This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and educational use, including for instruction at the author’s institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's Personal Copy Journal of Great Lakes Research 38 (2012) 49–57 Contents lists available at SciVerse ScienceDirect Journal of Great Lakes Research journal homepage: www.elsevier.com/locate/jglr Long-term patterns in Lake Champlain's zooplankton: 1992–2010 Timothy B. Mihuc a,⁎, Fred Dunlap b, Casey Binggeli a, Luke Myers a, Carrianne Pershyn a, Amanda Groves a, Allison Waring a a b Lake Champlain Research Institute, SUNY Plattsburgh, Plattsburgh, NY 12901, USA NY dept. of Environmental Conservation, Ray Brook, NY, USA a r t i c l e i n f o Article history: Received 1 October 2010 Accepted 20 June 2011 Available online 2 October 2011 Communicated by Doug Facey Index words: Lake Champlain Zooplankton Long-term patterns Community composition Invasive species a b s t r a c t We examined patterns in Lake Champlain zooplankton abundance from 1992 to 2010 using summer data from five study sites. Rotifer abundance (#/m3) for many common taxa such as Polyarthra, Kellicottia, and Keratella declined lakewide in the mid-1990s which coincided with the invasion of zebra mussels (Dreissena polymorpha) into Lake Champlain. The only rotifer to increase in density following zebra mussel invasion was Conochilus which is a colonial species. Long-term shifts in copepod and cladoceran community composition can be attributed to the arrival of another invasive species in 2004–2005, the alewife (Alosa pseudoharengus). Our results support previous findings that alewife predation can impact larger bodied zooplankton within temperate lake systems. Following alewife invasion into Lake Champlain, body length of Leptodiaptomus and Daphnia retrocurva decreased to a size at or below known alewife feeding preferences. In addition, smaller bodied copepods (primarily Diacyclops thomasi) have increased in abundance since alewife invasion while juvenile copepods have declined. Our results suggest that post-alewife zooplankton patterns are most likely due to alewife size-selective feeding strategies. Observed long-term changes in zooplankton community structure have potential implications for the lake's food web dynamics, particularly recent declines in large bodied zooplankton which may release smaller plankton from top-down control. © 2011 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. Introduction Lake Champlain is a unique large lake ecosystem in the Great Lakes drainage basin, containing a diverse zooplankton assemblage. The lake contains a mix of deep (N100 m) and shallow habitats, extensive shoreline, and dynamic hydrologic regime. Lake Champlain's zooplankton assemblage consists of 12 copepod, 14 cladoceran, and 19 rotifer taxa. Of these taxa 16 are considered common (see Table 1). Previous surveys of Lake Champlain found a zooplankton community typical for a deep oligotrophic, temperate lake (Carling et al., 2004a; Keen and Potash, 1978; Meyer and Gruendling, 1979; Muenscher, 1930; Shambaugh et al., 1999). Muenscher (1930) was the first to document the lake's plankton and found a community containing abundant limnetic cladocera (Bosmina, Daphnia, and Diaphanosoma), common shallow and deep water copepods (primarily Cyclops and Diaptomus) and a high abundance of rotifers (N 500,000/m3) including Conochilus and Polyarthra. More recent survey results suggest a shift to eutrophic conditions from the 1930s to the 1970s. Meyer and Gruendling (1979) along with Keen and Potash (1978) provide the most extensive historical survey of the lake's zooplankton and found many copepods such as Mesocyclops, Diaptomus and Diacyclops thomasi (formerly Cyclops ⁎ Corresponding author. Tel.: + 1 518 564 3039. E-mail address: mihuctb@plattsburgh.edu (T.B. Mihuc). thomasi) while rotifers, mainly Keratella and Polyarthra (both considered eutrophic indicators), were numerically abundant throughout the lake. Surveys in the 1970s also found cladocerans (Daphnia retrocurva and Daphnia mendotae) common in the early growth season with Bosmina, Eubosmina, Diaphanosoma (also eutrophic indicators) abundant in summer. We utilized monitoring data collected from 