Author's personal copy Journal of Great Lakes Research 36 (2010) 65–73
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Journal of Great Lakes Research j o u r n a l h o m e p a g e : w w w. e l s e v i e r. c o m / l o c a t e / j g l r
Temporal and spatial separation allow coexistence of predatory cladocerans: Leptodora kindtii, Bythotrephes longimanus and Cercopagis pengoi, in southeastern Lake Michigan Joann F. Cavaletto a,⁎, Henry A. Vanderploeg a, Radka Pichlová-Ptáčníková b, Steven A. Pothoven c, James R. Liebig a, Gary L. Fahnenstiel c a b c
NOAA Great Lakes Environmental Research Laboratory, 4840 S. State Rd. Ann Arbor, MI 48108-9719, USA ICBM, University of Oldenburg, Schleusenstrasse 1, DE-26382 Wilhelmshaven, Oldenburg, Germany NOAA Great Lakes Environmental Research Laboratory, Lake Michigan Field Station, 1431 Beach St., Muskegon, MI 49441-1098, USA
a r t i c l e
i n f o
Article history: Received 22 December 2009 Accepted 9 April 2010 Communicated by Hunter Carrick Index words: Predatory cladoceran Leptodora kindtii Bythotrephes longimanus Cercopagis pengoi Lake Michigan Zooplankton
a b s t r a c t The predatory cladocerans, Leptodora kindtii, Bythotrephes longimanus, and Cercopagis pengoi coexist in the waters of southeastern Lake Michigan near Muskegon, Michigan. Leptodora is indigenous, whereas Bythotrephes and Cercopagis are nonindigenous and became established in 1986 and 2000, respectively. To observe seasonal changes in their abundances, and relationships to each other, cladocerans were collected from 1994 to 2008 at an offshore (110-m) site, from 1998 to 2008 at a transitional (45-m) site and from 1999 to 2008 at a nearshore (15-m) site. Bythotrephes was most abundant at the offshore site compared to Leptodora and Cercopagis. Bythotrephes peak abundances usually occurred in autumn at all sites. Cercopagis tended to be more abundant at the nearshore site, and peak densities occurred in summer. At the mid-depth site, similar abundances occurred for all three predatory cladocerans, however, the date of peak abundance was usually earliest for Cercopagis, followed by Leptodora, and latest for Bythotrephes. In recent years, 2007 and 2008, densities of all three predatory cladocerans have increased. Temperature preference, fish predation, and competition between the invertebrate predators may all be important in allowing the dominance of one species over the other seasonally or spatially. Published by Elsevier B.V.
Introduction Leptodora kindtii (hereafter Leptodora), Bythotrephes longimanus (hereafter Bythotrephes), and Cercopagis pengoi (hereafter Cercopagis) respectively, are one native and two non-native predatory cladocerans that currently coexist in Lake Michigan. The cosmopolitan Leptodora was the dominant predatory cladoceran in waters of Lake Michigan until the invasion of Bythotrephes in 1986 (Evans, 1988; Barbiero and Tuchman, 2004). The initial years following the introduction of Bythotrephes, Leptodora densities declined substantially, thought to be a result of competition and predation by the newly invaded predator (Lehman, 1991; Branstrator, 1995). Cercopagis' invasion was originally discovered in two localized areas of Lake Michigan in 1999 (Charlebois et al., 2001), and by 2000, it was abundant at our study area in the southeastern part of the lake (Vanderploeg et al., 2002).
