Changes in Zooplankton and the Phenology of the Spiny Water Flea, Bythotrephes, Following Its Invasion of Harp Lake, Ontario, Canada

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Changes in zooplankton and the phenology of the spiny water flea, Bythotrephes, following its invasion of Harp Lake, Ontario, Canada

Norman D. Yan, Agnes Blukacz, W. Gary Sprules, Paul K. Kindy, David Hackett, Robert E. Girard, and Bev J. Clark

Abstract: The crustacean zooplankton community of Harp Lake, Ontario, Canada, has changed appreciably since the invasion by the spiny water flea, Bythotrephes. Crustacean species richness has declined, large-bodied Cladocera have replaced small-bodied ones, and there has been a downward trend in the total abundance of zooplankton because copepod abundance has remained stable while Cladoceran abundance has declined. Although the zooplankton community has now been stable for 4 years (1995–1998), the biology of the invader has changed dramatically. In particular, there have been 10-fold differences in the mean annual abundance of Bythotrephes in this 5-year period and substantial changes in the timing of population maxima. We attribute these changes to two factors: (i) transition from a summer to a fall switch from parthenogenesis to gametogenesis and (ii) interannual differences in the thickness of a warm, dark stratum in the lake. We hypothesize that this stratum provides a refuge for Bythotrephes from predation by lake herring, Coregonus artedii. Résumé : La communauté des crustacés du zooplancton du lac Harp, en Ontario, Canada, s’est modifiée de façon notable depuis l’invasion de la Puce d’eau épineuse, Bythrotrephes. La richesse en espèces des crustacés a décliné. Les cladocères de grande taille ont remplacé ceux de petite taille et il y a une tendance à la baisse dans l’abondance totale du zooplancton, car, bien que la densité des copépodes soit demeurée constante, celle des cladocères a baissé. La communauté zooplanctonique est restée stable depuis 4 ans (1995–1998); néanmoins, la biologie de l’espèce envahissante a changé de façon spectaculaire. En particulier, ilyaeudesvariations par un facteur de 10 des densités annuelles moyennes de Bythotrephes pendant cette période de 5 ans et des changements importants dans la phénologie des maximums de densité. Nous attribuons ces changements à deux facteurs : (i) un déplacement de l’été à l’automne du passage de la parthénogenèse à la gamétogenèse et (ii) aux différences inter-annuelles de l’épaisseur d’une strate obscure et chaude dans le lac. Nous croyons que cette strate fournit un refuge à Bythotrephes contre la prédation exercée par le Cisco de lac, Coregonus artedii. [Traduit par la Rédaction] Yan et al. 2350

Introduction predict the long-term demographics of introduced species in particular systems either from short-term studies in those The population dynamics of introduced species are diffi- systems or from longer-term studies in other invaded habi- cult to predict. “Boom and bust” dynamics are common for tats. both introduced plants (Creed and Sheldon 1995) and ani- The cladoceran Bythotrephes longimanus (Crustacea: mals (Williamson and Fitter 1996), but monotonic increases Branchiopoda: Onychopoda), until recently termed B. ceder- to steady states (Ramcharan et al. 1992) are also common. stroemi (Grigorovich et al. 1998), invaded each of the Lau- The dynamics of particular invaders may be system-specific. rentian Great Lakes in the 1980s. The probable source was For example, Ramcharan et al. (1992) noted both boom–bust the Baltic Sea, a population originating in Lake Ladoga, up- dynamics and monotonic increases in abundances in invad- stream of St. Petersburg (Berg et al. 2001). Bythotrephes ing zebra mussel populations. Hence, we cannot reliably first appeared in Canadian Shield lakes in 1989 (Yan et al.

Received April 3, 2001. Accepted October 24, 2001. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on December 4, 2001. J16295 N.D. Yan.1 Biology Department, York University, 4700 Keele Street, Toronto, ON M3J 1P3, Canada, and Dorset Environmental Science Centre, Ontario Ministry of Environment, Box 39, Dorset, ON P0A 1E0, Canada. A. Blukacz and W.G. Sprules. Department of Zoology, Erindale Campus, University of Toronto, 3359 Mississauga Road N., Mississauga, ON L5L 1C6, Canada. P.K. Kindy and D. Hackett. Department of Biology, Nipissing University, 100 College Drive, North Bay, ON P1B 8L7, Canada. R.E. Girard and B.J. Clark. Dorset Environmental Science Centre, Ontario Ministry of Environment, Box 39, Dorset, ON P0A 1E0, Canada.

1Corresponding author (e-mail: [email protected]).

