Additional Link in the Food Web Does Not Biomagnify a Persistent Contaminant in Lake Ontario: The Case of Cercopagis pengoi

J. Great Lakes Res. 31:210–218 Internat. Assoc. Great Lakes Res., 2005

Additional Link in the Food Web Does Not Biomagnify a Persistent Contaminant in Lake Ontario: The Case of Cercopagis pengoi Elizabeth Thompson1, Joseph C. Makarewicz*, and Theodore W. Lewis Department of Environmental Science and Biology State University of New York at Brockport Brockport, New York 14420 ABSTRACT. Cercopagis pengoi is a new and abundant non-indigenous predator species in the Lake Ontario food web. We explored the impact of this predator on the levels of a chlorinated hydrocarbon in the pelagic food web through assessments of seasonal abundance and mirex concentrations of Cercopagis pengoi (Ostroumov) and the planktivorous alewife (Alosa pseudoharengus). Abundance, stable isotope, and alewife stomach data indicate that Cercopagis pengoi has become an established portion of the Lake Ontario food web. Cercopagis, a predaceous cladoceran, feeds on the lower portion of the trophic web and is clearly fed upon by the planktivorous alewife. Cercopagis is a link in the Lake Ontario food web, in which energy and materials are being passed from one level of the trophic web to another. However, mirex levels of the planktivorous alewife did not increase during the period of highest Cercopagis abundance. The annual load of mirex (mass of Cercopagis times concentration) transferred from one level of the trophic web to the next is low. In the summer, when Cercopagis is abundant, alewives were not feeding on them. INDEX WORDS: analysis.

Food web, biomagnification, Lake Ontario, Cercopagis, alewife, mirex, stomach

INTRODUCTION The introduction of exotic species into ecosystems is one of the most ecologically damaging effects human activity has had on nature (Elton 1958, Ricciardi and Rasmussen 1998). The Laurentian Great Lakes continue to be a major recipient of exotic species via ballast water transfers from ocean going vessels from international ports (Duggan et al. 2004). Many of the most recent invaders are native to the Ponto-Caspian region (Mills et al. 1993, MacIsaac et al. 1999, Ricciardi and MacIsaac 2000). Such invaders include zebra and quagga mussels (Dreissena polymorpha and D. bugensis), round gobies (Neogobius melanostomus) and the amphipod Echinogammarus ischnus (MacIsaac et al. 1999, Ricciardi and MacIsaac 2000). The most recent zooplankton invader of the Great Lakes is a pelagic, predatory cladoceran Cercopagis pengoi (Makarewicz et al. 2001, MacIsaac et al. 1999). Founded by ancestral Black Sea populations

(Cristescu et al. 2001), Cercopagis was first observed outside of its native waters in the Baltic Sea in 1992 (Ojaveer and Lumberg 1995) and has since been observed in Lake Ontario, Lake Michigan, Lake Erie, St. Lawrence River, and a growing number of the Finger Lakes in Upstate New York (MacIsaac et al. 1999, Makarewicz et al. 2001, Therriault et al. 2002, Charlebois et al. 2001). Lake Ontario, colonized by haplotypes (Makarewicz et al. 2001, MacIsaac et al. 1999) characteristic of the Baltic Sea and Black Sea (Cristescu et al. 2001), was the epicenter of the 1998 invasion into North America. Cercopagis abundances have reached as high as 6,000/m3 and field studies indicated a depression in populations of dominant members of the Lake Ontario zooplankton community (Daphnia retrocurva, Bosmina longirostris, and Diacyclops thomasi) when the abundance of Cercopagis increased (Laxson et al. 2003, Benoit et al. 2002). Laboratory experiments also demonstrated that Cercopagis fed on small-bodied species including D. retrocurva and B. longirostris (Laxson et al. 2003). In the Gulf of Riga, Baltic herring (Clupea harengus) feed on Cercopagis and even prefer Cer-

1

Current address: Battelle Memorial Institute, 505 King Avenue, Columbus, OH 43201 *Corresponding author. E-mail: [email protected]

