Abstract
As a result of their industrial past, legacy cites often have elevated concentrations of soil heavy metal contamination. Metal pollution can have negative and prolonged ecosystem impacts, and bees that forage in these urban ecosystems are at risk of exposure. Legacy cities are known to support species rich bee communities, which highlights the importance of determining the impact of heavy metal contamination on wild bee health. We examined how oral exposure to concentrations of four metals found within the provisions of bees foraging within Cleveland, Ohio, USA influenced colony growth of Bombus impatiens Cresson (Hymenoptera: Apidae), a common species within legacy cities across the eastern United States. Colony weight and brood survivorship were compared among hives fed uncontaminated sucrose solution (hereafter nectar), nectar spiked with one metal (arsenic, cadmium, chromium, or lead), and nectar containing all metals, after 15 or 30 d of exposure within flight tents. Across both exposure periods, we found a significantly higher proportion of dead brood in metal exposed hives. Additionally, colonies fed all four metals had a significantly higher proportion of dead brood than those fed a single metal. Our findings illustrate that even low, environmentally relevant concentrations of metals collected by B. impatiens in legacy cities can negatively influence bee colony growth. We highlight the need to identify metal exposure routes for bees in contaminated landscapes to minimize risk and bolster conservation habitat initiative success.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be uploaded to DRYAD upon acceptance of the manuscript.
Code availability
Not applicable.
References
Ali S, Ullah MI, Saeed MF et al (2019) Heavy metal exposure through artificial diet reduces growth and survival of Spodoptera litura (Lepidoptera: Noctuidae). Environ Sci Pollut Res 26:14426–14434. https://doi.org/10.1007/s11356-019-04792-0
Anderson EC, Minor ES (2017) Vacant lots: An underexplored resource for ecological and social benefits in cities. Urban for Urban Green 21:146–152. https://doi.org/10.1016/j.ufug.2016.11.015
Bromenshenk JJ, Carlson SR, Simpson JC, Thomas JM (1985) Pollution Monitoring of Puget Sound with Honey Bees. Science 227:632–634. https://doi.org/10.1126/science.227.4687.632
Burden CM, Amdam G, Smith BH et al (2016a) Sublethal Effects of Heavy Metal and Metalloid Exposure in Honey Bees: Behavioral Modifications and Potential Mechanisms. In: ASU Electronic Theses and Dissertations. Arizona State University
Burden CM, Elmore C, Hladun KR et al (2016b) Acute exposure to selenium disrupts associative conditioning and long-term memory recall in honey bees (Apis mellifera). Ecotoxicol Environ Saf 127:71–79. https://doi.org/10.1016/j.ecoenv.2015.12.034
Chaffin BC, Shuster WD, Garmestani AS et al (2016) A tale of two rain gardens: Barriers and bridges to adaptive management of urban stormwater in Cleveland, Ohio. J Environ Manage 183:431–441. https://doi.org/10.1016/j.jenvman.2016.06.025
Christoforidis A, Stamatis N (2009) Heavy metal contamination in street dust and roadside soil along the major national road in Kavala’s region, Greece. Geoderma 151:257–263. https://doi.org/10.1016/j.geoderma.2009.04.016
Conti ME, Botrè F (2001) Honeybees and Their Products as Potential Bioindicators of Heavy Metals Contamination. Environ Monit Assess 69:267–282. https://doi.org/10.1023/A:1010719107006
Crall JD, Switzer CM, Oppenheimer RL et al (2018) Neonicotinoid exposure disrupts bumblebee nest behavior, social networks, and thermoregulation. Science 362:683–686. https://doi.org/10.1126/science.aat1598
Davydova S (2005) Heavy metals as toxicants in big cities. Microchem J 79:133–136. https://doi.org/10.1016/j.microc.2004.06.010
Delgado de la Flor YA, Burkman CE, Eldredge TK, Gardiner MM (2017) Patch and landscape-scale variables influence the taxonomic and functional composition of beetles in urban greenspaces. Ecosphere 8:e02007. https://doi.org/10.1002/ecs2.2007
