Detecting copper toxicity in sediments

from the subindividual level to the population level

Katherine J. Jeppe, Jianghua Yang, Sara M. Long, Melissa E. Carew, Xiaowei Zhang, Vincent Pettigrove, Ary A. Hoffmann

Research output: Contribution to journalArticleResearchpeer-review

5 Citations (Scopus)

Abstract

Sediments accumulate chemicals that can be toxic to biota and often contribute to aquatic ecosystem decline. Measuring mortality in laboratory-bred organisms is a common way to assess sediment toxicity. However, mortality-based responses of resilient laboratory organisms may not reflect indigenous macroinvertebrate responses, which can be relatively more sensitive to sediment toxicants. A possible solution is to also measure responses at the subindividual level. Several organism responses to sediment copper toxicity were assessed in a field-based microcosm. Responses of laboratory-bred chironomids and snails deployed in microcosms were compared at subindividual (metabolomic and gene expression), individual (survival and dry weight) and population (reproduction) levels, and contrasted to the abundance of colonizing macroinvertebrates in the microcosms. Colonizing macroinvertebrate abundance showed a range of sensitivities based on EC50 (effect dose 50% change). Chironomidae made up 94·5% of the microcosm macroinvertebrates, with Paratanytarsus the most sensitive genus (EC50: 89 mg kg−1 copper) and Procladius the least sensitive (EC50: 681 mg kg−1). Survival of laboratory-bred organisms was the least sensitive response, comparable to decreased abundance of the least sensitive macroinvertebrate. Juvenile production in the snail, Potamopyrgus antipodarum, was the most sensitive population-level response (EC50: 121 mg kg−1), in contrast the snail Physella acuta was relatively more tolerant (EC50: 298 mg kg−1). Changes in subindividual responses (gene expression and metabolite abundance) in laboratory-bred chironomid, Chironomus tepperi, were evident at 60 mg kg−1. These changes likely reflect the direct effects of copper exposure and represent metal-specific responses. Synthesis and applications. We showed that copper toxicity in sediments could be readily detected through changes in gene expression and metabolites in laboratory-bred chironomids exposed in field-based microcosms. These responses were more sensitive than mortality, and detected copper levels that caused microcosm chironomid populations to decline. These novel approaches will provide managers with new tools to better assess sediment toxicity.

Original languageEnglish
Pages (from-to)1331-1342
Number of pages12
JournalJournal of Applied Ecology
Volume54
Issue number5
DOIs
Publication statusPublished - 1 Oct 2017
Externally publishedYes

Keywords

  • biomarkers
  • chironomids
  • copper toxicity
  • cysteine metabolism
  • gene expression
  • mesocosm
  • metabolomics
  • microcosm
  • sediment toxicity
  • transsulfuration

Cite this

Jeppe, K. J., Yang, J., Long, S. M., Carew, M. E., Zhang, X., Pettigrove, V., & Hoffmann, A. A. (2017). Detecting copper toxicity in sediments: from the subindividual level to the population level. Journal of Applied Ecology, 54(5), 1331-1342. https://doi.org/10.1111/1365-2664.12840
Jeppe, Katherine J. ; Yang, Jianghua ; Long, Sara M. ; Carew, Melissa E. ; Zhang, Xiaowei ; Pettigrove, Vincent ; Hoffmann, Ary A. / Detecting copper toxicity in sediments : from the subindividual level to the population level. In: Journal of Applied Ecology. 2017 ; Vol. 54, No. 5. pp. 1331-1342.
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abstract = "Sediments accumulate chemicals that can be toxic to biota and often contribute to aquatic ecosystem decline. Measuring mortality in laboratory-bred organisms is a common way to assess sediment toxicity. However, mortality-based responses of resilient laboratory organisms may not reflect indigenous macroinvertebrate responses, which can be relatively more sensitive to sediment toxicants. A possible solution is to also measure responses at the subindividual level. Several organism responses to sediment copper toxicity were assessed in a field-based microcosm. Responses of laboratory-bred chironomids and snails deployed in microcosms were compared at subindividual (metabolomic and gene expression), individual (survival and dry weight) and population (reproduction) levels, and contrasted to the abundance of colonizing macroinvertebrates in the microcosms. Colonizing macroinvertebrate abundance showed a range of sensitivities based on EC50 (effect dose 50{\%} change). Chironomidae made up 94·5{\%} of the microcosm macroinvertebrates, with Paratanytarsus the most sensitive genus (EC50: 89 mg kg−1 copper) and Procladius the least sensitive (EC50: 681 mg kg−1). Survival of laboratory-bred organisms was the least sensitive response, comparable to decreased abundance of the least sensitive macroinvertebrate. Juvenile production in the snail, Potamopyrgus antipodarum, was the most sensitive population-level response (EC50: 121 mg kg−1), in contrast the snail Physella acuta was relatively more tolerant (EC50: 298 mg kg−1). Changes in subindividual responses (gene expression and metabolite abundance) in laboratory-bred chironomid, Chironomus tepperi, were evident at 60 mg kg−1. These changes likely reflect the direct effects of copper exposure and represent metal-specific responses. Synthesis and applications. We showed that copper toxicity in sediments could be readily detected through changes in gene expression and metabolites in laboratory-bred chironomids exposed in field-based microcosms. These responses were more sensitive than mortality, and detected copper levels that caused microcosm chironomid populations to decline. These novel approaches will provide managers with new tools to better assess sediment toxicity.",
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Jeppe, KJ, Yang, J, Long, SM, Carew, ME, Zhang, X, Pettigrove, V & Hoffmann, AA 2017, 'Detecting copper toxicity in sediments: from the subindividual level to the population level', Journal of Applied Ecology, vol. 54, no. 5, pp. 1331-1342. https://doi.org/10.1111/1365-2664.12840

Detecting copper toxicity in sediments : from the subindividual level to the population level. / Jeppe, Katherine J.; Yang, Jianghua; Long, Sara M.; Carew, Melissa E.; Zhang, Xiaowei; Pettigrove, Vincent; Hoffmann, Ary A.

