischnus were identified using morphological characteristics (Holsinger 1976, Witt et al. 1997) of uropods and antennae. Hyalella azteca was identified by gnathopod morphology and the presence of dorsal teeth (Fig. 2): dorsal teeth are not present in G. fasciatus or E. ischnus. The characteristics of the base of pereopod 7 and the basal segments of the second antennae in the male were used to identify Crangonyx sp. (Holsinger 1976, Zhang and Holsinger 2003). The presence of red-pigmented antennae (Dermott et al. 1998) was not used as an identifying character for E. ischnus as Figure 2. Hyalella azteca female (left) and male (right) showing dorsal teeth (paired arrows) and the large gnathopods on the male (concave arrow) used as identifying characteristics. Scale bar = 0.5 mm. 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 255 many Oneida Lake G. fasciatus also have red pigment on their antennae, which remains visible for several months after collection. Statistical analyses Mean amphipod species densities were compared in relation to transect, water depth, and substrate using the non-parametric Kruskal-Wallis (KW; SAS 2001) test on non-transformed data. The distribution of the test statistic, H, approximates that of the chi-square distribution and compares the ranks of the measured variable. The KW test does not require assumptions of normality of data distribution. KW tests were used to compare the means of the ranks of density of each of three amphipod species in relation to transect and depth (α = 0.008 after Bonferroni correction for multiple comparisons), and to compare means of ranks of density of each of three amphipod species to seven substrates (Table 1): cobble with or without macroalgae (cobble always had Dreissena), sand with macroalgae and Dreissena, sand with SVP (with or without Dreissena), and sand without vegetation (with or without Dreissena). The cumulative distributions of mean density by depth for the three more abundant amphipod species were compared using the Kolmogorov-Smirnov test. Calculated values for oxygen saturation were compared to mean ranks of amphipod density at six depths for July (time of lowest oxygen saturation) using KW to determine if there was any effect of low oxygen saturation on density; a significantly lower mean rank at >3.8 m depth compared to other depths would indicate an effect. Density of Dreissena was compared across transects and depths using KW. Mean ranks (based on density) of the three amphipod species were compared to the mean ranks of conductivity, depth, and density of Dreissena using Spearman rank correlation. An additional amphipod species, Crangonyx, was excluded from statistical analysis because only one individual was recorded. Results We collected four species of amphipods in Oneida Lake. Gammarus fasciatus was the most abundant amphipod species with a mean density of 0.09 individuals/cm2 (SE = 0.01) and accounted for 83.1% of all amphipods collected. Hyalella azteca was second in abundance with a mean density of 0.01 individuals/ cm2 (SE = 0.004) and accounted for 15.1% of all amphipods collected, while E. ischnus was collected at low density (0.001 individuals/cm2, SE = 0.0007; 1.8% of all amphipods collected). One Crangonyx sp. was collected at Short Point. Dreissena was present at all sampling locations except for depths <1.8 m at Oneida Bay Marina and >3.8 m depth at Dutchman Island, Oneida Bay Marina, and Shackelton Point (Table 1) and had a mean density of 0.85 individuals/cm2 (SE = 0.28). Percent dissolved oxygen saturation was lowest in July (27%) at depths > 3.8 m but was >50% at all depths in other sampling months. The low saturation did not result in lower mean ranks of density; G. fasciatus mean ranks were significantly 256 Northeastern Naturalist Vol. 19, No. 2 greater (H = 24.4, P < 0.0002) at depths between 1.8 and >3.8 m than at shallower depths, and there was no apparent effect on H. azteca abundance as there was no significant difference (H = 13.9, P = 0.02) in mean ranks by depth. Conductivity measured in this study ranged from intermediate to high (220–400 μS/cm, mean = 327 ± 32), and was 40% lower at Constantia (220 μS/cm) and Jewell (230 μS/ cm) than at the other transects. We found no significant correlation between the mean ranks of the three amphipod species and conductivity (Spearman rank = 0.38, P = 0.6). Our conductivity values were similar to those in the long-term data set measured at the five open-water stations. Amphipod density as a function of transect and depth There was considerable variation in amphipod species density by transect. Gammarus fasciatus was collected at all transects, but its