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1992). We predict that it will become an important member veloped, and if the Harp Lake changes are unusual in com- of the Shield lake plankton for three reasons. Firstly, the in- parison with neighboring lakes that have not been invaded; vader is spreading rapidly. Since 1989, Bythotrephes has (ii) if the unusual life-history characteristics of Bythotrephes colonized at least 34 inland lakes in Ontario (MacIsaac et al. observed by Yan and Pawson (1998) have been maintained; 2000). Secondly, many Shield lakes have suitable and (iii) if there is evidence that a refuge from lake herring Bythotrephes habitat, given its apparent preference for large, predation is important in the demographics of Bythotrephes oligotrophic lakes in its native Eurasia (MacIsaac et al. in Harp Lake, as suspected by Yan and Pawson (1998). 2000). Finally, Bythotrephes has had large impacts on the structure of zooplankton communities (Lehman and Caceres 1993; Yan and Pawson 1997) soon after its establishment. Materials and methods Unfortunately, the available North American Bythotrephes case studies are too brief to determine if the invader has Study lake descriptions characteristic demographics or if the effects of the invader Harp Lake is a single-basin, relatively small (71.4 ha), deep are permanent. Both European (Manca and Ruggiu 1998) (zmax of 37.5 m) lake located in southcentral Ontario, Canada. Its and North American Great Lakes’ studies (Johannsson et al. waters are soft and nutrient-poor (Table 1), as is typical of the region. Before the arrival of Bythotrephes, an average of 16 crusta- 1991) indicate that Bythotrephes populations are character- cean zooplankton taxa was recorded each year in the lake (Yan and ized both by large interannual variations in abundance and Pawson 1997). Copepods contributed roughly 80% of the biomass. by flexible demographic and behavioural responses to preda- Because the hypolimnion of the lake is both deep and well oxygen- tors (Bilkovic and Lehman 1997; Straile and Hälbich 2000). ated, several of these were cold stenotherms and (or) glacial relicts, Hence, we should not assume that the patterns in zooplank- including Epischura lacustris, Leptodiaptomus sicilis,andSenecella ton detected soon after North American Bythotrephes inva- calanoides. Coregonus artedii, lake herring, is the dominant pe- sions will be stable. lagic zooplanktivorous fish in the lake (Coulas et al. 1998). Bythotrephes first appeared in Harp Lake, Ontario, Can- Bythotrephes first appeared in this region of Ontario in 1989 (Yan et al. 1992). It first appeared in zooplankton samples in Harp Lake ada, in 1993 (Hall and Yan 1997). By 1995, the crustacean in the summer of 1993, having perhaps invaded a year or two earlier. zooplankton of the lake had changed in several ways. The We compare the changes in the zooplankton of Harp Lake, asso- abundance of two small taxa, Bosmina longirostris and ciated with the arrival of Bythotrephes, with those in the neigh- Tropocyclops extensus, declined appreciably, and three small bouring Blue and Red Chalk lakes, which have not been colonized cladocerans, Chydorus sphaericus, Diaphanosoma birgei, by Bythotrephes. Like Harp Lake, the two reference lakes are and Bosmina (Neobosmina) tubicen, disappeared from our nonacidic, oligotrophic, clear-water, stratified lakes (Table 1) with collections. In contrast, the abundance of a few larger taxa, largely forested catchments. Yan et al. (1996) describe their zoo- Holopedium gibberum and especially Daphnia mendotae plankton communities. and Leptodiaptomus sicilis, increased to previously unre- corded levels (Yan and Pawson 1997). Eliminating compet- Sampling and sample enumeration ing hypotheses, Yan and Pawson (1997) suggested that Each time that we visited Harp Lake, we estimated the euphotic Bythotrephes was responsible for these changes. Dumitru et zone depth as twice the Secchi depth. We also quantified thermal al. (2000) provided supporting evidence, demonstrating that stratification using a temperature profile taken at 1-m intervals at despite substantial predation from lake herring (Coulas et al. the deepest spot in the lake. We identified the top of the hypolimnion as the depth at which the decline of temperature with 1998), the Bythotrephes population in Harp Lake consumed depth fell to <1°C·m–1. all, and occasionally even more than all, of the productivity Yan and Pawson (1997) detail the methods used for locating the of crustacean zooplankton in the lake during the summer of one sampling station and for collecting, identifying, measuring, 1995. and counting crustacean zooplankton from Harp Lake between 1978 We now suspect that the interactions quantified by Dumitru and 1995. We used identical methods between 1996 and 1998 in et al. (2000) between Bythotrephes and its Harp Lake prey Harp Lake and in all years in Blue Chalk and Red Chalk lakes might have been short-lived. After all, Bythotrephes growth (Yan et al. 1996). Yan and Pawson (1998) detail the methods using was unusual in 1995. Bythotrephes typically grow between for locating the 10 Bythotrephes sampling stations in Harp Lake and for collecting Bythotrephes in 1994 and 1995. They also detail each instar (e.g., Burkhardt 1994; Straile and Hälbich 2000), methods that were used to assess the gender, developmental stage, but there was no growth between instars II and III in Harp fecundity, stage of brood development, and clutch size of partheno- Lake in the summer (Yan and Pawson 1998). The life history genetic and gametogenic broods. We used identical methods for of Bythotrephes was also unusual. Bythotrephes normally collecting and counting Bythotrephes from 1996 to 1998 with the switches from parthenogenetic to gametogenic reproduction following exceptions. The filtration efficiency of the Bythotrephes in the fall (Straile and Hälbich 2000), but this switch hap- net (0.75 m diameter, 2.5 m long, 285 µm mesh) averaged 88% be- pened in midsummer in Harp Lake in 1994 and 1995. Yan tween 1995 and 1997. Efficiency was not measured in 1988; the and Pawson (1998) hypothesized that these peculiarities in 1995–1997 mean value was employed instead. Vertical hauls were demographics were attributable to a scarcity of prey in mid- taken from 2 to 3 m above bottom to the surface at all 10 stations summer, an observation supported by Dumitru et al. (2000). in all years except 1996, when samples were collected only from the four stations within the 21-m contour and only from the bottom Here, our goal is to determine if the Bythotrephes population of the metalimnion. or its zooplankton prey changed after 1995. In particular, our Most samples were examined in their entirety for Bythotrephes. objectives are to determine (i) if the short-term changes in We examined 550, 1144, 30, 237, and 1641 Bythotrephes annually the zooplankton community observed by Yan and Pawson from 1994 to 1998, respectively. Gender was not assessed in 1996 (1997) have been maintained, if any new changes have de- or 1997.