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1978), mirex was first discovered in Lake Ontario fish in 1974 and has contaminated the entire food web (Kaiser 1974). The use of mirex as a pesticide was banned in Canada in 1977 and in the United States in 1978 (Environment Canada 1977, Kaiser 1978). Recent evidence (Makarewicz et al. 2003) indicates that mirex levels in Lake Ontario salmon tissue have significantly decreased since the 1970s. Even so, health advisories on eating Lake Ontario salmon are still in effect (NYSHD 2001) indicating that contaminant concentrations in salmonines of Lake Ontario are a continuing concern to fishery managers (Jackson 1997). A major question is what happens to mirex concentrations in top-level predators as non-indigenous predator species are inserted into the middle of a food web? In Lake Ontario, an enhancement of mirex levels due to biomagnification would become apparent first at the trophic level directly above Cercopagis: that is with the planktivorous alewives. If Cercopagis is an important food source for alewives and thus acts as an additional link and step in the food web, we hypothesize that concentrations of mirex in alewife tissue should increase seasonally in response to a diet of Cercopagis. FIG. 1. web.

Simplified Lake Ontario pelagic food

copagis to the native species of zooplankton (Ojaveer and Lumberg 1995). In Lake Ontario, presence and absence data suggest that adult alewife (Alosa pseudoharengus) are feeding on Cercopagis while consumption of Cercopagis by young of the year alewife is low (Bushnoe et al. 2003). Based on diet analysis and laboratory experiments, Cercopagis appears to be an additional seasonal link in the Lake Ontario pelagic food web during the summer months. Here the term link implies that energy or materials flow between species; that is, Daphnia is eaten by Cercopagis which is in turn eaten by an alewife (Fig. 1). Similarly, alewife feed on the predaceous Mysis which may feed on the predator Cercopagis and the herbivorous Daphnia. A link, Mysis, exists between alewife and Cercopagis and Daphnia and does not necessarily imply different trophic levels. Mirex, an organochlorine insecticide, is a major contaminant of Lake Ontario sediments and biota (Environment Canada 1977, Armstrong and Sloan 1980). Manufactured in the Lake Ontario watershed from 1959 through 1976 (Comba et al.1993, Kaiser

METHODS Zooplankton Analysis Seasonal Cercopagis samples were collected weekly from May through November of 2000 due north of Hamlin Beach State Park (43° 25.110′ latitude and 77° 53.986′ longitude), Lake Ontario, New York. Cercopagis was collected using a double Bongo net (571-µm mesh size, 50-cm diameter) following the method of Makarewicz et al. (2001) with seasonal results reported by Laxson et al. (2003). The remainder of the zooplankton community was collected using a Wisconsin net (63-µm mesh net, 50-cm diameter) equipped with a flow meter (see Makarewicz et al. 2001). Both samples were preserved in 10% buffered formalin. Before zooplankton samples were counted, they were mixed thoroughly and diluted individually to obtain 150–350 organisms per subsample. Three replicate 10-mL subsamples were withdrawn using a Hensen-Stemple pipette. Additional zooplankton samples were collected for isotope analysis during their seasonal population peaks in the summers of 2000 and 2001. Cercopagis pengoi, Daphnia retrocurva, Leptodora kindtii, and Holopedium gibberum were collected

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using either a double Bongo net (571-µm mesh size, 50-cm diameter) or a Wisconsin net (63-µm mesh size, 50-cm diameter) during their seasonal population peaks. Representative portions of the samples were visually examined for relative percent composition. Each sample of Daphnia, Holopedium, Cercopagis, and Leptodora samples contained > 75% of a single species. Samples were placed in solvent rinsed glass jars, kept in ice and transported back to the lab and immediately frozen until analysis. Fish Analysis Alewives (Alosa pseudoharengus) were collected monthly from May through September of 2000 and 2002 by gill netting. Floating gill nets were set in 6 m of water west of Sandy Creek (43°21.347′ latitude and 77° 55.077′ longitude), Hamlin, New York. Fish length and weight were determined by standard procedures (Jearld 1983), while age was determined by counting annuli on the otoliths (Robert O’Gorman, personal communication; Watson 1964). Up to ~100 organisms were frozen whole in food storage bags for contaminant analysis. Prior to pesticide analysis, fish (age 2, 1998 year class) were thawed and the entire fish (minus eggs) was homogenized in a food blender. In the field, stomachs of 2001 alewives (age 3) not frozen were removed for diet analysis. Contents were flushed into vials with 10% buffered formalin. Diet analysis generally followed Strus and Hurley (1992). All organisms in the entire stomach were counted with the following exception. If the most abundant species numbered more than 200, a subsample was counted. Concentration of the dominant organism was adjusted to at least 100 individuals per 3 mL by adding water to the stomach contents. If sub-sampling was necessary, three 3-mL aliquots taken with a Hensen-Stempel pipette from each sample were examined in a glass counting dish. All prey items in the stomachs were identified to species level and counted, while the lengths of the first 20 whole organisms of each species were measured. Recognizable body parts were counted for invertebrates that were not intact. Spines were not used to enumerate Cercopagis, as spines tend to have longer retention times in fish stomachs than soft-bodied zooplankton parts (Parker et al. 2001); instead heads were counted. The total numbers of organisms in the stomachs were estimated from the subsample by direct proportion (Mills et al. 1995). Feeding preference was