In: Journal of Applied Ecology, Vol. 54, No. 5, 01.10.2017, p. 1331-1342.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Detecting copper toxicity in sediments

T2 - from the subindividual level to the population level

AU - Jeppe, Katherine J.

AU - Yang, Jianghua

AU - Long, Sara M.

AU - Carew, Melissa E.

AU - Zhang, Xiaowei

AU - Pettigrove, Vincent

AU - Hoffmann, Ary A.

PY - 2017/10/1

Y1 - 2017/10/1

N2 - Sediments accumulate chemicals that can be toxic to biota and often contribute to aquatic ecosystem decline. Measuring mortality in laboratory-bred organisms is a common way to assess sediment toxicity. However, mortality-based responses of resilient laboratory organisms may not reflect indigenous macroinvertebrate responses, which can be relatively more sensitive to sediment toxicants. A possible solution is to also measure responses at the subindividual level. Several organism responses to sediment copper toxicity were assessed in a field-based microcosm. Responses of laboratory-bred chironomids and snails deployed in microcosms were compared at subindividual (metabolomic and gene expression), individual (survival and dry weight) and population (reproduction) levels, and contrasted to the abundance of colonizing macroinvertebrates in the microcosms. Colonizing macroinvertebrate abundance showed a range of sensitivities based on EC50 (effect dose 50% change). Chironomidae made up 94·5% of the microcosm macroinvertebrates, with Paratanytarsus the most sensitive genus (EC50: 89 mg kg−1 copper) and Procladius the least sensitive (EC50: 681 mg kg−1). Survival of laboratory-bred organisms was the least sensitive response, comparable to decreased abundance of the least sensitive macroinvertebrate. Juvenile production in the snail, Potamopyrgus antipodarum, was the most sensitive population-level response (EC50: 121 mg kg−1), in contrast the snail Physella acuta was relatively more tolerant (EC50: 298 mg kg−1). Changes in subindividual responses (gene expression and metabolite abundance) in laboratory-bred chironomid, Chironomus tepperi, were evident at 60 mg kg−1. These changes likely reflect the direct effects of copper exposure and represent metal-specific responses. Synthesis and applications. We showed that copper toxicity in sediments could be readily detected through changes in gene expression and metabolites in laboratory-bred chironomids exposed in field-based microcosms. These responses were more sensitive than mortality, and detected copper levels that caused microcosm chironomid populations to decline. These novel approaches will provide managers with new tools to better assess sediment toxicity.

AB - Sediments accumulate chemicals that can be toxic to biota and often contribute to aquatic ecosystem decline. Measuring mortality in laboratory-bred organisms is a common way to assess sediment toxicity. However, mortality-based responses of resilient laboratory organisms may not reflect indigenous macroinvertebrate responses, which can be relatively more sensitive to sediment toxicants. A possible solution is to also measure responses at the subindividual level. Several organism responses to sediment copper toxicity were assessed in a field-based microcosm. Responses of laboratory-bred chironomids and snails deployed in microcosms were compared at subindividual (metabolomic and gene expression), individual (survival and dry weight) and population (reproduction) levels, and contrasted to the abundance of colonizing macroinvertebrates in the microcosms. Colonizing macroinvertebrate abundance showed a range of sensitivities based on EC50 (effect dose 50% change). Chironomidae made up 94·5% of the microcosm macroinvertebrates, with Paratanytarsus the most sensitive genus (EC50: 89 mg kg−1 copper) and Procladius the least sensitive (EC50: 681 mg kg−1). Survival of laboratory-bred organisms was the least sensitive response, comparable to decreased abundance of the least sensitive macroinvertebrate. Juvenile production in the snail, Potamopyrgus antipodarum, was the most sensitive population-level response (EC50: 121 mg kg−1), in contrast the snail Physella acuta was relatively more tolerant (EC50: 298 mg kg−1). Changes in subindividual responses (gene expression and metabolite abundance) in laboratory-bred chironomid, Chironomus tepperi, were evident at 60 mg kg−1. These changes likely reflect the direct effects of copper exposure and represent metal-specific responses. Synthesis and applications. We showed that copper toxicity in sediments could be readily detected through changes in gene expression and metabolites in laboratory-bred chironomids exposed in field-based microcosms. These responses were more sensitive than mortality, and detected copper levels that caused microcosm chironomid populations to decline. These novel approaches will provide managers with new tools to better assess sediment toxicity.

KW - biomarkers

KW - chironomids

KW - copper toxicity

KW - cysteine metabolism

KW - gene expression

KW - mesocosm

KW - metabolomics

KW - microcosm

KW - sediment toxicity

KW - transsulfuration

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U2 - 10.1111/1365-2664.12840

DO - 10.1111/1365-2664.12840

M3 - Article

VL - 54

SP - 1331

EP - 1342

JO - Journal of Applied Ecology

JF - Journal of Applied Ecology

SN - 0021-8901

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