Delgado de la Flor YA, Perry KI, Turo KJ et al (2020) Local and landscape-scale environmental filters drive the functional diversity and taxonomic composition of spiders across urban greenspaces. J Appl Ecol 57:1570–1580. https://doi.org/10.1111/1365-2664.13636
Delibes M, Gaona P, Ferreras P (2001) Effects of an attractive sink leading into maladaptive habitat selection. Am Nat 158:277–285. https://doi.org/10.1086/321319
Di N, Hladun KR, Zhang K et al (2016) Laboratory bioassays on the impact of cadmium, copper and lead on the development and survival of honeybee (Apis mellifera L.) larvae and foragers. Chemosphere 152:530–538. https://doi.org/10.1016/j.chemosphere.2016.03.033
dos Santos CF, Acosta AL, Dorneles AL et al (2016) Queens become workers: pesticides alter caste differentiation in bees. Sci Rep 6:31605. https://doi.org/10.1038/srep31605
Edgington T (2020) Beirut explosion: What is ammonium nitrate and how dangerous is it? BBC News
Foster D, Swanson F, Aber J et al (2003) The Importance of Land-Use Legacies to Ecology and Conservation. Bioscience 53:77–88. https://doi.org/10.1641/0006-3568(2003)053[0077:TIOLUL]2.0.CO;2
Foust RD, Bauer A-M, Costanza-Robinson M et al (2016) Arsenic transfer and biotransformation in a fully characterized freshwater food web. Coord Chem Rev 306:558–565. https://doi.org/10.1016/j.ccr.2015.03.005
Gajbhiye T, Kim K-H, Pandey SK, Brown RJC (2016) Foliar Transfer of Dust and Heavy Metals on Roadside Plants in a Subtropical Environment. 9
Gardiner M, Delgado de la Flor Y, Parker D, Harwood J (2020) Rich and abundant spider communities result from enhanced web capture breadth and reduced overlap in urban greenspaces. Ecol Appl. https://doi.org/10.1002/eap.2282
Gardiner MM, Burkman CE, Prajzner SP (2013) The value of urban vacant land to support arthropod biodiversity and ecosystem services. Environ Entomol 42:1123–1136. https://doi.org/10.1603/EN12275
Haase A, Rink D, Grossmann K et al (2014) Conceptualizing Urban Shrinkage. Environ Plan Econ Space 46:1519–1534. https://doi.org/10.1068/a46269
Harrison T, Winfree R (2015) Urban drivers of plant-pollinator interactions. Funct Ecol 29:879–888. https://doi.org/10.1111/1365-2435.12486
Hartley D (2013) Urban Decline in Rust-belt Cities. Econ Comment
Heinrich B (2002) The Natural History of Bumblebees: A Sourcebook for Investigations. By Carol A Kearns and James D Thomson. Q Rev Biol 77:206–206. https://doi.org/10.1086/343965
Jennings AA, Cox AN, Hise SJ, Petersen EJ (2002) Heavy Metal Contamination in the Brownfield Soils of Cleveland. Soil Sediment Contam Int J 11:719–750. https://doi.org/10.1080/20025891107069
Johnson RM, Mao W, Pollock HS et al (2012) Ecologically Appropriate Xenobiotics Induce Cytochrome P450s in Apis mellifera. PLoS ONE 7.https://doi.org/10.1371/journal.pone.0031051
Kelly J, Thornton I, Simpson PR (1996) Urban Geochemistry: A study of the influence of anthropogenic activity on the heavy metal content of soils in traditionally industrial and non-industrial areas of Britain. Appl Geochem 11:363–370. https://doi.org/10.1016/0883-2927(95)00084-4
Kim H-S, Kim K-R, Lim G-H et al (2015) Influence of airborne dust on the metal concentrations in crop plants cultivated in a rooftop garden in Seoul. Soil Sci Plant Nutr 61:88–97. https://doi.org/10.1080/00380768.2015.1028873
Liu N (2008) Recent advances in insect physiology, toxicology and molecular biology 2008. Research Signpost, Trivandrum, India
Martinez-Fernandez C, Audirac I, Fol S, Cunningham-Sabot E (2012) Shrinking Cities: Urban Challenges of Globalization. Int J Urban Reg Res 36:213–225. https://doi.org/10.1111/j.1468-2427.2011.01092.x
Meindl GA, Bain DJ, Ashman T-L (2014) Variation in nickel accumulation in leaves, reproductive organs and floral rewards in two hyperaccumulating Brassicaceae species. Plant Soil 383:349–356. https://doi.org/10.1007/s11104-014-2184-8
Merritt TJS, Bewick AJ (2017) Genetic Diversity in Insect Metal Tolerance. Front Genet 8:.https://doi.org/10.3389/fgene.2017.00172
Moroń D, Grześ IM, Skórka P et al (2012) Abundance and diversity of wild bees along gradients of heavy metal pollution. J Appl Ecol 49:118–125. https://doi.org/10.1111/j.1365-2664.2011.02079.x
