A cross-lake comparison of crustacean zooplankton communities in the Laurentian Great Lakes, 1997–2016

Journal of Great Lakes Research 45 (2019) 672–690

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Journal of Great Lakes Research journal homepage: www.elsevier.com/locate/jglr

A cross-lake comparison of crustacean zooplankton communities in the Laurentian Great Lakes, 1997–2016☆ Richard P. Barbiero a,⁎, Lars G. Rudstam b, James M. Watkins b, Barry M. Lesht c a b c

GDIT, 1359 W Elmdale Ave, Suite #2, Chicago, IL, USA Department of Natural Resources, Cornell University, Biological Field Station, 900 Shackelton Point Road, Bridgeport, NY 13030, USA GDIT and Department of Earth and Environmental Sciences, University of Illinois at Chicago, 845 W. Taylor St., Chicago, IL 60607, USA

a r t i c l e

i n f o

Article history: Received 19 September 2018 Accepted 24 March 2019 Available online 6 April 2019 Communicated by Joseph Makarewicz Keywords: Zooplankton Cladocerans Copepods Invertebrate predation Fish predation Spatial distribution

a b s t r a c t Spring and summer open-water crustacean zooplankton communities were examined across all five Laurentian Great Lakes from 1997 to 2016. Spring communities were dominated by calanoid (lakes Superior, Huron and Michigan) or cyclopoid (lakes Erie and Ontario) copepods. Volumetric biomass of summer communities increased along an assumed trophic gradient (Superior, Huron, Michigan, Ontario; eastern, central and western Erie), as did dominance by cyclopoids and cladocerans. Over the time series of the study, summer communities in lakes Michigan, Huron and Ontario shifted towards greater dominance by calanoids and greater similarity with Lake Superior. Trajectories of changes were different; however, reductions in cladocerans accounted for most of the change in lakes Michigan and Huron while reductions in cyclopoids and increases in Leptodiaptomus sicilis were behind the changes in Lake Ontario. Shifts in the predatory cladoceran community in Lake Ontario from Cercopagis pengoi to occasional dominance by Bythotrephes longimanus, a species much more vulnerable to planktivory, as well as the appearance of Daphnia mendotae in a daphnid community previously consisting almost exclusively of the smaller Daphnia retrocurva, suggest impacts of reduced vertebrate predation. In contrast, strong correlations between cladocerans and chlorophyll in lakes Michigan and Huron point to the possible importance of bottom-up forces in those lakes. Large interannual shifts in cladoceran community structure in the central and eastern basins of Lake Erie suggest intense but variable vertebrate predation pressure. The zooplankton communities of lakes Huron, Michigan and Ontario may be approaching a historic community structure represented by Lake Superior. © 2019 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

Introduction Crustacean zooplankton are a main conduit of energy from phytoplankton to higher trophic levels in the Laurentian Great Lakes and thus of great interest to both water quality and fisheries managers. The past 20 years have been a period of dramatic change throughout most of the Great Lakes. For example, some parts of the lakes have become more oligotrophic (Barbiero et al., 2012) while others have experienced a resurgence of eutrophication (Michalak et al., 2013). Exotic mussels have expanded into profundal regions of the lakes (Burlakova et al., 2018; Nalepa et al., 2010), and there have been dramatic changes in fisheries in some of the lakes (Clapp et al., 2001; Riley et al., 2008). All of these phenomena can be expected to impact crustacean zooplankton communities. ☆ This paper is dedicated to Dr. Glenn J. Warren, long in service to Great Lakes science, on the occasion of his recent retirement. ⁎ Corresponding author. E-mail address: [email protected] (R.P. Barbiero).

While studies of zooplankton have been conducted on the Great Lakes for over 100 years (e.g., Forbes, 1882, 1891; Marsh, 1895; Smith, 1874), quantitative, multi-lake comparative studies are rare, dated, and have often relied on data generated using different methodologies (Davis, 1966; Robertson, 1966; Sprules and Jin, 1990). A series of surveys were carried out by Canada Centre for Inland Waters in the late 1960s and again in the early 1970s on all lakes but Lake Michigan, using largely (but not entirely) consistent methods. Results from the earlier series of these cruises were reported by Patalas (1972); Watson and Carpenter (1974) presented results on lakes Huron, Erie and Ontario from the later series of cruises. Watson (1974) updated this work with the inclusion of 1974 data for Lake Michigan. Among the more interesting attempts at a multi-lake comparative study of Great Lakes zooplankton was that of Swain et al. (1970), who used a semi-quantitative continuous plankton recorder (Hardy, 1926) to sample transects along lakes Superior, Huron and Michigan in the late 1960s. In spite of these efforts, Robertson (1984) still had reason in the mid-1980s to point out the inability to generalize about spatial and interannual distributions of zooplankton, as most zooplankton

https://doi.org/10.1016/j.jglr.2019.03.012 0380-1330/© 2019 International Association for Great Lakes Research. Published by Elsevier B.V. All rights reserved.

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

studies in the Great Lakes were limited to one lake and typically to a couple of years. Although a number of agencies now generate longerterm zooplankton data series on individual lakes (e.g., Markham and Holeck, 2018; Rudstam et al., 2017; Vanderploeg et al., 2012), these programs remain lake specific. The U.S. EPA Great Lakes National Program Office (GLNPO) Biology Monitoring Program is unique among Great Lakes monitoring programs in that it samples all five lakes on an annual basis. Sampling is conducted by one agency, and samples from each year are analyzed by one laboratory, so analytical methods and taxonomy remain largely consistent both across the lakes and over time. We presented data on zooplankton communities across all five lakes from the first year (1998) in which deep (100 m) zooplankton tows had been analyzed by our program (Barbiero et al., 2001). To our knowledge, this represented the first presentation of comparative zooplankton community data across all five Laurentian Great Lakes taken from a single survey. Most subsequent analyses of this data set have either focused on a limited number of lakes (e.g., Barbiero et al., 2009a, 2014, 2018b) or did not consider community composition (Bunnell et al., 2014) (however, also see Kovalenko et al., 2018). Here we present an analysis of crustacean zooplankton data from 1997 to 2016 from all five Great Lakes, data that represent an internally consistent time series of crustacean zooplankton spanning a period of great ecosystem change across the Great Lakes. Our purpose is primarily descriptive. We first provide an overview of current crustacean zooplankton communities in the lakes using the most recent five years of data from our program. We then evaluate temporal changes in zooplankton communities over the course of our time series in terms of both taxonomic composition and the size distribution of biomass. Finally, we use ordination analysis to assess zooplankton community composition across regions and time, relating the ordination to selected external variables, in particular those related to productivity and/or predation.

673

Methods Samples were collected for zooplankton analysis between 1997 and 2016 during spring (generally April) and summer (generally August) cruises from 72 stations located throughout the main basins of the five Great Lakes (Fig. 1). Vertical tows were taken at each station to a depth of 100-m (or 2 m above the bottom at stations b100 m), using a metered, 153-μm mesh net. These deeper 100-m tows were not initiated by our program until summer of 1997 (Barbiero et al., 2018a). After collection, samples were immediately narcotized with soda water and preserved with sucrose formalin solution (Haney and Hall, 1973) approximately 20 min later. Samples were split in the lab using a Folsom plankton splitter until 200–400 animals were present in a split. Two such splits were counted; rarer animals were counted in two successively less dilute splits. Large organisms such as Cercopagis pengoi and Bythotrephes longimanus were removed prior to splitting and enumerated from the entire sample. All counts were done with a stereoscopic microscope. Sample analyses were completed by four laboratories: Grace Analytical Lab. (1997–1999), University of Wisconsin Superior (2000–2006), University of Michigan (2007–2011) and Cornell University (2012–2016). Both analytical methods and taxonomic references used have remained consistent throughout the period of our study. Crustacean taxonomy largely followed Balcer et al. (1984); other sources consulted included Hudson et al. (1998), Brooks (1957), Evans (1985) and Rivier (1998). Because of difficulties in the assignment of bosminids to species (De Melo and Hebert, 1994), three categories for this group had been used prior to 2012: Bosmina longirostris, Eubosmina coregoni, and Bosmina spp. for individuals with characteristics intermediate between the two genera. These categories were, therefore, lumped for long-term analyses. Immature calanoids and cyclopoids were identified to the lowest taxonomic level possible, usually suborder or genus. Nauplii were enumerated in separate counts, and those data will not be reported here.

Fig. 1. Map of GLNPO sampling stations, showing division of lakes into basins. SU = Lake Superior, HU N = northern basin of Lake Huron, HU S = southern basin of Lake Huron, MI N = northern basin of Lake Michigan; MI S = southern basin of Lake Michigan; ON W = western basin of Lake Ontario, ONC = central basin of Lake Ontario ER-E = eastern basin of Lake Erie; ER-C = central basin of Lake Erie; ER-W = western basin of Lake Erie.