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Table 1. Limnological comparison of Harp, Blue Chalk, and Red Fig. 1. Long-term changes in (a) total and Cladoceran zooplankton Chalk lakes.a abundance, (b) crustacean species richness, and (c) mean Cladoceran body length in Harp Lake between 1978 and 1998. Harp Blue Chalk Red Chalk Bythotrephes was first detected in 1993. Lake Lake Lake Latitude 45°23′ 45°12′ 45°11′ Longitude 79°07′ 78°56′ 79°56′ Lake area (ha) 71.4 52.4 57.1 Mean depth (m) 13.32 8.5 14.2 Maximum depth (m) 37.5 23 38 Total phosphorus (µg·L–1) 6.78 5.97 5.27 pH 6.27 6.6 6.30 Secchi depth (m) 3.98 6.56 5.95 Conductivity (µS) 35.7 28.6 28.8 aLong-term average of annual means from 1975 to 1999 (K. Somers, Ontario Ministry of Environment, Dorset, Ont., unpublished data).

Hall and Yan (1997) noted that only 2% of the Bythotrephes population was located in the hypolimnion during the day in Harp Lake; hence, we report Bythotrephes abundance per unit volume of epilimnion + metalimnion. Bythotrephes abundance did not differ among the nine sampling strata when tested in 1994 and again in 1998; hence, we report the descriptive statistics of the population without correcting for the areas of the sampled strata.

Analytical methods We can be certain that Bythotrephes was in Harp Lake in 1993. Hence, for statistical comparisons, we treat 1993 to 1998 as the postinvasion period. All statistical analyses were performed on ice- free season averages. We used several univariate metrics, including total zooplankton abundance (log-transformed), average species richness, i.e., the average number of species recorded in our stan- dardized counts of roughly 250 animals, and the size of all Cladocera measured in the year. To test if the community changed after the arrival of Bythotrephes, we calculated a t statistic assum- ing unequal variances, given the unbalanced design (15 preinvasion overall abundance of zooplankton in Harp Lake; however, and 6 postinvasion years). If significance levels were close to 0.05 this now appears to be changing. The geometric mean of the in this conventional assessment, we retested the significance of the mean annual zooplankton abundances fell from 22.1 animals· t statistic using a randomization procedure, i.e., by reshuffling the –1 2 time series 999 times and recalculating the difference between L (s = 1.02, n = 13) before the arrival of Bythotrephes to –1 2 means of the last six shuffled data points in comparison with the 18 animals·L (s = 1.02, n = 6) between 1993 and 1998 mean of previous data points in the series. This approach was used (Fig. 1a). This change in mean total crustacean zooplankton because our time series of annual means should not be considered abundance, while not significant at p = 0.05 (t = 1.83, p = a random sample, and it is unbalanced, implying some risk of bias 0.096 by conventional assessment, and t = 1.86, P = 0.075 in the use of conventional statistical tables (Manly 1991). Because with 999 randomizations, after log-transformation), does multivariate metrics may provide more sensitive indications of suggest a trend. This trend was entirely attributable to a sig- change in communities than do univariate ones (Yan et al. 1996), nificant decline in the mean abundance of Cladocera (log- we also described changes in average community composition in transformed) after 1992 (t = 5.6, p < 0.001), not to any the lake using the correspondence analysis routines in Statistica. We used the same 17 zooplankton taxa previously used by Yan and change in the abundance of Copepoda (Fig. 1a). Pawson (1997), with log-transformed, ice-free season mean abun- There is no doubt about the changes in overall crustacean dances of these taxa as our input. species richness and size structure. Zooplankton richness has declined in Harp Lake since the arrival of Bythotrephes Results (Fig. 1b). The average number of species detected in our standard counting protocol was 9.92 species per count be- The zooplankton community of Harp Lake has changed tween 1980 and 1992. It fell by 18% to a mean of 8.1 spe- dramatically since the arrival of Bythotrephes in 1993. How- cies per count in the 6 years after Bythotrephes was detected ever, there have been no substantial changes in the commu- (t = 4.18, p < 0.001 with 999 randomizations). The mean in- nity since the 1995 field season, i.e., since Dumitru et al. dividual body length of Cladocera in our samples doubled (2000) predicted transitions in the zooplankton community from 0.43 mm before the invasion to 0.85 mm after the inva- and (or) in the Bythotrephes population. sion (Fig. 1c, t = 11.7, p < 0.001 after 999 randomizations). With only 3 years of postinvasion data (1993–1995), Yan The change in mean Cladoceran size was principally at- and Pawson (1997) were not able to detect a change in the tributable to a change in the relative abundances of different

