See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/279985702 The Little Penguin (Eudyptula minor) as an indicator of coastal trace metal pollution ARTICLE in ENVIRONMENTAL POLLUTION · JULY 2015 Impact Factor: 4.14 · DOI: 10.1016/j.envpol.2015.06.022 READS 57 7 AUTHORS, INCLUDING: Annett Finger Jennifer Lavers Victoria University Melbourne University of Tasmania 7 PUBLICATIONS 0 CITATIONS 28 PUBLICATIONS 150 CITATIONS SEE PROFILE SEE PROFILE Peter M Dann Dayanthi Nugegoda Phillip Island Nature Parks RMIT University 135 PUBLICATIONS 759 CITATIONS 104 PUBLICATIONS 1,335 CITATIONS SEE PROFILE SEE PROFILE Available from: Annett Finger Retrieved on: 24 September 2015 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 b Institute for Marine and Antarctic Studies, 20 Castray Esplanade, Battery Point, Tasmania 7004, Australia c 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 article info abstract Article history: Monitoring trace metal and metalloid concentrations in marine animals is important for their conser- Received 17 February 2015 vation and could also reliably reflect pollution levels in their marine ecosystems. Concentrations vary Received in revised form across tissue types, with implications for reliable monitoring. We sampled blood and moulted feathers of 2 June 2015 the Little Penguin (Eudyptula minor) from three distinct colonies, which are subject to varying levels of Accepted 11 June 2015 anthropogenic impact. Non-essential trace metal and metalloid concentrations in Little Penguins were Available online xxx 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 Keywords: fi Trace element and feathers for mercury, lead and iron. This study represents the rst reported examination of trace Blood metals and metalloids in the blood of any penguin species and demonstrates that this high trophic feeder Seabird is an effective bioindicator of coastal pollution. Australia © 2015 Elsevier Ltd. All rights reserved. Bioindicator 1. Introduction internal tissues and samples are often collected destructively, i.e. by sacrificing randomly selected members of a population (Bacher, Toxicants are present in our environment, particularly in the 1985; Smichowski et al., 2006), or opportunistically, i.e. starved marine environment, because the ocean acts as a sink (Neff, 2002). or killed 'by misadventure' (Lock et al., 1992; Gibbs, 1995; Choong Influx from rivers, agricultural and urban land runoff, sewage et al., 2007). While the former has ethical implications and outfalls, long-range atmospheric transport and deposition all cannot be applied to species of conservation concern, the latter contribute to elevated levels of contaminants in marine ecosystems carries potentially unquantified biases including (1) the sample not (Lamborg et al., 2014). Monitoring this pollution and assessing its being representative of a random cross-section of the population, ecological and human health effects has become a global concern (2) unknown provenance, (3) unknown cause of death, and (4) (Islam and Tanaka, 2004). Metals in particular, have been shown to altered lipid content in a starved organ which can lead to falsely have a negative impact on coastal ecosystems in highly industri- elevated elemental concentrations (Bryan et al., 2007). Feather alised areas (Geens et al., 2010). Metals are released by both natural collection is the most common non-destructive sampling protocol (erosion, volcanism and upwelling) and anthropogenic sources (Burger, 1993). Moulted feathers can be obtained non-invasively (mining, smelting, metallurgy), often accumulate in organisms at and transported and stored with minimal cost. Shunting non- higher trophic levels and have been studied in a range of seabirds to essential trace metals to the feathers is a main method of detoxi- investigate temporal and spatial variation (Furness, 1993; Becker, fication in seabirds (Furness et al., 1986), but feather metal con- 2003; Vo et al., 2011). centrations are often a poor indicator for internal tissue Many researchers report on trace metal concentrations in concentrations (Eagles-Smith et al., 2008; Lavers and Bond, 2013) and results can be highly biased by external contamination (Jaspers et al., 2004). * Corresponding author. Recent advances in trace analysis such as atomic absorption E-mail address: [email protected] (A. Finger). spectrometry (AAS) and inductively-coupled plasma spectrometry http://dx.doi.org/10.1016/j.envpol.2015.06.022 0269-7491/© 2015 Elsevier Ltd. All rights reserved. 