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Length measurements were made on the first twenty individuals of each taxon encountered/sample with an electronic tablet or an ocular insert. Dry weights were estimated for each length measurement using length-weight regressions with coefficients derived from the literature, and these estimates were averaged to obtain an average dry weight for the species in that sample. Our program recently underwent a review of regression coefficients used for biomass calculation, as a result of which some values might diverge somewhat from those in previous presentations of this data. Current coefficients are available in Standard Operating Procedure for Zooplankton Analyses (SOP LG403, Revision 07, July 2016). Data are mostly presented in volumetric units (mg DW/m3). Comparisons of average volumetric biomass in the water column across lakes with different maximum depths are problematic because individuals are not evenly distributed throughout the water column. Zooplankton densities in deep water are low, causing average water column values in deep lakes to be lower than those in shallow lakes, even if values in the upper mixed layer are the same. Therefore, recent summary data are also presented in areal units (mg DW/m2) for comparison. However, comparisons among the deeper four lakes are not affected by using whole water column summed values (areal) or average values/m3 because the depths sampled are similar (upper 100 m). Past analyses have shown that differences exist both in the biology and the chemistry of different regions of most of the lakes, corresponding largely to differences in lake-basin morphometry. In addition to the well-known distinctions between basins in Lake Erie (Burns, 1985), differences are also seen between the shallower, more productive southern regions of Lake Michigan and Lake Huron and the deeper, less productive northern regions (Lesht and Rockwell, 1987), as well as the central and western regions of Lake Ontario (Johannsson, 2003; Patalas, 1969). Therefore, for some analyses we allocated stations to either the northern or the southern portions of lakes Huron and Michigan, based largely on basin morphometry (Barbiero et al., 2012), and to the central and western regions of Lake Ontario, roughly divided by the Scotch Bonnet Ridge (Barbiero et al., 2014). This allocation is illustrated in Fig. 1. Because spatial variability in Lake Superior was low, whole-lake averages were used for that lake. Overall monotonic temporal trends in the biomass of major zooplankton groups (Cladocera, Cyclopoida, Calanoida) were assessed using Spearman rank correlations between basin-averaged biomass and year (Gauthier, 2001; Yue et al., 2002). Unlike linear regression, this non-parametric test does not assume a constant relationship between the two variables tested, a condition unlikely to be the case here. This analysis did not take into account possible autocorrelation. Because of its special interest as an indicator of oligotrophy and a historical dominant in the Great Lakes (Gannon and Stemberger, 1978; Robertson, 1966), the large, deep-living calanoid Limnocalanus macrurus was split out from the rest of the calanoids in this analysis, as well as in most presentations of the data. In addition, given its presumed importance in structuring zooplankton communities (Barbiero and Tuchman, 2004; Lehman, 1991; Yan et al., 2001), separate trend analyses were conducted on the predatory B. longimanus. The distribution of crustacean biomass among size groups can lend insights into prey availability for planktivorous fish. Therefore, basinaveraged biomass by size category was calculated for all crustaceans and presented by major taxonomic group. Noting that measurements were made on the first twenty individuals of each taxon/sample, length measurements for each taxon from each station in the basin were increased proportionately to the taxon density at that station relative to the basin-wide average using a random sampling routine, such that the total number of length measurements equaled the basin-wide average density for that taxon. Biomass was then calculated for each length measurement and summed by size category for the different taxonomic groups. Patterns in zooplankton community composition across the lakes were explored with the use of non-metric multidimensional scaling

(nMDS) analysis (Clarke and Warwick, 2001). Basin-wide averages were used in all cases except Lake Superior, in which case lake-wide averages were used. Analyses were restricted to the summer survey due to low species richness in the spring. A Bray-Curtis similarity matrix based on square root-transformed biomass values was used as input for the ordination. In cases where copepodites had not been identified to species (e.g., diaptomid copepodites), for nMDS analyses their biomass was allocated proportionately to constituent species on the basis of adult biomass. Because B. longimanus is thought to play a large role in structuring zooplankton communities in the Great Lakes (Barbiero and Tuchman, 2004; Bunnell et al., 2011; Lehman, 1991; Vanderploeg et al., 2012), this species was excluded from the ordination and used instead as an external explanatory variable. It should be noted, however, that due to its relatively low biomass, axis scores for ordinations with and without B. longimanus were virtually identical. To help identify the external factors potentially influencing zooplankton community structure, Pearson product-moment correlations were calculated between axis scores for each point and a number of environmental variables, as well as B. longimanus biomass as noted above. Environmental variables included average April–July surface chlorophyll a, as estimated by remote sensing using the GLF algorithm (Lesht et al., 2013, 2016), chlorophyll a concentrations at the deep chlorophyll maximum (DCM), spring and summer total phosphorus and summer Secchi depth. Average April–July chlorophyll a concentrations were used to provide an index of production up to the point of our August surveys. Analytical methods for total phosphorus are provided elsewhere (Barbiero et al., 2018b). DCM concentrations were measured as in vivo fluorescence from vertical casts taken at each station during the summer survey with a SeaBird CTD (conductivity, temperature, depth) probe equipped with a fluorometer. In addition, as an indication of the thermal environment crustacean communities had been exposed to prior to the time of sampling, average surface temperatures for the period July 15 to August 15 were calculated for offshore regions of each basin (lake for Lake Superior) from the daily Great Lakes Environmental Analysis (GLSEA) fields (Schwab et al., 1999) obtained from NOAA/GLERL's Great Lakes Coastwatch program (https://coastwatch. glerl.noaa.gov). The resulting correlation coefficients between these environmental variables and the nMDS axes were plotted against axis scores, and the relationships between environmental variables and ordination axes were represented in ordination space as lines, with the angle of the line indicating the degree of correlation with the two axes, and the length of the line indicating the strength of that correlation. As a further indication of the strength of bottom-up forces in shaping crustacean communities, Pearson product-moment correlations were run between August basin-averaged total crustacean biomass and average April–July chlorophyll. Comparable inter-lake measures of prey fish density are not available, so a direct examination of the association between ordination scores and vertebrate predation pressure was not possible. To provide an indication of differences in species distributions in ordination space, results of the nMDS ordination were plotted with symbols sized according to the square-root transformed biomass of individual taxa. Results Zooplankton status 2012–2016 As a comparative overview of recent biomass and gross taxonomic makeup across the five lakes, lake-wide (basin-wide for Lake Erie) average biomass for our most recent years of data (2012–2016) are presented in Fig. 2; average biomass by species for spring and summer is given in Tables 1 and 2, respectively. Biomass was lower in spring than in summer across all the lakes. Spring volumetric biomass was much higher in the central basin of Lake Erie than in other areas of the lakes. Total zooplankton biomass in the upper 100 m (areal units), in

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

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Fig. 2. Lake-wide (basin-wide for Lake Erie) average volumetric (μg/m3), areal (μg/m2) and relative (%) biomass of major crustacean groups for spring and summer, 2012–2016 in each Laurentian Great Lake. Zooplankton were collected from the shallower of 100 m or 2 m above the bottom; biomass in all subsequent figures is for this depth layer. Error bars represent one standard error for the total biomass estimates. SU = Lake Superior; HU = Lake Huron; MI = Lake Michigan; ON = Lake Ontario, ER-E = eastern basin of Lake Erie; ER-C = central basin of Lake Erie; ER-W = western basin of Lake Erie.

contrast, was highest in the three upper lakes and lowest in the shallow western basin of Lake Erie. All spring communities were dominated by copepods; appreciable cladoceran biomass, consisting mostly of bosminids, was seen only in the central basin of Lake Erie (Fig. 2; Table 1). The relative importance of cyclopoid (mostly Diacyclops thomasi) copepods was higher in lakes Erie and Ontario, while calanoid copepods dominated the three upper lakes. An exception to this was the western basin of Lake Erie, where diaptomid calanoids, in particular Leptodiaptomus sicilis, as well as L. macrurus, contributed a substantial proportion of spring biomass (Table 1). Average summer volumetric biomass for 2012–2016 increased along a putative trophic gradient (Superior, Huron, Michigan, Ontario; eastern, central, and western Erie), with the greatest differences seen between the elevated biomass levels in the western and central basins of Lake Erie and the other regions of the lakes (Fig. 2). Areal biomass (i.e., total biomass in the upper 100 m), on the other hand, was highest in Lake Ontario, followed by Michigan, Superior, Huron and Erie, with the lowest areal biomass seen in the western basin of Lake Erie. Community composition showed a progression from dominance by calanoid copepods in the three upper lakes, through a mixed community with a greater proportion of cladocerans and cyclopoid copepods in Lake Ontario, to cladoceran and cyclopoid-dominated communities in Lake Erie. Composition by major group was similar in the three upper lakes, as was total biomass, which was slightly higher in Lake Michigan than in lakes Huron and Superior. Diaptomid calanoid copepods dominated

these lakes (Leptodiaptomus ashlandi and Leptodiaptomus minutus in Michigan and Huron; L. sicilis in Superior), along with L. macrurus. Lake Ontario was unusual in supporting substantial populations of both cyclopoids and L. macrurus. In Lake Erie, Skistodiaptomus oregonensis and Leptodiaptomus siciloides were the dominant calanoids (Table 2). Diacyclops thomasi was the dominant cyclopoid in all lakes except Erie, which supported high populations of Mesocyclops edax and Tropocyclops prasinus mexicanus as well as a number of rarer cyclopoid species (Table 2). The non-native B. longimanus was the dominant predatory cladoceran across all lakes, except for Lake Ontario (where another nonnative, C. pengoi, as well as the native predators Polyphemus pediculus and Leptodora kindtii, all shared dominance) and the western basin of Lake Erie (where L. kindtii was dominant) (Table 2). Biomass of B. longimanus was approximately an order of magnitude higher in central and eastern Erie than anywhere else in the lakes. Daphnia mendotae was the dominant herbivorous cladoceran in most regions, with Daphnia retrocurva dominant in western Erie and subdominant in Lake Ontario. Bosmina longirostris was prominent in Lake Ontario and Lake Erie. Trends 1997–2016 Lake Superior In both spring and summer, the overall composition of crustacean communities in Lake Superior was the most consistent of our dataset

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Table 1 Average spring lake-wide (basin-wide for Lake Erie) biomass (μg/m3) of crustacean zooplankton taxa from 2012 to 2016 for the Laurentian Great Lakes. Zooplankton were collected from the shallower of 100 m or 2 m above the bottom. + indicates b1 μg/m3. Numbers in parentheses indicate areal biomass (μg/m2). * indicates non-native species. SU = Lake Superior; HU = Lake Huron; MI = Lake Michigan; ON = Lake Ontario, ER-E = eastern basin of Lake Erie; ER-C = central basin of Lake Erie; ER-W = western basin of Lake Erie. Diaptomid copepodites includes the genera Leptodiaptomus and Skistodiaptomus. Cyclopoid copepodites includes the genera Diacyclops, Acanthocyclops, Macrocyclops, Microcyclops and Cyclops.