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Fig. 2. Long-term changes in the ice-free season mean abundances of all common zooplankton species in Harp Lake. Note that the species are ordered from top left to bottom right based on their scores on CA axis I (see Fig. 4).

Fig. 3. Long-term changes in the mean annual body lengths of zooplankton species in the lake rather than to a change in Cladoceran taxa in Harp Lake. The taxa are Bosmina longirostris size of individual species. The abundance of mostly small Chydorus sphaericus (᭹), Daphnia mendotae (), Daphnia Cladocera decreased by orders of magnitude (Fig. 2). These ,(ٗ) retrocurva (᭞), Bosmina (Neobosmina) tubicen (᭜), Holopedium included Chydorus sphaericus (long-term mean length of gibberum (᭺), and Diaphanosoma birgei (×). The length of 0.29 mm in Harp Lake), which declined in abundance in H. gibberum has been corrected for shrinkage in formalin. 1991, before we had actually detected Bythotrephes in the lake, Daphnia retrocurva (0.86 mm), Diaphanosoma birgei (0.65 mm), Bosmina (Neobosmina) tubicen (0.39 mm), and Bosmina longirostris (0.31 mm). In contrast, the abundance of the two larger Cladocerans, Holopedium gibberum (0.84 mm) and Daphnia mendotae (0.93 mm), has increased appreciably. There were no long-term changes in the mean sizes of individual cladoceran taxa if we ignore some recent artifactual increases in variability of the size of those species with plummeting populations (Fig. 3). Hence, it is clear that the cause of the overall increase in Cladoceran size in the lake (Fig. 1c) was the replacement of small taxa with larger taxa after 1993. These enormous changes in the zooplankton community of Harp Lake were complete by 1995. There were no ap- pearances, disappearances, or appreciable changes in the abundance of taxa between 1995 and 1998 (Fig. 2). Hence, there were no appreciable changes in abundance, richness, or

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Fig. 4. A scattergram of first and second axis scores of a correspondence analysis of the mean annual abundances of 17 common zooplankton species (see Fig. 2) in Harp Lake. The left-hand plot locates the year scores in ordination space, years with similar community composition being near neighbours. The right-hand plot locates the taxa in ordination space, namely Bosmina (Neobosmina) tubicen (Btub), Bosmina longirostris (Blon), calanoid copepodids (cal), cyclopoid copepodids (cyc), Chydorus sphaericus (Csph), Cyclops bicuspidatus thomasi (Cbt), Daphnia mendotae (Dmen), Daphnia retrocurva (Dret), Diaphanosoma birgei (Dbir), Epischura lacustris (Elac), Leptodiaptomus minutus (Lmin), Leptodiaptomus sicilis (Lsic), nauplii (nau), Senecella calanoides (Scal), and Tropocyclops extensus (Text). Note the different x-axes lengths.

