Survival, growth, and production of Hexagenia bilineata mayflies in fluidized sediment from lower Green Bay, Lake Michigan
Introduction
As the largest freshwater estuary in the Laurentian Great Lakes, Green Bay is a relatively shallow and highly productive arm of Lake Michigan (Klump et al., 1997). As in other large bays and estuaries in the Great Lakes, organic pollution and nutrient loading over the past century have caused excessive primary production in the water column and have driven up biological oxygen demand in benthic environments. Frequent seasonal hypoxic and anoxic conditions have been common in the lower bay during stratification in the summer months (Kennedy, 1982, Conley, 1983, Klump et al., 1997, Qualls et al., 2009) in addition to the presence of other adverse effects on the benthos of lower Green Bay (Schloesser et al., 2009). For example, we observe that the high volume of organic matter accumulating on the benthos is not being fully processed, resulting in a highly fluidized “sludge-like” gyttja substrate across the majority of the open water benthic habitat of the lower bay. This fluidized gyttja presence is suggestive of inadequate zoobenthic sediment reworking via bioturbation and detritivorous feeding relative to the amount and/or rate of autochthonous organic matter deposition. These large areas of fluidized gyttja have the potential to serve as sources for nutrient regeneration to perpetuate primary production even if allochthonous inputs are abated. Comparatively, the fluidized gyttja water phase has a greater exchange capacity with overlying water than a more consolidated firm gyttja; all things being equal (e.g., concentration gradient, organic content, bioturbation) the greater the porosity, the greater the flux from bottom. Zoobenthic reworking of fluidized gyttja by large, burrowing invertebrates like Hexagenia represents a forceful process that could reduce porosity. As faunal reworking by digestion/defecation is a “dewatering process”, feeding bioturbation in fluidized sediment deposits may result in a firmer substrate.
Organic pollution over the past century has had adverse effects on populations of benthic invertebrate fauna of lower Green Bay (Schloesser et al., 2009) which is designated by the U.S.-Canada Great Lakes Water Quality Agreement as an Area of Concern (AOC) (WDNR, 2013). Benthic invertebrates have for decades been used in several metrics as indicators of biological quality of ecosystems (Howmiller and Scott, 1977, Hilsenhoff, 1988, Cairns and Pratt, 1993, Resh et al., 1995, Schloesser et al., 1996). Burrowing mayflies of the genus Hexagenia are widely recognized for their comparative intolerance of habitat degraded by organic pollution (Hilsenhoff, 1988, Fremling, 1989, Reynoldson et al., 1989, Fremling and Johnson, 1990, Bauernfeind and Moog, 2000). They exist as substrate-burrowing nymphs for all but a few hours of their life cycles when they emerge as winged sub-adults (sub-imago) to undergo a final molt (imago) and mate, expiring shortly thereafter (Brittain, 1982). Nymph burrows are ‘u-shaped’ tunnels averaging 4–5 cm in depth (Charbonneau and Hare, 1998), and must be kept open and irrigated via gill ventilation to allow adequate oxygenation (Wang et al., 2001) and food (detritus) transfer to the burrow as well as waste removal (Kristensen, 1988, Riisgard, 1991).
Hexagenia, primarily H. limbata (Howmiller and Beeton, 1971), were once abundant to the point of nuisance in lower Green Bay. A decline in their numbers was noted in 1938 (Wisconsin State Committee on Water Pollution, 1939), and the last officially reported Hexagenia nymph was found in 1955 (Balch et al., 1956), after which Hexagenia was considered locally extirpated. Other comparable Great Lakes sites saw similar Hexagenia declines or extirpations during the same time period, but more recently recovery has been documented to varying degree at those sites. In Lake Erie's western basin, nymphs were found sporadically in very low densities prior to the mid 1990s, but the population experienced a near 40-fold increase in mean density between 1993 and 1997 (Madenjian et al., 1998, Schloesser et al., 2000). This density proved to be highly variable over the next few years but still remained comparable to densities prior to the Hexagenia decline in the 1950s (Schloesser et al., 2000, Schloesser and Nalepa, 2001, Bridgeman et al., 2006, Krieger et al., 2007). In contrast, Saginaw Bay has more recently seen a minor recovery of Hexagenia. Sampling in 2010 and 2012 (Siersma et al., 2014) revealed both slightly higher densities and also a moderately expanded distribution of Hexagenia nymphs in Saginaw Bay as compared to data reported between 1965 and 2001, with the modern distribution pattern generally reflecting that of the 1950s.