⁎ Corresponding author. Tel.: +1 734 741 2235. E-mail addresses:
[email protected] (J.F. Cavaletto),
[email protected] (H.A. Vanderploeg),
[email protected] (R. Pichlová-Ptáčníková),
[email protected] (S.A. Pothoven),
[email protected] (J.R. Liebig),
[email protected] (G.L. Fahnenstiel). 0380-1330/$ – see front matter. Published by Elsevier B.V. doi:10.1016/j.jglr.2010.04.006
The near translucent Leptodora appears much different morphologically than Bythotrephes and Cercopagis, which have a spherical body that is equipped with a barbed spine that exceeds their body length by 3 to 5 times. These three predatory cladocerans are potential competitors, and Bythotrephes, the largest in mean body weight, can consume Leptodora and Cercopagis (Branstrator, 1995; Witt and Caceres, 2004). Although Bythotrephes can consume larger prey items than both Leptodora and Cercopagis, all three have overlapping size ranges for preferred prey items such as cladocerans Daphnia spp., Bosmina, Eubosmina, and many rotifers (Branstrator and Lehman, 1991; Vanderploeg et al., 1993; Rivier, 1998; Schultz and Yurista, 1999; Laxson et al., 2003; Pichlová-Ptáčníková and Vanderploeg, 2009). In addition to competition amongst themselves, invertebrate predators are competitors to larval fish, potentially consuming plankton in the same size range (Francis et al., 1996; Shuter and Mason, 2001). Invertebrate predators, especially a new invader, add more trophic levels into the ecosystem and shift energy paths through the food web (Lehman and Caceres, 1993; Strecker and Arnott, 2008; Foster and Sprules, 2009). The size of invertebrate predators like Leptodora, Bythotrephes and Cercopagis make them potential food for planktivorous fishes that may also structure dynamics among the three predatory cladocerans. Bythotrephes is preferred prey for many adult
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forage fish and is readily consumed if present (Pothoven and Vanderploeg, 2004; Pothoven et al., 2007, 2009). Leptodora and Cercopagis are also consumed by adult fish (Herzig, 1995; Gorokhova et al., 2004; Pothoven et al., 2007, 2009). The co-occurrence of all three predatory cladocerans is unique in Lake Michigan and contrasts with other invaded regions like Lake Ontario or the Baltic Sea, where usually only one or two of the three prevail (Makarewicz and Jones, 1990; Laxson et al., 2003; Ojaveer et al., 2004; Polunina, 2005; Pollumae and Kotta, 2007). Herein, we address (1) to what extent do the predatory cladocerans coexist in southeastern Lake Michigan and (2) what mechanism(s) influence the coexistence or segregation of the three predatory cladocerans? Additionally, we report a unique data set of densities of Leptodora, Bythotrephes, and Cercopagis over an extended period during the 1990s and 2000s in southeastern Lake Michigan and from sites spanning nearshore to offshore. Methods Predatory cladocerans were collected at three sites located along a transect from nearshore to offshore in southern Lake Michigan, off Muskegon, Michigan, U.S.A. (Fig. 1). The 110-m deep site was sampled biweekly to monthly from summer through fall in 1994–2003 and 2007–2008 (Figs. 2 and 3). The mid-transect, or transition site, was 45-m deep, and it was sampled biweekly to monthly from summer through fall in 1998–2003 and 2007–2008 (Fig. 4). The nearshore site was 15-m deep, and it was sampled biweekly to monthly from summer through fall in 1999–2003 and 2007–2008 (Fig. 5). Surface water temperatures were measured directly with a thermometer or a Seabird CTD (conductivity, temperature and depth) during most sampling events, however for some sampling dates, water temperature data are missing (Figs. 2–5). We collected total zooplankton with a 0.5 m diameter, 153 µm mesh-size net. The net was vertically
towed through the water column at a speed of 0.5 m/s from one to two meters above the bottom to the surface. The net was washed thoroughly, the contents were transferred to a sample bottle, narcotized with Alka-Seltzer ™, and preserved with the addition of sugar formaldehyde to form a two percent solution (Haney and Hall, 1973). Duplicate net samples were collected at each site. In the lab, the whole sample was rinsed through a 600 µm mesh sieve to remove most of the zooplankton smaller than the cladoceran predators. All the cladoceran predators in each sample were then identified and counted using an Olympus SZX12 stereomicroscope. Instars I–IV were identified based on number of paired barbs present for Bythotrephes and Cercopagis. Mean densities of the replicates were reported as number/m2 to facilitate comparisons across sites with differing depths. To evaluate the effects of collection sites, years and seasons on densities of each of the predatory cladocerans, the mean density data from each collection was pooled into three seasonal groups; early summer (June and July), late summer (August and September), autumn (October, November and December), in each of the groups there were one to four observations. For Cercopagis only two seasons were analyzed, early and late summer, as their densities in autumn were either zero or very low. In order to handle temporal pseudoreplication present in the data as well as unequal number of observations in cells, we employed a linear mixed-effects model approach using the statistical software package R (R Development Core Team, 2009) R; P values were estimated by using Markov Chain Monte Carlo samples. To observe relationships between predatory cladocerans, Pearson correlations with Bonferroni probability were done with data collected from each year using SYSTAT (version 11.0, copyright SYSTAT Software, Inc. 2004). Data were log (x + 1) transformed prior to analysis. To examine trends among years, we determined a mean annual density for each predatory cladoceran. This was done by determining
Fig. 1. Map of collection sites in southeastern Lake Michigan for predatory cladocerans.
