Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)

Many species exhibit social living which offers ecological advantages such as increased foraging opportunities, more efficient locomotion and reduced predation risk. Additionally, exposure to multiple individuals of the same species can decrease an individual’s stress and metabolic demand, termed so...

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Main Authors: Sienna L. Overduin, Shaun S. Killen, Alex M. Zimmer, Jenelle D. McCuaig, Lucy Cotgrove, Isabel Aragao, Kelly J. Rozanitis, Kurt O. Konhauser, Daniel S. Alessi, Tamzin A. Blewett
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324015082
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author Sienna L. Overduin
Shaun S. Killen
Alex M. Zimmer
Jenelle D. McCuaig
Lucy Cotgrove
Isabel Aragao
Kelly J. Rozanitis
Kurt O. Konhauser
Daniel S. Alessi
Tamzin A. Blewett
author_facet Sienna L. Overduin
Shaun S. Killen
Alex M. Zimmer
Jenelle D. McCuaig
Lucy Cotgrove
Isabel Aragao
Kelly J. Rozanitis
Kurt O. Konhauser
Daniel S. Alessi
Tamzin A. Blewett
author_sort Sienna L. Overduin
collection DOAJ
description Many species exhibit social living which offers ecological advantages such as increased foraging opportunities, more efficient locomotion and reduced predation risk. Additionally, exposure to multiple individuals of the same species can decrease an individual’s stress and metabolic demand, termed social buffering. If disruption to an animal’s social structure occurs and prevents social buffering, an elevated metabolic rate and thus ventilation frequency and gill permeability are likely. A potential consequence of this physiological response could be the increased accumulation of toxicants. The objective of this study was to investigate whether inducing social stress in marine threespine stickleback (Gasterosteus aculeatus) through social isolation during a sublethal water-borne copper (Cu) exposure would affect Cu uptake and whether that would translate to differences in behaviour and biochemical functioning. We hypothesized that isolating threespine stickleback during a Cu exposure would increase Cu uptake and sublethal toxicity compared to a grouped exposure. Wild-caught fish were exposed to control, low Cu or high Cu conditions (0 – 150 µg/L of Cu, nominally), either in isolation or groups of six for 96 h. Isolated stickleback travelled three times less distance, took six times longer to consume food and exhibited moderately increased gill sodium-potassium ATPase activity than group exposed fish, with no effect of Cu. Isolated stickleback also demonstrated significantly higher Cu levels in their gill and liver tissue compared to the group exposed fish. However, this Cu distribution was also present within the control fish, which had not been exposed to Cu, suggesting that the social context affects endogenous Cu distribution under stressful conditions. Our results illustrate the differences in physiology and behaviour that can arise when social contexts are manipulated and stress the importance of considering sociality when conducting toxicity tests with social organisms.
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spelling doaj-art-fcbac889a4944d75b1c7c0c6f9c587292025-01-23T05:25:31ZengElsevierEcotoxicology and Environmental Safety0147-65132025-01-01289117432Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)Sienna L. Overduin0Shaun S. Killen1Alex M. Zimmer2Jenelle D. McCuaig3Lucy Cotgrove4Isabel Aragao5Kelly J. Rozanitis6Kurt O. Konhauser7Daniel S. Alessi8Tamzin A. Blewett9Department of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada; Bamfield Marine Sciences Centre, Bamfield, BC V0R 1B0, Canada; Corresponding author at: Department of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada.School of Biodiversity, One Health, and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United KingdomDepartment of Biological Sciences, University of Alberta, Edmonton T6G 2E9, CanadaDepartment of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada; Bamfield Marine Sciences Centre, Bamfield, BC V0R 1B0, CanadaSchool of Biodiversity, One Health, and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow G12 8QQ, United KingdomDepartment of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada; Bamfield Marine Sciences Centre, Bamfield, BC V0R 1B0, CanadaDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton T6G 2E3, CanadaDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton T6G 2E3, CanadaDepartment of Earth and Atmospheric Sciences, University of Alberta, Edmonton T6G 2E3, CanadaDepartment of Biological Sciences, University of Alberta, Edmonton T6G 2E9, Canada; Bamfield Marine Sciences Centre, Bamfield, BC V0R 1B0, CanadaMany species exhibit social living which offers ecological advantages such as increased foraging opportunities, more efficient locomotion and reduced predation risk. Additionally, exposure to multiple individuals of the same species can decrease an individual’s stress and metabolic demand, termed social buffering. If disruption to an animal’s social structure occurs and prevents social buffering, an elevated metabolic rate and thus ventilation frequency and gill permeability are likely. A potential consequence of this physiological response could be the increased accumulation of toxicants. The objective of this study was to investigate whether inducing social stress in marine threespine stickleback (Gasterosteus aculeatus) through social isolation during a sublethal water-borne copper (Cu) exposure would affect Cu uptake and whether that would translate to differences in behaviour and biochemical functioning. We hypothesized that isolating threespine stickleback during a Cu exposure would increase Cu uptake and sublethal toxicity compared to a grouped exposure. Wild-caught fish were exposed to control, low Cu or high Cu conditions (0 – 150 µg/L of Cu, nominally), either in isolation or groups of six for 96 h. Isolated stickleback travelled three times less distance, took six times longer to consume food and exhibited moderately increased gill sodium-potassium ATPase activity than group exposed fish, with no effect of Cu. Isolated stickleback also demonstrated significantly higher Cu levels in their gill and liver tissue compared to the group exposed fish. However, this Cu distribution was also present within the control fish, which had not been exposed to Cu, suggesting that the social context affects endogenous Cu distribution under stressful conditions. Our results illustrate the differences in physiology and behaviour that can arise when social contexts are manipulated and stress the importance of considering sociality when conducting toxicity tests with social organisms.http://www.sciencedirect.com/science/article/pii/S0147651324015082SocialityFishMetalActivityMarineSodium-potassium ATPase
spellingShingle Sienna L. Overduin
Shaun S. Killen
Alex M. Zimmer
Jenelle D. McCuaig
Lucy Cotgrove
Isabel Aragao
Kelly J. Rozanitis
Kurt O. Konhauser
Daniel S. Alessi
Tamzin A. Blewett
Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
Ecotoxicology and Environmental Safety
Sociality
Fish
Metal
Activity
Marine
Sodium-potassium ATPase
title Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
title_full Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
title_fullStr Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
title_full_unstemmed Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
title_short Social context affects tissue-specific copper distribution and behaviour of threespine stickleback (Gasterosteus aculeatus)
title_sort social context affects tissue specific copper distribution and behaviour of threespine stickleback gasterosteus aculeatus
topic Sociality
Fish
Metal
Activity
Marine
Sodium-potassium ATPase
url http://www.sciencedirect.com/science/article/pii/S0147651324015082
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