determined using Ivlev’s electivity index (Ivlev 1961). Contaminant Analysis Mirex methodology, detection equipment, quality assurance, extraction techniques, and cross-laboratory comparisons used for fish analysis are reported in Makarewicz et al. (2003). Typically, Makarewicz et al. (2003) extracted salmon tissue overnight (16± 4 hrs) in a Soxhletic extractor (a minimum of 200 cycles) with 75 mL of methylene chloride/hexane (20:80 v/v) solvent mixture. Procedures differed from Makarewicz et al. (2003) in the following manner. Cercopagis weight was determined by removing excess water by blotting with a kimwipe for wet weight determination and dried in an oven at 20°C overnight for dry weight determination. The dried tissue sample was then mixed with 20 grams of anhydrous sodium sulfate prior to extraction. To increase the detection limit of organisms lower in the food chain, the amount of extract taken to the evaporation stage was increased. For example, a 15-mL aliquot from the salmonine extraction, a 30mL aliquot from the alewife extraction, and a 75mL aliquot from Cercopagis extractions were concentrated to 1 mL under nitrogen gas, and then cleaned-up through a 5-g florisil column (at a rate of 4 mL/min) to a volume of 50 mL. This eluant was then concentrated under nitrogen gas to a final volume of 1 mL for the salmonine and alewives, and 0.1 mL for zooplankton. This allowed detection limits to be lowered to 20 parts per trillion. Prior to clean-up, percent extractable lipid content of salmonine and alewife was determined by evaporating a known volume of the extract and weighing the residue (Hesselberg et al. 1990). Stable Isotope Analysis All samples were analyzed for stable isotopes of carbon and nitrogen with a dedicated mass spectrometer (Finnigan Delta Plus) interfaced to a Carlo Erba elemental analyzer at the Cornell-Boyce Thompson Stable Isotope Laboratory (CoBSIL). Homogenized samples were freeze-dried at –40°C and ground to a fine powder with a mortar and pestle. Samples were weighed out (0.5 mg) on a Sartorius microbalance MC5 (readable to 1 µg), placed into tin capsules (3.5 × 5 mm), combusted at 1,000°C with gasses transported to the Faraday cup detector by an ultra-high purity helium carrier gas. The isotopic ratio was calculated as follows:

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δX = ((15N/14N of sample)/(15N/14N of standard)–1) × 1,000. Atmospheric N 2 and PeeDee limestone were used as the nitrogen and carbon standards, respectively (Peterson and Fry 1987). Statistics Logarithmic transformations were required to correct for heteroscedastic variances in alewife mirex concentrations to meet the assumptions of analysis of variance (ANOVA). ANOVA was used to test for differences in alewife mirex concentration between months. Linear regressions tested for relationships between the dependent variable of alewife mirex concentration and the independent variables of fish weight, percent lipid, isotope signature, and fish length.

FIG. 2. Seasonal Cercopagis pengoi abundance and mirex concentration in Alosa pseudoharengus (age 2+), Lake Ontario, 2000. Eggs are removed from fish prior to analysis for mirex. Values are the mean ±S.E.

RESULTS A maximum of 11.7 Cercopagis/m 3 was observed in the months of May, June, and mid-July 2000. At the end of July the population increased dramatically; in 1 week the population increased from 35/m3 on 27 July to 434/m3 on 3 August. The Cercopagis population continued to increase to the maximum abundance of 680/m 3 on 19 August. After this peak, there was a sharp decline in the population to 275/m3 on 24 August. The population fluctuated around 200 organisms/m3 in September and slowly decreased through November to only one organism/m3 on 13 November (Fig. 2). Age two alewife mirex concentrations ranged from 0.004 mg/kg to 0.009 mg/kg (Table 1, Fig. 2). No significant differences were observed in mean monthly mirex concentrations (P = 0.47, ANOVA), percent lipid (P = 0.24, ANOVA) and weight (P = 0.15, ANOVA) in the 1998 alewife year class collected in 2000 (age two). There were no significant correlations between alewife mirex concentration