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Fig. 2. Mean (± SE) densities from the 110-m site for Bythotrephes (solid circle), and Leptodora (open square), from 1994 to 1999, and temperatures (asterisk) from 1995 to 1999; temperature not available for 1994. Densities are plotted for each collection date.
the mean (±SE) of all samples collected from June to December; N varied by number of collections for each year. The timing and temperature of peak densities for each predatory cladocerans was examined to observe seasonal trends. Since temperature data was not
available for 1994, the mean (±SE) temperature on the day of peak density was determined by using data from years 1995–2003, 2007 and 2008. The mean (±SE) day of peak density was determined by using data from all years (1994–2003, 2007 and 2008).
Fig. 3. Mean (± SE) densities from the 110-m site for Bythotrephes (solid circle), Leptodora (open square), Cercopagis (solid triangle), and temperatures (asterisk) from 2000 to 2003, 2007 and 2008. Densities are plotted for each collection date.
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Fig. 4. Mean (± SE) densities from the 45-m site for Bythotrephes (solid circle), Leptodora (open square), Cercopagis (solid triangle), and temperatures (asterisk) from 1998 to 2003, 2007 and 2008. Densities are plotted for each collection date.
Results
at the 45-m site, and 28%, 49%, 22%, and 2%, respectively at the 15-m site.
Bythotrephes longimanus Leptodora kindtii Bythotrephes densities tended to be highly variable seasonally and annually at all three sites (Figs. 2–5). The highest densities were reached at the 110-m and 45-m deep sites (Figs. 2–4). In November 1998 at the 45-m site, a density of 2,076/m2 (±262 SE) was the highest observed for the study period (Fig. 4), followed by 1,926/m2 (±199 SE) at the 110-m site a decade later (Fig. 3). The 15-m deep site had the lowest densities of Bythotrephes (Fig. 5). Despite the variability, there were a few apparent trends. Annually, two peak densities were often present at the 110-m and 45-m deep sites; the first occurred at the end of July or early August when water temperatures were around 20 °C, and a second peak, usually the more prominent, occurred in October or November as water temperatures were declining from the seasonal maximum (Figs. 2–4). At the 15-m deep site, peak densities of Bythotrephes appeared in the later part of year in October or November as water temperatures were declining (Fig. 5). Instars I–III of Bythotrephes were usually found together during all months, except during the very beginning and ends of their annual population cycle. Instar IV of Bythotrephes was occasionally found during the early part of the year in June or July. Instar II tended to be the most numerous. Averaging over all years, instars I, II, III, and IV as a proportion of the population were 29%, 43%, 28%, and 0.2%, respectively at the 110-m site, 25%, 48%, 24%, and 1.5%, respectively
Timing of peak Leptodora densities varied widely and occurred in late July or August (Figs. 2–5). The highest mean densities of Leptodora usually occurred at the 45-m site (Fig. 4). At this site, the highest Leptodora density observed was 4,047/m2 (±316 SE) on July 7, 2008. At the 110-m site, the densities of Leptodora were very low in 1994, 1995, 1998, and 1999; however, since 2000, it appears that Leptodora densities have increased (Figs. 2 and 3). Similarly, at the 15-m site, Leptodora densities were very low from 1999 to 2001, and more recently their peak densities increased in 2002, 2003, and 2008 (Fig. 5). Summarizing all sites, Leptodora densities have increased in 2007 and 2008, especially at the 45-m site where Leptodora are often the most numerous predatory cladoceran (Fig. 4). Cercopagis pengoi Cercopagis was found at all three study sites in 2000 (Figs. 3–5). On August 9, 2000, a maximum density of 13,585/m2 (±421 SE) was observed for Cercopagis at the 15-m deep site. Since its establishment in Lake Michigan, Cercopagis densities are highest at the 15-m site compared to the 45-m and 110-m sites. However, in 2003 and especially in 2008, Cercopagis had very high peak densities at all three sites
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Fig. 5. Mean (± SE) densities from the 15-m site for Bythotrephes (solid circle), Leptodora (open square), Cercopagis (solid triangle), and temperatures (asterisk) from 1999 to 2003, 2007 and 2008. Densities are plotted for each collection date.
