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Use of Stable Isotopes (δ13C and δ15N) to Infer Post-breeding Dispersal Strategies in Iberian Populations of the Kentish Plover (Charadrius alexandrinus)

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22 March 2024

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25 March 2024

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Abstract
Beaches are among the habitats most frequented by migratory birds for breeding and/or wintering. However, threats such as human pressure and sea level rise can reduce the availability of these habitats for different species. The presence of alternative areas, such as salt pans and brackish habitats, is essential for many migratory shorebird populations. This study addresses the post-breeding dispersal of the Kentish plover (Charadrius alexandrinus) in the Iberian Peninsula by analysing C and N isotopes in feathers. The study was conducted at six locations along the Iberian coast, which were categorized in three areas: NW Atlantic coast, the Atlantic coast of Andalusia and the Mediterranean coast. Although linear mixed models did not reveal any significant effects of sex or coastal area on isotopic levels, the variability in the data suggests different habitat-use strategies in the post-reproductive period. Birds from the northwest of the Iberian Peninsula exhibit greater fidelity to a single habitat type, i.e. coastal beaches, while populations from the Mediterranean coast and the Atlantic coast of Andalusia show different individual dispersal strategies, occupying coastal habitats and freshwater wetlands. The lack of alternative habitats for the northwest Iberian population, the reduction in available habitat due to rising sea levels and human pressure together pose a serious threat to the survival of this species, already with an unfavourable conservation status.
Keywords: 
Subject: Biology and Life Sciences  -   Animal Science, Veterinary Science and Zoology

1. Introduction

Migratory shorebirds migrate between breeding and staging areas along generally consistent routes [1], frequently using beaches and saline and/or brackish habitats [2,3]. Beaches are important breeding and foraging habitats for shorebirds, but they are threatened by resort development, road construction, coastal erosion, sea level rise and human disturbance [4,5,6]. Increasing global temperatures will result in increases in sea level due to the expansion of oceanic water and melting of glaciers and ice sheets [7]. Inundations due to sea level rise could lead to conversion of intertidal to subtidal habitat and, therefore, a reduction in the availability of the habitats available to shorebirds [6,8]. Moreover, overwash and the associated consequences are expected to increase because of both sea level rise and intensification of coastal occupation [9]. The impacts of such habitat changes on shorebird populations will depend on the availability of alternative areas that the birds can use and where similar levels of survivorship and fecundity can be reached [10]. Salt pans and wetlands are included among alternative areas that can support large populations of migratory waterbirds, such as shorebirds [11,12,13,14].
Unravelling migratory connectivity between breeding, stopover and wintering areas is important to predict the influence of habitat change on population demographics [15,16]. Stable isotope analysis has been used to investigate dispersal and migratory movements in shorebirds [3,16,17,18], as natural patterns of geographic variation have been observed in isotopic ratios on land [19].
The Kentish plover (Charadrius alexandrinus) is a common shorebird in the temperate and subtropical belt of Eurasia and N Africa [20]. However, most breeding populations in Europe have undergone a marked decline since the early part of the twentieth century [21].
The Iberian population is the largest in Europe [20] and is concentrated along the coast, being less common in inland wetlands [22,23]. The species has undergone a strong decline in the area it occupies, and it has disappeared from some coastal areas, especially from the Mediterranean coast [23] and also the coast of Portugal [24]. In the northwest Iberian peninsula, the birds breed exclusively on beaches, but along the Portuguese coast, southern Spain and the Mediterranean coast they also occupy salt pans and salt marshes, as well as sparsely vegetated salt flats and coastal grasslands [2,22,23,25]. Inland populations of Kentish plovers typically nest on the sandy margins of brackish lagoons, but also on the shores of reservoirs or on islands and rice fields [2,22,26,27]. In the context of climate change, the rise in sea level and the increase in the rate or severity of maritime storms are restricting the useful strip of beaches available [28]. This situation increases the importance of supratidal habitats such as salt pans for the species.
The objective of this study was to unravel the post-breeding dispersal strategy in Iberian Kentish plovers by analysis of the isotopic levels of C and N in feathers of breeding adults.

2. Materials and Methods

2.1. Study Area

Samples were taken from 6 breeding locations on the Iberian coast. Three sites are located on the Mediterranean coast and 3 on the Atlantic coast, one in southern Spain and 2 in north Portugal and northwestern Spain (Figure 1).
The Mediterranean localities were the Ebro Delta wetland, Laguna de la Mata and the Serradal beach (Figure 1). In the Ebro Delta, the most important breeding area for the Kentish plover in Spain [29], nests were found in zones bordering brackish water and coastal beaches. Nests in Laguna de la Mata were also found in zones bordering brackish water, while on Serradal beach, nests were found in deep sandy areas among dry interdunal depressions.
The Atlantic location in Andalusia (southern Spain) was the Tinto-Odiel estuary, where breeding areas were located on beaches of the marine zone, while in northern Portugal (Carreço and Ancora beaches) and northwestern Spain (Rostro, Carnota and Balieiros beaches) nests were found exclusively on coastal sandy beaches (Figure 1).