density was nearly twice as great at Short Point than at Jewell, which had the second greatest density, and more than three times as great as at Constantia, where density was least. Mean ranks of density of G. fasciatus were significantly greater at Short Point than at Constantia (H = 17.9, P = 0.003) but not statistically different from other transects. Density of H. azteca was three times greater at Oneida Bay Marina than at Dutchman Island, 60 times greater than at Shackelton Point, and mean ranks of density were significantly greater at Dutchman Island, Oneida Bay Marina, and Short Point than at Shackelton Point, Constantia, or Jewell (H = 48.5, P < 0.0001). Echinogammarus ischnus was collected at four of the six transects, but two transects, Jewell and Constantia, accounted for nearly 80% of all E. ischnus, and mean ranks of density at Jewell and Constantia were significantly greater than at Shackelton Point and Short Point (H = 20.2, P = 0.001). Dreissena collected at Short Point, Jewell, and Constantia accounted for nearly 80% of all Dreissena, and mean ranks were significantly greater at Short Point than at other transects. Mean ranks of density at Jewell and Constantia were significantly greater than at Dutchman Island, Oneida Bay Marina, and Shackelton Point (H = 108.8, P < 0.0001). Gammarus fasciatus was collected at all depths, as was H. azteca, while E. ischnus was collected only at depths 1.8 m or less (Fig. 3), primarily at <0.2 m and 0.6 m (73.1% and 24.6% of all E. ischnus). Each amphipod species showed a different cumulative distribution in density by depth. Gammarus fasciatus density was more evenly distributed over depth (Fig. 3) than was H. azteca, from which it was significantly different (KS = 0.26, D = 0.52, P < 0.0001). The distribution of E. ischnus was more limited and was significantly different from that of the other species (G. fasciatus: KS =0.41, D = 0.83, P < 0.0001; H. azteca: KS = 0.19, D = 0.39, P < 0.0001). Mean ranks of G. fasciatus density were significantly less at <0.2 m depth (H = 31.0, P < 0.0001) than at other depths, while there was no signifi cant difference in mean ranks of H. azteca density by depth (H = 10.7, P = 0.06). Echinogammarus ischnus mean ranks of density were greater at <0.2 and 0.6 m than at 1.8 m and 3 m depth (H = 30.9, P < 0.0001). Dreissena was collected at all depths (Fig. 4) but not at all transect–depth combinations (Table 1). Mean ranks of Dreissena density were not significantly different by depth (H = 13.3, P = 0.02, 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 257 critical α = 0.008). There was a significant correlation between Dreissena mean ranks of density and E. ischnus mean ranks of density (Spearman rank = 0.14, P = 0.01), but there was no significant correlation (P > 0.4) between Dreissena mean ranks and the mean ranks of G. fasciatus or H. azteca density. Amphipod density as a function of substrate More than half (58.9%) of all G. fasciatus collected occurred on sand substrates, and the mean ranks of density for G. fasciatus were significantly greater Figure 3. Mean density (individuals/cm2, bars = 1 SE) by depth of three amphipod species collected (all transects combined) in Oneida Lake in 2005 and 2006. Figure 4. Mean density (individuals/cm2, bars = 1 SE) by depth of Dreissena collected in 2005 (all transects combined). 258 Northeastern Naturalist Vol. 19, No. 2 (H = 28.2, P < 0.0001) on sand substrates (with or without SVP or Dreissena) than on cobble with macroalgae and Dreissena (Tables 2, 3). Nearly 87% of H. azteca were collected from sand substrates, with 40.9% coming from sand substrate with SVP in the absence of Dreissena. Mean ranks of density of H. azteca were significantly greater (H = 21.8, P = 0.001) on sand substrate with SVP (with or without Dreissena) than on sand substrate without vegetation but with Dreissena. Mean ranks of H. azteca were significantly correlated with G. fasciatus mean ranks (Spearman rank = 0.33, P < 0.0001). Echinogammarus ischnus was generally less abundant than G. fasciatus or H. azteca and occurred primarily on shallow cobble substrate (97.7% of all E. ischnus) with or without macroalgae, but always with Dreissena. Mean ranks of density were greater (H = 35.4, P < 0.0001) on cobble substrate with macroalgae, and cobble without macroalgae, than on sand substrate with SVP and Dreissena, and sand substrate with Dreissena but without vegetation. Table 3. Amphipod and Dreissena mean density (individuals/cm2 with 1 SE in parentheses) collected on cobble substrate with or without macroalgae. All cobble samples were colonized by Dreissena. Percent refers to the proportion of the