Marine Pollution Bulletin 133 (2018) 144–149
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Trace elements in biomaterials and soils from a Yellow-legged gull (Larus michahellis) colony in the Atlantic Islands of Galicia National Park (NW Spain)
T
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X.L. Oteroa, , S. de la Peña-Lastraa, D. Romerob, G.N. Nobregab, T.O. Ferreirab, A. Pérez-Albertic a
Departamento de Edafoloxía e Química Agrícola, Facultade de Bioloxía, Universidade de Santiago de Compostela, Galicia, Spain Departamento de Solos, Escola Superior de Agronomia Luiz Queiroz, Universidade de Sao Paulo, Brazil c Departamento de Xeografía, Facultade de Xeografía e Historia, Universidade de Santiago de Compostela, Spain b
A R T I C LE I N FO
A B S T R A C T
Keywords: Seabird colonies Pellets Excrement Feathers Eggs
Seabird colonies drastically transform the sites that they inhabit. Although the influence of seabirds on nutrient cycling has been investigated in numerous studies, the effects on trace elements has scarcely been considered. In this study, we determined the total contents of 9 trace elements in biomaterials (excrement, pellets, feathers and eggs) and soils in relation to the presence the Yellow-legged gull Larus michahellis. The concentrations of Zn, Cu and As were particularly high in the pellets and excrement. The total contents of the trace elements were significantly higher in the soils in the sub-colonies in which Yellow-legged gulls predominate than in soil from the control zone (with no gulls). The difference was even higher for the most reactive geochemical fractions. We observed that the oxidizable fraction was the most relevant fraction for almost all trace elements, indicating the importance of organic matter in trace element retention in sandy soils.
Seabirds strongly influence the environments where they establish their breeding colonies (Ellis, 2005; Otero et al., 2018). Many studies have focused on the direct effects of the seabirds on the vegetation and the dynamics of macronutrients such as N and P (Sobey and Kenworthy, 1979; Portnoy, 1990; Anderson and Polis, 1999; Vidal et al., 1998, 2000; Otero and Fernández-Sanjurjo, 2000; Otero et al., 2015). However, studies of the effects of seabird colonies on the concentrations of potential toxic elements in the underlying soil are relatively scarce (Otero, 1998; Rajakaruna, 2009; Wojtun et al., 2013; Ziółek et al., 2017). The continual presence of seabirds in breeding colonies (3–12 months) leads to the incorporation in the soil of large amounts of biomaterials (biomaterials such as excrement, pellets, feathers, egg remains and cadavers) (Fig. 1). Previous studies have demonstrated the presence of pollutants in different types of biomaterials generated by seabirds (Otero, 1998; Otero and Fernández-Sanjurjo, 2000; Liu et al., 2006; Bond and Diamond, 2009; Peck et al., 2016). The aim of the present study was to obtain further knowledge about the effects of seabird colonies on trace element concentrations and dynamics in the marine environment. Some of the trace elements (Mo, Se and As) have not previously been considered in this type of study. We studied different sub-colonies of seabirds inhabiting the cliffs on the Islands of Cies and Ons in the Atlantic Islands of Galicia National Park
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Corresponding author. E-mail address:
[email protected] (X.L. Otero).
https://doi.org/10.1016/j.marpolbul.2018.05.027 Received 1 March 2018; Received in revised form 28 April 2018; Accepted 13 May 2018 0025-326X/ © 2018 Elsevier Ltd. All rights reserved.
(Fig. 1). The cliffs were selected on the basis of the current or previous presence of the Yellow-legged gull in the breeding areas and were grouped into three categories: control site (with no gulls, cliffs of Cape Home, CS); colonies with a low-intermediate (L-I) proportion of Yellowlegged gulls (Cíes Islands: Faro da Porta, Monte das Herbas, Figueiras, and the Island of Ons: Punta Xubenco) and colonies with a high proportion of the gulls (Cíes Islands: Percha, Ruzo. Island of Ons: O Centulo; H) (Barcena et al., 1987; Otero, 1998; Pérez et al., 2012; Otero et al., 2015). However, the areas considered strongly affected by the gulls are the least accessible cliffs, which the breeding colonies occupied when the archipelago was inhabited by humans until the 1960s. In addition to the effect of the current density, the breeding population of the Yellow-legged gull has influenced the soil during a longer time than in the areas with a low-intermediate population density, i.e. more recently colonized areas (Otero et al., 2015). Two or three plots (7 × 5 m) were established in each colony site, and 6–8 samples of the surface soil layer (depth, 0–15 cm) were obtained in each of these at the end of the breeding season (August/ September) in 2012. The soil samples were collected within a sampling quadrat (0.50 × 0.50 m) thrown various times to fall inside the site. The following types of biomaterials were collected within the colony, and care was taken to avoid including the substrate in the samples,
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Fig. 1. A) Location of the Atlantic Islands of Galicia National Park and of the seabird subcolonies. CS: Control site, H: High density of gulls, L-I: Low-intermediate density of gulls. B) Overall view of the control site at Cape Home (control site, CS). C) Overall view of the Percha cliffs and plot location, site with high influence of gulls with predominance of Dactylis glomerata subsp. maritima. D) Accumulation of excrement in perching areas in the Yellow-legged gull colonies. E) Pellets containing remains of the crab Polybius henslowii. More than half of the diet of the Yellow-legged gull during the breeding season consists of Polybius henslowii (Munilla et al., 2014).
