Metals and metal isotopes incorporation in insect wings: Implications for geolocation and pollution exposure

Anthropogenic activities are exposing insects to elevated levels of toxic metals and are altering the bioavailability of essential metals. Metals and metal isotopes have also become promising tools for the geolocation of migratory insects. Understanding the pathways of metal incorporation in insect tissues is thus important for assessing the role of metals in insect physiology and ecology and for the development of metals and metal isotopes as geolocation tools. We conducted a diet-switching experiment on monarch butterflies [Danaus plexippus (L.)] with controlled larval and adult diets to evaluate the sources of 23 metals and metalloids, strontium isotopes, and lead isotopes to insect wing tissues over a period of 8 weeks. Concentrations of Ca, Co, Mo, and Sb differed between the sexes or with body mass. Ni and Zn bioaccumulated in the insect wing tissues over time, likely from the adult diet, while increases in Al, Cr, Cd, Cu, Fe, and Pb were, at least partially, from external sources (i.e., dust aerosols). Bioaccumulation of Pb in the monarch wings was confirmed by Pb isotopes to mainly be sourced from external anthropogenic sources, revealing the potential of Pb isotopes to become an indicator and tracer of metal pollution exposure along migratory paths. Concentrations of Ba, Cs, Mg, Na, Rb, Sr, Ti, Tl, and U appeared to be unaffected by intrinsic factors or additions of metals from adult dietary or external sources, and their potential for geolocation should be further explored. Strontium isotope ratios remained indicative of the larval diet, at least in males, supporting its potential as a geolocation tool. However, the difference in strontium isotope ratios between sexes, as well as the possibility of external contamination by wetting, requires further investigation. Our results demonstrate the complexity of metal incorporation processes in insects and the value of studying metals to develop new tools to quantify pollution exposure, metal toxicity, micronutrient uptake, and insect mobility.

This study was funded by the New Frontiers in Research Fund (CB and GT) and Syngenta Canada, Inc. (RN). GT acknowledges funding from the grant PID2020-117739GA-I00 from MCIN/AEI/10.13039/501100011033 and the grant LINKA20399 from the CSIC iLink program. MR was supported by the Queen Elizabeth II Graduate Scholarship in Science and Technology (QEII-GSST) and an OntarioGraduate Scholarship.

1. Introduction 2. Materials and methods 2.1. Diet-switching experiment 2.1.1. Trace element analysis 2.1.2. Strontium isotope ratios analysis 2.1.3. Lead isotope ratios analysis 2.1.4. Statistical analysis 2.1.5. Mobility index and enrichment factors 2.2. Wetting experiment 2.3. Natural metal concentrations in monarchs 3. Results 3.1. Metals classified into four categories 3.2. Strontium and strontium isotope ratios 3.3. Lead and lead isotope ratios 3.4. Natural metal concentrations in lab-raised and wild monarchs 4. Discussion 4.1. Regulation of metals in insect wings 4.2. Bioaccumulation of metals in insect wings 4.3. Geolocation using metals and metal isotopes 4.4. Natural metal concentrations 5. Conclusion Data availability statement Author contributions Funding Acknowledgments Conflict of interest Publisher’s note Supplementary material References