Calanoida Senecella calanoides Senecella copepodites Limnocalanus macrurus Limnocalanus copepodites Epischura lacustris Epischura copepodites Eurytemora affinis* Eurytemora copepodites Leptodiaptomus ashlandi Leptodiaptomus minutus Leptodiaptomus sicilis Leptodiaptomus siciloides Skistodiaptomus oregonensis Skistodiaptomus pallidus Skistodiaptomus reighardi Diaptomid copepodites Total Calanoida

Cyclopoida Acanthocyclops vernalis Diacyclops thomasi Diacyclops nanus Macrocyclops albidus Microcyclops rubellus Cyclops strenuus Cyclopoid copepodites Eucyclops agilis Eucyclops elegans Eucyclops prionophorus Eucyclops copepodites Mesocyclops edax Mesocyclops copepodites Tropocyclops prasinus mexicanus Tropocyclops copepodites Orthocyclops modestus Paracyclops chittoni Total Cyclopoida

Cladocera Bythotrephes longimanus* Cercopagis pengoi* Leptodora kindtii Bosmina longirostris Eubosmina coregoni Alona spp. Chydorus sphaericus Eurycercus lamellatus Leydigia spp. Daphnia mendotae Daphnia retrocurva Daphnia longiremis Daphnia pulicaria Daphnia spp. Ilyocryptus spp. Macrothrix spp. Holopedium gibberum Latona setifera Total Cladocera

SU

HU

MI

ON

ER-E

ER-C

ER-W

62 5 1332 145

150 55 1255 56 + +

96 6 1172 21

622 133

4

12 3

496 100

+

+ 4

+

2000 1962 4708

3707 1907 2015

+ 177 494

55

271

57 8212 (818,222)

732 10,975 (872,688)

1626

609

6612

299

6 105 4 6 2181

14 166 40 59 14,366

1102 10,296 (1,004,220)

389 2115 (199,073)

7 2313 (101,943)

8 53 14,723 (296,954)

912

1219

2747

3244

12 19,520 +

1015

1272

1107

2426

2953

244 161 166 +

+

2235 (222,737)

+ 2

4

+

1 52 +

1929 (145,027)

2495 (243,886)

3855 (355,792)

5723 (253,756)

23,057 (469,881)

2 +

11 +

7 48

215 3182

22

67 + + 578

10

35

+

7 +

87 (3730)

4085 (82,142)

+ 32 381 269 355 779 1 182 1 176 2773 (20,022)

8 262 1 1 + 5 203 2 + 1 + 492 114 1 + + + 1092 (8079)

+ + 2

1

20 1 +

68

39

+

12 129 13 + + 1 21 370

2 +

+

+

+

3 (270)

92 (6753)

2

+ 42 (3994)

(Fig. 3). In fact, this was the only lake in which no shifts in zooplankton groups were seen over time. Spring biomass was overwhelmingly dominated by just three species, the calanoids L. sicilis, L. macrurus and the cyclopoid D. thomasi, with the former contributing approximately 60% and the latter two slightly b20% each. These contributions varied little from year to year. In summer, over 80% of biomass was contributed by L. macrurus and L. sicilis, with approximately equal contributions from both species (Electronic Supplementary Material

13 (1314)

28 + + + + 575 (4306)

(ESM) Fig. S1). The importance of cladocerans varied from year to year, averaging just b10%, with both D. mendotae and Holopedium gibberum co-dominant cladocerans in most years. Cyclopoids, mainly D. thomasi, made up a relatively small (5%) but constant percentage of summer biomass from year to year. Overall, there was no evidence of change over time; no significant correlations with year were seen for any major taxonomic group in either spring or summer (Table 3).

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

677

Table 2 Average summer lake-wide (basin-wide for Lake Erie) biomass (μg/m3) of crustacean zooplankton taxa from 2012 to 2016 for the Laurentian Great Lakes. Zooplankton were collected from the shallower of 100 m or 2 m above the bottom. + indicates b1 μg/m3. Numbers in parenthesis indicate areal biomass (μg/m2). * indicates non-native species. Column headings and taxonomic notes as in Table 1.

Calanoida Senecella calanoides Senecella copepodites Limnocalanus macrurus Limnocalanus copepodites Epischura lacustris Epischura copepodites Eurytemora affinis* Eurytemora copepodites Leptodiaptomus ashlandi Leptodiaptomus minutus Leptodiaptomus sicilis Leptodiaptomus siciloides Skistodiaptomus oregonensis Skistodiaptomus pallidus Skistodiaptomus reighardi Diaptomid copepodites Total Calanoida

Cyclopoida Acanthocyclops vernalis Diacyclops thomasi Diacyclops nanus Macrocyclops albidus Microcyclops rubellus Thermocyclops crassus* Cyclopoid copepodites Eucyclops agilis Eucyclops prionophorus Eucyclops copepodites Mesocyclops edax Mesocyclops copepodites Tropocyclops prasinus mexicanus Tropocyclops copepodites Total Cyclopoida

Cladocera Bythotrephes longimanus* Cercopagis pengoi* Polyphemus pediculus Leptodora kindtii Bosmina longirostris Eubosmina coregoni Alona spp. Chydorus sphaericus Eurycercus lamellatus Graptoleberis spp. Leydigia spp. Ceriodaphnia spp. Daphnia mendotae Daphnia retrocurva Daphnia longiremis Daphnia lumholtzi* Daphnia pulicaria Daphnia ambigua Daphnia spp. Ilyocryptus spp. Holopedium gibberum Diaphanosoma spp. Latona setifera Sida crystallina Total Cladocera

SU

HU

MI

ON

ER-E

ER-C

ER-W

66 349 10,356 364 74 32

44 479 4969 152 366 157

58 445 10,804 62 427 200

65

96

132

1124 1002

1875 1045

2 50 271

7194

2 111 287 1 94 23,786

1516 273 1211 514 59 444

+ 1 2771

1077 1244 710

1513 668 1699

63 1718

49

149

487

4685 18,699 (1,860,381)

2 9833 19,082 (1,506,926)

7712 23,739 (2,303,030)

3736 18,547 (1,729,368)

1 5441 15,151 (656,620)

23 12,371 39,692 (776,030)

562

476

967

4262

3115

27 878

14 12,166 43 201 118 2

12,438 776 227 847 5998 24,434 (166,329)

685 19 1

8

421

345

551

1345

4225

851

2 +

60 16 1

3 10 +

984 (97,461)

897 (70,261)

6 + 1 + 1525 (149,204)

1617 492 14 5 9468 (425,634)

9523 4422 37 9 15,756 (310,852)

2 12 917 + 3 1 12,230 7142 23 2 21,037 (148,309)

158

428 + + 1 331 6

551 34 24 13 124 3

76 158 222 160 1468 348

4341 +

5992

379

502 1370 37 +

590 571 78 3 3 100

4207 1078 16,129 + 2

68 +

9

5619 (492,906)

2

+ 6 1165 +

2111

11 4400 2722

4023

7514 522

19,910 147 23

142 9992 35,283 51

17 1

+

3 + 3

415 +

251

+

1807 (179,371)

3155 (242,478)

4779 (471,232)

The size distribution of biomass in Lake Superior was distinctly bimodal, with L. macrurus biomass forming a peak between 2.2 and 3 mm, and primarily diaptomid copepods forming a broader peak centered around 1 mm (Fig. 4). Approximately equal biomass resided in the size categories 0.5–1.5 mm and N 2.2 mm, with much less in intermediate or smaller categories. Little change was seen over time.

9

81

46 +

1537 +

2

321

11,112 (955,360)

14,370 (605,303)

27,790 (550,998)

55 2 31 8268 + 4 75,623 (541,044)

Lake Huron Spring communities in Lake Huron were comprised mainly of diaptomid calanoids (L. ashlandi, L. sicilis and L. minutus), with L. macrurus also contributing (Fig. 3). Cyclopoids, primarily D. thomasi, made up a substantial percentage of spring biomass in 1999–2002 and were also seen in 2009–2013, but were notably absent in the

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Fig. 3. Basin-averaged crustacean biomass, by major group, for spring (1998–1999, 2001–2016; upper panels) and summer (1997–2016; lower panels) for each Laurentian Great Lake. Error bars indicate one standard error for total biomass estimates. Spring samples for 2000 were not analyzed. Note difference in scale for central and western Lake Erie summer plots.

intervening years. A marked decline in crustacean biomass was seen in 2004; in both basins, average total spring 2004–2016 biomass was less than half that of 1998–2003. These declines were primarily due to reductions in populations of L. ashlandi, D. thomasi, and also to an extent L. minutus, and resulted in a shift in dominance towards L. sicilis. A significant declining trend was seen in spring calanoid (exclusive of L. macrurus) biomass in both basins (Table 3). Summer communities during 1997 to 2002 were dominated by L. macrurus, D. mendotae and diaptomid copepodites, which combined made up approximately 75% of biomass. The adults of L. sicilis,

L. ashlandi and L. minutus each contributed on average between 2 and 4% to crustacean biomass, while cyclopoid copepodites and adults (mostly D. thomasi) contributed between 5 and 10% during this period. Summer biomass declined dramatically in 2003, a year before the decline seen in spring, and has been relatively stable since 2005; from 2003 onwards, total crustacean biomass has averaged 44 and 29% of pre-2003 levels in the northern and southern basins, respectively (Fig. 3). The declines were mostly due to a reduction in cladocerans; this was most clearly seen in the northern basin where the dominant cladocerans, D. mendotae and bosminids, virtually disappeared in 2003

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

679

Table 3 Results of non-parametric Spearman rank correlations between zooplankton biomass, by major group, and year. Significant correlations (α = 0.05) are shown in bold. Cladocera

Spring Superior Huron North South Michigan North South Ontario Central West Erie East Central West Summer Superior Huron North South Michigan North South Ontario Central West Erie East Central West a

Calanoidaa

Cyclopoida

L. macrurus

B. longimanus

r

P

r

P

r

P

r

P

r

P

−0.31

0.205

−0.10

0.711

0.26

0.285

0.26

0.301

–

–

−0.10 −0.32

0.680 0.824

−0.45 −0.58

0.059 0.011

−0.48 −0.51

0.042 0.031

−0.12 −0.26

0.632 0.281

– –

– –

−0.05 0.29

0.824 0.241

−0.18 −0.35

0.461 0.146

−0.36 −0.59

0.143 0.010

0.20 −0.23

0.431 0.343

– –

– –

−0.38 −0.24

0.120 0.330

−0.50 −0.72

0.035 b0.001

0.52 0.40

0.025 0.102

−0.04 −0.22

0.850 0.378

– –

– –

0.57 0.54 0.14

0.014 0.020 0.574

0.53 0.35 −0.59

0.023 0.153 0.010

0.81 0.84 −0.68

b0.001 b0.001 0.002

0.49 0.33 −0.57

0.038 0.178 0.013

– – –

– – –

−0.24

0.302

−0.26

0.266

−0.06

0.792

−0.02

0.937

−0.14

0.551

−0.64 −0.82

0.003 b0.001

−0.70 −0.63

b0.001 0.003

−0.28 −0.18

0.225 0.437

−0.44 −0.58

0.049 0.008

−0.41 −0.37

0.075 0.105

−0.79 −0.78

b0.001 b0.001

−0.32 −0.04

0.167 0.856

−0.15 −0.33

0.525 0.159

0.52 −0.46

0.019 0.039

−0.27 −0.30

0.244 0.191

−0.32 −0.21

0.161 0.371

−0.50 −0.67

0.023 0.001

0.60 0.56

0.005 0.011

0.25 0.24

0.275 0.302

0.60 0.56

0.006 0.010

−0.03 −0.26 0.15

0.911 0.266 0.529

0.08 −0.28 −0.12

0.726 0.225 0.599

−0.33 0.10 0.76

0.164 0.663 b0.001

0.09 0.29 0.50

0.710 0.208 0.025

0.10 −0.07 0.25

0.678 0.753 0.277

Excluding Limnocalanus macrurus.

