Elsevier

Ecotoxicology and Environmental Safety

Volume 179, 15 September 2019, Pages 62-70
Ecotoxicology and Environmental Safety

Accumulation of trace elements in feathers of the Kentish plover Charadrius alexandrinus

https://doi.org/10.1016/j.ecoenv.2019.04.051Get rights and content

Highlights

  • Feather analysis allows identification of possible contaminants of concern.

  • Hg is a major threat for conservation of Kentish plover in Venice Lagoon.

  • Exposure to Cd and Se may be of concern for Kentish plover conservation.

Abstract

A non-invasive study of trace element accumulation in tail feathers of the Kentish plover (Charadrius alexandrinus) was performed along the coastline of the northern littoral strip of the Venice Lagoon, with the aim to verify whether contamination may be a factor affecting conservation status of Kentish plover populations.

Body burdens in feathers of 11 trace elements including toxic metals/metalloids and essential elements (As, Cd, Co, Cr, Cu, Hg, Ni, Pb, Se, V, Zn) were quantified by ICP-MS, then concentrations were normalized to feather's age calculated using ptilochronology in order to obtain daily deposition rates.

Mercury emerged as a major threat to the conservation of the species, since average feather concentration was clearly above the adverse-effect threshold associated with impairment in the reproductive success in a number of bird species. Also Cd and Se occurred at levels that may impact on the conservation status of the studied species at local scale, even if to a lesser extent than Hg.

Gender-related differences in trace element accumulation emerged only for As, although for this element the risks associated to environmental exposure seem to be negligible.

Introduction

The Kentish plover Charadrius alexandrinus (hereafter KP) is a small wader of Family Charadriidae, breeding in wetlands and coastal areas of Europe, North-Africa, Middle-East and Central-Asia (Delany et al., 2009). Population size of KP is declining all over its distribution range, and the cause of the decline has been recognized in habitat loss and fragmentation, increased human uses of the sandy coastal areas for commercial and recreational purposes, and increased predation by birds and mammals taking advantage of human activities (Delany et al., 2009; Domínguez and Vidal, 2003; Scarton, 2017). For this reasons, the species was listed in the Annex I of the Directive 2009/147/EC and was included in the IUCN Italian Red List as an endangered (EN) species (Rondinini et al., 2013).

Biology, breeding ecology and behaviour of KP have been widely studied in all its distribution range (Argüelles-Ticó et al., 2016; Fraga and Amat, 1996; Kosztolányi et al., 2009; Lessells, 1984). Nevertheless, no researches were performed up to date to assess the impact of environmental contamination on its conservation status, and few data are available concerning bioaccumulation (Kim and Koo, 2008; Zheng et al., 2018).

In coastal areas and wetlands KP feeds mostly on polychaetes (nereidae), small crustaceans (isopods, ostracods and amphipods), small bivalves, coleopterans and dipterans (Castro et al., 2009; Cramp and Simmons, 1983; Perez-Hurtado et al., 1997). Although KP is not a top predator in coastal food webs, its dietary habits make it susceptible to bioaccumulation and, possibly, biomagnification of toxicants. In estuarine and coastal areas, trace elements are of concern due to their ubiquitous distribution and the potential detrimental effects they can exert on birds physiology (Furness, 1996; Ohlendorf and Heinz, 2011). Toxic effects from trace elements includes changes in behaviour, impairments in development and reproduction. Mercury (Hg) has been proven to cause embryo malformations, lowered hatchability, decreased chick growth, reduced survival of young, changes in reproductive behaviour and endocrine disruption in waterbirds (Burger and Gochfeld, 1997; Jayasena et al., 2011). Lead (Pb) may disrupt the heme biosynthetic pathway and cause also death (Blus et al., 1995 and citation herein). Cadmium (Cd) may induce growth retardation, anaemia, suppression of egg production, kidney damage and marrow hyperplasia (Furness, 1996; Spahn and Sherry, 1999). Selenium (Se) is highly toxic for the early developmental and embryonic stages and causes reproductive impairments, reduction of hatching success and teratogenicity (Ohlendorf and Heinz, 2011; Spallholz and Hoffman, 2002). For many other elements little is known about possible detrimental effects in birds.

Trace elements concentration in birds may be measured in various organs (liver, kidneys, brain), tissues (muscle, bones, fat), excrements, feathers and eggs (Dauwe et al., 2000; Markowski et al., 2013; Zheng et al., 2018).