2.2. Methods

Plovers were captured from nests using a funnel-trap and were sexed by dichromatic plumage characteristics [30].
Feathers were collected between March and July 2009 from 44 adult Kentish plovers (17 males and 27 females) breeding on the Mediterranean coast (18 birds), the Atlantic coast of southern Spain (9 birds) and northern Portugal and northwestern Spain (17 birds).
The inner first primary feather of each bird was clipped. Although little is known about temporal and spatial moulting patterns in the Iberian Kentish plovers [27], moulting of primary feathers in European populations usually takes place in the post-breeding period (August-October), although it may begin in June [31,32]. Each feather sample was placed in a (separate) plastic bag and stored at −20 °C prior to analysis.

2.3. Chemical Analysis

The feathers were washed in a solution of 0.25 M sodium hydroxide and pure water to remove waxes and oils. The washed feathers were placed in clean, screw-top vials and dried overnight at 60ºC, in the oven of an elemental analyzer. The dried feathers were cut into small sections (< 1 mm sections) in the sample vials with surgical scissors.
Stable isotope ratios were measured in a continuous-flow isotope-ratio mass spectrometer (Deltaplus, ThermoFinnigan) coupled to an elemental analyzer (FlashEA1112, ThermoFinnigan Instruments) through a Conflo II interface (ThermoFinnigan). Tin-encapsulated samples were combusted at 1020°C in a quartz column containing chromium oxide and silvered colbatous/cobaltic oxide. After combustion, excess oxygen and nitrogen oxides were reduced in a reduction column (reduced copper at 650°C). N2 and CO2 were separated on a GC column prior to isotope-ratio mass spectrometry. A series of international reference materials for δ15N (IAEA-N-1, IAEA-N-2, USGS25) and δ13C (NBS 22, IAEA-CH-6, USGS24) were also analyzed along with some test batches. Replicate assays of the laboratory standard acetanilide indicated measurement errors of ± 0.15 ‰ for δ13C and δ15N.
Delta values are expressed relative to international standards: Vienna Pee Dee Belemnite (VPDB) for δ13C and Atmospheric Air for δ15N.

2.4. Statistical Analysis

Locations were clustered by geographical proximity in three coastal areas: the Iberian NW coast (locations 1–2), the Atlantic coast of Andalusia (3) and the Mediterranean coast (4–6) (Figure 1).
Linear mixed models (LMMs) were used to account for the statistical non-independence of data [33]. The LMMs were fitted using sex and coastal area as fixed categorical predictors and location (nested within coastal area) as a random factor. δ13C and δ15N were considered dependent variables, and where necessary a log transformation was applied to ensure the normality and homoscedasticity of the data. To find the significance of each fixed term, the F-statistic was determined using the restricted maximum likelihood (REML) approach. The coefficient of variation was used to visualize the data dispersion in the three coastal areas.
The values are reported throughout the paper as means ± SE. IBM SPSS Statistics 29 software was used to conduct all statistical tests.

3. Results

The mean δ13C values were -16.47‰±1.05 (n=18) for Kentish plovers breeding on the Mediterranean coast, -16.07‰±1.11 (n=9) for those breeding on the Atlantic coast of Andalusia and -14.18‰ ± 0.27 (n=17) for those breeding on the NW Iberian coast. Regarding the δ15N, mean values for the Mediterranean coast, the Atlantic coast of Andalusia and NW Iberian coast were respectively 13.57‰±0.57, 14.60‰±0.61 and 14.20‰±0.19. The values for the Mediterranean coast and the Atlantic coast of Andalusia were much more widely dispersed than those corresponding to the NW Iberian coast (Figure 2), with coefficients of variation in δ13C and δ15N of 8% and 6% for the NW Iberian coast, 20% and 12% for the Atlantic coast of Andalusia and 27% and 18% for the Mediterranean coast.
The LMMs showed that neither δ13C or δ15N concentrations were significantly affected by sex or coastal section (Table 1).