and alewife total length (r 2 = 0.07, P = 0.14), weight (r2 = 0.01, P = 0.54) or percent lipid (r2 = 0.02, P = 0.44). The carbon signatures of biota characteristic of the Lake Ontario pelagic food web ranged from –22.83 to –28.85‰ (Table 2). Carbon signatures of Cercopagis pengoi, alewives (Alosa pseudoharengus), coho (Oncorhynchus kisutch), and chinook (Oncorhynchus tshawytscha) salmon were not significantly different (P > 0.05, ANOVA). Holopedium gibberum and Leptodora kindtii had similar carbon signatures (average range: –23.52 and –23.90‰, Table 2) to the proceeding group of fish and zooplankton (average range: –22.83 to –24.04‰) but were not statistically comparable because of small sample size (n = 2). Daphnia retrocurva had isotopically lighter carbon signatures ranging from –31.76 to –26.55‰ (average = –28.85 ‰, Fig. 3). ANOVA followed by a Tukey HSD revealed that the carbon signatures of Daphnia retrocurva were significantly different (P <

TABLE 1. Average weight, total length, percent lipid and mirex concentrations (mg/kg wet weight) of the 1998 alewife year class (age 2) collected in 2000. Values are the mean ± S.E. Date 22/5/00 19/6/00 19/7/00 14/8/00 14/9/00 27/10/00

N 4 4 5 4 17 1

Weight (g) 13.9 ± 1.4 17.6 ± 3.1 18.7 ± 1.9 18.1 ± 5.0 18.6 ± 1.0 17.1

Length (mm) 129 ± 3.7 138 ± 7.9 131 ± 3.9 129 ± 2.5 132 ± 3.0 126

% Lipid 5 ± 3.1 9 ± 4.0 6 ± 1.9 5 ± 2.2 10 ± 2.4 8

Mirex (mg/kg) 0.0076 ± 0.0006 0.0077 ± 0.0004 0.0088 ± 0.0010 0.0072 ± 0.0005 0.0062 ± 0.0008 0.0042

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Thompson et al. TABLE 2. Carbon and nitrogen signatures (‰) and mirex concentrations of selected Lake Ontario fish and zooplankton collected in 1999, 2000, and 2001. Values are the mean ± S.E. Values followed by the same letter are not significantly different (ANOVA, P>0.05). A star“*”indicates that no statistical analysis was possible because of the low number of samples.

Oncorhynchus tshawytscha Oncorhynchus kisutch Alosa pseudoharengus Cercopagis pengoi Leptodora kindtii Holopedium gibberum Daphnia retrocurva

N 5 5 39 7 2 2 4

δ13C –23.35 ± 0.32a –22.83 ± 0.12a –24.02 ± 3.90a –24.04 ± 0.37a –23.90 ± 0.05* –23.52 ± 0.02* –28.85 ± 0.07

0.001, ANOVA) from those of Cercopagis, alewives, coho, and Chinook salmon. Based on nitrogen signatures, coho and chinook salmon were the top predators in the pelagic food web with average nitrogen signatures of 17.33 and 17.38‰, respectively (Table 2). Alewives, the major forage fish in Lake Ontario, were a trophic level below the salmonines with nitrogen signatures ranging from 11.73 to 13.79‰. Two predators, Leptodora kindtii and the non-indigenous species Cercopagis, and two herbivores, Daphnia retrocurva and Holopedium gibberum, appeared to be part of the same trophic level, with nitrogen average nitrogen signatures ranging from 7.16 to 9.05‰ (Table 2, Fig. 3).

FIG. 3. Lake Ontario food web as described by stable isotopes of nitrogen (delta N) and carbon (delta C) in organisms collected in 1999, 2000, and 2001.