size structure of the community since 1995 (Fig. 1). Further, female–1) and in 1998 (at 0.36). The persistence of the popu- the correspondence analysis confirms that the community lation into the fall of 1998 suggests a major change from the had two periods of compositional stability separated by a earlier life-history pattern in the lake. Indeed, in comparison transition in the early 1990s (Fig. 4). with 1994 and 1995, there were far fewer males in midsum- Although there have been no appreciable recent changes mer in 1998 (Fig. 7a). Of greater importance, no females in the crustacean zooplankton assemblage in Harp Lake, the were producing clutches of resting eggs in July and early situation for Bythotrephes is quite different. Patterns of August of 1998, whereas most females had switched to abundance, growth, and life history have changed both resting-egg production in the summers of 1994 and 1995 within and among years. (Fig. 7b). The abundance patterns of Bythotrephes have changed since Growth patterns of Bythotrephes also changed during our 1995 in several ways. The mean abundance of Bythotrephes for study. In 1995, there was very little growth between instars the ice-free season was 2 animals·m–3 in 1994 and 3.2 m–3 in II and III in the summer, and body sizes actually fell through 1995. In both years, the population was very small in the August (Fig. 8). In contrast, in 1998, mean lengths increased spring, lagging well behind increases in water temperature from instar II to III at all times, and the body size of each and population increases of small Cladocera (Yan and Pawson instar increased almost continuously throughout the year. 1998). The Bythotrephes population then reached a single maximum in July, after which it fell in response to a switch Discussion from parthenogenesis to gametogenesis and resting-egg production. The only similarity to this 1994–1995 pattern in re- Yan and Pawson (1997) detected a change in the richness cent years is the low population size in the spring (Fig. 5). All of the zooplankton community of Harp Lake after the Bytho- else has changed. In 1996 and 1997, the population was small trephes invasion but did not report a change in mean Clado- at all times, averaging only 0.26 and 1.32 animals·m–3, ceran size or abundance. Our addition of 3 years to the time respectively. At 5.14 m–3, the population was larger in 1998 series confirms that the richness of the community has in- than in any other year. The interannual changes in seasonality deed fallen. We supplement the previous work with our evi- were dramatic. The summer maximum of 1994 and 1995 dis- dence that total abundance of zooplankton appears to be appeared to be replaced by an unprecedented fall maximum in declining in the lake in response to a large drop in Clado- 1998. ceran abundance. The summer maximum failed to appear from 1996 to 1998 Although reductions in total zooplankton abundance have despite good aestival fecundity. During July and August, the been observed in mesocosm experiments with Bythotrephes average sizes of parthenogenic clutches were quite similar (Wahlström and Westman 1999), our observation of a reduc- between 1994 and 1998 at around 3 embryos per clutch tion in the abundance of an entire natural zooplankton com- (Fig. 6). Further, the number of gravid animals was similar, so munity appears to be novel. There certainly have been that the summer egg ratio was similar in 1995 (at 0.24 eggs· reports of dramatic alterations in the daphniid component of

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Fig. 5. Seasonal changes in the mean (± standard error) abundances of Bythotrephes in the epilimnion + metalimnion of Harp Lake from 1994 to 1998 (Figs. 5a to 5e, respectively).

Fig. 6. Seasonal changes in the size of parthenogenic clutches of e.g., Leptodiaptomus minutus, in other lakes in the region -Bythotrephes in Harp Lake in 1994 (᭿), 1995 (+), 1997 (ٗ), and (Rusak et al. 1999) and attributed to annual variations in cli 1998 (). Dates where <3 clutches could be sized are excluded. mate. Hence, it is possible that the decline in zooplankton abundance detected in Harp Lake, although real, may have had nothing to do with the arrival of Bythotrephes. The decline in species richness observed is unprecedented in nonacidifying lakes on the Shield (Arnott et al. 1999); however, we have no readily available published data to compare with the changes in mean Cladoceran size and total zooplankton abundance. Hence, we compared these long- term changes in Harp Lake with those in Blue Chalk and Red Chalk lakes. The reference lake comparisons support our conclusion that Cladoceran size and total zooplankton abundance have changed in Harp Lake as a result of the invasion, not as a result of a regional climatic anomaly. Al- though mean zooplankton abundance in Harp Lake declined after 1992, there was no change in mean annual abundance in Blue Chalk Lake (t = 0.66, p = 0.52, tested on log- transformed data) or in Red Chalk Lake (t = –1.53, p = 0.16) after 1992 (Fig. 9a). Hence, the decrease in mean zooplankton abundance observed in Harp Lake was not a pattern found across the region. No formal analysis is required to determine that the increase in Cladoceran body size ob- the Cladoceran assemblage (Manca and Ruggiu 1998; served after 1992 in Harp Lake was unusual in comparison Lehman and Caceres 1993) but apparently not for the total with the reference lakes (Fig. 9b). Hence, we conclude that zooplankton assemblage. If we are to attribute this change in the zooplankton community of Harp Lake changed after Harp Lake to the arrival of Bythotrephes, we must, as a min- 1992 for reasons peculiar to the lake. We hypothesize that imum, prove both that the observed changes are unusual in the arrival of Bythotrephes is this peculiarity. magnitude for the region and that synchronous changes have Although the zooplankton community has not changed ap- not occurred in nearby uninvaded lakes. Such interlake syn- preciably since 1995, the Bythotrephes population certainly chrony has been observed for some zooplankton species, has. The change in seasonality cannot be explained by exam-

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Fig. 7. Seasonal changes in 1994 (᭺), 1995 (᭿), and 1998 ()of Fig. 8. Seasonal changes in the body + head length of female (a) males, as percent of the total Bythotrephes population, and Bythotrephes (± standard error (SE)) in Harp Lake in (a) 1995 (b) the percent of the total broods produced by Bythotrephes that and (b) 1998. These years were selected given their large sample were resting-egg broods. Too few animals were caught in 1996 for size. Instar IV animals are present only in the spring. Very few the sex ratio assessment, and gender was not recorded in 1997. The were captured; hence, their estimates are poor. Instars: I (᭿), II small, late-June peak in 1998 in Fig. 7a represents only one animal. (᭺), III (᭜), IV (*).

