Historical changes and current status of crayfish diversity and distribution in the Laurentian Great Lakes

Despite increasing recognition of the importance of invertebrates, and specifically crayfish, to nearshore food webs in the Laurentian Great Lakes, past and present ecological studies in the Great Lakes have predominantly focused on fishes. Using data from many sources, we provide a summary of crayfish diversity and distribution throughout the Great Lakes from 1882 to 2008 for 1456 locations where crayfish have been surveyed. Sampling effort was greatest in Lake Michigan, followed by lakes Huron, Erie, Superior, and Ontario. A total of 13 crayfish species occur in the lakes, with Lake Erie having the greatest diversity (n = 11) and Lake Superior having the least (n = 5). Five crayfish species are non-native to one or more lakes. Because Orconectes rusticus was the most widely distributed non-native species and is associated with known negative impacts, we assessed its spread throughout the Great Lakes. Although O. rusticus has been found for over 100 years in Lake Erie, its spread there has been relatively slow compared to that in lakes Michigan and Huron, where it has spread most rapidly since the 1990s and 2000, respectively. O. rusticus has been found in both lakes Superior and Ontario for 22 and 37 years, respectively, and has expanded little in either lake. Our broad spatial and temporal assessment of crayfish diversity and distribution provides a baseline for future nearshore ecological studies, and for future management efforts to restore native crayfish and limit non-native introductions and their impact on food web interactions.     

Dolichospermum blooms in Lake Superior: DNA-based approach provides insight to the past,present and future of blooms

Cyanobacterial blooms are increasing in frequency, duration, and severity globally in freshwater ecosystems. The Laurentian Great Lakes are prone to toxin-producing cyanobacterial blooms and have experienced annually recurring blooms. Because of its oligotrophic nature, Lake Superior has been relatively free of bloom occurrences. However, in recent years, Dolichospermum blooms have occurred with increasing frequency, especially in the western arm. During a Dolichospermum bloom in 2018, opportunistic samples were collected from the offshore bloom and investigated with shotgun metagenomics. We identified a near-complete Dolichospermum genome that is highly similar to genomes from cultures recovered in Lakes Erie and Ontario. The genomes from the Laurentian Great Lakes are typified by their putative ability to produce a suite of secondary metabolites like anabaenopeptin, but not toxins like microcystin. Additionally, we recovered a Dolichospermum lemmermannii 16S rRNA gene from the bloom and using datasets collected from the epilimnion and sediments in Lake Superior show this organism is ubiquitous and that several strains may exist. While there is much to learn about Lake Superior cyanobacterial bloom development and triggers, understanding this organism is endemic to the region, what its genome is capable of and that specific strains may have provenance within the lake provides a distinct ecological basis for understanding and working towards a predictive framework for future blooms.     

Status of the major aquaculture carps of China in the Laurentian Great Lakes Basin

There is concern of economic and environmental damage occuring if any of the four major aquacultured carp species of China, black carp Mylopharyngodon piceus, bighead carp Hypophthalmichthys nobilis, silver carp H. molitrix, or grass carp Ctenopharyngodon idella, were to establish in the Laurentian Great Lakes. All four are reproducing in the Mississippi River Basin. We review the status of these fishes in relation to the Great Lakes and their proximity to pathways into the Great Lakes, based on captures and collections of eggs and larvae. No black carp have been captured in the Great Lakes Basin. One silver carp and one bighead carp were captured within the Chicago Area Waterway System, on the Great Lakes side of electric barriers designed to keep carp from entering the Great Lakes from the greater Mississippi River Basin. Three bighead carp were captured in Lake Erie, none later than the year 2000. By December 2019, at least 650 grass carps had been captured in the Great Lakes Basin, most in western Lake Erie, but none in Lake Superior. Grass carp reproduction has been documented in the Sandusky and Maumee rivers in Ohio, tributaries of Lake Erie. We also discuss environmental DNA (eDNA) results as an early detection and monitoring tool for bighead and silver carps. Detection of eDNA does not necessarily indicate presence of live fish, but bigheaded carp eDNA has been detected on the Great Lakes side of the barriers and in a small proportion of samples from the western basin of Lake Erie.     

