Metamorphosis Affects Metal Concentrations and Isotopic Signatures in a Mayfly (Baetis tricaudatus): Implications for the Aquatic-Terrestrial Transfer of Metals.

Insect metamorphosis often results in substantial chemical changes that can alter contaminant concentrations and fractionate isotopes. We exposed larval mayflies (Baetis tricaudatus) and their food (periphyton) to an aqueous zinc gradient (3-340 μg Zn/l) and measured zinc concentrations at different stages of metamorphosis: larval, subimago, and imago. We also measured changes in stable isotopes (δ15N and δ13C) in unexposed mayflies. Larval zinc concentrations were positively related to aqueous zinc, increasing 9-fold across the exposure gradient. Adult zinc concentrations were also positively related to aqueous zinc, but were 7-fold lower than larvae. This relationship varied according to adult substage and sex. Tissue concentrations in female imagoes were not related to exposure concentrations, but the converse was true for all other stage-by-sex combinations. Metamorphosis also increased δ15N by ∼0.8‰, but not δ13C. Thus, the main effects of metamorphosis on insect chemistry were large declines in zinc concentrations coupled with increased δ15N signatures. For zinc, this change was largely consistent across the aqueous exposure gradient. However, differences among sexes and stages suggest that caution is warranted when using nitrogen isotopes or metal concentrations measured in one insect stage (e.g., larvae) to assess risk to wildlife that feed on subsequent life stages (e.g., adults).

[1]  L. Michel.  Using stable isotopes to estimate trophic position , 2018 .

[2]  L. Balistrieri,et al.  Larval aquatic insect responses to cadmium and zinc in experimental streams , 2017, Environmental toxicology and chemistry.

[3]  Joseph S. Meyer,et al.  The Use of Field and Mesocosm Experiments to Quantify Effects of Physical and Chemical Stressors in Mining-Contaminated Streams. , 2016, Environmental science & technology.

[4]  S. Sulliván,et al.  Factors influencing aquatic-to-terrestrial contaminant transport to terrestrial arthropod consumers in a multiuse river system. , 2016, Environmental pollution.

[5]  Richard McElreath,et al.  Statistical Rethinking: A Bayesian Course with Examples in R and Stan , 2015 .

[6]  M. Hooten,et al.  Bayesian Models: A Statistical Primer for Ecologists , 2015 .

[7]  C. Mebane,et al.  Recovery of a mining-damaged stream ecosystem , 2015 .

[8]  Jeff S. Wesner,et al.  Metamorphosis alters contaminants and chemical tracers in insects: implications for food webs. , 2014, Environmental science & technology.

[9]  Jeff S. Wesner,et al.  Metamorphosis enhances the effects of metal exposure on the mayfly, Centroptilum triangulifer. , 2014, Environmental science & technology.

[10]  R. Wanty,et al.  Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs. , 2014, Ecological applications : a publication of the Ecological Society of America.

[11]  B. Peckarsky,et al.  Shifts in isotopic signatures of animals with complex life-cycles can complicate conclusions on cross-boundary trophic links , 2013, Aquatic Sciences.

[12]  R. Wanty,et al.  Emergence flux declines disproportionately to larval density along a stream metals gradient. , 2013, Environmental science & technology.

[13]  J. Trumble,et al.  Trophic Transfer of Arsenic from an Aquatic Insect to Terrestrial Insect Predators , 2013, PloS one.

[14]  P. Cadmus,et al.  Responses of aquatic insects to Cu and Zn in stream microcosms: understanding differences between single species tests and field responses. , 2013, Environmental science & technology.

[15]  B. Jackson,et al.  Spatial and Temporal Variation in the Diet of Tree Swallows: Implications for Trace-Element Exposure After Habitat Remediation , 2013, Archives of Environmental Contamination and Toxicology.

[16]  J. Kennedy,et al.  Effects of fish on emergent insect-mediated flux of methyl mercury across a gradient of contamination. , 2013, Environmental science & technology.

[17]  K. Kim,et al.  Dietary (periphyton) and aqueous Zn bioaccumulation dynamics in the mayfly Centroptilum triangulifer , 2012, Ecotoxicology.

[18]  J. Peters,et al.  Effects of Trophic Level and Metamorphosis on Discrimination of Hydrogen Isotopes in a Plant-Herbivore System , 2012, PloS one.

[19]  P. Townsend,et al.  Lake to land subsidies: experimental addition of aquatic insects increases terrestrial arthropod densities. , 2011, Ecology.

[20]  P. Warren,et al.  Environmental impact propagated by cross-system subsidy: chronic stream pollution controls riparian spider populations. , 2011, Ecology.

[21]  S. Lawler,et al.  Nonnative trout impact an alpine-nesting bird by altering aquatic-insect subsidies. , 2010, Ecology.

[22]  K. Fritz,et al.  Spider-mediated flux of PCBs from contaminated sediments to terrestrial ecosystems and potential risks to arachnivorous birds. , 2010, Environmental science & technology.

[23]  K. Fritz,et al.  The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. , 2008, Ecological applications : a publication of the Ecological Society of America.

[24]  A. White,et al.  The Movement of Aquatic Mercury Through Terrestrial Food Webs , 2008, Science.

[25]  F. Ollevier,et al.  Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality , 2008 .

[26]  C. M. Rio,et al.  Isotopic enrichment without change in diet: an ontogenetic shift in δ15N during insect metamorphosis , 2007 .

[27]  津田 松苗.  Aquatic entomology , 2007 .

[28]  K. Fausch,et al.  Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones , 2005 .

[29]  D. Post.  USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[30]  M. Murakami,et al.  Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  W. Clements,et al.  Effects of Heavy Metals on a Macroinvertebrate Assemblage from a Rocky Mountain Stream in Experimental Microcosms , 1994, Journal of the North American Benthological Society.

[32]  L. Gray.  Response of Insectivorous Birds to Emerging Aquatic Insects in Riparian Habitats of a Tallgrass Prairie Stream , 1993 .

[33]  W. Brand,et al.  Automated analysis system for coupled .delta.13C and .delta.15N measurements , 1992 .

[34]  Peter Dalgaard,et al.  R Development Core Team (2010): R: A language and environment for statistical computing , 2010 .

[35]  D. Toetz,et al.  Determination of Diets of Alpine Aquatic Insects Using Stable Isotopes and Gut Analysis , 1994 .

[36]  P. Walker,et al.  The fate of trace metals during the metamorphosis of chironomids (diptera, chironomidae). , 1989, Environmental pollution.

[37]  K. Suzuki,et al.  Excretion of cadmium and change in the relative ratio of iso-cadmium-binding proteins during metamorphosis of fleshfly (Sarcophaga peregrina). , 1984, Comparative biochemistry and physiology. C, Comparative pharmacology and toxicology.