total collected of each species. Cobble / Dreissena / macroalgae Cobble/ Dreissena / no macroalgae Taxa Mean density (1 SE) % Mean density (1 SE) % Gammarus fasciatus 0.025 (0.005) 6.5 0.143 (0.034) 34.5 Hyalella azteca 0.005 (0.001) 4.2 0.007 (0.003) 9.2 Echinogammarus ischnus 0.005 (0.002) 46.2 0.004 (0.002) 51.5 Dreissena 0.25 (0.04) 5.0 1.79 (0.07) 47.0 Number of samples 40 48 Table 2. Amphipod and Dreissena mean density (individuals/cm2 with 1 SE in parentheses) collected on sand (fine and coarse sand combined) substrate with or without vegetation or Dreissena. Percent refers to the proportion of the total collected of each species. SVP = submersed vascular plants. Sand / Sand / Sand / Sand / Sand / Dreissena / Dreissena / no Dreissena / Dreissena / no Dreissena / macroalgae no vegetation no vegetation SVP SVP Density Density Density Density Density Taxa (1 SE) % (1 SE) % (1 SE) % (1 SE) % (1 SE) % Gammarus 0.153 7.1 0.102 14.9 0.070 5.3 0.098 26.1 0.076 5.5 fasciatus (0.086) (0.025) (0.023) (0.020) (0.017) Hyalella 0.004 4.5 0.007 5.6 0.014 5.7 0.020 29.8 0.10 40.9 azteca (0.002) (0.004) (0.007) (0.007) (0.009) Echinogammarus 0 0.0 0.0005 0.6 0 0.0 0.0005 1.7 ischnus (0.00005) (0.00009) Dreissena 0.02 0.6 0.23 13.6 0 0.0 0.99 33.8 (0.01) (0.04) (0.13) Number of samples 16 48 24 88 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 259 Dreissena occurred in 83% of all possible samples (Table 1), and density on cobble substrate without macroalgae was nearly double the density occurring on sand with SVP, the two substrates with greater density (Tables 2, 3). Mean ranks of density were greater on cobble without macroalgae than on sand with SVP, cobble with macroalgae, sand with macroalgae, or sand without vegetation (H = 100.6, P < 0.0001). Discussion Gammarus fasciatus was the most abundant amphipod species in Oneida Lake, with a mean density nine times greater than H. azteca, and 90 times greater than the exotic E. ischnus. Significant differences in mean ranks of density among transects could be due to effects of relative wave energy, substrate, depth, and conductivity. Gammarus fasciatus had greater density at Short Point, Dutchman Island, and Oneida Bay Marina, where wave energy would be relatively low; these transects have less fetch from the prevailing westerly winds than the other transects. Kang et al. (2007) did not find G. fasciatus to be abundant in high-energy habitats in the Great Lakes. Gammarus fasciatus density in Oneida Lake was also less in the most shallow areas (<0.2 m) of each transect, perhaps as a result of amphipods avoiding the higher-energy shoreline. We did not find a significant correlation between conductivity and mean ranks of density for G. fasciatus in Oneida Lake, perhaps because abundance would only be affected by low conductivity and not by the intermediate or high conductivity levels we measured. Kestrup and Ricciardi (2010) reported that G. fasciatus was more abundant at intermediate and high conductivity than low conductivity in the upper St. Lawrence River at 0.5 –1 m depth. Gammarus fasciatus was collected at similar depths in Oneida Lake to those in western Lake Erie (up to 3.6 m; Van Overdijk et al. 2003). The reported preference by G. fasciatus for macrophytes rather than Dreissena (Gonzalez and Burkart 2004) was not evident in Oneida Lake, where more G. fasciatus was collected on substrates colonized by Dreissena than on substrates with only SVP (macrophytes), although the difference was not significant. Hyalella azteca was more abundant over sand substrate than cobble substrate at all transects, and was 5 times more abundant at Oneida Bay Marina than at other transects, similar to the results of Baker (1918). The association of H. azteca with low-energy transects was not as apparent as was found for G. fasciatus, and, although mean density was generally greater at lowenergy transects (with higher conductivity) than at high-energy transects (with intermediate conductivity), we did not find a significant correlation with conductivity. We collected H. azteca at all depths to >3.8 m, as did Baker (1918), in contrast to Limen et al. (2005), who collected H. azteca only in water less than 1 m deep in western Lake Erie. In Oneida Lake, E. ischnus was most abundant in shallow water (0.6 m or less) at two transects, Constantia and Jewell, which had higher wave energy, 260 Northeastern Naturalist Vol. 19, No. 2 cobble substrate colonized by Dreissena, and an intermediate level of conductivity. Our results were similar to the results of Dermott et al (1998; <1 m depth), Kang et al. (2007), and Palmer and Ricciardi (2004), who reported greater E. ischnus