1992 to 2010 by the New York State Department of Environmental Conservation (NYSDEC) as part of the Lake Champlain Long-Term Water Quality and Biological Monitoring Program (LTMP) to determine patterns in zooplankton assemblage structure. These data represent the longest continuous plankton data set available for Lake Champlain. Effective long-term environmental monitoring can be a critical tool for providing advances in science and policy (Lindenmayer and Likens, 2009; Lovett et al., 2007). In the Great Lakes long-term data has been used successfully to understand and interpret patterns in plankton assemblages over time (Barbiero and Warren, in review; Makarewicz, 1993; Makarewicz et al., 1998), providing useful information for lake managers. The purpose of this study was to assess long-term population and community trends in Lake Champlain from 1992 to 2010 to provide information that will inform scientists and managers alike. Among the species introduced to Lake Champlain since 1990 are two taxa that have also impacted the Great Lakes: the zebra mussel (Dreissena polymorpha) and the alewife (Alosa pseudoharengus). Zebra mussels were found in southern Lake Champlain in 1993 with 0380-1330/$ – see front matter © 2011 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research. doi:10.1016/j.jglr.2011.08.006 Author's Personal Copy 50 T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 deep temperate lakes (Harman et al., 2002; Wells, 1970). One reason for the decline seen in native forage fish may be due to alewife competition with other fish species for zooplankton resources (Crowder, 1984). Previous studies have shown that, while feeding, alewives select larger sized zooplankton (Hutchinson, 1971). Gut examinations found the average length of zooplankton consumed by alewife was usually N0.9 mm (O'Gorman et al., 1991). This size selective predation can have a direct negative effect on zooplankton communities in temperate lakes, such as Lake Champlain. In other lakes in the Great Lakes basin alewives select larger sized zooplankton as prey, resulting in size selective impacts on plankton communities (Brandt et al., 2007; Evans, 1992; Harman et al., 2002; Mills et al., 1995; Wells, 1970). For example, in Lake Michigan and Ostego Lake (NY) zooplankton communities shifted from larger to smaller sized zooplankton following alewife invasion, a result of alewife size selective predation (Brandt et al., 2007; Harman et al., 2002). Large copepods and cladocerans decreased in abundance while smaller (b0.9 mm) copepods and cladocerans increased following alewife invasion in Lake Michigan (Wells, 1970). In addition, a decrease a 16 South Lake 14 Northeast Arm Copepoda Main Lake Grand Isle 12 # of taxa veligers found lakewide by 1996 (Smeltzer et al., 2012). Zebra mussel densities peaked in 1996 at most lake sites and remained high through 2010. The impacts of zebra mussels in the Great Lakes are known to include alterations to both phytoplankton and zooplankton (primarily rotifer) populations, increased water clarity, sequestering of energy from the pelagic to benthic zone, and a myriad of indirect food web impacts (MacIsaac, 1996; Thorp and Casper, 2003; Wong and Levinton, 2005). In Lake Champlain the primary impacts observed have been increased water clarity (Smeltzer et al., 2012) and a decline in rotifer biodiversity and abundance (Carling et al., 2004a). Little is known about zebra mussel impacts on phytoplankton in Lake Champlain due to lack of consistent long-term data but studies from other systems have shown shifts in community structure such as an increase in Microcystis following zebra mussel invasion (MacIsaac, 1996). Lake Champlain's phytoplankton has shifted from Aphanizomenon as the pre-dominant cyanobacterium in 1970 to Microcystis in 2005 (Bouyea, 2008), a pattern potentially mediated by eutrophication and/or zebra mussel introduction in the mid-1990s. Alewife was first discovered in Lake Champlain's Missisquoi Bay in 2003, and the Northeast Arm in 2004 and finally the Main Lake during 2005 (Vermont Fish and Wildlife, 2008). The overall impact of this new pelagic fish on zooplankton communities in Lake Champlain remains uncertain. However, it has been shown that once