Fig. 9. Comparison of long-term changes in (a) the total crustacean abundance and (b) Cladoceran body length of zooplankton in Harp Lake () with two noninvaded reference lakes, Blue .(Chalk Lake (ٗ), and the main basin of Red Chalk Lake (᭺

ining the demographics of Bythotrephes itself. If the seasonality of Bythotrephes in Harp lake was responding solely to its inherent biology, there should have been a large population in the summer of 1998. After all, fecundity was the same as in earlier years but far more females were reproduc- ing parthenogenetically. As the summer population was actually relatively small in 1998, there must have been a dramatic increase in mortality to offset the increased natal- ity. Fish predation is the most likely source of this extra mortality. Lake herring is the principal pelagic planktivorous fish in Harp Lake, and Bythotrephes is its preferred prey. Coulas et al. (1998) examined the diet of lake herring in Harp Lake on seven occasions in 1995 and noted that lake herring selected Bythotrephes over four other prey categories on every date, with the highest selection evident when Bythotrephes populations peaked. Yan and Pawson (1998) estimated the vulner- ability of Bythotrephes to lake herring predation as the

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Fig. 10. Comparison of seasonal changes from 1993 to 1998 (Figs. 10a to 10f, respectively) in the presence and size of the refuge of Bythotrephes from predation by lake herring, i.e., the difference between the depth at the top of the hypolimnion and twice the Secchi depth. Positive values indicate the presence of the refuge, i.e., warm dark water.

Fig. 11. Scattergram of mean abundance of Bythotrephes in Harp ferred hypolimnetic habitat (Coulas et al. 1998) if Lake in July and August (called “summer”) vs. the summer epilimnetic prey were visible. mean of the refuge indicator (see Fig. 10). We suggest that the long-term changes in summer population size of Bythotrephes in Harp Lake can be explained by two factors: changes in the availability of the refuge from lake herring predation and changes in Bythotrephes life history. This refuge was both thick and long-lasting in 1993, the first year that Bythotrephes appeared in our zooplankton samples (Fig. 10). We suggest that this presented an ideal situation for the new colonists to prosper in the lake. As noted by Yan and Pawson (1998), the refuge did not exist in the spring of 1994 or 1995. It was available in July and Au- gust of 1994 and 1995 but not in the summers of 1996 through 1998. The mean abundance of Bythotrephes in July and August was correlated with the thickness of refuge between 1994 and 1997 (Fig. 11), the thicker the warm dark layer, the more abundant the Bythotrephes (r = 0.97, n =4, p < 0.05) in the summer. However, 1998 does not fit the pattern. In comparison with the previous 4 years, there are too many Bythotrephes given the absence of the hypothesized predation refuge. We suggest that the risk of predation fails to predict summer Bythotrephes population size in 1998 because the invader’s life history changed in that year. Clutch difference between the depth at the top of hypolimnion and sizes and egg ratios were similar in the summer, but unlike the euphotic zone depth (estimated as twice the Secchi depth, in earlier years, all of the summer clutches were parthe- see their fig. 8). Where the euphotic zone includes some of nogenic in 1998. the hypolimnion, the metric is negative, the mixed waters of Changes in body size are consistent with the hypothesis the lake are well illuminated, and the risk of predation by that predatory mortality varies among years. Instar II and III the hypolimnetic lake herring was assumed to be high. animals were smaller in the summer of 1998 than in 1995, When the top of the hypolimnion was deeper than twice the suggesting increased size-selective predation by lake herring Secchi depth, a warm, dark layer existed which was hypoth- (Bilkovic and Lehman 1997; Coulas et al. 1998). esized to offer Bythotrephes a refuge from predation on the We cannot explain the change from aestival to autumnal assumption that lake herring would only leave their pre- resting-egg production in the lake. However, it is worth not-