(Figs. 3–5). The highest densities of Cercopagis usually occur in July and August (site and year dependent) when water temperatures were near highest of the year. By September, their numbers diminish (Figs. 3–5). Instar distributions for Cercopagis were determined for 2000–2003 only. All instars, I–III, of Cercopagis co-occurred during most months. Instar IV does occur in Cercopagis, (Makarewicz et al., 2001a,b; Simm and Ojaveer, 2006) but none were found during this study. Instar II tended to be the most common at the 110-m and 45-m sites, and all instars were rather evenly distributed at the 15-m site. For all years, instars I, II, and III as a portion of the population were 24%, 48%, and 28% , respectively at the 110-m site, 21%, 48%, and 31%, respectively, at the 45-m site, and 31%, 31%, and 38%, respectively, at the 15-m site.
was significant for Leptodora (P = 0.035), and Cercopagis (P = 0.020), and was highly significant for Bythotrephes (P b 0.001). Overall variation among years was significant for Bythotrephes (P = 0.020) and Leptodora (P = 0.001) but not for Cercopagis. Densities in selected seasons (early summer, late summer and autumn; see methods for monthly divisions) were significant only for Bythotrephes (P = 0.009) because of its high densities in autumn. The effect of season was not significant for Cercopagis and marginally non-significant for Leptodora (P = 0.056). The non-significant difference for Cercopagis between early summer and late summer seasons may be explained by the chosen split between early and late summer seasonal categories that fell between Cercopagis' peak densities.
Annual trends from nearshore to offshore Coexistence of species Annual mean densities of predatory cladocerans reveal offshore to nearshore shifts in dominance between species. Annual densities were highest for Bythotrephes at the 110-m site, for Leptodora at the 45-m site, and for Cercopagis at the 15-m site (Fig. 6). In 2000, densities were higher than other years for all species at their respective dominant sites (Fig. 6). A recent trend is the increase of predatory cladocerans in 2007 and 2008 at all sites. Annual densities for Bythotrephes are higher in 2007 and 2008 at the 110-m site compared to previous years. Annual densities for Leptodora increased at all sites in 2007 and 2008, and annual densities for Cercopagis increased at all sites in 2008 (Fig. 6). Linear mixed-effects model The effects of site, year and season were evaluated on the densities of each predatory cladoceran. The effect of collection site on density
All three predatory cladocerans occurred at all three sites in Lake Michigan, however their co-occurrence varied dependent on the day of year and location. Leptodora was observed most often with both Bythotrephes and Cercopagis. Correlation analysis revealed a significant positive relationship with Leptodora and Cercopagis at all sites and during all years (P b 0.05; Fig. 7a–b). Leptodora had a significant positive relationship with Bythotrephes at the 110-m and 45-m sites (P b 0.05), and at the 15-m site, their relationship was not significant (P N 0.05; Fig. 7a). By year, Leptodora and Bythotrephes had significantly high correlations in years 1995, 1999, and 2002 only (P b 0.05; Fig. 7b). Bythotrephes and Cercopagis had a significant negative relationship 15-m site only (P b 0.05; Fig. 7a), their negative relationships were not significant at the other sites. By year, Bythotrephes and Cercopagis had a significant negative relationship in 2000 and 2007 (P b 0.05; Fig. 7b).
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Fig. 6. Mean (± SE) densities plotted annually for Bythotrephes (a), Leptodora (b), and Cercopagis; note different scale for Y axis (c) at the 110-m (closed circle), 45-m (open square), and 15-m (open triangle) sites.