(ESM Fig. S1). Other taxa have also declined; B. longimanus biomass in 2003–2016 was about half that of 1997–2002, while both cyclopoid and L. macrurus biomass showed significant downward trends, as did cladoceran biomass (Table 3). Calanoids exclusive of L. macrurus showed no overall trend, although both L. ashlandi and L. minutus declined, remaining depressed from approximately 2003 to 2009 before rebounding somewhat (ESM Fig. S1). The decline in L. ashlandi in particular followed that of D. thomasi; biomass of the two species were positively correlated in both basins (North: r = 0.56, P = 0.01; South: r = 0.61, P = 0.004). A distinct shift in biomass size distribution was seen in Lake Huron corresponding to the species shifts in 2003 noted above. Biomass was initially distributed with roughly three peaks: copepod biomass centered around 1 mm, biomass associated with Daphnia concentrated between roughly 1.5 and 2.0 mm, and L. macrurus biomass between 2.5 and 3 mm (Fig. 4). This changed abruptly in 2003, coincident with the loss of cladocerans in the lake, resulting in a strongly bimodal distribution of biomass much like Lake Superior. It is interesting to note that the loss of smaller individuals was due not only to the disappearance of bosminids and cyclopoids noted above but also to a reduction in smaller diaptomid copepodites. Since 2005 approximately equal amounts of biomass in the northern basin have resided in the 0.5 to 1.5-mm individuals and N2.2-mm individuals, as is the case in Lake Superior. In the southern basin, in contrast, substantially more biomass is still contributed by 0.5 to 1.5-mm individuals than by larger (N2.2 mm) individuals. Lake Michigan Species composition of spring communities in Lake Michigan was similar to that of Lake Huron, although similarly dramatic declines were not seen (Fig. 3). A significant decline was only noted in calanoids (exclusive of L. macrurus) in the southern basin (Table 3). As was the case in Lake Huron, populations of D. thomasi were low in the middle

years of our time series; 2007 and 2008 stand out as particularly low years for this species in Lake Michigan. Summer communities in Lake Michigan were similar to those in Lake Huron; most biomass was contributed by L. macrurus, D. mendotae and diaptomid copepodites. As in Lake Huron, biomass declined after 2002; average 2003–2016 biomass in the north and south was 73% and 54% of pre-2003 values, respectively. Despite broad similarities, some notable differences were seen between the two lakes and indeed within the two basins of Lake Michigan. The reduction in cladoceran biomass in Lake Michigan, while significant (Table 3), was not as pronounced as in Lake Huron. Interestingly, 2010 and 2012 were years of higher cladoceran biomass in both Lake Huron and Lake Michigan. Whole-lake cladoceran biomass has been seen to be strongly correlated in the two lakes (Barbiero et al., 2018b). As in Lake Huron, Lake Michigan has experienced a marked shift towards greater dominance of calanoids; this was augmented in the northern basin by a sustained and significant increase in L. macrurus biomass (ESM Fig. S2; Table 3). In contrast, L. macrurus showed a significant downward trend in the southern basin, although the limited magnitude of the decline, coupled with the relatively stable biomass of L. sicilis, resulted in an increased proportion of calanoids in that basin as well. Summer cyclopoid copepod biomass showed substantial declines in Lake Michigan, roughly paralleling those of Lake Huron, with populations at very low levels by 2005. However, unlike Lake Huron, summer populations rebounded in 2010, and thus no overall trend was seen in Lake Michigan (Table 3). Populations of D. thomasi showed some coherence with those of bosminids, with peaks (e.g., 1999, 2011, 2013) and troughs (2005–2010) in the two groups often, but not always, coinciding. Changes in size distribution in Lake Michigan since the mid-2000s, while broadly similar to those in Lake Huron, differed in a few notable ways. The reduction in cladocerans and concurrent increase in L. macrurus in the northern basin from 2003 on resulted in a greater

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R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

Superior 6 8

6

Huron North 8

1997

6

1997

10

1998

10

10

8

1998

6 6 6

14

2002

6

2003

12

6

6 6 6

Biomass (mg m3)

6

12 8

2005

6 6

2007

6

2008

8

2007

6

2008

6

6

2004 8

2005 6

2006

8

2007

2007

10

8

6

2016

0 0.0

4 1.0

2.0

3.0

6

Size (mm)

2005

4

2012

2006

2009

2009 8

2010

6

2010

2007

2013 4

6

2004

2008 10

2008

2011 8

6

2003

2006

2010

2014 2015

2005

2009

6 6

2002

2004

10 14

2012 2013

2003

2003

2006

2010 6

8

2002

8

4

2011

8

2001

2005

2009

4 4

2001

2004

8

6

4

12

16

6 6

2000

2003 12

2006

4 8

2000

2002

2004

6 8

2001 8

2001 2002

1999

2000

1999

2000

8 6

1999 12

6

1998

1999

2000 2001

1997

1998 12

6 6

Michigan South 10

1997

1998

1999 10

6

Michigan North

Huron South 16

1997

6

2014

6

2015 2016

0 0.0

6

1.0

2.0

3.0

6

12

2011

2011

4 8

2012 6

2013

6

2014

2012

10

2008 2009 2010

2011

2013

Size (mm) 8

6

2015

8 6

6

2014

6

2015

2012 2013

2016 6

0 0.0 Limnocalanus Calanoids Cyclopoids Predatory Cladocerans Daphnia Non−daphnid Cladocerans

6 1.0

2.0

Size (mm)

3.0

2014

2016 4

0 0.0

1.0

2.0

3.0

6

2015 2016

Size (mm) 0 0.0

1.0

2.0

3.0

Size (mm) Fig. 4. Distribution of summer crustacean biomass, by major taxonomic group, among size classes for lakes Superior, Huron and Michigan, 1997–2016.

relative concentration of biomass in larger sizes than was seen in any other lake, including Lake Superior (Fig. 4). A high degree of interannual variability was seen in both basins in intermediate (0.5–1.5 mm) sizes, a range mostly made up of diaptomid copepods. This was more

pronounced in the northern basin. In the more productive southern basin, the loss of cladocerans was not as pronounced as it was in either the northern basin or in Lake Huron, nor was there a sustained increase in L. macrurus, as occurred in the northern basin. As a result, less

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

biomass resided in larger sizes, and more in intermediate sizes, relative to the northern basin. Lake Ontario Spring communities in Lake Ontario were dominated by a mix of cyclopoid and calanoid copepods (Fig. 3), with the latter consisting of L. macrurus, L. sicilis, S. oregonensis and L. minutus, and the former largely D. thomasi. A shift towards greater calanoid biomass was apparent in 2005, due to increases in L. macrurus, and somewhat later in L. sicilis and L. minutus. This was accompanied by decreases in D. thomasi, which were statistically significant in both regions of the lake (Table 3) in spite of recovery of this species in the later years of our data series. Interestingly, cyclopoid biomass was low in the middle years of the data series, a pattern also seen in Lake Michigan and Lake Huron. Summer communities in Lake Ontario during the early part of our time series were dominated by the cyclopoid D. thomasi, cladocerans represented by bosminids and D. retrocurva, and the calanoid L. macrurus (Fig. 3). Predatory cladocerans were represented mostly by C. pengoi at this time (Fig. S3). A shift occurred in 2004 with a reduction in cyclopoid populations and a greater proportion of biomass contributed by cladocerans and calanoids. This was most pronounced at western stations, where the biomass contribution of D. thomasi decreased from approximately 50% in 1997–2003 to b15% in 2004–2016; this decline was accompanied by an increase in absolute L. macrurus biomass. The decline in cyclopoids was statistically significant in both regions of the lake (Table 3). While L. macrurus was the second and third most dominant species by biomass from 1997 to 2003 (at western and central stations, respectively), it has been dominant in both regions since 2004. A further shift occurred in 2008, marked by increases in L. sicilis, a shift in the predatory cladoceran community towards occasional dominance by B. longimanus, and the appearance in substantial numbers for the first time of D. mendotae as well as H. gibberum (ESM Fig. S3). While the increase in L. macrurus has been sustained, the makeup of the cladoceran community, as well as biomass contributed by D. thomasi, has varied notably in recent years. From 1997 to 2003, biomass in Lake Ontario was strongly bimodally distributed; most biomass was concentrated in smaller (b1.5 mm) individuals and was constituted mainly of bosminids, cyclopoids, and the smaller daphnid D. retrocurva (Fig. 5). A dramatic shift in biomass size distribution occurred with the decrease in cyclopoids after 2003 and the subsequent increase in L. macrurus. This was most pronounced at western stations where, after 2005, roughly equal amounts of biomass were contributed by the 0.5–1.5 and N2.2-mm size categories. The further shift from D. retrocurva to the larger D. mendotae, as well as the increase in the relatively large diaptomid L. sicilis, resulted in a more even distribution of biomass across sizes in the later years of our time series, although this varied substantially from year to year. Lake Erie Opposite patterns in spring biomass were seen in the western basin and the central and eastern basins of Lake Erie (Fig. 3). The western basin of Lake Erie experienced the most dramatic decline in spring crustaceans of any region of the lakes; average 2004–2016 biomass was b25% of that in 1998–2003. These declines may be partly due to the simultaneous reductions seen in Lake Huron and a consequent reduction in wash-through into the western basin. In the central and eastern basins of Lake Erie, spring biomass varied from year to year; while absolute biomass densities differed between these two basins, patterns of biomass were remarkably similar (Fig. 3). Increasing trends were seen in a number of groups, most notably calanoids (primarily S. oregonensis) and cladocerans (primarily bosminids) (Table 3). Summer crustacean communities in the western basin of Lake Erie showed a high degree of inter-annual variability, with little apparent overall trend in total biomass (Fig. 3). While volumetric biomass tended

