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