The analysis of the timing and the temperatures of annual peak densities for Bythotrephes, Leptodora and Cercopagis reveal patterns of their coexistence in Lake Michigan. The mean temperature at peak density for Bythotrephes (14.6 ± 0.9 ºC SE) is lower than the temperatures for Leptodora (18.9 ± 0.8 ºC SE) and Cercopagis (20.2 ± 0.6 ºC SE). Both Leptodora and Cercopagis reach peak densities at similar mean temperatures although the temperature is slightly higher for Cercopagis (Fig. 8a). Corresponding to the temperatures at peak densities is the mean day of year that peak density occurs. The mean day that peak density occurs is earliest for Cercopagis in July (day 205 ± 4 SE), followed Leptodora in August (day 230 ± 5 SE) and lastly by Bythotrephes in October (day 288 ± 7 SE) (Fig. 8b). Discussion The survey of nearshore to offshore sites in southeastern Lake Michigan demonstrates that three predatory cladocerans (Bythotrephes, Cercopagis, and Leptodora) with overlapping prey preferences all manage to survive together. However, it their coexistence depends on some temporal and spatial (horizontal) separation (Enz et al., 2001). Temporal and spatial differences in occurrence
Fig. 7. Correlation coefficients (r) for numerical density of three predatory cladocerans at different sites represented by site depths (a) and for years over the study period 1994–2008 (b). Correlations coefficients are plotted as Leptodora vs. Bythotrephes (LxB; diamond), Leptodota vs. Cercopagis (LxC; square) and Bythotrephes vs. Cercopagis (BxC; triangle). Solid symbols represent significant relationships (P b 0.05), and open symbols represent non-significant relationships. The number of observations (N) for each relationship is for plot (a) LxB; 15-m = 58, 45-m = 67, 110-m = 83; for LxC and BxC; 15-m = 52, 45-m = 52, 110-m = 51. For plot (b) N equals the following for all three combinations: 1994 = 5, 1995 = 11, 1996 = 6, 1997 = 7, 1998 = 17, 1999 = 18, 2000 = 30, 2001 = 24, 2002 = 29, 2003 = 33, 2007 = 27, and 2008 = 18.
In general, the seasonal pattern for the three predatory cladocerans in southeastern Lake Michigan is Cercopagis reaches highest densities first, followed closely by or at the same time as Leptodora, and finally by Bythotrephes, whose densities usually peak in autumn when the water temperature has cooled. Populations of Leptodora and Cercopagis overlap at times at all sites. Both Leptodora and Cercopagis densities are highest when Bythotrephes densities are low or zero. Because Bythotrephes will eat Cercopagis (Witt and Caceres, 2004) and probably Leptodora as well (Branstrator, 1995), their declines may be the result of Bythotrephes predation (Branstrator and Lehman, 1991). Cercopagis and Leptodora usually appear earlier in the season than
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during the same time period. At the offshore site, the timing of the predatory cladocerans highest densities tends to be more variable than at the transition and nearshore sites. A general and consistent scenario that may explain the seasonal patterns of predatory cladoceran densities is that fish control Bythotrephes and when fish decline, Bythotrephes increase and in turn may prey upon Cercopagis and Leptodora as well as their prey base resulting in their seasonal decline. Coexistence of predatory cladocerans—competition, predation, and temperature
Fig. 8. Mean (± SE) of all years and sites combined of the temperature at peak density (a) and the day of year at peak density (b) for the three predatory cladocerans.