abundance in habitats of greater wave energy or current velocity, and Gonzalez and Burkart (2004), who reported that E. ischnus was more abundant in Dreissena colonies than in macrophytes. However, our findings were contrary to that of Kestrup and Ricciardi (2010) from the upper St. Lawrence River, where E. ischnus was rare at intermediate levels of conductivity. Habitats occupied by H. azteca were not considered by Kang et al. (2007) to be suitable for E. ischnus because the species shared fewer habitat requirements, and our results would support this to the extent that H. azteca was more abundant on sand than cobble substrate, and that E. ischnus was associated more with shallow water, whereas H. azteca showed no significant difference in abundance by depth. The lowering of the water level in winter in Oneida Lake would reduce Dreissena density at depths of less than 1 m (Dreissena density was greater at 1.8 and 3 m), and would prevent E. ischnus from utilizing the preferred cobble substrate that predominates at <0.6 m during normal lake-elevation periods. This artificial limitation of cobble-and-Dreissena habitat available to E. ischnus in Oneida Lake could reduce the relative survival of E. ischnus in comparison to G. fasciatus and H. azteca, which can utilize the deeper areas of the lake as well as shallow water. Two environmental factors, calcium and dissolved oxygen saturation, were not limiting to amphipods in Oneida Lake. Calcium values ranged from 18–74 mg/l (mean = 38 ± 0.6) from 1967 to 2011, which are greater than the level implicated in reducing post-molting survival in Gammarus pseudolimnaeus Bousfield (<0.2 mg/l; Zehmer et al. 2002). Adverse effects of low oxygen saturation were determined to be 14% for H. azteca and 3.6% for Gammarus lacustris G.O. Sars (Nebeker et al. 1992); these percentages are much lower than those observed in Oneida Lake. Amphipods also have the option of moving to more favorable areas of the lake. Mean density of G. fasciatus was much lower in Oneida Lake than in Lake Ontario and the Niagara and St. Lawrence rivers (2.1/cm2; Dermott et al. 1998) or Lake Erie (0.4/cm2; Van Overdijk et al. 2003), and less on SVP in Oneida Lake than in Lake Erie (0.5/cm2; Gonzalez and Burkart 2004). Density of G. fasciatus was similar between Oneida Lake and Lake Erie Dreissena beds. Mean density of H. azteca in Oneida Lake was greater than in Lake Erie (0.002/cm2; van Overdijk et al. 2003) but less than that from the Niagara River to the St. Lawrence River (1.8/cm2; Dermott et al. 1998). The mean density of E. ischnus in Oneida Lake was much less than the range reported (0.01–1.09/ cm2) in Dermott et al. (1998), Gonzalez and Burkart (2004), and van Overdijk et al. (2003). Dermott et al. (1998) suggested that E. ischnus had displaced G. fasciatus on shallow rocky substrates colonized by Dreissena within 1 year, based on an 2012 J.E. Cooper, E. Wallquist, K.T. Holeck, C.E. Hoffman, E.L. Mills, and C.M. Mayer 261 inverse relationship in density of the two species. Van Overdijk et al. (2003) also reported an inverse relationship in field surveys where the measured density of E. ischnus was >0.7/cm2, and concluded that this could be a density-dependent threshold. In Oneida Lake, density of E. ischnus was always at least one order of magnitude less than the density-dependent threshold, and there was no evidence that E. ischnus had replaced G. fasciatus, despite having been present for at least five years at the end of our study. Kang et al (2007) did not find evidence that E. ischnus was replacing G. fasciatus in the Great Lakes nor did Palmer and Ricciardi (2004) in the St. Lawrence River, rather that habitat heterogeneity was promoting coexistence by allowing the amphipod species to utilize different physicochemical gradients. Fish predation on amphipods has been suggested as a controlling factor of the amphipod assemblage. Gammarus fasciatus might be less vulnerable to predation as it is less active on a complex benthic surface than is E. ischnus (Palmer and Ricciardi 2005), but activity of G. fasciatus increases as habitat complexity decreases (Mayer et al. 2001); thus, G. fasciatus might be more susceptible on bare sand substrates. Density of G. fasciatus was lower on bare sand substrate in Oneida Lake but not significantly less than on a sand substrate with SVP. The presence of SVP would afford some refuge from predators for G. fasciatus, but perhaps not for E. ischnus because their red coloration would make them more visible to Yellow Perch (Gonzalez and Burkart 2004). Although E. ischnus was more active on Dreissena than G. fasciatus, a laboratory study showed that Yellow Perch