Lake whitefish (Coregonus clupeaformis) energy and nutrient partitioning in lakes Michigan,Erie and Superior

A concurrent decrease in lake whitefish (Coregonus clupeaformis) condition and Diporeia spp. abundance in Lake Michigan has spurred investigations into possible links between the two phenomena. We examined female lake whitefish δ¹³C and δ¹⁵N stable isotopes, growth, reproductive investment, dorsal muscle total lipid and docosahexaenoic acid (DHA) contents from lakes Erie, Michigan and Superior to determine whether differences in food source were correlated with measures of stock success. Stocks with higher somatic growth rates and mean reproductive potential had higher energy stores in terms of percent total lipid. Stocks with low muscle lipid concentration also had smaller egg sizes as egg number increased. Diet varied among stocks as evidenced by δ¹³C and δ¹⁵N stable isotope analyses; however, muscle total lipid and DHA were not correlated to apparent Diporeia spp. prey use. When compared to stocks from lakes Erie and Superior, Lake Michigan stocks had lower growth, reproduction, and lipid stores. While stocks in Lake Michigan with access to declining Diporeia spp. populations may still feed on the amphipod, it appears that they are unable to consume the quantities necessary to maintain historical growth and reproduction. Stable isotope analyses of lakes Erie and Superior stocks, with higher growth rates and lipid values, indicated different feeding strategies with no indication of reliance on Diporeia spp. While differences in prey resources may have an effect on lake whitefish stocks, differences in Diporeia spp. abundance alone cannot explain differences in lake whitefish condition observed among the Great Lakes included in this study.     

A New Biological Marker Layer in the Sediments of the Great Lakes: Bythotrephes cederstroemi (Schödler) Spines

The European cladoceran, Bythotrephes cederstroemi (Schödler), recently invaded the Laurentian Great Lakes. Based on recent zooplankton records, it most likely appeared first in 1984 in Lakes Ontario, Erie, and Huron, and in 1985 in Lake Michigan. It has yet to be reported from Lake Superior. This species is a relatively large-bodied predatory form that possesses a long, caudal, latterally barbed spine. B. cederstroemi spines and spine fragments were found in the upper fractions (predominantly 0–4 cm) of 35 sediment cores collected from seven areas of deposition in the eastern basin of Lake Erie. All remains were well preserved and easy to identify. Very few to 0 spines were found in core depths greater than 4 cm suggesting that the invasion of this species has resulted in a new, readily distinguishable time horizon marker.     

The Invasive New Zealand Mud Snail (Potamopyrgus antipodarum) in Lake Erie

The New Zealand mud snail (Potamopyrgus antipodarum) is an invasive species in Europe, Japan, Australia, and North America. In the western United States it is a species of special concern where population densities in some rivers and streams are very large (∼300,000 per m²) and considerable ecological effects of its presence have been reported. Much less about the effects of this species is known in the Great Lakes, where the snail was found in Lake Ontario and the St. Lawrence River in 1991. Here we report the occurrence of the snail in Lake Erie. Two P. antipodarum were collected in 18 m deep water (sampling range 5–18 m) in Lake Erie off shore of Presque Isle State Park near Erie, Pennsylvania in the summer of 2005 and others were collected off of Sturgeon Point in Lake Erie (sampling range 5–20 m) south of Buffalo, NY and in the central basin of Lake Erie (18 m) in 2006. This finding demonstrates that this species continues to expand its range in the Great Lakes. The range expansion increases the likelihood that it may become established in rivers and streams emptying into the Great Lakes where higher densities and greater ecological damage may result.     

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

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.     

Glyphosate influence on phytoplankton community structure in Lake Erie

In this study we investigated the effect of the phosphonate herbicide glyphosate (N-(phosphonomethyl)glycine) on the phytoplankton community structure in Lake Erie using lake water incubations, laboratory growth experiments and phylogenetic analysis of phosphonate metabolism genes. In microcosms, addition of glyphosate to Sandusky Bay water resulted in a significant increase in phytoplankton abundance, specifically causing an increase in the abundance of Planktothrix spp. In microcosms using Maumee Bay water, glyphosate did not stimulate phytoplankton growth but caused a decrease in Microcystis spp. abundance. The difference in the ability of Planktothrix spp. and Microcystis spp. to grow in the presence of glyphosate was confirmed in laboratory growth experiments. Further, an examination of the molecular pathways involved in phosphonate metabolism demonstrated that heterotrophic bacteria may be critical in allowing this proliferation. The results indicate that glyphosate has both positive and negative influences on phytoplankton community structure, serving as a nutrient source to microbes able to tolerate the herbicidal effects of the compound while killing those less tolerant. Moreover, this work highlights that in natural environments microorganisms function as communities, and the metabolic abilities of individual species are often less important than the collective ability of the community.     