populations become established, they can quickly dominate the forage fish community in Missisquoi Bay 10 8 6 4 2 0 b 16 Cladocera 14 # of taxa 12 10 8 6 4 2 0 c 16 Rotifera 14 # of taxa 12 10 8 6 4 2 19 92 19 93 19 94 19 95 19 96 19 97 19 98 19 99 20 00 20 01 20 02 20 03 20 04 20 05 20 06 20 07 20 08 20 09 20 10 0 Year Fig. 1. Map of Lake Champlain including the 5 study sites. Fig. 2. Trends in taxa richness in a) Copepoda, b) Cladocera, and c) Rotifera in Lake Champlain from 1992 to 2010. Taxa richness data for 1992–2001 are from Carling et al. (2004a). Author's Personal Copy T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 in zooplankton body size was observed in some Lake Michigan taxa following alewife invasion (Wells, 1970). The objective of our study was to use a long-term zooplankton monitoring data set (1992–2010) to determine whether community structure in Lake Champlain has shifted following zebra mussel and alewife invasion in 1996 and 2005, respectively. Long-term comparisons were made for all taxa among the three major zooplankton groups (copepods, cladocerans, rotifers) to detect changes in individual taxa and community composition. Methods Samples were collected from Long Term Monitoring Program (LTMP) sites at the South Lake, Main Lake, Northeast Arm, Grand Isle, and Missisquoi Bay which represent the entire lake from south to north and deep to shallow sites (Fig. 1). Together these sites constitute the longest continuous record of zooplankton data for Lake Champlain and are representative of the lake's physiography (main lake and shallow lake regions). Shallow water sites (South Lake and Missisquoi Bay) ranged in depth from 4 to 10 m contain primarily epilimnetic water during the summer season. Deep water sites (Main Lake, Northeast Arm, and Grand Isle) ranged from 50 to 100 m and stratify during the summer season. Field samples at each study site were collected in July and August (one sample per month) by the New York State Department of Environmental Conservation (Table 1). Plankton were collected using 30 cm diameter, 153 μm zooplankton nets. Vertical net tows were taken during daylight (between 10 am and 3 pm) through the entire water column (lake bottom to surface) with a net retrieval rate of 1 m per second. Samples were preserved in 5% formalin-rose bengal solution in 125 ml bottles and are held in an archived collection at SUNY Plattsburgh's Lake Champlain Research Institute (LCRI). Samples used for this study are from mid-summer (July–August) of each year. From 1992 to 2006 monthly samples were taken. Bi-weekly samples were taken from 2007 to 2010. Plankton identification was completed by taking a 1 ml sub-sample from each sample bottle with a Stensen–Hempel pipette and placing the sample in a sedgewick-rafter cell for identification and counting. All zooplankton were counted in each 1 ml sub-sample and additional sub-samples until a minimum of 100 zooplankton were counted and identified. Samples were counted using a Leica inverted microscope (model DMIL) and appropriate taxonomic keys, primarily Balcer et al., 1984 and the key to Lake Champlain zooplankton (Carling et al., 2004b). Finally, zooplankton total length was measured using a calibrated ocular micrometer at 100× for all common taxa across the study sites between 2002 and 2010 to compare body size before and after alewife invasion. Data analysis Species counts were summarized as July/August abundance (#/m 3) for all taxa present in each site/year. Mean zooplankton abundance (#/m 3) in deep versus shallow sites served as the primary comparison across the study period. Community ordination using non-metric multidimensional scaling (NMS) was performed on a relative abundance zooplankton species by sample (site/year) matrix using PC ORD software (version 4.25). Canonical Correspondence Analysis (CCA) was used to determine relationships between zooplankton 350000 Copepoda 300000 51 a Cladocera Rotifer Density (# / m3) 250000 200000 150000 100000 50000 0 50000 b Density (# / m3) 40000 30000 20000 10000 0 Fig. 3. Total abundance (#/m3) for major zooplankton groups in a) shallow and b) deep sites in Lake Champlain from 1992 to 2010. Please note scale differences between deep and shallow sites. Author's