Environmental Pollution 205 (2015) 365e377
Contents lists available at ScienceDirect
Environmental Pollution journal homepage: www.elsevier.com/locate/envpol
The Little Penguin (Eudyptula minor) as an indicator of coastal trace metal pollution Annett Finger a, *, Jennifer L. Lavers b, Peter Dann c, Dayanthi Nugegoda d, John D. Orbell a, Bruce Robertson e, Carol Scarpaci a a
Victoria University, Institute for Sustainability & Innovation, Hoppers Crossing, Werribee, Victoria 3030, Australia Institute for Marine and Antarctic Studies, 20 Castray Esplanade, Battery Point, Tasmania 7004, Australia Phillip Island Nature Parks, Research Department, PO Box 97, Cowes, Victoria 3922, Australia d RMIT University, School of Applied Science, GPO Box 2476, Melbourne, Victoria, Australia e Department of Environmental Management and Ecology, LaTrobe University, Wodonga, Victoria 3689, Australia b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 February 2015 Received in revised form 2 June 2015 Accepted 11 June 2015 Available online xxx
Monitoring trace metal and metalloid concentrations in marine animals is important for their conservation and could also reliably reflect pollution levels in their marine ecosystems. Concentrations vary across tissue types, with implications for reliable monitoring. We sampled blood and moulted feathers of the Little Penguin (Eudyptula minor) from three distinct colonies, which are subject to varying levels of anthropogenic impact. Non-essential trace metal and metalloid concentrations in Little Penguins were clearly linked to the level of industrialisation adjacent to the respective foraging zones. This trend was more distinct in blood than in moulted feathers, although we found a clear correlation between blood and feathers for mercury, lead and iron. This study represents the first reported examination of trace metals and metalloids in the blood of any penguin species and demonstrates that this high trophic feeder is an effective bioindicator of coastal pollution. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Trace element Blood Seabird Australia Bioindicator
1. Introduction Toxicants are present in our environment, particularly in the marine environment, because the ocean acts as a sink (Neff, 2002). Influx from rivers, agricultural and urban land runoff, sewage outfalls, long-range atmospheric transport and deposition all contribute to elevated levels of contaminants in marine ecosystems (Lamborg et al., 2014). Monitoring this pollution and assessing its ecological and human health effects has become a global concern (Islam and Tanaka, 2004). Metals in particular, have been shown to have a negative impact on coastal ecosystems in highly industrialised areas (Geens et al., 2010). Metals are released by both natural (erosion, volcanism and upwelling) and anthropogenic sources (mining, smelting, metallurgy), often accumulate in organisms at higher trophic levels and have been studied in a range of seabirds to investigate temporal and spatial variation (Furness, 1993; Becker, 2003; Vo et al., 2011). Many researchers report on trace metal concentrations in
* Corresponding author. E-mail address: [email protected] (A. Finger). http://dx.doi.org/10.1016/j.envpol.2015.06.022 0269-7491/© 2015 Elsevier Ltd. All rights reserved.
internal tissues and samples are often collected destructively, i.e. by sacrificing randomly selected members of a population (Bacher, 1985; Smichowski et al., 2006), or opportunistically, i.e. starved or killed 'by misadventure' (Lock et al., 1992; Gibbs, 1995; Choong et al., 2007). While the former has ethical implications and cannot be applied to species of conservation concern, the latter carries potentially unquantified biases including (1) the sample not being representative of a random cross-section of the population, (2) unknown provenance, (3) unknown cause of death, and (4) altered lipid content in a starved organ which can lead to falsely elevated elemental concentrations (Bryan et al., 2007). Feather collection is the most common non-destructive sampling protocol (Burger, 1993). Moulted feathers can be obtained non-invasively and transported and stored with minimal cost. Shunting nonessential trace metals to the feathers is a main method of detoxification in seabirds (Furness et al., 1986), but feather metal concentrations are often a poor indicator for internal tissue concentrations (Eagles-Smith et al., 2008; Lavers and Bond, 2013) and results can be highly biased by external contamination (Jaspers et al., 2004). Recent advances in trace analysis such as atomic absorption spectrometry (AAS) and inductively-coupled plasma spectrometry
366
A. Finger et al. / Environmental Pollution 205 (2015) 365e377
(ICP) promote non-destructive cross-section sampling, e.g. the taking of a small sample of blood (