4. Discussion

Although the LMMs did not show any significant influence of sex and coastal area on isotopic levels, the coefficients of variation suggest different strategies regarding habitat use in the post-breeding period. Kentish plovers breeding on the Mediterranean coast and the Atlantic coast of Andalusia showed greater variability in isotope values than birds in the NW Iberian Peninsula, both in δ13C and δ15N. Trophic web carbon and nitrogen values are known to differ between habitats [34,35]. Thus, the size of carbon and nitrogen isotopic niches seems to be related to different individual strategies, such as birds making latitudinal movements in coastal environments and others moving to freshwater wetlands in the post-breeding season, implying that δ13C and δ15N isotope values are lower than in coastal areas [36,37,38]. The coefficient of variation for the Mediterranean birds suggests very marked habitat changes in plover populations. The high δ13C values (-6.59‰ or -9.88‰) may indicate that these birds frequented hypersaline environments [37,39] at the time of feather growth. Conversely, low δ13C values (-21.92‰ or -20.95‰) may indicate that the birds frequented environments with low salinity [37,39], including inland lakes [40]. Such migratory movements have been reported by other authors [27,40]. By contrast, the results obtained for the northwestern Iberian plover suggest greater fidelity of this population to a single habitat type, i.e. coastal beaches, with a lower coefficient of variation. In this population, most ringed birds exclusively occupied coastal beaches throughout the annual cycle [41](unpublished data), although tracking of some tagged plovers revealed that they use freshwater wetlands in winter (unpublished data).
In recent years, beaches have been subjected to strong anthropogenic pressure (urban planning, industrial development, tourism) [6,42]. The rise in sea level due to climate change is an additional threat [43,44,45]. The most widely accepted projection for the next 100 years is a global sea level rise of 0.63 – 1.02 m under a scenario of very high greenhouse gas emissions [46]. More specifically, a sea level rise of 0.6 – 0.8 m is expected in the northwest Iberian Peninsula by 2100 [47]. Inundation of the intertidal zone will result in conversion of intertidal habitats to subtidal habitats [6] and lead to reductions in habitat availability for many shorebirds. Species that use a wide range of habitats may be better able to cope with these rapid climatic or habitat changes [48,49,50]. By contrast, 90% of the Kentish plovers in the Iberian Peninsula are concentrated on coastal sandy beaches, although a wide variety of habitats are occupied by this species, including salt pans, salt marshes and endorheic lagoons [2,23,27]. Specifically, in the NW Iberian Peninsula, beaches are the only habitat available for the species [51,52]. In the absence of alternative habitats, the expected rise in sea level due to the effect of climate change will therefore pose a serious problem for the survival of this population, as it will cause a gradual reduction in the availability of suitable habitats for the species. A similar problem has been observed in other coastal populations of this species [53] and of the Snowy plover (Charadrius nivosus) [54].

5. Conclusions

This study highlights the heterogeneity in the post-breeding dispersal strategies of Iberian Kentish plovers, with populations in the southern Iberian Peninsula and the Mediterranean showing a wider range of habitats than those in the NW Iberian Peninsula, which are much more dependent on coastal environments and therefore more vulnerable to rising sea levels.

Acknowledgments

The isotopic analyses were conducted by the Servicios de Apoio á Investigación (SAI) of the A Coruña University. Feathers were collected with the permission of the Spanish and Portuguese authorities.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Kentish plover sampling sites used in this study. Locations: 1, Galician beaches (Rostro, Carnota and Balieiros beaches); 2, Carreço and Ancora beaches; 3; Tinto-Odiel estuary; 4, Laguna de la Mata; 5, Serradal beach; 6, Delta del Ebro. Sample size by sex is shown for each locality.
Figure 1. Kentish plover sampling sites used in this study. Locations: 1, Galician beaches (Rostro, Carnota and Balieiros beaches); 2, Carreço and Ancora beaches; 3; Tinto-Odiel estuary; 4, Laguna de la Mata; 5, Serradal beach; 6, Delta del Ebro. Sample size by sex is shown for each locality.
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Figure 2. δ13C and δ15N isotopic values in Kentish plovers breeding along the Iberian coast. ■, NW Atlantic; ♦, Atlantic coast of Andalusia; ▲, Mediterranean coast.
Figure 2. δ13C and δ15N isotopic values in Kentish plovers breeding along the Iberian coast. ■, NW Atlantic; ♦, Atlantic coast of Andalusia; ▲, Mediterranean coast.
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Table 1. Linear Mixed Models using δ13C and δ15N in Iberian Kentish plover feathers as response variable, Coastal section and Sex as fixed categorical predictors and location (nested within coastal section) as random factor. F values and significance are shown (*, P < 0.05; **, P < 0.01; ***, P < 0.001).
Table 1. Linear Mixed Models using δ13C and δ15N in Iberian Kentish plover feathers as response variable, Coastal section and Sex as fixed categorical predictors and location (nested within coastal section) as random factor. F values and significance are shown (*, P < 0.05; **, P < 0.01; ***, P < 0.001).
Predictors δ13C δ15N
Coastal section 0.325 0.013
Sex 0.612 2.322
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