Personal Copy 52 T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 abundance and environmental variables (chloride, chlorophyll a, secchi depth, total nitrogen and total phosphorus). All variables used for CCA were July/August means for each study site/year. To compare assemblage structure all taxa were rank ordered within each site/year and summarized as mean rank in shallow and deep water sites within three time periods (pre-zebra mussel: 1992–96, post-zebra mussel: 1997–2004, and post-alewife: 2005–2010). Kendall's w statistic was used to compare assemblage structure (rank order) between the reference period (1992–1996) and the other two study periods (1996–2004, 2005–2010) in deep and shallow sites. Body size data among sites were summarized as the lakewide annual mean body length for each taxon in each year. the study period with some increases in Cladocera richness since 2005 (Fig. 2). Long-term patterns in total cladocera, copepod, and rotifer density (#/m 3) illustrate several shifts in assemblage structure from 1992 to 2010 (Fig. 3). Rotifers were the most abundant zooplankton throughout the study period in both deep and shallow lake sites, with higher densities in shallow versus deep sites (Fig. 3). Shallow site densities averaged ~ 140,000/m 3 between 1992 and 96 while rotifers in deep lake sites averaged b 30,000/m 3. Rotifer abundance declined lakewide following 1996, with average densities b5000/m 3 in deep sites and b 20,000/m 3 in shallow sites from 1996 to 2005. Rotifer abundance increased during 2005–2010, primarily in shallow sites where the mean total density increased to ~65,000/m 3. In general, cladocera and copepod total abundance remained similar in deep sites throughout the study period (1992–2010) with much lower densities than rotifers (Fig. 3). Copepod and cladoceran abundance was typically ~5000/m3 in deep sites and ~20,000–40,000/m3 in shallow sites. Cladocera in shallow sites increased in total density following 2005, averaging ~44,000/m 3. Results Species richness for cladocera and copepods remained similar from 1992 to 2010 in both deep and shallow sites (Fig. 2). Rotifer richness ranged from 6 to 13 taxa from 1992 to 96 and declined to less than 6 taxa across all sites from 1996 until 2002 (post-zebra mussel). Rotifers exhibited some recovery in taxa richness at both deep and shallow sites from 2002 to 2010, with 11 taxa found in the South Lake in 2010. Copepod and cladoceran taxa richness remained similar throughout Population abundance trends among common copepods, cladocera and rotifer taxa are presented in Figs. 4–6. Copepods (Fig. 4) Juvenile calanoid Juvenile cyclopoid Leptodiaptomus Acanthocyclops robustus Mesocyclops edax Eucyclops serrulatus 45000 40000 35000 Density (# / m3) Population trends a Diacyclops thomasi Cyclops scutifer 30000 25000 20000 15000 10000 5000 0 12000 b Density (# / m3) 10000 8000 6000 4000 2000 10 20 09 20 07 06 05 04 08 20 20 20 20 20 02 01 00 99 03 20 20 20 20 19 97 96 95 94 98 19 19 19 19 19 93 19 19 92 0 Fig. 4. Copepod abundance (#/m3) from 1992 to 2010 in a) shallow and b) deep sites in Lake Champlain. Please note scale differences between deep and shallow sites. Author's Personal Copy T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 comprised ~ 28% of the total zooplankton abundance during the study period with D. thomasi (8.5%), Leptodiaptomus (5.5%), and Mesocyclops edax (5.2%) as the most common taxa. Copepods remained similar in composition from 1992 to 2005 with total copepod density usually below 20,000 individuals/m 3 in shallow sites and 5000 individuals/m 3 in deep sites (Fig. 4). Copepod species composition shifted following 2005 as D. thomasi increased in both deep and shallow sites. Other taxa, particularly juvenile copepods, declined in abundance over the same time period (Fig. 4). Cladocerans (Fig. 5) comprised ~30% of the total zooplankton abundance for the entire study period with D. retrocurva (9.4%), Bosmina longirostris (9.4%), D. mendotae (3.3%) and Diaphanosoma birgei (2.4%) as the most abundant taxa. Cladocerans showed a high degree of inter-annual variation (boom and bust years) with shallow sites containing higher densities (often N 20,000/m3) compared to deep water sites (b10,000/m3). During 2006–2010 total cladocera density in shallow sites increased to N 35,000/m3 during 4 of the 5 years. Population trends include several taxa which increased in abundance since alewife invasion into Lake Champlain (post-2005), particularly bosminids in shallow water sites (e.g., B. longirostris, Eubosmina coregoni) (Fig. 5). Rotifers (Fig. 6) comprised ~42% of the total zooplankton abundance from 1992 to 2010 with Conochilus (15.7%), Keratella cochlearis (8.7%), Polyarthra (6%), Kellicottia (4.1%), and Asplanchna (3%) the most common taxa. Rotifers suffered a major decline in abundance in both shallow and deep sites in the mid 1990s. Rotifers accounted for N 70% of all zooplankton abundance (#/m 3) in both deep and shallow sites from 1992 to 1996, which declined to 29% in deep/shallow sites during 1997–2005 and recovered to 41/49% in deep/shallow 50000 Density (# / m3) sites respectively in 2005–2010. Rotifers were more abundant in shallow sites with the highest densities in 1992–96, often exceeding 100,000/m 3 in shallow sites and 20,000/m 3 in deep sites (Fig. 6). Between 1996 and 2005 rotifer densities declined, rarely exceeded 25,000/m 3 and 5000/m 3 in shallow and deep sites, respectively. Since 2005 shallow site rotifer densities have shown some recovery, increasing to above 50,000/m 3. Species composition among rotifers has shifted from taxa such as Polyarthra, Kellicottia, and Keratella prior to zebra mussel invasion to predominantly Conochilus after 1996. Some rotifer taxa that were abundant from 1992 to 1996 were not detected again at any of the lake monitoring sites from 1997 to early-mid 2000s. For example, Filinia was collected in 1996 and was not observed again until 2003. Other taxa (Ascomorpha and Gastropus) were absent from all samples from 1996 to 2003. During 2005–2010 recovery is evident among rotifers as several taxa increased in both deep and shallow sites (e.g., Polyarthra, Kellicottia). With the exception of Conochilus the rebound in many rotifer taxa from 2005 to 2010 is concentrated primarily in deep (main lake) sites. Community ordination Community patterns from the NMS ordination are presented in Fig. 7, illustrating shifts in community composition, particularly following the zebra mussel invasion (post-1996). The primary taxa responsible for the shift in community structure following zebra mussel invasion were rotifers. Polyarthra, Kellicottia, and Keratella were dominant community members prior to 1996 with a shift to predominantly Conochilus after 1996. Conochilus and Asplanchna Diaphanosoma Daphnia retrocurva Daphnia mendotae Daphnia juvenile Ceriodaphnia Eubosmina coregoni Bosmina longirostrus 60000 40000 53 a 30000 20000 10000 0 b 12000 Density (# / m3) 10000 8000 6000 4000 2000 0 92 993 994 995 996 997 998 999 000 001 002 003 004 005 006 007 008 009 010 1 1 1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 19 Fig. 5. Cladocera abundance (#/m3) from 1992 to 2010 in a) shallow and b) deep sites in Lake Champlain. Please note scale differences between deep and shallow sites. Author's Personal Copy 54 T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 Polyarthra 250000 a Conochilus Keratella quadrata 200000 Density (# / m3) Keratella cochlearis Kellicottia 150000 Asplanchna 100000 50000 0 45000 b 40000 Density (# / m3) 35000 30000 25000 20000 15000 10000 5000 09 08 07 06 05 10 20 20 20 20 20 04 02 01 00 03 20 20 20 20 20 99 97 96 95 94 93 98 20 19 19 19 19 19 19 19 19 92 0 Fig. 6. Rotifer abundance (#/m3) from 1992 to 2010 in a) shallow and b) deep sites in Lake Champlain. Please note scale differences between deep and shallow sites. were the only rotifers that showed increased abundance in postzebra mussel samples in the ordination. Patterns among rotifer taxa resulted in an overall shift in pre and post-1996 site scores in the NMS ordination across all lake sites. NMS results also indicate that community structure was similar throughout the study period among copepods and cladocerans. Most copepod and cladocera taxa were separated in ordination space into two groups, both of which clustered around the origin (0,0) point of the ordination. This indicates that rotifer assemblage patterns are primarily responsible for