366 A. Finger et al. / Environmental Pollution 205 (2015) 365e377 (ICP) promote non-destructive cross-section sampling, e.g. the Little Penguins from the St Kilda colony (Fig. 1) forage exclusively taking of a small sample of blood (<2 mL) from a free-ranging bird within Port Phillip Bay (Preston et al., 2008) a semi-enclosed body without sacrificing it (Becker, 2003). The success of non-lethal of water bordering the highly industrialised metropolis of Mel- blood sampling techniques is evident in the literature (Eagles- bourne, Australia. This relatively shallow bay (mean depth 13.6 m, Smith et al., 2008; Carvalho et al., 2013; Fort et al., 2014). Trace area 1930 km2) is joined to Bass Strait through a 3 km-wide channel element concentrations in avian blood reflect current dietary and contains areas with highly contaminated sediments due to exposure and often correlate strongly with those in internal tissues, historical and current industrial discharges through storm water presenting a potentially more suitable non-lethal matrix than run-off (Harris et al., 1996). Semi-enclosed coastal areas are feathers for investigating a biologically relevant contaminant load contamination hotspots; with sediments remaining polluted, (Monteiro and Furness, 2001). sometimes for decades after the primary source is removed due to Penguins are ideal sentinels for marine pollution monitoring restricted currents and wave action (Aly et al., 2012). Notably, little (Boersma, 2008) due to their high trophic position, long lifespan, is known about the contaminant load in Little Penguins breeding at philopatry, conspicuous nature and our extensive knowledge of St Kilda and how it compares to that of conspecifics at less urban their life history (Trathan et al., 2014). Compared to other seabird environments, such as the nearby Phillip Island colony and more bioindicators, they have the advantage of being relatively seden- remote Bass Strait island colonies. tary, therefore reflecting local conditions (Ropert-Coudert et al., Our emphasis in this study was to evaluate high-level trophic 2004). While penguins have been used in ecotoxicological studies feeding Little Penguins as indicators of the presence of bioavailable using internal tissues and feathers (Gibbs, 1995; Smichowski et al., metals and metalloids within their relatively small foraging areas. 2006; Jerez et al., 2011), there are to date no trace metal concen- The specific objectives were to: (1) investigate the spatial variation tration data published from the blood of any penguin species. of trace metals and metalloids in the blood and feathers of Little Little Penguins (Eudyptula minor) are the smallest of the pen- Penguins; and (2) investigate correlations between the two sam- guins, breeding on offshore islands and small mainland colonies in pling matrices in order to (3) assess the usefulness of blood and southern Australia and New Zealand (Marchant and Higgins, 1990). feathers as non-destructive sampling matrices for assessing expo- Extensive research has been conducted on their breeding and sure of Little Penguins to trace metal and metalloid pollution. foraging ecology (Reilly and Cullen, 1981; Fortescue, 1999; Dann and Chambers, 2013). Little Penguins are generalist feeders 2. Materials and methods whose diet can vary greatly among colonies and even years at the same colony (Chiaradia et al., 2010; Kowalczyk et al., 2013). They 2.1. Study sites inhabit a wide range of coastal habitats - from relatively pristine offshore islands in the Bass Strait (Hoskins et al., 2008) to human- We collected blood (n ¼ 31) and moulted feathers (n ¼ 35) from made structures in highly urbanised bays (Preston et al., 2008). wild Little Penguins during February and March of 2012 at three Fig. 1. Little Penguin breeding colonies sampled in February and March 2012: St Kilda, Phillip Island and Notch Island. A. Finger et al. / Environmental Pollution 205 (2015) 365e377 367 locations: St Kilda, Phillip Island and Notch Island (Fig. 1). The St 50 mL digestion tubes (DigiTubes by SCP Science, product number Kilda colony is located 5 km from the central business district of 010-500-261) for