First report of tubenose goby (Proterorhinus semilunaris) in the eastern basin of Lake Erie

The tubenose goby (Proterorhinus semilunaris), native to the Ponto-Caspian region, was first discovered in the Laurentian Great Lakes in 1990 after it was introduced through ballast water discharge. Compared with Neogobius melanostomus, another exotic gobiid from the Ponto-Caspian, colonization of the Great Lakes by P. semilunaris has been slow, with reports of the species being largely confined to the Huron-Erie Corridor (HEC) and western portions of Lake Erie and Lake Superior. This is the first report of P. semilunaris in the Great Lakes east of the western basin of Lake Erie. Between 28 June and 27 July, 2012, 176 P. semilunaris were collected from shallow (< 1.2 m) water of Marina Lake, a 40 ha embayment in Presque Isle State Park (Erie, PA). The large number of P. semilunaris collected at the site and the presence of individuals as small as 17 mm total length suggest an established population. However, the mechanism by which P. semilunaris was introduced to Presque Isle Bay is not clear.     

The effect of mayfly (Hexagenia spp.) burrowing activity on sediment oxygen demand in western Lake Erie

Previous studies support the hypothesis that large numbers of infaunal burrow-irrigating organisms in the western basin of Lake Erie may increase significantly the sediment oxygen demand, thus enhancing the rate of hypolimnetic oxygen depletion. We conducted laboratory experiments to quantify burrow oxygen dynamics and increased oxygen demand resulting from burrow irrigation using two different year classes of Hexagenia spp. nymphs from western Lake Erie during summer, 2006. Using oxygen microelectrodes and hot film anemometry, we simultaneously determined oxygen concentrations and burrow water flow velocities. Burrow oxygen depletion rates ranged from 21.7 mg/nymph/mo for 15 mm nymphs at 23 °C to 240.7 mg/nymph/mo for 23 mm nymphs at 13 °C. Sealed microcosm experiments demonstrated that mayflies increase the rate of oxygen depletion by 2–5 times that of controls, depending on size of nymph and water temperature, with colder waters having greater impact. At natural population densities, nymph pumping activity increased total sediment oxygen demand 0.3–2.5 times compared to sediments with no mayflies and accounted for 22–71% of the total sediment oxygen demand. Extrapolating laboratory results to the natural system suggest that Hexagenia spp. populations may exert a significant control on oxygen depletion during intermittent stratification. This finding may help explain some of the fluctuations in Hexagenia spp. population densities in western Lake Erie and suggests that mayflies, by causing their own population collapse irrespective of other environmental conditions, may need longer term averages when used as a bio-indicator of the success of pollution-abatement programs in western Lake Erie and possibly throughout the Great Lakes.     

Lipid Concentration and Size Variation of Bythotrephes (Cladocera: Cercopagidae) from Lakes Erie,Huron, and Michigan

Lipid concentrations of Bythotrephes cederstroemi were compared among three Great Lakes, Erie, Huron, and Michigan, in an effort to investigate the phenotypic plasticity in size displayed among the lakes. Four developmental stages were measured in Lakes Erie and Huron and two stages were studied in Lake Michigan. With a gravimetric extraction method, the total lipid concentration range (μg lipid μg dry weight⁻¹, expressed as percent) for Bythotrephes was estimated to be 10–19%. Statistically significant differences were found in lipid concentrations of Bythotrephes among lakes and developmental stages. Lake Erie had significantly higher lipid concentration values than Lake Huron for stages 2 through 4, and had similar values to Lake Michigan for the analyzed stages 1 and 4. The first instar had indistinguishable lipid concentrations among Lakes Erie, Huron,and Michigan. Even though animals from Lake Erie were significantly smaller, the data suggest that they were not less well nourished. We hypothesize that selective mortality imposed by visual predators on larger Bythotrephes and the lack of deep water refuges in Lake Erie has encouraged the smaller size of Bythotrephes found there in comparison to those found in Lakes Huron and Michigan.     