δ15N 17.33 ± 0.23b 17.38 ± 0.12b 12.75 ± 0.09 8.66 ± 0.29c 7.16 ± 0.01* 7.67 ± 0.03* 9.05 ± 0.08c

Mirex (µg/kg wet weight) 75 ± 9 81 ± 1.3 10 ± 1 0.1 ± 0.01 0.1 ± 0.03 .05 ± 0.01 0.1 ± 0.03

Alewife stomach contents generally matched seasonal changes in the most abundant prey species (Daphnia retrocurva, Bosmina longirostris and Diacyclops thomasi) available in the water (Table 3). In June, July, and August, Diacyclops thomasi and Bosmina longirostris were the most abundant prey species and had the highest percent abundance in age 3 alewife stomachs (Table 3). Cercopagis was not observed in plankton tows in July but made up 41% of the alewife diet during that month. Similarly, calanoid copepods represented only 4.5% of the zooplankton community in May but represented 59% of the diet of alewives. Bosmina longirostris and Daphnia retrocurva were most abundant in water samples in September and October; both were the major prey items in the alewife stomach in September, making up 43 and 42% of the stomach contents, respectively. In October, Bosmina longirostris composed 76% of the alewife diet and Pontoporeia made up 23%. Fairly consistent negative (avoidance) values for Ivlev’s electivity index were evident for Bosmina longirostris, Daphnia retrocurva, and Cercopagis in May, June, July, August, September, and October (Table 4). However, Bosmina longirostris was the major food item for alewives in August (Table 3) and Campthocampus and Cercopagis were preferred (+0.95 and +0.60, respectively) in July (Table 4). No species were positively selected for in August; however, Bosmina longirostris had the least negative Ivlev’s index of –0.34. There was no consistently positive (preference) value for any one species throughout the sampling period. For example in May, Ivlev’s index indicated that Mysis relicta was the preferred species (+0.17) while in June Holopedium gibberum and Diacyclops thomasi were preferred (+0.20 and +0.64, respec-

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TABLE 3. Percent abundance of major food items in the ambient water (W) and in the stomachs (S) of 1998 alewife year class (age 3) from May through October 2001, Lake Ontario. 0.0 indicates that an organism was not observed. May W Fish Examined (n) TAXA Bosmina longirostris Daphnia retrocurva Holopedium gibberum Ceriodaphnia spp. Campthocampus spp. Polyphemus pediculus Cercopagis pengoi Leptodora kindtii Diacylops thomasi Calanoida Mysis relicta Pontoporeia spp.

June S 6

4.9 0.0 3.7 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.01 0.0 0.0 0.0 91.0 34.9 4.5 58.6 0.0 6.5 0.0 0.0

W

July S 4

10.2 0.2 11.5 0.1 0.0 0.05 35.0 0.0 0.6 0.0 0.0 0.0 0.03 0.06 0.0 0.0 35.0 99.6 7.0 0.0 0.0 0.0 0.0 0.0

W

S 5

August W S 6

82.0 4.8 0.0 0.0 0.0 0.0 0.0 0.0 11.0 1.7 0.0 0.0

22.4 2.2 3.0 0.0 7.5 0.7 41.0 6.0 12.7 0.0 1.2 0.0

39.0 44.7 4.7 0.01 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.06 0.02 0.0 0.0 56.0 55.3 0.0 0.0 0.0 0.0 0.0 0.0

September W S 4

October W S 5

29.0 42.9 46.0 41.7 22.0 5.3 1.2 3.8 0.0 0.0 0.0 1.3 0.04 0.4 0.32 0.1 0.3 1.7 0.0 0.1 0.0 0.0 0.0 2.5

38.0 76.0 23.0 0.0 28.0 0.0 4.0 0.0 0.0 0.3 0.0 0.0 5.0 0.3 1.0 0.0 0.4 0.7 1.0 0.0 0.0 0.0 0.0 22.7

TABLE 4. Average values for Ivlev’s electivity index for the 1998 alewife year class (age 3) from May through October 2001, Lake Ontario. Taxa Bosmina longirostris Daphnia retrocurva Holopedium gibberum Ceriodaphnia spp. Campthocampus spp. Polyphemus pediculus Cercopagis pengoi Leptodora kindtii Diacylops thomasi Calanoida Mysis relicta Pontoporeia spp.