Bythotrephes allowing them a period of respite from putative predation from Bythotrephes. In addition, unlike Bythotrephes, Leptodora and Cercopagis may not be as susceptible to visual fish predators because of their transparent body and small size, respectively (Vanderploeg et al., 2002; Pothoven and Vanderploeg, 2004; Pothoven et al., 2007). The large size and conspicuous pigmentation (Vanderploeg et al., 2002) of Bythotrephes make it more susceptible to adult planktivorous fish predation; therefore their seasonal distribution may be more directly shaped by fish predation (Mills et al., 1992; Yan and Pawson, 1998; Pothoven and Vanderploeg, 2004). Nearshore at the 15-m site, Bythotrephes were not found in appreciable numbers until September or October, likely the result of intense summer fish predation inshore (Pothoven et al., 2007). As for Cercopagis, and to a smaller degree Leptodora, they are more abundant at the 15-m site during the early to mid-summer period when fish predation should be highest. Indeed, it was observed that when both Bythotrephes and Cercopagis are found together in the nearshore, the preferred prey for alewives are Bythotrephes (Pothoven et al., 2007). As for Leptodora, despite their transparent body as defense mechanism, they are vulnerable to fish predation when they reach a large size (Herzig, 1995). Overall at the nearshore site, Cercopagis appears to be best equipped to obtain higher densities than Leptodora and Bythotrephes. At the transition (45-m) and offshore (110-m) sites, Bythotrephes density distributions often have a seasonal bimodal pattern with an increase in early summer followed by a mid-summer decline and finally by a greater increase in autumn. This bimodal pattern is often more pronounced at sites that are a greater distance from shore. The mid-summer decline may be the result of adult forage fish, mainly alewife, predation (Pothoven and Vanderploeg, 2004). The summer decline in Bythotrephes may be the result of fish moving from feeding nearshore to offshore as the epilimnetic water temperature increases and the thermocline deepens and moves away from shore (Brandt, 1980; Stewart and Binkowski, 1986). The timing of Cercopagis and Leptodora seasonal distributions for the transition site is similar to the nearshore site, where Cercopagis appears earliest in the season, followed by Leptodora. However, 2008 was an exception to this pattern as both Leptodora and Cercopagis reach very high densities
Leptodora and Cercopagis appear to be primary competitors, but not to the level of total exclusion, as they have similar times of occurrence, temperature and prey size preferences (Pichlová-Ptáčníková and Vanderploeg, 2009; Brown and Balk, 2008; Ojaveer et al., 2004). At the 15-m site, Cercopagis often out numbers Leptodora. Cercopagis may be a superior competitor to Leptodora in its ability to consume larger prey (Branstrator, 2005; Pichlová-Ptáčníková and Vanderploeg, 2009). At the 45-m site, densities of Cercopagis and Leptodora are usually similar, possibly due to a higher concentration of prey available there. It is also possible that at the 15-m site, where predation from both age 0 and adult fish is intense (Pothoven et al., 2007), the protection afforded by the tail spine may tip the balance in favor of Cercopagis. Unlike Bythotrephes, the size of Cercopagis may make it unable to directly prey on adult Leptodora. Leptodora and Cercopagis do not appear to be able to coexist easily with Bythotrephes. Both Leptodora and Cercopagis numbers declined when Bythotrephes was present, possibly due to direct predation (Witt and Caceres, 2004; Branstrator, 2005) as well as competition for food with the larger predator (Branstrator, 2005; Pichlová-Ptáčníková and Vanderploeg, 2009) that can efficiently consume a broader size range of prey than the other two species (Vanderploeg et al., 1993; Schultz and Yurista, 1999; Branstrator, 2005; Pichlová-Ptáčníková and Vanderploeg, 2009). When Lake Michigan was first invaded in the mid 1980s by Bythotrephes, Leptodora declined in number (Lehman, 1991; Branstrator, 1995). As an adaptation to the Bythotrephes invasion Leptodora maintains a population at lower overall densities with peak abundances that occur earlier in the year than prior to the invasion by Bythotrephes. Additionally, vertical separation in the water column between Leptodora and Bythotrephes as found in Lake Constance (Enz et al., 2001) and Swiss lakes (Palmer et al., 2001) may assist in the survival of Leptodora in Lake Michigan. To the benefit of all three species, temporal separation allows the predatory cladocerans to exist and reproduce over the annual cycle. Different tolerances in temperature may in part drive the differences in seasonal distribution. Comparatively, Cercopagis peak densities are often reached earliest in the season at the highest water temperature of the three predatory cladocerans, followed by Leptodora at slightly lower water temperature and finally by Bythotrephes later in the season at water temperatures several degrees cooler than the other two species (Fig. 8). Although Bythotrephes tolerates a relatively