Feather analysis is a non-destructive and ethically preferable techniques as compared with organ and tissue analysis, since feathers may be easily collected and, if necessary, repeatedly sampled to study the accumulation of trace elements without affecting welfare or survival of the individuals (Adout et al., 2007). A feather is connected with the blood circulation only during its growth period; in this phase elements taken up through the food are incorporated into the sulphydryl rich keratinous matrix of the developing feather, where they are stored. When the feather has completely grown, the vascular connection shrivels up and trace elements cannot be further allocated into the keratin (Burger, 1993). Thus, their accumulation in feathers may be associated with a definite time-span, corresponding to the time needed to fully develop the feather, variable from species to species (García-Fernández et al., 2013; Grubb, 2006). This time-span can be determined using ptilochronology, the study of the alternating pale and dark bands of feathers which is indicative of the daily growth (Grubb, 2006), so that the deposition rates of the contaminants can be calculated (García-Fernández et al., 2013), and the dilution artefact due to feather growth rates and mass reported by Bortolotti (2010) can be minimized. The author, indeed, postulated that for elements and compounds functionally incorporated in the feather (as sulphur and other elements), the deposition should follow a mass-dependent model, whilst the deposition of non-structural elements, as contaminants and hormones, occurs incidentally and should be time-dependent, so that growth rate of the feather becomes a critical parameter (Bortolotti, 2010). Moreover, in the case of resident populations and non-migratory species, the determination of trace elements in feathers represents a reliable method for monitoring the uptake of contaminants though the local food web (Rothschild and Duffy, 2005).

To verify whether KPs breeding in the area of the Venice Lagoon are exposed to levels of trace elements that may, directly or indirectly, contribute to the local decline of the species - estimated by Scarton (2017) as loss of 30% of the breeding pairs in the last three decades - an accumulation study using feathers collected from specimens breeding along the littoral strips of the lagoon was performed.

The focus was mainly on those elements known to cause detrimental effects on birds, for which threshold concentrations for adverse effects are available in the literature (such as Hg, Cd, Pb and Se); the concentrations of metals and metalloids possibly involved in toxic effects, but for which no threshold data are available (including As, Co, Cr, Cu, Ni, V, Zn) were measured as well.

The extent to which KP deposited contaminants in the feathers was also assessed by comparing trace element concentrations in KP feathers with literature data concerning other waterbirds in different geographical areas.

Section snippets

Study area

Feathers have been collected in the Cavallino-Treporti peninsula, the northernmost littoral strip separating the Lagoon of Venice from Adriatic Sea (Fig. 1). Along the 13 km of the coasts of the peninsula, develops a fragmented system of natural and restored dunes covering a surface of about 350,000 m2 (Cecconi and Nascimbeni, 1997). Here the sandy substrate is characterized by the typical herbaceous vegetation of drift lines (habitat “1210 - Annual vegetation of drift lines” according to the

Ptilochronology

The average length of the sixth rectrix of KP was 51.6 ± 1.6 mm (n = 13). Nevertheless, growth bars were clearly discernible only in six rectrices (4 retrieved from males, 2 from females); since no significant differences have been observed among individuals (one-way ANOVA: F5,32 = 0.729, p = 0.232), the pooled average width of 2.38 ± 0.30 mm was used as daily growth rate for estimating feather age. According to these data, the average feather age for rectrices of KP has been estimated to be

Discussion

Accumulation of trace elements in feathers is a topic that was treated in several studies, but the possible contribution of environmental contamination to the conservation status of the threatened species Charadrius alexandrinus was never assessed before. The use of surrogate species to estimate exposure in a study area, although it is a feasible and often exploited approach, should be avoided, whenever possible. In facts, as stated by Miller et al. (2019) “surrogate species of varying body

Conclusions

This work represents the first study aimed at identifying possible disturbances related to environmental contamination on the conservation status of the threatened species Charadrius alexandrinus, by using a non-invasive approach. Although the sample size was relatively small, it allowed to gain an insight into possible harmful exposure of the local population of KP to trace elements, especially as concern the identification of main threats for the species.

Mercury emerged as a major threat to

Funding sources

This work was partly supported by the Cavallino-Treporti municipality (det. 355/2017 and det. 1552/2018).

Declarations of interest

None.

References (90)

  • A. Goede et al.

    Selenium, mercury, arsenic and cadmium in the life-cycle of the Dunlin, Calidris alpina, a migrant wader

    Sci. Total Environ. Elsevier Sci. Publ. B.V

    (1989)
  • K. Honda et al.

    Seasonal changes in mercury accumulation in the black-eared kite, Milvus migrans lineatus

    Environ. Pollut. Ser. A Ecol. Biol.

    (1986)
  • N. Jayasena et al.

    Endocrine disruption in white ibises (Eudocimus albus) caused by exposure to environmentally relevant levels of methylmercury

    Aquat. Toxicol.

    (2011)
  • E.-Y. Kim et al.

    Metal accumulation in tissues of seabirds from Chaun, northeast Siberia, Russia

    Environ. Pollut.

    (1996)
  • M. Lucia et al.

    Trace element accumulation in relation to trophic niches of shorebirds using intertidal mudflats

    J. Sea Res.

    (2014)
  • M.W.C. Miller et al.

    Interspecific patterns of trace elements in sea ducks: can surrogate species be used in contaminants monitoring?

    Ecol. Indicat.

    (2019)
  • H. Ochoa-acunã et al.