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ing that the current pattern, the autumnal switch, is the typi- References cal one in Eurasia. It was the aestival switch of 1994 and 1995 that was the unusual pattern. It is possible that one Arnott, S.E., Yan, N.D., Magnuson, J.J., and Frost, T.M. 1999. strategy of the invader for coping with the multiple, novel Interannual variability and species turnover of crustacean zoo- cues in a new environment is early resting-egg production. plankton in Shield lakes. Can. J. Fish. Aquat. Sci. 56: 162–172. Certainly, aestival resting-egg production has been interpreted Arts, M.T., and Sprules, W.G. 1987. Energy reserves of three zoo- as a stress response in other Cladocera (Arts and Sprules plankton species from two lakes with different metal concentra- 1987), and Panov et al. (2000) recorded aestival resting-egg tions. Can. J. Fish. Aquat. Sci. 44: 458–466 production in the invading fish-hook water flea, Cercopagis Berg, D.J., Garton, D.W., MacIsaac, H.J., Panov, V.E., and Telesh, pengoi, in the Neva Estuary of the Baltic Sea. I.V. 2001. Changes in genetic structure of North American Bythotrephes populations following invasion from Lake Ladoga, It is clear that short data series collected soon after coloni- Russia. Freshw. Biol. In press. zation are not adequate to quantify Bythotrephes abundance Bilkovic, D.M., and Lehman, J.T. 1997. Lipid concentration and size or typify Bythotrephes demographics. There was a great deal variation of Bythotrephes (Cladocera: Cercopagidae) from Lakes of interannual variability in demographics in Harp Lake. Erie, Huron and Michigan. J. Great Lakes Res. 23: 149–159. Similarly, Bythotrephes peak in Lake Ontario only in poor Buckingham, D.E. 1998. Does the World Trade Organization care alewife years (Johannsson et al. 1991). We should not be about ecosystem health? The case of trade in agricultural prod- surprised if single stable endpoints between Bythotrephes ucts. Ecosyst. Health, 4: 92–108. and their predators or prey do not develop. Burkhardt, S. 1994. Seasonal size variation in the predatory clado- There has been a substantial recent increase in interest in ceran Bythotrephes cederstroemii in Lake Michigan. Freshw. Biol. the study of nonindigenous species. We now know that the 31: 97–108. economic cost of such species is enormous (Pimental et al. Carlton, J.T., and Geller, J.B. 1993. Ecological roulette: the global 2000) and that they can fundamentally change the structure transport of nonindigenous marine organisms. Science (Wash- and functioning of food webs (Vander Zanden et al. 1999). ington, D.C.), 261: 78–82. Furthermore, more invasions will certainly occur. Major in- Coulas, R.A., MacIsaac, H.J., and Dunlop, W. 1998. Selective preda- vasion corridors remain open and transport mechanisms tion on an introduced zooplankter (Bythotrephes cederstroemi)by remain active (Carlton and Geller 1993). Intentional intro- lake herring (Coregonus artedii) in Harp Lake, Ontario. Freshw. ductions are still being planned (Ewel et al. 1999; Dextrase Biol. 40: 343–355. and Coscarelli 2000). Finally, a changing climate (Dukes Creed, R.P., Jr., and Sheldon, S.P. 1995. Weevils and watermilfoil: and Mooney 1999) and the increased internationalization of did a North American herbivore cause the decline of an exotic trade (Buckingham 1998) foster the global spread of species. plant? Ecol. Appl. 5: 1113–1121. Dextrase, A.J., and Coscarelli, M.A. 2000. Intentional introduc- Given the magnitude of this issue, our lack of understand- tions of nonindigenous freshwater organisms in North America. ing of the current impacts and the future risks of non- In Nonindigenous freshwater organisms: vectors, biology and indigenous species is alarming. We must re-evaluate long-held impacts. Edited by R. Claudi and J.H. Leach. Lewis Publishers notions about the factors that render habitats vulnerable to in- Inc., Boca Raton, Fla. pp. 61–98. vaders (Lozon and MacIsaac 1997). We must build tools that Dukes, J.S., and Mooney, H.A. 1999. Does global change increase the can be used to predict the capacity of biota to survive trans- success of biological invaders? Trends Ecol. Evol. 14: 135–139. port, successfully colonize, and, finally, alter their new com- Dumitru, C., Sprules, W.G., and Yan, N.D. 2000. Impact of Bytho- munities to the point that they become “nuisances” (Ricciardi trephes longimanus on zooplankton assemblages of Harp Lake, et al. 1998). If we exclude the zebra mussel (Strayer et al. Canada: an assessment based on predator consumption and prey 1996), we have little of the information needed to build such production. Freshw. Biol. 46: 241–251. tools for any freshwater invaders (Ojaveer et al.2). Our Harp Ewel, J.J., O’Dowd, D.J., Bergelson, J., Daehler, C.C., D’Antonio, Lake work suggests that such information cannot be devel- C.M., Gomez, L.D., Gordon, D.R., Hobbs, R.J., Holt, A., Hop- oped quickly. Nonetheless, the importance of the task indi- per, K.R., Hughes, C.E., LaHart, M., Leakey, R.R.B., Lee, W.G., cates we should begin developing this information, taking Loope, L.L., Lorence, D.H., Louda, S.M., Lugo, A.E., McEvoy, every opportunity to exploit existing long-term or large-scale P.B., Richardson, D.M., and Vitousek, P.M. 1999. Deliberate in- data sets for the head start to understanding that they provide. troductions of species: research needs. Bioscience, 49: 619–630. Grigorovich, I.A., Pashkova, O.V., Gromova, Y.F., and van Overdijk, C.D.A. 1998. Bythotrephes longimanus in the Commonwealth of Independent States: variability, distribution and ecology. Hydro- biologia, 379: 183–198. Acknowledgements Hall, R.I., and Yan, N.D. 1997. Comparing annual population growth estimates of the exotic invader Bythotrephes using sediment and We thank K. Somers for the randomization programme, plankton records. Limnol. Oceanogr. 42: 112–120. D. Geiling, J. Muirhead, and T. Pawson for technical assis- Johannsson, O.E., Mills, E.L., and O’Gorman, R. 1991. Changes in tance, and two anonymous referees for comments on the the nearshore and offshore zooplankton communities in Lake manuscript. The Ontario Ministry of the Environment, the Ontario: 1981–88. Can. J. Fish. Aquat. Sci. 48: 1546–1557. Natural Sciences and Engineering Research Council of Lehman, J.T., and Caceres, C.E. 1993. Food-web responses to spe- Canada, and the Canada Trust Friends of the Environment cies invasion by a predatory invertebrate: Bythotrephes in Lake Canada Fund provided financial support for the research. Michigan. Limnol. Oceanogr. 38: 879–891.