Investigation of viruses in Diporeia spp. from the Laurentian Great Lakes and Owasco Lake as potential stressors of declining populations

The benthic amphipod Diporeia is an ecologically and biogeochemically important constituent of deep freshwater lakes in North America. The proliferation of dreissenid mussels in the mid-1990s coincided with a sharp decrease in Diporeia populations in several Laurentian Great Lakes; however the ultimate cause and mechanisms of their decline are still unknown. Here we examined the composition of DNA viruses associated with Diporeia collected from populations of Lake Michigan that had declined and stable populations in Lake Superior and Owasco Lake (Finger Lake in central New York State). Viral metagenomic libraries from Owasco Lake and Lake Superior were comprised primarily of bacteriophages, which may infect bacteria within the amphipod microbiome. In contrast, the metagenomic library from Lake Michigan contained well-represented ssDNA circular viral genomes. The prevalence and viral load of one putative Type V ssDNA circular virus (LM29173) that recruited almost 30% of total viral sequence reads in the Lake Michigan library was analyzed by quantitative PCR. The prevalence of LM29173 was over two orders of magnitude greater in Lake Michigan compared to the other two lakes. Although further research is necessary to establish the pathology and epidemiological extent of viral-Diporeia interactions, our data suggest that viruses may be numerically significant constituents of the Diporeia microbiome, and if pathogenic some of these viruses may be a stressor of Great Lakes Diporeia populations. Our data further indicate that special attention should be given to the circovirus that was prevalent in the declining Michigan population but uncommon in the other two lakes.     

An assessment of water quality in two Great Lakes connecting channels

Compared to the Great Lakes, their connecting channels are relatively understudied and infrequently assessed. To address this gap, we conducted a spatially-explicit water quality assessment of two connecting channels, the St. Marys River and the Lake Huron-Lake Erie Corridor (HEC) in 2014–2016. We compared the condition of the channels to each other and to the up- and downriver Great Lakes with data from an assessment of the Great Lakes nearshore. In the absence of channel-specific thresholds, we assessed the condition of the area of each channel as good, fair, or poor by applying the most protective water quality thresholds for the downriver lake. Condition of the St. Marys River was rated mostly fair for total phosphorus (TP, 56% of the area) and mostly good (61% of the area) for chlorophyll a. Area-weighted mean concentrations of these parameters were intermediate to Lake Superior and Lake Huron. Unlike Lake Superior and Lake Huron, a large proportion (97%) of the area of the St. Marys River was in poor condition for water clarity based on Secchi depth. Area-weighted mean concentrations of TP and chlorophyll a in the HEC were more like Lake Huron than Lake Erie. For these indicators, most of the area of the HEC was rated good (81% and 86%, respectively). Interpretation of assessment results is complicated by variation in thresholds among and within lakes. Appropriate thresholds should align with assessment objectives and in the case of connecting channels be at least as protective as thresholds for the downriver lake.     

The impact of phytoplankton community composition on optical properties and satellite observations of the 2017 western Lake Erie algal bloom

Since the early 2000s Lake Erie has seen a dramatic increase in phytoplankton biomass, manifested in particular by the rise in the severity of cyanobacteria blooms and the prevalence of potentially toxic taxa such as Microcystis. Satellite remote sensing has provided a unique capacity for the synoptic detection of these blooms, enabling spatial and temporal trends in their extent and severity to be documented. Algorithms for satellite detection of Lake Erie algal blooms often rely on a single consistent relationship between algal or cyanobacterial biomass and spectral indices such as the Maximum Chlorophyll Index (MCI) or Cyanobacteria Index (CI). Blooms, however, are known to vary significantly in community composition over space and time. A suite of phytoplankton and optical property measurements during the western Lake Erie algal bloom of 2017 showed highly diverse bloom composition with variable absorption and backscatter properties. Elevated backscattering coefficients were observed in the Maumee Bay, likely due to phytoplankton cell morphology and buoyancy regulating gas vacuoles, compared with typically Planktothrix dominated blooms in Sandusky Bay. MCI and CI calibrated to historical chlorophyll observations and applied to Sentinel 3's OLCI sensor accurately captured the 2017 bloom in Maumee Bay but underestimated the Sandusky Bay bloom by nearly 80%. The phycoerythrin-rich picocyanobacteria Aphanothece and Synechococcus were found in abundance throughout the western and central basins, resulting in substantial biomass underestimations using blue to green ratio-based algorithms. Potential misrepresentation of bloom severity resulting from phytoplankton optical properties should be considered in assessments of bloom conditions on Lake Erie.     