Moroń D, Szentgyörgyi H, Skórka P et al (2014) Survival, reproduction and population growth of the bee pollinator, Osmia rufa (Hymenoptera: Megachilidae), along gradients of heavy metal pollution. Insect Conserv Divers 7:113–121. https://doi.org/10.1111/icad.12040
Morton MJ (2002) The Suburban Ideal and Suburban Realities: Cleveland Heights, Ohio, 1860–2001. J Urban Hist 28:671–698. https://doi.org/10.1177/0096144202028006001
Nanda KP, Firdaus H (2021) Dietary cadmium (Cd) reduces hemocyte level by induction of apoptosis in Drosophila melanogaster. Comp Biochem Physiol Part C Toxicol Pharmacol 250:109188. https://doi.org/10.1016/j.cbpc.2021.109188
Perry KI, Hoekstra NC, Delgado de la Flor YA, Gardiner MM (2020) Disentangling landscape and local drivers of ground-dwelling beetle community assembly in an urban ecosystem. Ecol Appl 30:e02191. https://doi.org/10.1002/eap.2191
Perugini M, Manera M, Grotta L et al (2011) Heavy Metal (Hg, Cr, Cd, and Pb) Contamination in Urban Areas and Wildlife Reserves: Honeybees as Bioindicators. Biol Trace Elem Res 140:170–176. https://doi.org/10.1007/s12011-010-8688-z
Petersen EJ, Jennings AA, Ma J (2006) Screening Level Risk Assessment of Heavy Metal Contamination in Cleveland Area Commons. J Environ Eng 132:392–404. https://doi.org/10.1061/(ASCE)0733-9372(2006)132:3(392)
Polykretis P, Delfino G, Petrocelli I et al (2016) Evidence of immunocompetence reduction induced by cadmium exposure in honey bees (Apis mellifera). Environ Pollut 218. https://doi.org/10.1016/j.envpol.2016.08.006
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci Int J Exp Plant Biol 180:169–181. https://doi.org/10.1016/j.plantsci.2010.08.016
Reeves RD, Baker AJM, Jaffré T et al (2018) A global database for plants that hyperaccumulate metal and metalloid trace elements. New Phytol 218:407–411. https://doi.org/10.1111/nph.14907
Rega-Brodsky CC, Nilon CH (2016) Vacant lots as a habitat resource: nesting success and body condition of songbirds. Ecosphere 7:e01578. https://doi.org/10.1002/ecs2.1578
Riley CB, Gardiner MM (2020) Examining the distributional equity of urban tree canopy cover and ecosystem services across United States cities. PLoS ONE 15:e0228499. https://doi.org/10.1371/journal.pone.0228499
Riley CB, Herms DA, Gardiner MM (2018) Exotic trees contribute to urban forest diversity and ecosystem services in inner-city Cleveland, OH. Urban for Urban Green 29:367–376. https://doi.org/10.1016/j.ufug.2017.01.004
Robinson SL, Lundholm JT (2012) Ecosystem services provided by urban spontaneous vegetation. Urban Ecosyst 15:545–557. https://doi.org/10.1007/s11252-012-0225-8
Rothman JA, Leger L, Kirkwood JS, McFrederick QS (2019) Cadmium and Selenate Exposure Affects the Honey Bee Microbiome and Metabolome, and Bee-Associated Bacteria Show Potential for Bioaccumulation. Appl Environ Microbiol 85:e01411-e1419. https://doi.org/10.1128/AEM.01411-19
Sampson N, Nassauer J, Schulz A et al (2017) Landscape care of urban vacant properties and implications for health and safety: Lessons from photovoice. Health Place 46:219–228. https://doi.org/10.1016/j.healthplace.2017.05.017
Sánchez-Bayo F, Wyckhuys KAG (2019) Worldwide decline of the entomofauna: A review of its drivers. Biol Conserv 232:8–27. https://doi.org/10.1016/j.biocon.2019.01.020
Sansalone JJ, Buchberger SG, Al-Abed SR (1996) Fractionation of heavy metals in pavement runoff. Sci Total Environ 189–190:371–378. https://doi.org/10.1016/0048-9697(96)05233-3
Sharma K, Basta NT, Grewal PS (2015) Soil heavy metal contamination in residential neighborhoods in post-industrial cities and its potential human exposure risk. Urban Ecosyst 18:115–132. https://doi.org/10.1007/s11252-014-0395-7
Sivakoff FS, Prajzner SP, Gardiner MM (2018) Unique Bee Communities within Vacant Lots and Urban Farms Result from Variation in Surrounding Urbanization Intensity. Sustainability 10:1926. https://doi.org/10.3390/su10061926
Sivakoff FS, Prajzner SP, Gardiner MM (2020) Urban heavy metal contamination limits bumble bee colony growth. J Appl Ecol n/a: https://doi.org/10.1111/1365-2664.13651