changes in ordination site scores. Results from the CCA ordination indicate that there are no strong relationships between zooplankton abundance and physical/chemical environmental variables (Table 1). Variation in zooplankton abundance did not relate to patterns in water quality variables (Chloride, Chlorophyll a, Secchi depth, total Nitrogen and total Phosphorus) with only 8.7% variance explained across three ordination axes. This suggests that these factors are not the primary drivers of community change in the Lake Champlain zooplankton community during the study period, 1992–2010. Community composition: rank order Using rank ordered data we compared community structure between three time periods (pre-zebra mussel, post-zebra mussel and post-alewife) across deep vs shallow sites (Table 2). Rank order assemblage structure differed between the reference period and the other two time periods in both deep and shallow sites (Table 2, Kendall's w p b 0.01). There was a lake-wide decline in rotifer taxa rank order after 1996 (zebra mussel invasion) and a concomitant increase in several copepods (e.g., D. thomasi, Leptodiaptomus) and cladocera. In addition there were shifts among copepods and cladoceran rank order following alewife invasion (2005–2010), notably an increase in D. thomasi from among the lowest ranked taxa in 1992–96 to a top five ranked taxon by 2005–2010. Rotifer taxa that declined in rank position following zebra mussel invasion (post-1996) included Kellicottia, K cochlearis, Keratella quadrata, and Polyarthra in deep water sites and K. cochlearis and Polyarthra in shallow sites. Kellicottia and K. quadrata were uncommon throughout the entire study period in shallow sites. Most rotifers declined to a low rank position in the community from 1997 to 2004 with the exception of Conochilus which was common in both deep and shallow sites from 1996 to 2010. In deep sites several rotifer taxa exhibited an increase in community rank following alewife invasion (2005–10) including Polyarthra, K. cochlearis, and Kellicottia (Table 2). Rank order patterns among cladocerans included higher rank position for E. coregoni, Ceriodaphnia, D. retrocurva and B. longirostris following 1996 as rotifers declined in rank order, particularly in deep sites (Table 2). D. retrocurva was less common in deep water sites from 1992 to 96, illustrating a preference for shallow waters but this trend disappeared in later years with D. retrocurva becoming Author's Personal Copy T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 Year 55 Acanthocyclops Bosmina Diacyclops thomasi Eubosmina Leptodiaptomus Limnocalanus Senecella Tropocyclops 1992-1996 1997-2005 2006-2009 Conochilus Asplanchna D. retrocurva Macrocyclops Eucyclops Diaphosoma Ceriodaphnia Leptodora kindti D. mendotae Chydorinae Ascomorpha Holopedium Cladocera Kellicottia D. longimanus (boxed) Epischura Thermocyclops Keratella quadrata Filinia Ploesoma Polyarthra Synchaeta Rotifers Keratella cochlearis Monostylus (shaded) Trichocera Brachionus Fig. 7. Non-metric multidimensional scaling (NMS) results for all five study sites from 1992 to 2009. Open circles indicate pre-zebra mussel invasion, shaded triangles post-zebra mussel, and open inverted triangles post-alewife invasion. Plot stress value for the two axis ordinations was 12.7 (p = 0.03). Shaded names correspond to rotifers, boxed names to cladocera and no shading or box to copepods. the most common cladoceran in both deep and shallow sites by the late 1990s. E. coregoni and Ceriodaphnia responded to zebra mussel invasion in deep sites by increasing in rank order position. Copepods in general showed increasing rank position in the community following the decline in rotifers (1996), particularly for D. thomasi in deep sites which became the most abundant copepod in Lake Champlain by 2008. Other copepods, notably Tropocyclops and Acanthocyclops robustus declined in rank order after 2005 and alewife invasion into Lake Champlain (Table 2). An analysis of zooplankton body size from 2002 to 2010 revealed a pattern of declining body size in large zooplankton (D. retrocurva, Leptodiaptomus) since alewife invasion (Fig. 8). Rotifers and smaller Table 1 Results of CCA ordination on zooplankton