681

to be higher in this basin than in other areas of the Great Lakes, the lowest biomass value recorded in our time series was also found in the western basin (2001). Daphnia biomass, in particular that of D. retrocurva, varied substantially from year to year (ESM Fig. S4), being completely absent some years and dominating in others years. The western basin was unique in that L. kindtii was the dominant predatory cladoceran, attaining substantial biomass in some years. The basin was also unique in that M. edax, rather than D. thomasi, was the dominant cyclopoid; this species was the second biggest contributor of biomass overall. Calanoid copepods showed some indication of greater biomass in later years, a trend which was statistically significant (Table 3). Substantial interannual variability was also seen in the other basins of Lake Erie, though not to the extent of that in the western basin. Makeup of the cladoceran community differed substantially between the western and the central and eastern basins. Daphnia mendotae, rather than D. retrocurva, was the dominant cladoceran in the latter two basins, while B. longimanus was the dominant predatory cladoceran, with a biomass substantially higher in the central and eastern basins of Lake Erie than in any other area of the lakes. While some cooccurrence was seen between B. longimanus and L. kindtii in the central basin, high densities of L. kindtii tended to occur only during years of low B. longimanus (ESM Fig. S4). A similar pattern was not seen in the eastern basin, where peaks in the two species often coincided. Calanoid copepods contributed a higher proportion of biomass to the central and eastern basins, compared to the western basin. Interestingly, there was little relation between spring and summer communities; years of high spring biomass did not coincide with those of high summer biomass (Fig. 3), while increases seen in crustacean groups in spring were not seen in summer (Table 3). Size distribution of summer biomass in the western basin of Lake Erie differed from all other lakes/basins in being largely unimodal (Fig. 5). Limnocalanus macrurus, which accounted for the concentrations of biomass in large individuals in the other lakes, was absent from this basin (except in spring), while the dominant daphnid was the smaller D. retrocurva. The western basin was also unusual in having substantial biomass in extremely large (N3.5 mm) individuals, in this case mostly L. kindtii. The central and eastern basins differed from the western basin in occasionally having substantial biomass in large (N2 mm) size categories, which sometimes, but not always, coincided between the two basins. Unlike the other lakes, these large individuals were D. mendotae, rather than L. macrurus. When present, these were often accompanied by substantial biomass in extremely large (N3.5) individuals, in this case B. longimanus. In contrast, years lacking these large individuals of D. mendotae tended to have larger biomass in bosminids and cyclopoids, perhaps indicating higher levels of vertebrate predation. Ordination of summer samples Ordination analysis, based on square root transformed basinaveraged summer volumetric biomass, indicated that all lakes supported distinct communities, with the notable exception of lakes Huron and Michigan which showed substantial overlap (Fig. 6). Communities in Lake Erie were the most distinct, being widely separated in the ordination space from all other lakes. Within Lake Erie, communities in the western basin were distinguished from those in the central and eastern basin, while the latter two showed substantial overlap. Overall variability in community composition was highest in Lake Erie, judging from the area of ordination space occupied by samples from that lake. Lake Superior, in contrast, showed very little variability, occupying a small portion of the ordination space furthest removed from western Lake Erie samples. Recent communities in Lake Huron and Lake Michigan showed greater similarity with those in Lake Superior, through a reduction in both axis 1 and axis 2 scores, although there was no actual overlap in the ordination between lakes Huron and Michigan and Lake Superior. Recent communities in Lake Ontario, in turn,

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R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

Ontario West 10 14 24

20

1998

12 14 12 8 8 10 8 14

24 2000

14 8 Biomass (mg m3)

8 8 8 10 8

14

8

1999

10

2000

12 8

14

2002

14

2003

24

2004

18

2001

20 1998

26

16

2000

16

2001

8

2007

8

2008 2009

8

2010

8 8

2011

18

2012 2013

8

2014

8

2015

8

2016

0 0.0

8

1.0

2.0

Size (mm)

3.0

8 8

14

2005 2006

32

2007

12

1999

12

2000

10 2001

8 8

2002

12

2003 22

2004

10

2002

2003 14

8 1998

1999

2005 2006

8

1997

8

22 2002

Erie East

Erie Central 12

1997

1998

2001

8 8

30

1997

1999 12

8

Erie West

Ontario Central 12

1997

12 2003 8

2004

8 18

2005 12

2006

18

2008

12

2004

18 2005 8

2006

8

2009 2010

10 32

2011

10

2007

26

2008

8

2007

8

2008

10

1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010 2011

2012 2013 2014 2015 2016

0 0.0

2012 2013

16

2014

16

2015 52

1.0

2.0

1.0

2009

2.0

3.0

Size (mm)

2009 32

2016

0 0.0

1997

2010

2010

3.0

Size (mm) 42

24

2011 30

10 34

2013

18

16 Limnocalanus Calanoids Cyclopoids Predatory Cladocerans Daphnia Non−daphnid Cladocerans

18

2012

2012

10

18

2011

2014

10 12

2015

2013 2014

2015 2016

0 0.0 2016

0 0.0

1.0

2.0

3.0

Size (mm)

1.0

2.0

3.0

Size (mm) Fig. 5. Distribution of summer crustacean biomass, by major taxonomic group, among size classes for lakes Ontario and Erie, 1997–2016.

have become more similar to those of lakes Michigan and Huron, particularly from the early portion of our time series, largely through an increase in axis 2 scores.

Correlations between external variables and ordination axes were all highly significant (P b 0.001 for at least one axis). Variables associated with trophic state (summer Secchi depth, April–July chlorophyll a,

R.P. Barbiero et al. / Journal of Great Lakes Research 45 (2019) 672–690

683

compared with early ones, also contributed to the direction of this gradient. Average surface temperatures were strongly correlated with axis 1 scores, and as such were associated with the extreme separation between the western basin of Lake Erie and Lake Superior. Bythotrephes longimanus biomass was strongly associated with a gradient orthogonal to that of the trophic gradient. Extremes were represented by central and eastern Erie on the one hand, and early Lake Ontario on the other. More recent Lake Ontario samples exhibited both increases in axis 2 scores and decreases in axis 1 scores, suggesting associations with both increasing B. longimanus and decreasing DCM concentrations. Species distributions

Fig. 6. Ordination of basin-wide (lake-wide in the case of Lake Superior) average August crustacean communities for 1997–2016 using non-metric multidimensional scaling. Each symbol corresponds to a basin/year. Lighter symbols for Lake Huron and Lake Michigan indicate samples from 2004 to 2016; lighter symbols for Lake Ontario indicate samples from 2008 to 2016. Inset plot indicates correlations between select external variables and axis scores, with the angle of the line indicating the degree of correlation with the two axes, and the length of the line indicating the strength of that correlation. DCM = chlorophyll a concentration at the deep chlorophyll maximum; °C = average surface temperature from 15 July to 15 August; Chl = average surface chlorophyll a, estimated from remote sensing data, for April through July; Secchi = summer Secchi depth; TPsp and TPsu = spring and summer total phosphorus, respectively. Circle corresponds to r = 1.0. Gray lines are drawn orthogonal to a generalized trophic gradient derived from average correlations of Chl, TPsp, TPsu and inverse of Secchi with the ordination axes.

spring and summer TP) defined a gradient of decreasing trophy extending from the lower right of the ordination to the upper left. The following rough groupings were separated along this gradient, from low to high trophy: Lake Superior/recent Lake Huron and Lake Michigan; early Lake Michigan and Lake Huron and recent Lake Ontario; early Lake Ontario and central and eastern Lake Erie; and western Lake Erie (Fig. 6). A strong relationship existed between basin-averaged total summer crustacean volumetric biomass across all lakes and April–July surface chlorophyll (Pearson product-moment correlation: r = 0.54, P b 0.001, n = 190). Most of this relationship with chlorophyll, however, was due to inter-lake differences; when tested separately, only northern (r = 0.78, P b 0.001, n = 19) and southern (r = 0.81, P b 0.001, n = 19) Lake Huron and southern Lake Michigan (r = 0.76, P b 0.001, n = 19) showed significant correlations between chlorophyll and total crustacean biomass. Similarly, when analyses were restricted to herbivorous cladocerans, a strong overall relationship was seen with chlorophyll (r = 0.62, P b 0.001, n = 190), but when tested separately, significant correlations were found only in Lake Huron (r = 0.74, r = 0.84, North and South, respectively; P b 0.001, n = 19) and Lake Michigan (r = 0.62, r = 0.84, North and South, respectively; P b 0.001, n = 19). Correlations between ordination axes and DCM concentrations implied a gradient somewhat different from that of other trophic staterelated variables. This was probably due in part to the absence of a DCM in the unstratified western basin of Lake Erie. Higher DCM concentrations in Lake Ontario, compared to all other lakes, as well as reductions in those concentrations in recent Lake Ontario samples