wide temperature range, its tolerance to temperatures in the low end of its range (Garton et al., 1990) gives it an opportunity to increase in abundance late in the season when fish predation pressure on it has relaxed. As for Leptodora and Cercopagis, they have been found to exist at similar temperatures in other bodies of water where they occur together (Polunina, 2005; Pollumae and Kotta, 2007; Brown and Balk, 2008). The occurrence of peak densities of Bythotrephes at lower temperatures relative to Cercopagis may be a reflection of the more northerly native distribution of the former species (Vanderploeg et al., 2002). Years 2007 and 2008 During the most recent years of the study, 2007–2008, predatory cladocerans have noteworthy shifts in abundances. Densities of
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Leptodora were generally up at all sites in both 2007 and 2008. At the 45-m site in 2008, densities of Leptodora were four times higher than the highest maximum density from the previous highest year (2000). Densities of Cercopagis were very low at all sites in 2007 and increased dramatically in 2008 with some of the highest densities ever observed. At the 15-m site, densities of Cercopagis were the highest since their invasion year in 2000, and at the 45-m and 110-m sites, the densities of Cercopagis were the highest ever observed at these sites. Densities of Bythotrephes were robust at the 110-m site in both 2007 and 2008. Densities of Bythotrephes were low in 2007 at the 45-m and 15-m sites, and increased at these two sites in 2008. Prey fishes, mainly alewives, have been decreasing in recent years (Warner et al., 2008; Bunnel et al., 2009), which may release some predation pressure from the three predatory cladocerans. Bythotrephes being the most susceptible to fish predation may benefit the most from a decline in forage fish. However since Bythotrephes, Leptodora, and Cercopagis are all relatively large prey items, they will continue to be susceptible to visual feeders. In addition, a recent increase in water clarity (Mida et al., 2010; Fahnenstiel et al., 2010; Barbiero et al., 2009) may alter the environment to the advantage of the visual predator (vertebrate or invertebrate) and to the disadvantage of the prey. Conclusion Our long-term seasonal study clearly demonstrated that the coexistence of Leptodora, Bythotrephes, and Cercopagis in Lake Michigan is dependent on temporal and spatial separation. However, further study is necessary to determine the degree of vertical separation of these species in the water column, their competition for food, predatory interactions, and the spatial distribution and effects of fish predation on these species. Recent decreases in planktivorous fish populations may lead to an increasingly important role for these cladocerans if fish predation on them continues to be relaxed. Acknowledgments For excellent assistance in laboratory and field we would like to thank K. Rice, L. Stara, A. Belinky, Q. Thai, S. Bickel, D. Frankowski, A. Flood, D. Ruberg, and the crews of the R/V Shenehon and R/V Laurentian. We thank the Great Lakes Commission and the NOAA Coastal Ocean Program Episodic Events Great Lakes Experiment for support of this research. This is GLERL contribution #1556. References Barbiero, R.P., Tuchman, M.L., 2004. Changes in the crustacean communities of Lakes Michigan, Huron, and Erie following the invasion of the predatory cladoceran Bythotrephes longimanus. Can. J. Fish. Aquat. Sci. 61, 2111–2125. Barbiero, R.P., Bunnel, D.B., Rockwell, D.C., Tuchman, M.L., 2009. Recent increases in the large glacial-relict calanoid Limnocalanus macrurus in Lake Michigan. J. Great Lakes Res. 35, 285–292. Brandt, S.B., 1980. Spatial segregation of adult and young-of-the-year alewives across a thermocline in Lake Michigan. Trans. Am. Fish. Soc. 109, 469–478. Branstrator, D.K., 1995. Ecological interactions between Bythotrephes cederstroemi and Leptodora kindtii and the implications for species replacement in Lake Michigan. J. Great Lakes Res. 21, 670–679. Branstrator, D.K., 2005. Contrasting life histories of the predatory cladocerans Leptodora kindtii and Bythotrephes longimanus. J. Plank. Res. 27, 569–585. Branstrator, D.K., Lehman, J.T., 1991. Invertebrate predation in Lake Michigan: regulation of Bosmina longirostris by Leptodora kindtii. Limnol. Oceanogr. 36, 483–495. Brown, M.E., Balk, M.A., 2008. The potential link between lake productivity and the invasive zooplankter Cercopagis pengoi in Owasco Lake (New York, USA). Aquat. Invasions 3, 28–34. Bunnel, D.B., Madenjian, C.P., Holuszko, J.D., Adams, J.V., French, J.R.P., 2009. Expansion of Dreissena into offshore waters of Lake Michigan and potential impacts on fish populations. J. Great Lakes Res. 35, 74–80. Charlebois, P.M., Raffenberg, M.J., Dettmers, J.M., 2001. First occurrence of Cercopagis pengoi in Lake Michigan. J. Great Lakes Res. 27, 258–261. Enz, C.A., Heller, C., Muller, R., Burgi, H.R., 2001. Investigations on fecundity of Bythotrephes longimanus in Lake Lucerne (Switzerland) and on niche segregation of
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