relative abundance and environmental variables (eigenvalues and percent variance explained for each ordination axis). Eigenvalue Variance in species data % of variance explained Cumulative % explained Axis 1 Axis 2 Axis 3 0.044 0.030 0.025 3.9 3.9 2.6 6.5 2.2 8.7 bodied cladocerans and copepods showed little change in body size over the same time period (2005–2010). D. retrocurva and Leptodiaptomus declined in body length from at or above 1 mm prior to 2005 to below 0.90 mm by 2009, indicating that they have been reduced in mature body size following alewife invasion in Lake Champlain. Discussion Community patterns Lake Champlain's zooplankton community has exhibited two shifts in composition in the past two decades, one associated with the zebra mussel invasion (post-1996) and a second following the alewife invasion (post-2005). This has implications for middle food web dynamics in Lake Champlain, most notably the recent decline in larger bodied zooplankton following alewife invasion. Furthermore, these shifts represent modern-day alterations to the lake's zooplankton assemblage when compared to historical lake surveys. D. thomasi and Conochilus are now the pre-dominant copepod and rotifer taxa, respectively, having replaced a mixed assemblage of codominant species including Mesocyclops, Diaptomus and D. thomasi copepods and several rotifers, Keratella and Polyarthra (Meyer and Gruendling, 1979; Muenscher, 1930). Long-term changes in the lake's water chemistry do not explain recent changes in zooplankton Author's Personal Copy 56 T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 Table 2 Mean rank order for abundant zooplankton in Lake Champlain in deep (Main Lake, Grand Isle, Northeast Arm) and shallow (South Lake, Missisquoi Bay) sites. Rank order between 1992 and 96 (reference period) and each subsequent time period (1997–2004 and 2005–2010) are compared using Kendall's w test for both deep and shallow sites. Taxa which exhibit an increase or decrease of N 5 positions in the rank position between time periods are denoted with an arrow (up for increase in rank position and down for decrease). Shallow sites 1992–96 1997–2004 2005–10 0.001 0.015 18.0 9.4 18.8 12.8 ↑ 8.8 7.2 14.0 ↑ 7.9 5.7 9.3 16.4 8.1 6.7 10.8 13.6 13.3 6.2 8.8 6.7 11.8 13.4 11.8 3.9 7.9 16.7 17.5 4.5 18.3 12.7 3.4 ↑ 11.9 14.4 ↓ 13.8 18.0 ↑ 7.7 ↓ 16.5 Kendall's w p value Copepoda Diacyclops thomasi Mesocyclops edax Acanthocyclops Leptodiaptomus Cladocera B. longirostris Eubosmina Ceriodaphnia Daphnia mendotae Daphnia retrocurva Diaphanosoma Rotifera Asplanchna Kellicottia Keratella cochlearis Keratella quadrata Conochilus Polyarthra Deep sites community structure. Zooplankton patterns are more likely explained by biotic interactions associated with invasive exotic species. Post-zebra mussel trends Lake Champlain's zooplankton response to zebra mussel invasion is reflected primarily through increased abundance of Conochilus, which was the predominant rotifer lakewide (with highest abundance at shallow sites) from 1996 to 2010. Prior to 1996 Lake Champlain contained a mix of co-dominant rotifers Keratella, Kellicottia, and Polyarthra (Meyer and Gruendling, 1979; Muenscher, 1930, this study). Since 1996 the lake's rotifer community has shifted to Conochilus as a single dominant taxon with densities approaching 100,000 m 3 in some sites. A concurrent decrease in all other rotifer taxa following 1996 suggests that 1992–96 1997–2004 2005–10 0.001 0.001 10.6 13.3 18.6 11.9 ↑ 4.8 ↑ 7.2 12.9 ↑ 6.0 4.9 7.3 16.6 8.8 3.4 11.3 14.7 10.8 5.3 8.8 7.6 18.9 23.1 11.5 10.2 20.9 4.2 ↑ 13.3 ↑ 18.5 9.1 ↑ 4.9 ↑ 13.7 4.1 12.2 17.8 10.8 4.8 14.1 ↑ 8.3 14.8 12.7 18.8 ↑ 2.4 ↑ 11.6 15.7 4.7 1.7 11.3 9.3 2.6 ↑ 10.1 ↓ 10.5 ↓ 16.3 ↓ 16.3 6.3 ↓ 18.7 9.2 ↑ 6.6 ↑ 10.3 15.9 4.3 ↑ 11.8 these small bodied plankton in Lake Champlain may have lost niche space on a relatively permanent basis following zebra mussel invasion. As noted by Carling et al. (2004a) the decline in rotifers is most likely due to direct zebra mussel filtration (sensu MacIsaac et al., 1992, 1995), which apparently did not impact Conochilus, a colonial species that may be capable of avoiding zebra mussel filtration impacts. Based on colonization of only 1 m of shoreline at a