To help visualize species distributions across both lakes and time periods, ordination results with symbols sized on the basis of square roottransformed volumetric biomass of selected species are shown in Fig. 7. Among calanoids, Senecella calanoides had the most restricted distribution, being almost entirely limited to lakes Superior, Huron and Michigan. Distributions of L. macrurus and L. sicilis were very similar; both were commonly found in all lakes except Lake Erie, though L. sicilis differed from L. macrurus in its relative scarcity in earlier Lake Ontario samples. Leptodiaptomus ashlandi was confined largely to lakes Michigan and Huron and in some eastern and central basin Erie samples, while the similar diaptomid L. minutus was also found throughout Lake Erie as well as in recent Lake Ontario samples. Epischura lacustris was found throughout the lakes, although rarely in early Lake Ontario samples. Skistodiaptomus oregonensis was found in greatest abundance throughout Lake Erie and in limited numbers in lakes Ontario, Michigan and Huron, while L. siciloides and the non-native Eurytemora affinis were largely confined to the western basin of Lake Erie. Among cyclopoids, D. thomasi was widely distributed throughout all lakes, with the notable exception of the western basin of Lake Erie. Tropocyclops prasinus mexicanus was found primarily in Lake Erie and occasionally in lakes Huron and Michigan, while M. edax was prominent in all basins of Lake Erie but rare elsewhere. The general distribution of calanoid species can thus be summarized in the following sequence, from regions of lower to higher trophic state: S. calanoides → L. sicilis/L. macrurus → L. ashlandi → L. minutus/E. lacustris → S. oregonensis → L. siciloides/E. affinis. Among cyclopoids, a truncated progression was seen from the nearly ubiquitous D. thomasi, to T. prasinus mexicanus to M. edax. Distributions of cladoceran species exhibited substantially different patterns than those of copepods and seemed more dependent upon the identity of the dominant predatory cladoceran. Bythotrephes longimanus was the most widely distributed predatory cladoceran, dominating most regions/periods except western Lake Erie and early Lake Ontario samples. Leptodora kindtii was found in greatest numbers in the western basin of Lake Erie, where it was the overwhelmingly dominant predatory cladoceran, and was also seen in the other two basins of that lake as well as in Lake Ontario. The degree of co-occurrence between L. kindtii and B. longimanus varied from lake to lake. In the western basin, approximately a third of the samples containing either species contained both; these percentages were 44% and 86% for the central and eastern basins, respectively. In Lake Ontario, where B. longimanus was much less frequent, 42% of samples containing either species contained both, while in Lake Michigan this was 26%. Leptodora kindtii was absent for the most part from Lake Huron and Lake Superior. Cercopagis pengoi was largely restricted to Lake Ontario samples, though it was occasionally found in Lake Michigan and Lake Erie. Polyphemus pediculus, the least common cladoceran predator, was mostly restricted to Lake Ontario where it occasionally was the dominant predatory cladoceran by biomass. The two main herbivorous cladoceran species D. retrocurva and D. mendotae showed largely inverse distributions in ordination space, with the latter overlapping to a substantial degree with B. longimanus and the former showing virtually no overlap with that species (Fig. 7).

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Fig. 7. Ordination of basin-wide (lake-wide in the case of Lake Superior) average August crustacean communities for 1997–2016 using non-metric multidimensional scaling, with symbols sized by square root-transformed biomass of selected taxa. Time periods for lakes Huron, Michigan and Ontario are as in Fig. 6. Black dots indicate taxon was not found in that basin/year.

Daphnia retrocurva was most abundant in the western basin of Lake Erie as well as in early Lake Ontario samples, while D. mendotae was the dominant daphnid in most other regions/periods. Bosminids were widely distributed, although as noted this group most likely includes a number of species. Populations of this group were lowest in Lake

Superior and in later Lake Michigan and Lake Huron samples. Holopedium gibberum was unusual in being found most frequently in lakes Superior, Ontario and Huron, the only species with such a distribution. It was one of the few species to be found in Lake Huron but rarely in Lake Michigan.

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Discussion In the 20 years of this study, offshore zooplankton communities have undergone dramatic changes in several of the Great Lakes. Among the most notable of these has been the shift towards calanoid copepoddominated communities in lakes Ontario, Michigan and Huron. During the height of eutrophication in the late-1960s, Patalas (1972) had pointed out a pattern of diminishing proportions of calanoids in the Great Lakes, accompanied by increasing predominance of cyclopoids and cladocerans, when zooplankton communities were viewed along a gradient of increasing trophy from Lake Superior to the western basin of Lake Erie. Since Patalas' (1972) study, broad regions of the lakes have experienced decreases in nutrient levels as a result of phosphorus abatement programs (Beeton et al., 1999). More recently, lakes Michigan and Huron have shown signs of increasing oligotrophication (Barbiero et al., 2012; Evans et al., 2011), perhaps due in part to impacts of dreissenid mussels (Barbiero et al., 2018b; Fahnenstiel et al., 2010). At the same time, most planktivorous fish populations in the lakes have seen declines since the late 1980s (USGS, 2017), including the almost complete disappearance of alewife (Alosa pseudoharengus) from Lake Huron in 2003 (Riley et al., 2008). There is evidence that another major planktivore, the mysid shrimp Mysis diluviana, has also declined since the 1980s (Jude et al., 2018). The current study has shown that differences in community composition among the deeper four lakes have diminished greatly in the past 20 years, moving communities in lakes Huron, Michigan and Ontario closer to the calanoid-dominated community seen in Lake Superior. The reductions in cladocerans in lakes Huron and Michigan, and consequent increased importance of calanoid copepods, have resulted in communities whose total biomass, composition, and size distribution of biomass have very closely approached that of Lake Superior. The increased concentration of biomass in large, deep-living calanoids has also likely altered its depth distribution. This can have important consequences for trophic transfers, given both size selectivity of many planktivores and differences in their vertical distribution, and thus potential overlap with prey. In Lake Ontario, the reductions in cyclopoids and increased importance of the cladocerans B. longimanus and D. mendotae and the calanoids L. macrurus and L. sicilis have resulted in a community similar in composition to those of Lakes Michigan and Huron in the late 1990s. Both decreased nutrient loading and decreased zooplanktivory have likely contributed to the changes in zooplankton community composition we have documented here, though the relative importance of these two factors probably differed from lake to lake. Below we examine spatial and temporal distributions of the major taxa encountered in our study and assess the likely determining factors for those distributions. Calanoid copepods A notable consequence of the shifts in community structure that we have observed in our time series is that the two large calanoids L. macrurus and L. sicilis currently make up a substantial proportion of biomass in all lakes except Erie. Vertical distribution of both species is confined to the region below the epilimnion during stratified periods, with L. macrurus primarily hypolimnetic and L. sicilis metalimnetic (Barbiero et al., 2005; Watkins et al., 2017). Both species are considered indicative of oligotrophy in the Great Lakes (Gannon and Stemberger, 1978; Patalas, 1972) and are characteristic dominants of deep subarctic North American lakes (Patalas, 1975). Limnocalanus macrurus is thought to be among the historically dominant species in the lakes (Robertson, 1966), while the abundance of L. sicilis in Lake Michigan was noted in one of the earliest papers on Great Lakes zooplankton (Forbes, 1882). Assessing the exact importance of these species to pre-impact communities, however, is hampered by a lack of quantitative data. Both species were also once common in Lake Erie (Fish, 1960), although populations in the western basin were limited to winter/spring and most likely

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represented transient individuals flushed in from Lake Huron (Gannon and Beeton, 1971). Limnocalanus macrurus declined throughout Lake Erie during the late 1950s, likely as a result of hypolimnetic oxygen depletion and increased fish predation (Gannon and Beeton, 1971), and its continued low densities in the eastern and central basins has been attributed to high predation by rainbow smelt Osmerus mordax (Kane et al., 2004). While the relative importance of L. macrurus and L. sicilis has increased in lakes Huron, Michigan and Ontario, actual increases in biomass have only occurred in Lake Ontario and northern Lake Michigan; elsewhere these species have been stable or declined. Vanderploeg et al. (2012) reported increases in both L. macrurus and L. sicilis between 1994–2003 and 2007–2008 from a NOAA long-term monitoring site in southeastern Lake Michigan and attributed these to decreases in alewife predation, while Barbiero et al. (2009b) had ascribed earlier increases in L. macrurus in part to planktivore declines. Limnocalanus macrurus is a seasonally important food item of alewife (Morsell and Norden, 1968; Pothoven and Vanderploeg, 2004; Wells, 1980) and there is circumstantial evidence that its populations can be controlled by alewife predation (Wells, 1970). Little direct information is available on the vulnerability of L. sicilis to vertebrate predation. While populations of alewife have declined in both lakes Huron and Michigan during the course of our study (USGS, 2017), only in northern Lake Michigan did we see a sustained increase in absolute L. macrurus biomass. Notably, the crash in alewife abundance in Lake Huron in 2003 (Riley et al., 2008) did not result in a persistent increase in either L. macrurus or L. sicilis, which suggests that factors other than predation are controlling their populations in that lake. Both species are omnivorous (Bowers, 1980; Bundy et al., 2005; Warren, 1985; Wong and Chow-Fraser, 1985) and have been shown to consume, in particular, large diatoms (Branstrator and Lehman, 1991; Bundy et al., 2005), which have been in decline in the spring bloom in Lake Michigan and, more precipitously, Lake Huron (Barbiero et al., 2018b). Thus, resource limitation could have precluded any response to reduced alewife predation in these lakes. Even so, a decreasing resource base might provide a relative competitive advantage to calanoids (McNaught, 1975), at least to the extent of lessening their rate of decline relative to that of cladocerans and cyclopoids. A better case for decreased predation having promoted increases in these species can be made in Lake Ontario. In that lake, declines in productivity in the past decade, such as have occurred in Michigan and Huron, have not been seen (Barbiero et al., 2014; Dove and Chapra, 2015), while there has been evidence of other shifts in zooplankton community structure consistent with reduced vertebrate planktivory (Barbiero et al., 2014; Rudstam et al., 2015), as will be discussed further below. The sudden increase in L. sicilis coincident with the appearance of B. longimanus, a species thought to have been previously suppressed in the lake due to intense planktivory (Makarewicz and Jones, 1990; Mills et al., 1992), is particularly suggestive of decreased vertebrate predation pressure. Leptodiaptomus sicilis resides substantially higher in the water column of Lake Ontario than L. macrurus (Barbiero, unpublished data; Watkins et al., 2017), thus a more pronounced response of L. sicilis to decreased predation by the shallow-dwelling alewife (Olson et al., 1988; Riha et al., 2017) might be expected. However, trends in alewife abundance in Lake Ontario are ambiguous; marked declines in biomass seen in midsummer lake-wide hydroacoustic surveys since 2000 (Holden et al., 2018) have not been apparent in spring bottom trawls (Weidel et al., 2018). Other prey fish make up a relatively small proportion of the planktivore community (Weidel et al., 2018). Regardless of the causes, the increase in relative importance of these two copepod species has shifted biomass in lakes Michigan, Huron and Ontario to both larger sizes and presumably greater depths, which can have consequences for energy transfer, and has also moved the composition of crustacean communities in all three lakes closer to that of Lake Superior, and also likely closer to their historic makeup. The smaller, shallower-dwelling calanoids L. ashlandi and L. minutus are characteristic members of the calanoid communities in lakes