Documented reports of Hexagenia occurrence in lower Green Bay have, to date, been few. Cochran (1992) collected 13 adults from the lower Fox River in 1991. A single nymph was found during an educational sampling activity aboard the R/V Jackson near the Green Bay Metropolitan Sewerage District outfall during the summer of 2012 An individual adult was observed aboard the R/V Neeskay (UW-Milwaukee School of Freshwater Sciences) in summer 2012 (Klump, V., University of Wisconsin-Milwaukee School of Freshwater Sciences, personal communication, July 2012). During the same summer, the United States Geological Survey (USGS) encountered eight nymphs while taking benthic samples near the mouth of the lower Menominee River and another eight in a similar location on the Oconto River (Eikenberry et al., 2014). Three adults were found at Riley's Bay on the western shore of lower Green Bay in summer 2014, having been attracted by shore lights (Janssen, J. University of Wisconsin-Milwaukee School of Freshwater Sciences, personal communication, 2015). Two Hexagenia (adults) were also observed during the summer of 2015 near the De Pere dam on the lower Fox River which empties into Green Bay (Harris, H. J., University of Wisconsin-Green Bay, personal communication, July 2015). In light of the infrequent and low number of Hexagenia observed in the lower Green Bay area, populations do not appear to be actively recovering.
Critical processes such as burrow oxygenation, food accumulation, and waste removal can only occur if burrows are able to remain structurally stable for extended periods of time. Frequently collapsing burrows likely pose an energetic imbalance for Hexagenia to adequately maintain a ventilated burrow. Highly fluidized substrate present in much of lower Green Bay's benthic habitat may inhibit burrow construction and/or maintenance, thus limiting H. limbata's ability to complete its life cycle. An observation by the authors that H. bilineata nymphs were present at a site with an observably fluid substrate in the Upper Mississippi River backwaters (“Little Lake”) during July 2014 suggested that H. bilineata (as opposed to H. limbata the primary Hexagenia species historically present in Green Bay) is successful at constructing and maintaining burrows in fluidized substrates, given their high density at the Upper Mississippi River site (1110 m− 2, n = 12 Ponar grab samples). This suggests that H. bilineata may be a better candidate than H. limbata for initial stocking in fluidized sediments as a predecessor to H. limbata re-colonization. In Lake Erie, Bustos and Corkum (2013) suggested that H. rigida was a predecessor to H. limbata re-colonization. These three Hexagenia species coexist in varying dominance in habitats across the Great Lakes region (Masteller and Obert, 2000, Edsall et al., 2001), and primarily vary in terms of size (H. bilineata is the largest) (Fremling, 1960). In this study, H. bilineata's viability in terms of survival, growth, secondary production, and biomass turnover was tested in highly fluidized sediment collected from lower Green Bay in an oxygenated microcosm setting.
Section snippets
Hexagenia nymph and sediment collection
Approximately 60 L of fluidized sediment from central lower Green Bay (44° 48.092′N, 87° 44.144′W) was collected via standard Ponar grab (0.052 m− 2 opening) into a cooler for transport to the lab on October 15, 2014, and was stored at 4 °C. This site was selected due to the presence of notably fluidized substrate observed by the authors in prior sampling excursions. Approximately 30 L of substrate from the Upper Mississippi River site “Little Lake” (44° 9.435′N, 91° 47.485′W) at Merrick State Park
Results
Lower Green Bay substrate averaged 87.6% ± 1.7 water content, 0.0% sand, 90.2% ± 1.9 silt, and 9.8% ± 1.9 clay. Substrate from Little Lake, Upper Mississippi River averaged 51.4% ± 1.0 water content, 21.5% ± 3.4 sand, 33.3% ± 3.7 silt, and 45.2% ± 1.6 clay. Porosity averaged 2.02 ± 0.04 and 1.18 ± 0.02 in lower Green Bay and Upper Mississippi River substrates, respectively. Lower Green Bay substrates averaged 0.82% ± 0.05 nitrogen, 7.89% ± 0.36 total carbon, and 4.93% ± 0.11 organic carbon. Upper Mississippi River
Discussion
Based on our results, Hexagenia bilineata survival, growth, and secondary production were all higher in the fluidized lower Green Bay sediments than in the Upper Mississippi River sediments from which they were collected. Despite the water content results indicating that the Green Bay sediments are indeed more highly fluidized than are the Upper Mississippi River sediments (88% vs. 51% water respectively), the lower Green Bay sediment conditions do not appear to be factors inhibitory to H.
Conclusion
Highly fluidized substrate from lower Green Bay substrate did not negatively affect Hexagenia bilineata survival, growth, or production, and thus did not appear to hinder burrow construction or maintenance in an oxygenated laboratory setting. Based on these results, the current sediment condition of lower Green Bay does not seem to be inhibitory to Hexagenia bilineata. The mass stocking of H. bilineata and its reworking of fluidized substrate, especially in the Lower Green Bay and Fox River
Acknowledgements
The authors would like to acknowledge Captain Greg Stematelakys, the crew of the research vessel Neeskay (UW-Milwaukee School of Freshwater Science), Don Szmania (research specialist, UW-Milwaukee School of Freshwater Sciences), and Dr. J. Val Klump at the UW-Milwaukee School of Freshwater Sciences for assistance in collecting sediment from lower Green Bay, as well as UW-Milwaukee School of Freshwater Sciences graduate student Dylan Olson for field assistance on the Mississippi River. The
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2023, Wiley Interdisciplinary Reviews: Water