May –1.00 –1.00 0.00 0.00 0.00 0.00 –1.00 0.00 –0.97 –0.38 +0.17 0.00

Jun –0.92 –0.96 +0.20 0.00 –1.00 0.00 –0.26 0.00 +0.64 –1.00 0.00 0.00

tively). In July, a greater variety of organisms was observed in alewife stomachs. Preferred organisms included Holopedium gibberum (+0.20), Polyphemus pediculus (+0.20), Campthocampus (+0.95), Cercopagis (+0.60), Leptodora kindtii (+0.20), and Mysis relicta (+0.40). During the months of September, Pontoporia (+1), calanoid copepods (+0.25), and Polyphemus pediculus (+0.50) were selected. By October, selection focused on Pontoporia (+1) and Campthocampus (+0.20). DISCUSSION Prior to the introduction of Cercopagis, Leptodora, Daphnia, Holopedium, Bosmina, Diacyclops, calanoid copepods, Mysis, and Pontoporia

Jul –0.98 –0.96 +0.20 0.00 +0.95 +0.20 +0.60 +0.20 –0.92 –1.00 +0.40 0.00

Aug –0.34 –0.99 0.00 0.00 0.00 0.00 –0.84 –1.00 –0.63 0.00 0.00 0.00

Sep –0.93 –0.96 –0.99 –0.88 0.00 +0.50 –0.67 –0.98 –0.82 +0.25 0.00 +1.00

Oct –0.70 –1.00 –1.00 –1.00 +0.20 0.00 –0.99 –1.00 –0.78 –1.00 0.00 +1.00

were typically observed in adult alewife stomachs (Mills et al. 1992). After the introduction of Cercopagis, the same zooplankton genera, along with the invasive cladoceran species Cercopagis, were observed in the age 3 alewife stomachs collected. Bushnoe et al. (2003) concluded similarly and observed that young of the year alewife do not consume Cercopagis presumably due to gape size limitations. Generally, alewife consumption patterns reflect a tendency to take the larger prey items and the most abundant prey item (Brown 1972, Odell 1934). Both tendencies were observed in Lake Ontario as the alewife population switched to the most abundant prey seasonally. For example, during the months of May, June, August, Septem-

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ber, and October, Lake Ontario alewife stomach contents reflected the most abundant prey in the water column (Table 3). In July, when the small cladoceran Bosmina was dominant in the water column, the larger zooplankton Mysis, Pontoporia, Polyphemus, Canthocampus, Holopedium, and Cercopagis were selected for by alewife with Cercopagis representing 41% by abundance (Table 3) of the organisms observed in stomachs of alewife. Interestingly in August, when the large invasive species Cercopagis was most abundant (Fig. 2), alewives did not select for this species and they represented less than 0.1% by abundance of the stomach contents of alewife. In Lake Erie rainbow smelt stomachs, the occurrence of large boluses of spines of Bythotrephes, a species with a similar long caudal process as Cercopagis, was suggested as reducing smelt feeding presumably because the fish were satiated (Parker et al. 2001). In Lake Ontario, a similar mechanism may exist or alewives may have developed a learned response to avoid Cercopagis. The Lake Ontario result contrasted to the feeding behavior of the Baltic herring, where heavy feeding on Cercopagis was observed throughout the summer (Ojaveer and Lumberg 1995). Lakes with longer food chains tend to have top predators with higher levels of lipophillic contaminants (Cabana and Rasmussen 1994, Kidd et al. 1995, Rasmussen et al. 1990, Van Hoof et al. 1997). With the addition of a new invertebrate predator into Lake Ontario, an additional step in the food web would likely cause an increase in mirex in the high lipid-containing salmonines. However, the stable isotope data indicated Cercopagis was a link, but not an additional step in the food web as nitrogen signatures between cladoceran predators and prey were similar. In the post-Cercopagis Lake Ontario food web, salmon were the top predators in the pelagic food web while alewives, the major forage fish in Lake Ontario, were a trophic level below the salmonines (Table 2, Fig. 3). Generally, a 3–5‰ difference in nitrogen signatures is expected between each trophic level (Minagawa and Wada 1984, Peterson and Fry 1987). Cercopagis was a trophic level below alewives (Table 2). However two predators, Leptodora kindtii and the non-indigenous species Cercopagis, and two herbivores, Daphnia retrocurva and Holopedium gibberum, appeared to be part of the same trophic level, with nitrogen signatures ranging from 7.15 to 9.14‰ (Fig. 3). Other factors are known to affect isotope signatures, such as the organism’s location in the water column during thermally stratified periods and the