Contents lists available at ScienceDirect
Environmental Pollution journal homepage: www.elsevier.com/locate/envpol
The Little Penguin (Eudyptula minor) as an indicator of coastal trace metal pollution Annett Finger a, *, Jennifer L. Lavers b, Peter Dann c, Dayanthi Nugegoda d, John D. Orbell a, Bruce Robertson e, Carol Scarpaci a a
Victoria University, Institute for Sustainability & Innovation, Hoppers Crossing, Werribee, Victoria 3030, Australia Institute for Marine and Antarctic Studies, 20 Castray Esplanade, Battery Point, Tasmania 7004, Australia Phillip Island Nature Parks, Research Department, PO Box 97, Cowes, Victoria 3922, Australia d RMIT University, School of Applied Science, GPO Box 2476, Melbourne, Victoria, Australia e Department of Environmental Management and Ecology, LaTrobe University, Wodonga, Victoria 3689, Australia b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 17 February 2015 Received in revised form 2 June 2015 Accepted 11 June 2015 Available online xxx
Monitoring trace metal and metalloid concentrations in marine animals is important for their conservation and could also reliably reflect pollution levels in their marine ecosystems. Concentrations vary across tissue types, with implications for reliable monitoring. We sampled blood and moulted feathers of the Little Penguin (Eudyptula minor) from three distinct colonies, which are subject to varying levels of anthropogenic impact. Non-essential trace metal and metalloid concentrations in Little Penguins were clearly linked to the level of industrialisation adjacent to the respective foraging zones. This trend was more distinct in blood than in moulted feathers, although we found a clear correlation between blood and feathers for mercury, lead and iron. This study represents the first reported examination of trace metals and metalloids in the blood of any penguin species and demonstrates that this high trophic feeder is an effective bioindicator of coastal pollution. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Trace element Blood Seabird Australia Bioindicator
1. Introduction Toxicants are present in our environment, particularly in the marine environment, because the ocean acts as a sink (Neff, 2002). Influx from rivers, agricultural and urban land runoff, sewage outfalls, long-range atmospheric transport and deposition all contribute to elevated levels of contaminants in marine ecosystems (Lamborg et al., 2014). Monitoring this pollution and assessing its ecological and human health effects has become a global concern (Islam and Tanaka, 2004). Metals in particular, have been shown to have a negative impact on coastal ecosystems in highly industrialised areas (Geens et al., 2010). Metals are released by both natural (erosion, volcanism and upwelling) and anthropogenic sources (mining, smelting, metallurgy), often accumulate in organisms at higher trophic levels and have been studied in a range of seabirds to investigate temporal and spatial variation (Furness, 1993; Becker, 2003; Vo et al., 2011). Many researchers report on trace metal concentrations in
* Corresponding author. E-mail address: [email protected] (A. Finger). http://dx.doi.org/10.1016/j.envpol.2015.06.022 0269-7491/© 2015 Elsevier Ltd. All rights reserved.
internal tissues and samples are often collected destructively, i.e. by sacrificing randomly selected members of a population (Bacher, 1985; Smichowski et al., 2006), or opportunistically, i.e. starved or killed 'by misadventure' (Lock et al., 1992; Gibbs, 1995; Choong et al., 2007). While the former has ethical implications and cannot be applied to species of conservation concern, the latter carries potentially unquantified biases including (1) the sample not being representative of a random cross-section of the population, (2) unknown provenance, (3) unknown cause of death, and (4) altered lipid content in a starved organ which can lead to falsely elevated elemental concentrations (Bryan et al., 2007). Feather collection is the most common non-destructive sampling protocol (Burger, 1993). Moulted feathers can be obtained non-invasively and transported and stored with minimal cost. Shunting nonessential trace metals to the feathers is a main method of detoxification in seabirds (Furness et al., 1986), but feather metal concentrations are often a poor indicator for internal tissue concentrations (Eagles-Smith et al., 2008; Lavers and Bond, 2013) and results can be highly biased by external contamination (Jaspers et al., 2004). Recent advances in trace analysis such as atomic absorption spectrometry (AAS) and inductively-coupled plasma spectrometry
366
A. Finger et al. / Environmental Pollution 205 (2015) 365e377
(ICP) promote non-destructive cross-section sampling, e.g. the taking of a small sample of blood (