Su C, Jiang L, Zhang W (2014) A review on heavy metal contamination in the soil worldwide: Situation, impact and remediation techniques. 15
Szentgyörgyi H, Blinov A, Eremeeva N et al (2011) Bumblebees (Bombidae) along pollution gradient - Heavy metal accumulation, species diversity, and Nosema bombi infection level. Pol J Ecol 59:599–610
Tannous WK (2019) Notre-Dame fire: Lead test call for pregnant women and children. BBC News
Tovar-Sánchez E, Hernández-Plata I, Martínez M et al (2018) Heavy Metal Pollution as a Biodiversity Threat
Turo KJ, Gardiner MM (2019) From potential to practical: conserving bees in urban public green spaces. Front Ecol Environ 17:167–175. https://doi.org/10.1002/fee.2015
van der Steen JJM, de Kraker J, Grotenhuis T (2012) Spatial and temporal variation of metal concentrations in adult honeybees (Apis mellifera L.). Environ Monit Assess 184:4119–4126. https://doi.org/10.1007/s10661-011-2248-7
Venables WN, Ripley BD (2002) Modern Applied Statistics with S, Fourth edition. Springer, New York. ISBN 0–387–95457–0, https://www.stats.ox.ac.uk/pub/MASS4/
Wilson D, Wouters J (2003) Spatiality and Growth Discourse: The Restructuring of America’s Rust Belt Cities. J Urban Aff 25:123–138. https://doi.org/10.1111/1467-9906.t01-1-00002
Wuana RA, Okieimen FE (2011) Heavy Metals in Contaminated Soils: A Review of Sources, Chemistry, Risks and Best Available Strategies for Remediation. In: Int. Sch. Res. Not. https://www.hindawi.com/journals/isrn/2011/402647/. Accessed 22 Aug 2019
Xu J, Strange JP, Welker DL, James RR (2013) Detoxification and stress response genes expressed in a western North American bumble bee, Bombus huntii(Hymenoptera: Apidae). BMC Genomics 14:874. https://doi.org/10.1186/1471-2164-14-874
Xun E, Zhang Y, Zhao J, Guo J (2017) Translocation of heavy metals from soils into floral organs and rewards of Cucurbita pepo: Implications for plant reproductive fitness. Ecotoxicol Environ Saf 145:235–243. https://doi.org/10.1016/j.ecoenv.2017.07.045
Yoo J-W, Cho H, Lee K-W et al (2021) Combined effects of heavy metals (Cd, As, and Pb): Comparative study using conceptual models and the antioxidant responses in the brackish water flea. Comp Biochem Physiol Part C Toxicol Pharmacol 239:108863. https://doi.org/10.1016/j.cbpc.2020.108863
Zioga E, Kelly R, White B, Stout JC (2020) Plant protection product residues in plant pollen and nectar: A review of current knowledge. Environ Res 189:109873. https://doi.org/10.1016/j.envres.2020.109873
Acknowledgements
We thank all undergraduate assistants who helped with the collection and processing of samples for this project, Glenn Mills for providing assistance and support with the field cages, and Dr. P. Jourdan for lending germplasm cages for use in this project. Funding was provided by the USDA National Institute of Food and Agriculture (20176701326595) to M.M.G and F.S.S, and the US National Science Foundation Graduate Research Fellowship Program (DGE-1343012) to S.B.S, and OSU CFAES SEEDS grant to S.B.S.
Funding
Funding was provided by the USDA National Institute of Food and Agriculture (20176701326595) to M.M.G and F.S.S, and the US National Science Foundation Graduate Research Fellowship Program (DGE-1343012) to S.B.S, and OSU CFAES SEEDS grant to S.B.S.
Author information
Authors and Affiliations
Contributions
S.B.S., M.M.G., and F.S.S conceived the ideas and designed methodology; S.B.S collected the data; S.B.S and F.S.S. analyzed the data and interpreted the results; S.B.S led the writing of the manuscript with revisions from M.M.G and F.S.S; all authors gave final approval for publication.
Corresponding author
Ethics declarations
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Conflicts of interest
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Scott, S.B., Sivakoff, F.S. & Gardiner, M.M. Exposure to urban heavy metal contamination diminishes bumble bee colony growth. Urban Ecosyst 25, 989–997 (2022). https://doi.org/10.1007/s11252-022-01206-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11252-022-01206-x