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Michigan and Huron, and in both lakes these species exhibited similar patterns, dropping to low levels between approximately 2005 and 2010 and then partially rebounding. These patterns coincided to varying degrees with those of bosminids and cyclopoid copepods, which suggests similar factors might be controlling their abundances, as postulated by Vanderploeg et al. (2012) and discussed further below. Cyclopoid copepods In contrast to the relative, and in some cases absolute, increases in calanoids, cyclopoids exhibited absolute declines in lakes Ontario, Michigan and Huron, although these declines were not persistent in Lake Michigan. Diacyclops thomasi was the most widely distributed cyclopoid and among the most widely distributed crustaceans across all lakes. It was a notable summer component of all areas of the lakes with the exception of the western basin of Lake Erie, where it was probably limited by high temperatures (Andrews, 1953). In both lakes Huron and Michigan, D. thomasi populations exhibited declines between 2003 and 2005. Spring populations had largely recovered in both lakes within 5 years, although summer populations have remained depressed in Lake Huron. In Lake Ontario, D. thomasi populations decreased dramatically in the early 2000s and have remained low in comparison both to previous years in our study and to historical values (Patalas, 1969; Watson and Carpenter, 1974). Kerfoot et al. (2010) and Vanderploeg et al. (2012) had reported declines in cyclopoid copepods in the mid-2000s from various regions of southern Lake Michigan, which both ascribed to a reduction in food supplies by dreissenid filtration during the winter-spring transition. Given the continued expansion of dreissenids into profundal waters since 2005 in both lakes (Barbiero et al., 2013; Burlakova et al., 2018; Nalepa et al., 2014), during which time offshore spring populations of D. thomasi have recovered in Lake Michigan, direct competition of dreissenids with cyclopoids for phytoplankton (Kerfoot et al., 2010) or microzooplankton (Vanderploeg et al., 2012) seems unlikely to be a primary mechanism for their decline. Vanderploeg et al. (2012) also suggested that predation by B. longimanus on cyclopoid and diaptomid nauplii might have contributed to declines in those taxa at their southwestern Lake Michigan station. Rudstam et al. (2015) attributed the decline in D. thomasi in Lake Ontario to predation by B. longimanus, as well as by L. macrurus, which is a known predator of nauplii and is thought to be capable of substantially impacting naupliar mortality in the Great Lakes (Warren, 1983, 1985). Recent populations of D. thomasi in Lake Michigan and Lake Huron changed in tandem with those of smaller diaptomids, providing some support for predation on nauplii as a common causal mechanism, although corresponding changes in B. longimanus have not been as clear. Some degree of correspondence, however, was seen between D. thomasi declines and increases in L. macrurus in both Lake Michigan and Lake Ontario (ESM Figs. S2, S3). Vertical overlap between L. macrurus and nauplii has been reported from both Lake Michigan (Schulze and Brooks, 1987) and Lake Ontario (Watkins et al., 2017). In contrast, little correspondence was seen between L. macrurus and D. thomasi in Lake Huron. Cyclopoid biomass has been shown to be correlated with chlorophyll in this lake but not in Lake Michigan (Barbiero et al., 2018b). Thus, while invertebrate predation on nauplii seems a plausible mechanism behind the observed cyclopoid declines, a low resource base might also be playing a role in the continued suppression of cyclopoid populations in Lake Huron. In some instances, populations of D. thomasi showed a high degree of interannual variability, which could have been an indirect response to vertebrate planktivory. Diacyclops thomasi is known to increase in dominance in lakes subject to high levels of vertebrate predation (Almond et al., 1996; Brooks and Dodson, 1965; Hessen et al., 1995a). The predominance of cyclopoids in Lake Ontario has been attributed to heavy predation by alewife (Sprules and Jin, 1990; Taylor et al., 1987). In northern Lake Michigan, an anomalously high population of D. thomasi

was seen in 1999, which coincided with extremely high age-1 alewife biomass in that year (Vanderploeg et al., 2012), and thus probably represented a response to high planktivory. In central and eastern Lake Erie, large populations of D. thomasi often showed an inverse relationship with large Daphnia, again suggesting dominance under conditions of high vertebrate predation. Most cyclopoid species aside from D. thomasi were rare outside of Lake Erie, and their distribution was probably governed to an extent by temperature. Acanthocyclops vernalis, which is thought to favor warm, relatively high productivity environments (Robertson and Gannon, 1981), was largely restricted to the western basin of Lake Erie, as has been seen in previous studies (Watson, 1976). The small T. prasinus mexicanus was also largely confined to Lake Erie although never abundant. Mesocyclops edax, also thought to be a warm water form (Andrews, 1953; Wells, 1960), was found in greatest numbers in western Lake Erie although it appeared commonly, if not abundantly, in southern Lake Huron samples. Wells (1960) had reported this species to be abundant in Lake Michigan in the mid-1950s, and its subsequent decline in the 1960s was attributed to alewife predation (Wells, 1970), something that had also been seen in Connecticut (Brooks and Dodson, 1965) and New York (Hutchinson, 1971) lakes. Barbiero and Tuchman (2004) had noted a dramatic reduction in M. edax in lakes Huron, Michigan and Erie after the arrival of B. longimanus, an impact also seen in Harp Lake, Canada (Yan and Pawson, 1997). They attributed this reduction to B. longimanus predation on M. edax nauplii. Considering the continued rarity of M. edax in lakes Michigan and Huron in the face of the currently low alewife populations, this latter explanation for its distribution might be more compelling, though the relatively high populations of M. edax in eastern and central Lake Erie, where B. longimanus populations are highest, are not consistent with this hypothesis.

Predatory cladocerans Cladoceran communities in the Great Lakes have exhibited both long-term declines (lakes Huron and Michigan) and shifts in composition (Lake Ontario), as well as pronounced inter-annual changes in size and composition (central and eastern Lake Erie), with both bottom-up and top-down forces implicated to differing degrees. The broad distribution of cladoceran species across the lakes seemed to be governed to a large extent by invertebrate and vertebrate predation. For most regions and time periods, the non-native B. longimanus was the dominant predatory cladoceran and is a species capable of substantially impacting crustacean community structure (Barbiero and Tuchman, 2004; Lehman, 1991; Yan et al., 2001). We found a strong association between B. longimanus population size and zooplankton community makeup, an association largely independent of variables associated with production. Bythotrephes longimanus is a preferred prey item of alewives (Mills et al., 1993; Pothoven and Vanderploeg, 2004; Pothoven et al., 2007; Storch et al., 2007), the dominant planktivore in lakes Michigan, Huron and Ontario, and is also consumed by yellow perch, white perch, walleye, emerald shiners and rainbow smelt (Bur and Klarer, 1991; Parker et al., 2001; Pothoven et al., 2009; Storch et al., 2007), dominant planktivores in Lake Erie. Strong vertebrate predation can suppress B. longimanus (Pothoven et al., 2007) and allow proliferation of C. pengoi and L. kindtii (Cavaletto et al., 2010), species which are less susceptible to vertebrate predation due to their small size and transparency, respectively (Enz et al., 2001; Pothoven et al., 2007). Where not suppressed by vertebrate predation, B. longimanus is thought to limit C. pengoi and L. kindtii populations through direct predation (Branstrator, 1995; Ptáčníková et al., 2015; Witt and Cáceres, 2004) and perhaps food competition (Branstrator, 2005; Pichlová-Ptáčníková and Vanderploeg, 2009). Thus, the identity of the dominant predatory cladoceran in any region/period is probably due at least in part to the intensity of vertebrate predation.

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The western basin of Lake Erie was the only region of the Great Lakes in which the native L. kindtii was the dominant predatory cladoceran; B. longimanus populations were low in this region. Vertebrate predation, perhaps compounded by high temperature (Keeler et al., 2015), is thought to explain its relative absence in the summer in this basin (Garton et al., 1990, 1993). In the central basin of Lake Erie, where vertebrate predation can be intense (Pothoven et al., 2012), years of high L. kindtii abundances in our study were associated with low B. longimanus abundances, as well as a paucity of large Daphnia, further supporting the idea that high vertebrate predation allows the existence of L. kindtii. As with L. kindtii, the distribution of C. pengoi is thought to be limited by B. longimanus (Cavaletto et al., 2010); in our samples the lack of overlap of these two species was marked. It was the dominant predatory cladoceran only in Lake Ontario where B. longimanus populations are thought to be limited by alewife predation (Johannsson et al., 1991; Mills et al., 1992). The occasional appearance of C. pengoi in samples from lakes Michigan and Erie was almost always associated with the absence of B. longimanus. Non-predatory cladocerans While the level of vertebrate predation might play a large role in determining the dominant predatory cladoceran, this, in turn, appears to determine the dominant Daphnia species. Among the most striking distributional patterns we observed was the near total lack of overlap between D. retrocurva and B. longimanus. The former species was a prominent cladoceran only in areas (e.g., Lake Ontario, western Lake Erie) where or when the latter was absent, whereas in most situations in which B. longimanus was found, D. mendotae was the dominant daphnid. In the case of Lake Ontario, the appearance of B. longimanus in recent years has been associated with reduced D. retrocurva abundances and a shift towards D. mendotae, further supporting a role for B. longimanus in determining daphnid dominance. Daphnia retrocurva has been shown to be particularly susceptible to suppression by B. longimanus (Kerfoot et al., 2016; Strecker and Arnott, 2005; Yan and Pawson, 1997), while the relative resistance of D. mendotae to B. longimanus has made its dominance in post-invasion daphnid communities one of the more common consequences of B. longimanus invasions in North American lakes (Boudreau and Yan, 2003; Strecker et al., 2006; Yan et al., 2001). A shift from D. retrocurva to D. mendotae was seen in both Lake Michigan (Lehman and Cáceres, 1993) and Lake Erie (Barbiero and Rockwell, 2008) immediately after the invasion of those lakes by B. longimanus, perhaps due to greater diurnal vertical migration of D. mendotae (Lehman and Cáceres, 1993; Schulz and Yurista, 1999) and/or its greater escape abilities (Pichlová-Ptáčníková and Vanderploeg, 2011). The relatively small D. retrocurva is also characteristic of assemblages impacted by high size-selective vertebrate predation, in the absence of which larger bodied cladocerans, such as D. mendotae, should dominate by virtue of their more efficient grazing (Brooks and Dodson, 1965). Given the high selectivity of alewife for B. longimanus (Pothoven et al., 2007; Storch et al., 2007), vertebrate predation might thus have the double effect of shifting daphnid dominance from D. mendotae to D. retrocurva through size-selective predation on the larger daphnid while also reducing predation by B. longimanus on D. retrocurva. The central basin of Lake Erie seems to present a particularly striking example of interannual shifts in cladoceran community structure, most likely driven by changes in vertebrate predation. Bythotrephes longimanus showed a high degree of interannual variability in this basin; when B. longimanus populations were low, D. retrocurva appeared in appreciable numbers, as did bosminids and cyclopoids. The resulting community, with smaller-bodied cladocerans and evasive copepods, is indicative of high vertebrate predation. On the other hand, high B. longimanus populations were associated with a daphnid community dominated by extremely large individuals of D. mendotae and a relative lack of bosminids and cyclopoids.