consumed more G. fasciatus than E. ischnus on a Dreissena substrate, and more E. ischnus than G. fasciatus on macrophytes (Gonzalez and Burkart 2004). Historical amphipod abundance Hyalella azteca was the most abundant amphipod in the Lower South Bay area of Oneida Lake in 1916 (Baker 1918), comprising 96% of the amphipods collected; G. fasciatus was second in abundance at 3.5%. Lower South Bay (LSB) was represented by the Short Point and Oneida Bay Marina transects in the present study. Gammarus fasciatus accounted for 77.4% of amphipods collected and H. azteca accounted for 13.3%, a reversal from that seen in Baker (1918). Mean density of H. azteca at LSB has declined, while mean density of G. fasciatus has increased (Table 4). The shift to greater abundance of G. fasciatus (as well as total amphipod abundance) was apparent in LSB in 1967 (Clady 1975) and was attributed to increased organic matter inputs to the lake from extensive Table 4. Mean density (individuals/cm2) of Hyalella azteca and Gammarus fasciatus and percent change at two sites in Oneida Lake. Data for 1916 is from Baker (1918). Oneida Bay Marina Short Point Species 1916 2005–2006 % change 1916 2005–2006 % change Hyalella azteca 0.12 0.06 -50 0.08 0.01 -87.5 Gammarus fasciatus 0.002 0.07 +3500 0.02 0.21 +1050 262 Northeastern Naturalist Vol. 19, No. 2 agriculture and home construction. Mayer et al. (2002) replicated the methods of Baker (1918) and reported amphipod abundance similar to that in Clady (1975). Our use of a 0.5-mm screen may have reduced the number of smaller juveniles in our samples (Cooper 1965), and the resulting amphipod density, but our results show the same relative abundance of G. fasciatus as was reported by Clady (1975). The reason for the amphipod density increase was suggested by Mayer et al. (2002) to be due to a precipitous decline in total phosphorus (TP) from 1961 to 1976: the decline in TP resulted in increased water clarity and depth of light penetration that increased benthic algae and amphipod abundance. The introduction of Dreissena into Oneida Lake has increased habitat complexity but has not altered amphipod density as much as light penetration has (Mayer et al. 2002), in contrast to the increase in G. fasciatus following the introduction of Dreissena in the North American Great Lakes and the St. Lawrence River (Palmer and Ricciardi 2005), and the increase in D. villosus in Europe (Gergs and Rothhaupt 2008). Habitat complexity might have been increased to a greater extent in the latter two areas compared to Oneida Lake. Baker (1918) reported four species of amphipods in Oneida Lake: Gammarus fasciatus, G. limnaeus, Eucrangonyx gracilis (= Crangonyx gracilis), and Hyalella knickerbockeri (= Hyalella azteca). The identification of the amphipods in Baker is confounded by the possible representation of an undescribed species (related to E. shoemakeri = Crangonyx shoemakeri Hubricht and Mackin) (Shoemaker Crangonyctid) in the description of E. gracilis, and the identification of G. fasciatus, as described by Weckel (1907), having been based, in part, on specimens of G. limnaeus (Hubricht and Mackin 1940). Gammarus fasciatus has been confused with several amphipod species in earlier studies (Holsinger 1976), and has created uncertainty as to whether its native distribution would include Oneida Lake. Furthermore, Smith (1933) reported that G. fasciatus was present in Cayuga Lake (NY) as well as in several locations in western New York, and noted that stocking of amphipods (including G. fasciatus and G. limnaeus) was a common practice in New York in the early 1900s. Chace et al. (1959) suggested that G. fasciatus may represent an introduced species in the North American Great Lakes but did not elaborate on the evidence. The native distribution of G. fasciatus cannot be determined from the historical records due to this uncertainty of identification, but we are assuming that G. fasciatus was native to Oneida Lake until contrary evidence is forthcoming. Oneida Lake is highly productive with a diverse habitat that favors the native amphipods G. fasciatus and H. azteca, which can utilize all areas of the lake. The distribution of E. ischnus was limited to shallow high-energy sites with intermediate conductivity that were colonized by Dreissena. This combination of habitat characteristics might limit the success of E. ischnus since its abundance is greatest at high conductivity, which was found only at lower-energy sites in Oneida Lake. We did not find any evidence that E. ischnus will replace G. fasciatus or H. azteca. 2012 J.E. Cooper, E. Wallquist, K.T. 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