    Mercury in feathers from Chilean birds: influence of location, feeding strategy, and taxonomic affiliation

    Mar. Pollut. Bull.

    (2002)
  • R.F.N. Rothschild et al.

    Mercury concentrations in muscle, brain and bone of Western Alaskan waterfowl

    Sci. Total Environ.

    (2005)
  • P. Sánchez-Virosta et al.

    A review on exposure and effects of arsenic in passerine birds

    Sci. Total Environ.

    (2015)
  • J.E. Spallholz et al.

    Selenium toxicity: cause and effects in aquatic birds

    Aquat. Toxicol.

    (2002)
  • S. Zheng et al.

    Tissue distribution and maternal transfer of persistent organic pollutants in Kentish plovers (Charadrius alexandrinus) from Cangzhou wetland, Bohai Bay, China

    Sci. Total Environ.

    (2018)
  • A. Argüelles-Ticó et al.

    Geographic variation in breeding system and environment predicts melanin-based plumage ornamentation of male and female Kentish plovers

    Behav. Ecol. Sociobiol.

    (2016)
  • H.M. Ashbaugh et al.

    Evidence for exposure to selenium by breeding interior snowy plovers (Charadrius nivosus) in saline systems of the Southern Great Plains

    Ecotoxicology

    (2018)
  • A.L. Bond et al.

    Trace element concentrations in feathers of Flesh-footed Shearwaters (Puffinus carneipes) from across their breeding range

    Arch. Environ. Contam. Toxicol.

    (2011)
  • G.R. Bortolotti

    Flaws and pitfalls in the chemical analysis of feathers: bad news — good news for avian chemoecology and toxicology

    Ecol. Appl.

    (2010)
  • B.M. Braune et al.

    A mercury budget for the Bonaparte's gull during autumn moult

    Ornis Scand.

    (1987)
  • J. Burger

    Metals in avian feathers: bioindicators of environmental pollution

    Rev. Environ. Toxicol.

    (1993)
  • J. Burger et al.

    Lead, mercury, and cadmium in feathers of tropical terns in Puerto Rico and Australia

    Arch. Environ. Contam. Toxicol.

    (1991)
  • J. Burger et al.

    Heavy metal and selenium levels in Franklin's Gull (Larus pipixcan) parents and their eggs

    Arch. Environ. Contam. Toxicol.

    (1996)
  • J. Burger et al.

    Marine birds as sentinels of environmental pollution

    EcoHealth

    (2004)
  • J. Burger et al.

    Heavy metals and selenium in feathers of three shorebird species from Delaware bay

    Environ. Monit. Assess.

    (1993)
  • J. Burger et al.

    Mercury, lead, cadmium, cobalt, arsenic and selenium in the blood of Semipalmated sandpipers (Calidris pusilla) from Suriname, South America: age-related differences in wintering site and comparisons with a stopover site in New Jersey, USA

    Toxics

    (2018)
  • M. Castro et al.

    Sex-related seasonal differences in the foraging strategy of the Kentish plover

    Condor

    (2009)
  • G. Cecconi et al.

    Ricostruzione e naturalizzazione delle dune artificiali sul litorale del Cavallino

    (1997)
  • C.E. Clarkson et al.

    Using ptilochronology to determine daily mercury deposition in feathers of nestling waterbirds

    Environ. Toxicol. Chem.

    (2011)
  • S. Cramp et al.

    Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic: 3. Waders to Gulls

    (1983)
  • T. Dauwe et al.

    Can excrement and feathers of nestling songbirds be used as biomonitors for heavy metal pollution?

    Arch. Environ. Contam. Toxicol.

    (2000)
  • S. Del Vecchio et al.

    The response of plant community diversity to alien invasion: evidence from a sand dune time series

    Biodivers. Conserv.

    (2015)
  • S. Delany et al.

    The Wader Atlas: an Atlas of Wader Populations in Africa and Western Eurasia

    (2009)
  • J. Domínguez et al.

    Influencia del investigador en el éxito reproductivo del Chorlito Patinegro Charadrius alexandrinus

    ARDEOLA

    (2003)
  • C.A. Eagles-Smith et al.

    Mercury correlations among six tissues for four waterbird species breeding in San Francisco Bay, California, USA

    Environ. Toxicol. Chem.

    (2008)
  • N.P. Edwards et al.

    Elemental characterisation of melanin in feathers via synchrotron X-ray imaging and absorption spectroscopy

    Sci. Rep.

    (2016)
  • L.D. Einoder et al.

    Metal and isotope analysis of bird feathers in a contaminated estuary reveals bioaccumulation, biomagnification, and potential toxic effects

    Arch. Environ. Contam. Toxicol.

    (2018)
  • R. Eisler

    Mercury hazards to fish, wildlife, and invertebrates: a synoptic review

    Fish Wildl. Serv. Biol. Rep.

    (1987)
  • R. Eisler

    Handbook of Chemical Risk Assessment

    (2000)
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