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A number of hypotheses have been forwarded to explain the collapse of cladoceran populations in Lake Huron in 2003 and the more muted but still significant declines in Lake Michigan. A negative correlation between annually averaged June–November Daphnia and B. longimanus biomass in a 12-year (1994–2003, 2007, 2008) data series from a station in southeastern Lake Michigan led Vanderploeg et al. (2012) to conclude that invertebrate predation was responsible for reduced abundances of Daphnia, perhaps intensified by increased foraging efficiency of B. longimanus resulting from increasing transparency. There was some seasonal mismatch between the two taxa, however; peaks in Daphnia biomass occurred in August and September at their station, while B. longimanus biomass peaked in October and November. This in itself might be evidence of a predation effect, though one that wouldn't be captured in a correlation of seasonally-averaged data. Bythotrephes longimanus was estimated to be the dominant planktivore in Lake Huron in the bioenergetics model of Bunnell et al. (2011). However, in a follow-up study, Bunnell et al. (2012) saw little spatial overlap between October populations of B. longimanus and herbivorous cladocerans in northern Lake Huron and concluded that B. longimanus could not be exerting direct top-down control on these organisms. For Bythotrephes to have been the main cause for the shifts in zooplankton community composition seen here, which occurred most notably between 2003 and 2005, B. longimanus populations would have had to have increased during this period. There has been no evidence of this in our data set. In fact, B. longimanus biomass declined by half in most regions of the two lakes. In contrast, Vanderploeg et al. (2012) did report increased B. longimanus biomass from their station in southeastern Michigan in 2007 and 2008 compared to 1994–2003; data were not available for 2004–2006. The declines we noted in B. longimanus biomass were notably less than those of D. mendotae, particularly in Lake Huron. This raises the possibility that an increase in the relative predation pressure exerted by B. longimanus could have been a contributory factor in the continued suppression of D. mendotae. As noted, Bythotrephes populations peak in southeastern Lake Michigan in October or November, after our surveys were undertaken; similar seasonality was reported for northern Lake Huron (Bunnell et al., 2012). Thus B. longimanus impacts on the zooplankton community likely occur mainly in the fall, after our surveys; this would still leave the August declines in cladocerans unexplained. The other major invertebrate predator on Daphnia in these lakes, M. diluviana (Gal et al., 2006), has substantially lower populations in Lake Huron than in Lake Michigan (Jude et al., 2018), which is not consistent with the faster decline of cladocerans in Huron than in Michigan. In contrast, Barbiero et al. (2011) posited a role for reduced food supply in the shifts seen in the Lake Huron crustacean community. We found herbivorous cladoceran biomass to be highly correlated with average surface April–July chlorophyll in all basins of Lake Michigan and Lake Huron, suggesting a role for bottom-up mechanisms in the declines. Because declines in surface chlorophyll have been most pronounced in the spring, prior to the development of substantial cladoceran populations, Barbiero et al. (2018b) speculated that bottom up control of cladocerans in these lakes could be operating at least in part through changes in the deep chlorophyll layer (DCL), which is dependent on the magnitude of the spring bloom. Pothoven and Fahnenstiel (2013) reported declines in the DCL in southeastern Lake Michigan, which they attributed to a reduction in the spring bloom and disruption of horizontal transport of nutrients to the offshore, both caused by dreissenids. We have seen significant declines in the magnitude of the DCL between 1997 and 2016, as assessed by Spearman rank correlations, at our sites in both Lake Michigan (r = −0.21, P = 0.003) and Lake Huron (r = −0.47, P b 0.001). Vanderploeg et al. (2012) found a significant correlation between metalimnetic chlorophyll and cladoceran biomass at their station in southeastern Lake Michigan. Reductions in the DCL could be particularly important given the deeper daytime cladoceran distributions recently seen in both lakes (Bourdeau et al., 2015; Nowicki et al., 2017), although a reduction

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in DCL might be expected to also have an effect on deep-water calanoids (L. macrurus and L. sicilis), which we did not observe. It is likely that no single factor is responsible for the declines in cladocerans we have documented and that the mechanisms involved are both direct and indirect. Lower phytoplankton biomass decreases cladoceran growth rates, making the population more vulnerable to predation (Lampert, 1978; Nicolle et al., 2011). Increases in invertebrate predation pressure, in particular by B. longimanus and L. macrurus, as a response to lower fish predation would not only directly increase cladoceran mortality but could also induce greater vertical migration, making cladocerans move into deeper and colder water, thereby further decreasing cladoceran growth rates (Pangle et al., 2007). Increased light penetration (Barbiero et al., 2018b) increases both the magnitude of these migrations and the feeding rates of vertebrate and invertebrate predators (Boscarino et al., 2010; Pangle and Peacor, 2009), and both of those mechanisms can contribute to decreases in cladoceran populations. Clearly, a combination of both direct and indirect mechanisms needs to be considered to explain the declines in cladocerans in the Great Lakes. Unlike D. mendotae and bosminids, H. gibberum populations increased in Lake Huron after 2003. This species, a small-bodied cladoceran encased in a gelatinous sheath, had one of the more unusual distributions in the lakes. It was a co-dominant cladoceran in Lake Superior and was occasionally important in lakes Huron and Ontario. It is considered a soft-water species (Hutchinson, 1971), presumably due to a lower calcium requirement compared to daphnids (Hessen et al., 1995b; Jeziorski et al., 2014). However, the prominence of H. gibberum in the relatively hard-water lakes Huron and Ontario suggests that this is not the only controlling factor. Its small size might confer an advantage in the face of vertebrate predation (Hutchinson, 1971; Wells, 1970), although its appearance in substantial numbers in Lake Huron occurred after the collapse of alewife. Alternatively, its gelatinous sheath might afford some protection against invertebrate predators (Allan, 1973; Jeziorski et al., 2014), but its response to B. longimanus is mixed, with some reports showing declines (Kerfoot et al., 2016; Strecker et al., 2006; Wahlström and Westman, 1999) and some showing no change (Boudreau and Yan, 2003; Yan and Pawson, 1997; Yan et al., 2001). Bythotrephes longimanus can consume H. gibberum (Schulz and Yurista, 1999), and declines in H. gibberum after the B. longimanus invasion were reported in the Great Lakes (Barbiero and Tuchman, 2004). In our study, large H. gibberum populations were usually, though not always, associated with low B. longimanus abundances. We currently have no explanation for the distribution of H. gibberum in our lakes that is consistent with what is known about this species from other areas. Conclusions During the course of our study, substantial shifts have occurred in zooplankton communities in lakes Michigan, Huron and Ontario, with all three lakes showing a trend towards increasing similarity both with each other and with Lake Superior. Declines in cladocerans in lakes Michigan and Huron have left these communities dominated by calanoid copepods (by biomass), especially the larger deep cold-water species L. macrurus and L. sicilis, returning them to what is likely close to a historic community structure. In Lake Ontario, the replacement of D. retrocurva with D. mendotae, and of C. pengoi with B. longimanus, as well as the reduction in D. thomasi, have moved communities in this lake closer to those characteristic of lakes Huron and Michigan during the late 1990s–early 2000s. Both decreased productivity and changes in the degree and nature (i.e., fish versus invertebrate) of predation pressure have likely combined through direct and indirect pathways to cause these changes. In the case of Lake Ontario, the shifts seen have been consistent with a decrease in vertebrate predation, while in Lake Huron and Lake Michigan, bottom-up forces seem more important. Communities in Lake Erie have shown substantial inter-annual

variability with little directional change while those in Lake Superior have been remarkably stable during the 20 years of our study.

Acknowledgements We gratefully acknowledge the assistance of Julie Lietz in the preparation of this manuscript. This work was supported by the U.S. EPA Great Lakes National Program Office as part of EPA Contract No. EP-C-15-012, Scientific and Technical Support with GDIT under the direction of Louis Blume, Project Manager, as well as by an agreement with Cornell University, Department of Natural Resource under Prime Agreement Award GL-00E01184 from the U.S. EPA “Great Lakes Long Term Biological Monitoring of Zooplankton, Benthos, and Chlorophyll a”. This longer-term view of zooplankton in the Great Lakes would not have been possible without the efforts of Marc Tuchman, David Rockwell and Glenn Warren leading the GLNPO zooplankton monitoring program throughout this time, as well as the efforts of previous grantees (David Jude, University of Michigan, Mary Balcer, University of Wisconsin - Superior) and contractors (Linda Kuhns, Lori Schacht-DeThorne, Ruth Little). The views expressed in this paper are those of the authors and do not necessarily represent the views or policies of the USEPA. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.jglr.2019.03.012.

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