Coexistence of the native benthic amphipod Diporeia spp. and exotic dreissenid mussels in the New York Finger Lakes

Populations of the benthic amphipod Diporeia spp. have sharply declined since the early 1990s in all North America's Great Lakes except Lake Superior. The onset and continued decline coincides with the invasion of these lakes by zebra (Dreissena polymorpha) and quagga (Dreissena rostriformis bugensis) mussels and the spread of quagga mussels to deep habitats. The six deepest Finger Lakes of central New York (Seneca, Cayuga, Skaneateles, Canandaigua, Keuka, and Owasco) have historically been Diporeia habitat and have had dreissenids for more than a decade. These lakes represent a wide range of trophic state, maximum depth, and dreissenid invasion history. We hypothesized that Diporeia abundance would be negatively impacted by dreissenid mussel expansion in the Finger Lakes. During 2006–2010, we sampled Diporeia and mussel populations in these six lakes. Diporeia was present in all six lakes, and was abundant (2000/m²) in Owasco Lake that has only zebra mussels and in Cayuga and Seneca Lakes that have had zebra and quagga mussels since 1994. Diporeia abundance was lowest (1000/m²) in Skaneateles, Canandaigua, and Keuka Lakes where quagga mussels have recently expanded. Productivity indicators explained much of the variability of Diporeia abundance. The persistence of Diporeia with quagga mussels in these lakes may be because of available alternative food resources. Fatty acid tracers indicate that Diporeia from Owasco Lake, the lake without quagga mussels, utilize diatoms, but Diporeia from Cayuga Lake that coexist with abundant quagga mussels also use food resources associated with terrestrial detritus that cannot be intercepted by dreissenids.     

Range Expansion of the Exotic Zooplankter Cercopagis pengoi (Ostroumov) into Western Lake Erie and Muskegon Lake

Previously reported from Lakes Ontario and Michigan, the nonindigenous zooplankter Cercopagis pengoi was found for the first time in western Lake Erie, the Detroit River, and Muskegon Lake, Michigan, during summer 2001. A native of the Ponto-Caspian region, C. pengoi is currently expanding its range in North America. Analysis of mitochondrial gene ND5 sequences confirmed that the Lake Erie haplotype is identical to that reported previously from Lakes Ontario and Michigan and the Finger Lakes, New York. These findings support the hypothesis that C. pengoi's range expansion in the Great Lakes likely resulted from inter-lake transfer of ballast water, rather than from additional introductions from European locations. Pleasure-craft traffic operating between Lake Michigan and Muskegon Lake is likely responsible for this inland transfer of Cercopagis, a trend that likely will increase due to human activities.     

Trends in Diporeia populations across the Laurentian Great Lakes, 1997-2009

Benthic communities in the Laurentian Great Lakes have been in a state of flux since the arrival of dreissenid mussels, with the most dramatic changes occurring in population densities of the amphipod Diporeia. In response, the US EPA initiated an annual benthic macroinvertebrate monitoring program on all five Great Lakes in 1997. Although historically the dominant benthic invertebrate in all the lakes, no Diporeia have been found in Lake Erie during the first 13 years of our study, confirming that Diporeia is now effectively absent from that lake. Populations have almost entirely disappeared from our shallow (< 90 m) sites in lakes Ontario, Huron, and Michigan. In Lake Ontario, three of our four deep (> 90 m) sites still supported Diporeia populations in 2009, with densities at those sites ranging between 96 and 198/m². In Lake Michigan, populations were still found at six of our seven deep sites in 2009, with densities ranging from 57 to 1409/m². Densities of Diporeia in 2009 at the four deep sites in Lake Huron were somewhat lower than those in Lake Michigan, ranging from 191 to 720/m². Interannual changes in population size in Lake Huron and Lake Michigan have shown a degree of synchrony across most sites, with periods of rapid decline (1997-2000, 2003-2004) alternating with periods of little change or even increase (2001-2002, 2005-2009). There has been no evidence of directional trends at any sites in Lake Superior, although substantial interannual variability was seen.     

European Valve Snail Valvata piscinalis (Müller) in the Laurentian Great Lakes Basin

Previously reported from the lower Great Lakes basin and St. Lawrence and Hudson rivers, the nonindigenous gastropod Valvata piscinalis was found for the first time in Superior Bay (Minnesota) of Lake Superior, Lake Michigan (Wisconsin), and Oneida Lake (New York) of the Lake Ontario basin. This snail was not abundant in Lakes Superior and Michigan, whereas in eutrophic Oneida Lake it reached a maximum density of 1,690 individuals/m² (mean density = 216 individuals/m²). Human-mediated disturbances could facilitate the range extension of this snail by providing dispersal opportunities (e.g., canals, shipping traffic) or increasing nutrients (e.g., eutrophication). A native of the Palaearctic region, V. piscinalis has colonized sites across the Great Lakes basin, suggesting that it will likely become common in disturbed Great Lakes areas.