filtration rate of 1 l per day Carling et al. (2004a) determined that a lake-wide zebra mussel filtration impact on rotifers was feasible in Lake Champlain. Limnetic rotifers such as Polyarthra, K. cochlearis, and Kellicottia have shown some recovery since 2005 in the main lake (Fig. 6) indicating that deep limnetic habitats may have served as refugia for these taxa from zebra mussel filtration impacts. In general zooplankton, especially rotifers, were more severely impacted in shallow sites by zebra mussel introduction than deep pelagic sites. Some cladocera and copepod taxa increased (at least in community rank position) following zebra mussel invasion but these trends were not as pronounced as the declines in rotifer abundance and richness. Post-alewife trends Fig. 8. Mean body length for the four largest bodied zooplankton in Lake Champlain from 2002 to 2010. Shaded line indicates 0.9 mm alewife feeding size limit. Our results support previous findings that alewife are size selective predators of zooplankton and can have severe impacts on zooplankton populations within temperate lake systems. In general smaller bodied taxa such as D. thomasi and Bosminid Cladocera (B. longirostris, E. coregoni) have increased in abundance following alewife invasion. In addition, when alewife became widespread in the lake after 2005, the average length for large bodied zooplankton began to decline (Leptodiaptomus, D. retrocurva; Fig. 8). Leptodiaptomus and D. retrocurva body length was at or above known alewife food size limits (0.9 mm) prior to 2005 but both species decreased in average body length below this limit following the introduction of alewife (Fig. 8). Our plausible conclusion is that alewife foraging has resulted in decreased individual body size of these taxa in Lake Champlain. Alewife impacts could have long-term implications for several large bodied copepod taxa in Lake Champlain, primarily Leptodiaptomus, as copepods in general have slow growth rates and a more limited ability to achieve maturity at smaller sizes in the face of size selective predators (Ianora, 1998). This may result in reduced fitness and decreased importance in the community and food web over the long-term for these taxa. Cladocera (particularly Daphnia spp.) Author's Personal Copy T.B. Mihuc et al. / Journal of Great Lakes Research 38 (2012) 49–57 have a more flexible body plan (e.g., helmet cyclomorphosis) which results in the ability to mature at a smaller body size when they encounter size selective predators (Balcer et al., 1984; Stibor, 1992). Cladoceran taxa such as D. retrocurva may be capable of ameliorating the impacts of alewife predation by maturing at a smaller size in Lake Champlain. Conclusion Lake Champlain's zooplankton assemblage has shifted in composition several times over the past two decades. Post-zebra mussel shifts resulted in a decline in rotifer populations lake-wide. Post-alewife shifts in zooplankton abundance and body size has many implications for future shifts in the lake's food web dynamics. These alterations may include reduced food availability for native smelt, and/or decreased predation rates by larger bodied zooplankton on smaller bodied plankton (e.g. rotifers) which in turn could result in cascading effects. Potential new invaders into Lake Champlain, such as the quagga mussel (Dreissena rostriformis bugensis) or spiny waterflea (Bythotrephes cederstroemi) may also represent a similar threat to the lake's middle food web and fishery. Future research should address these potential impacts. Additional biological lake monitoring is also needed, particularly for Mysis relicta which is a key energetic link in Lake Champlain's food web, as well as continued monitoring to extend the nearly 20 year zooplankton data set to detect future trends. Patterns in Lake Champlain illustrate the importance of analysis of long-term biological data sets to detect ecosystem responses to stressors, in this case species invasions. Acknowledgments We thank the New York Dept of Environmental Conservation, especially Rob Bonham, and Lake Champlain Basin Program (funded by USEPA) for supporting the Lake Champlain Long-Term Monitoring Program (LTMP). 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