2 H. Ojaveer, E. Leppakoski, S. Olenin, and A. Ricciardi. Ecological impact of Ponto-Caspian invaders in the Baltic Sea, inland Europe, and the Great Lakes: an inter-ecosystem comparison. Unpublished.

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Lozon, J.D., and MacIsaac, H.J. 1997. Biological invasions: are predator defenses of an invertebrate pelagic predator, Bytho- they dependent on disturbance? Environ. Res. 5: 131–144. trephes longimanus. Ecology, 81: 150–163. MacIsaac, H.J., Ketelaars, H.A.M., Grigorovich, I.A., Ramcharan, Strayer, D.L., Powell, J., Ambrose, P., Smith, L.C., Pace, M.L., and C.W., and Yan, N.D. 2000. Modeling Bythotrephes longimanus Fischer, D.T. 1996. Arrival, spread, and early dynamics of a ze- invasions in the Great Lakes basin based on its European distri- bra mussel (Dreissena polymorpha) population in the Hudson bution. Arch. Hydrobiol. 149: 1–21. River estuary. Can. J. Fish. Aquat. Sci. 53: 1143–1149. Manca, M., and Ruggiu, D. 1998. Consequences of pelagic food- Vander Zanden, M.J., Casselman, J.M., and Rasmussen, J.B. 1999. web changes during a long-term lake oligotrophication process. Stable isotope evidence for the food web consequences of spe- Limnol. Oceanogr. 43: 1368–1373. cies invasions in lakes. Nature (London), 401: 464–467. Manly, B.F.J. 1991. Randomization and Monte Carlo methods in Wahlström, E., and Westman, E. 1999. Planktivory by the preda- biology. Chapman and Hall, London and New York. cious cladoceran Bythotrephes longimanus: effects on zooplank- Panov, V.E., Bolshagin, P.V., Krylov, P.I., Telesh, I.V., and ton size, structure, and abundance. Can. J. Fish. Aquat. Sci. 56: Baranova, L.P. 2000. Seasonal abundance and life history of native 1865–1872. Bythotrephes sp. and exotic Cercopagis pengoi (Cercopagids) in Williamson, M., and Fitter, A. 1996. The varying success of invad- Neva Estuary, Baltic Sea. Verh. Internat. Verein. Limnol. In press. ers. Ecology, 77: 1661–1666. Pimental, D., Lach, L., Zuniga, R., and Morrison, D. 2000. Envi- Yan, N.D., and Pawson, T.W. 1997. Changes in the crustacean zoo- ronmental and economic costs of nonindigenous species in the plankton community of Harp Lake, Canada, following the inva- United States. Bioscience, 50: 53–65. sion by Bythotrephes cederstroemi. Freshw. Biol. 37: 409–425. Ramcharan, C.W., Padilla, D.K., and Dodson, S.I. 1992. Models to Yan, N.D., and Pawson,T.W. 1998. Seasonal variation in the size predict potential occurrence and density of the zebra mussel, and abundance of the invading Bythotrephes in Harp Lake, On- Dreissena polymorpha. Can. J. Fish. Aquat. Sci. 49: 2611–2620. tario, Canada. Hydrobiologia, 361: 157–168. Ricciardi, A., Neves, R.J., and Rasmussen, J.B. 1998. Impending Yan, N.D., Dunlop, W.I., Pawson, T.W., and MacKay, L.E. 1992. extinctions of North American freshwater mussels (Unionidae) Bythotrephes cederstroemi (Schoedler) in Muskoka Lakes: first following zebra mussel (Dreissena polymorpha) invasion. J. records of the European invader in inland lakes in Canada. Can. Anim. Ecol. 67: 613–619. J. Fish. Aquat. Sci. 49: 422–426. Rusak, J.A., Yan, N.D., Somers, K.M., and McQueen, D.J. 1999. Yan, N.D., Keller, W., Somers, K.M., Pawson, T.W., and Girard, The temporal coherence of zooplankton population abundances R.E. 1996. Recovery of crustacean zooplankton communities in neighbouring north-temperate lakes. Am. Nat. 153: 46–58. from acid and metal contamination: comparing manipulated and Straile, D., and Hälbich, A. 2000. Life history and multiple anti- reference lakes. Can. J. Fish. Aquat. Sci. 53: 1301–1327.

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