time period over which the organisms are collected (Leggett 1998). For example during the summer, 15N availability is greater outside of the epilimnion, where it is not depleted as rapidly (Leggett 1998). If Daphnia and Holopedium migrate to the metalimnion for prolonged periods, their nitrogen signatures may be enriched. At least for Daphnia in Lake Ontario, Makarewicz et al. (2002) has demonstrated the migration of Daphnia into the metalimnion during the evening. A crude calculation of potential mirex mass transfer between trophic levels and field results indicated that the insertion of Cercopagis into the Lake Ontario food web would not and did not elevate mirex levels in Lake Ontario alewives. On an abundance basis, Cercopagis constituted ~0.2% of the alewife diet during the study period. Since Cercopagis mirex concentration was approximately ten times that of herbivorous zooplankton (Table 2), the increased load of mirex to the next trophic level would be ~2%, which is an increase of mirex concentration in alewives from 0.010 to 0.0102 mg/kg (Table 2). Thus a significant increase in mirex levels in alewives would not be expected. Furthermore, such a small increase would not be detectable in tissue given the variability in the analytical methodology. The field data provide a similar conclusion. Although Cercopagis is a predatory species of zooplankton and Cercopagis seasonal abundance was high, reaching 800 m–3 in August, we did not observe a significant difference in the monthly mirex concentrations of the 1998 alewife year class (Fig. 2). Cercopagis was simply not abundant in alewife stomachs. Without a significant increase in mirex levels in alewives, an increase in mirex concentration in top-level Lake Ontario salmonines would not be expected as suggested by the long-term timetrend data series of Makarewicz et al. (2003). Since Cercopagis is not heavily fed upon by alewives, these results suggest that Cercopagis acts as a vector for contaminants settling to the sediments thereby removing them from the pelagic food web. Similarly, lakes with greater productivity tend to have fish with lower levels of contaminants in their tissue as contaminants taken up by algae, but not consumed by zooplankton, settle to the sediment effectively removing them from the pelagic food web (Rowan and Rasmussen 1992, Connolly and Peterson 1988, and Larson et al. 1992). In conclusion, our data indicated that alewives were not utilizing Cercopagis as a major food source. Stomach analyses revealed that alewives se-

Invasive Species and Food Web Contaminant Levels lected Cercopagis during July when abundance was low but did not select for Cercopagis in August when abundance was high. The nitrogen isotope data support both our mirex and stomach analysis results, indicating that Cercopagis is a link but not an additional step in the Lake Ontario food web. The annual load of mirex (mass of Cercopagis times concentration) transferred from one level of the Lake Ontario trophic web to the next was low. As a result, an increase in a persistent contaminant, such as mirex, through the process of biomagnification and bioconcentration would not be expected. ACKNOWLEDGMENTS We thank R. Herendeen, K. Schlutz, K. Hornbuckle, and an anonymous reviewer for their constructive criticism and suggestions. New York Sea Grant provided funding for this project. We thank R. O’Gorman for taking time from his busy schedule to train us in aging otoliths. REFERENCES Armstrong, R.W., and Sloan, R.J. 1980. Trends in levels of several known chemical contaminants in fish from New York State waters. New York State Department of Environmental Conservation. Technical Report 802. Benoit, H.P., Johannsson, O.E., Warner, D., Sprules, W.G., and Rudstam, L. 2002. Assessing the impact of a recent predatory invader: The population dynamics, vertical distribution and potential prey of Cercopagis pengoi in Lake Ontario. Limnol. Oceanogr. 40: 626–635. Brown, E.H. 1972. Population biology of alewife, Alosa pseudoharengus, in Lake Michigan 1949–1970. J. Fish. Res. Board Can. 29:447–500. Bushnoe, T.M., Warner, D.M., Rudstam, L.G., and Mills, E.L. 2003. Cercopagis pengoi as a new prey item for alewife (Alosa psedoharengus) and rainbow smelt (Osmerus mordax) in Lake Ontario. J. Great Lakes Res. 29:205–212. Cabana, G., and Rasmussen, J.B. 1994. Modelling food chain structure and contaminant bioaccumulation using stable nitrogen isotopes. Nature 372:255–257. Charlebois, P.M., Raffenberg M.J., and Dettmers, J.M. 2001. First occurrence of Cercopagis pengoi in Lake Michigan. J. Great Lakes Res. 27:258–261. Comba, M.E., Norstrom R.J., Macdonald C.R., and Kaiser, K.L.E. 1993. A Lake Ontario-Gulf of St. Lawrence dynamic mass budget for mirex. Environ. Sci. Technol. 27:2198–2206. Connolly, J.P., and Pederson, C.J. 1988. A thermodynmic-based evaluation of organic chemical accumula-

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