Exchange rates of cadmium between a burrowing mayfly and its surroundings in nature

Abstract

We conducted a reciprocal transfer of nymphs of the burrowing mayfly Hexagenia limbata between two rivers harboring populations of this insect that differed in their cadmium (Cd) concentrations. We measured Cd uptake and loss rates simultaneously in the field at several levels of biological organization: in the gut and body of whole nymphs as well as in three subcellular fractions. The most marked changes in Cd concentrations occurred in the insect's gut, where Cd was largely associated with heat-stable proteins, a fraction that includes the metal-binding protein metallothionein. Because most of the Cd that entered nymphs was detoxified in this manner, we would not expect it to have direct toxic effects; however, it would be readily transferred to higher trophic levels. Our data on subcellular partitioning suggest that there is a fast-exchanging pool of Cd bound to heat-stable proteins such as metallothionein and a slowexchanging pool bound to either or both of the remaining fractions (heat-denatured proteins; remainder, which includes exoskeleton and granules). Nymphs of H. limbata responded rapidly to changes in bioavailable Cd, which suggests that they would be useful for monitoring changes in ambient Cd for weeks or months in the field. A one-compartment model successfully explained the changes we observed in nymph Cd values. Furthermore, values of the model constant for Cd loss were close to those reported for Hexagenia rigida in the laboratory, which suggests that accumulation patterns observed in the laboratory can be representative of those measured in nature.

Heavy metals in sediments and uptake by burrowing mayflies in western Lake Erie basin

“…This variation in sizes could be expected, based on analysis by Corkum and Hanes (1992), who suggested that a range in mayfly nymph lengths is attributable to a wide range of hatching times and nutrient availability, and hence larval size may not be a good indicator of larval age. Furthermore, Bartsch et al (1999) and Michaud et al (2005) demonstrated that nymphs accumulate a substantial amount of Cd within only a few weeks residence time in sediments. Therefore, the metal contents in the nymphs analyzed in this study are correlated to the metal contents available in the sediments and do not reflect residency time.…”

“…Hence, trophic transfer of Cd in mayflies may increase with increased sediment concentration because the Cd is in the sediment in the gut of the mayfly as well as in the gut tissue (Hare et al, 1989;Cain et al, 2004). Michaud et al (2005) concluded that Cd in the mayfly's gut was largely associated with heat-stable proteins such as the metal-binding protein metallothionein (in the cytosol), and these proteins, and thus associated metals, are readily available to consumers (i.e., fish) who assimilate metals from the cytosolic fraction of their food. Hence, the accumulation of Cd in the mayflies in the western basin of Lake Erie is of particular concern due to the high Cd levels found in the sediments, which exceeded the TEL at 27 of 28 sites and the PEL at 9 of 28 sites, and due to the potential for ready transfer to consumers.…”

“…Whole nymphs were analyzed without the removal of ingested sediments because we were interested in the concentrations of metals in Hexagenia potentially available for food-chain transfer (Michaud et al, 2005). Nymphs from each location and size-class were dried in an oven at 60°C for 12 hours (Mason et al, 2000), and were then homogenized using acid-washed glass vials and stirring rods.…”

“…In addition, studies of heavy metal contents in burrowing mayflies (Hexagenia bilineata and H. limbata) from both spiked and non-spiked Mississippi River sediments have documented the accumulation of cadmium and mercury (Beauvais et al, 1995;Bartsch et al, 1999). These investigations have shown the accumulation of Cd and Hg in mayfly nymphs was correlated to the concentrations of Cd and Hg in the sediments, and accumulation was largely through gut assimilation (Goodyear and McNeill, 1999;Michaud et al, 2005). Heavy metal levels in mayflies from the western Lake Erie basin are not known, but these sediments have higher metal concentrations than the nonspiked Mississippi River sediments (Painter et al, 2001).…”

Sediment and water quality limit mayfly survivorship in an urban lake undergoing remediation

“…Hexagenia was chosen because it is a large-bodied mayfly that lives in soft sediments, is an indicator of ecosystem health in the Great Lakes (Edsall 2001), and has been used extensively in both toxicity and bioaccumulation assays (Henry et al 1986, Gobas et al 1989, Milani et al 2003, Michaud et al 2005, Smith et al 2008, Van Geest et al 2011, Harwood et al 2014. Also, Hexagenia has an intermediate sensitivity (Milani et al 2003) and slightly lower tolerance score (6) than S. femoratum (7) (Bode et al 2002), making it a conservative addition to the study.…”