microwave-assisted acid digestion (9 ml HNO3: 3 ml HCl) for 25 min, and the total concentration of trace metals was determined by ICP-OES (Perkin Elmer, Optima 4300 DV). Certified ground soil standards were used to validate the method of extracting trace metals (SRM 2709a, SMR2710a, SRM2711a from NIST, U.S.A.), with a mean rate of recovery > 90%. Sequential extraction of the metals in the < 2 mm fraction was also carried out, following the method proposed by the Community Bureau of Reference (BCR), which enables separation of metals into three geochemically reactive fractions (see e.g. Rauret et al., 2000), as follows. Fraction F1 is soluble in acid medium (extracted from 1 g of soil with 40 ml of 0.11 M CH3COOH, shaking for 16 h at room temperature and centrifugation for 20 min at 8560g 4 °C) and includes exchangeable metals and metals associated with carbonates. These metals are readily released in the form of exchangeable ions as a result of slight changes in the soil conditions (e.g. salinity). Fraction F2 is the reducible fraction (extracted with 40 ml 0.5 M NH2OH-HCl, pH = 1.5, shaking for 16 h and centrifugation for 20 min at 8560g 4 °C) and is associated with amorphous Fe/Mn oxyhydroxides. Fraction F3 is the oxidizable fraction (extracted with 10 ml H2O2 30% at 85 °C for 1 h [twice] followed by addition of 20 ml of 1 M NH4COOCH3, pH = 2, shaking for 16 h and centrifugation for 20 min at 8560g, 4 °C), and is released on mineralization of the organic matter to which it is bound. One-way ANOVA and a post hoc U Mann–Whitney test were used to
particularly the excrement and pellet samples: excrement (n = 25), pellets (n = 6), egg remains (shell and membrane, n = 44) and feathers (n = 13). For both the pellets and excrement, composite samples were made by mixing 5–10 subsamples of fresh material, and these samples were then homogenized and stored at −20 °C until analysis. The P6 primary flight feathers (Martínez et al., 2012) were collected from fresh cadavers of individual adults. The feathers were washed carefully several times with distilled and ultrapure water, to completely remove adhering material. Fresh eggs were collected from the colony with permission from the National Park authorities. The following elements were analysed in the soils and biomaterials: As, Cd, Co, Cu, Hg, Mo, Pb, Se and Zn. The total trace metal content of each type of biomaterials was determined by microwave (Ethos Plus de Milestone)-assisted acid digestion with 5 ml nitric acid (HNO3) and 2 ml hydrochloric acid (HCl) for 45 min. The resulting extract was filtered (0.45 μm) and analysed by ICP-MS (Agilent 7700). In parallel, the concentration was determined in a certified standard sample (SMR rice flour 1568b from the NIST, U.S.A.) with a rate of recovery of 91 ± 6% (n = 3) for As, Cu, Hg, Mo, Zn, Hg and Se. All reagents used were Suprapur grade (Merck, Darmstadt, Germany). The soils were air-dried, passed through a 2 mm sieve and ground in an agate mortar (< 2 mm), and samples (0.5 g) were analysed to determine the total trace element contents. The elements were extracted from the soil samples by 145
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Table 1 Trace elements concentration (mg kg−1) in biomaterials generated by Yellow-legged gulls. Biomaterials
As
Feathers
Mean ± Median Mean ± Median Mean ± Median Mean ± Median Mean ± Median
Pellets Faecal materials Eggshells Eggshells membrane
SD SD SD SD SD
2.48 ± 0.02 50.2 ± 48.02 3.61 ± 3.61 0.01 ± 0.01 0.06 ± 0.05
6.12 19.9 0.74 0.01 0.05
Cd
Co
0.02 ± 0.01 0.02 6.36 ± 2.08 5.87 3.96 ± 4.36 1.94 0.003 ± 0.01 0.01 0.012 ± 0.01 0.01
0.03 0.01 5.29 5.29 3.64 3.70 2.17 1.53 0.09 0.08
Cu ± 0.04 ± 0.22 ± 1.59 ± 1.0 ± 0.05
Hg
4.21 4.06 20.0 18.5 17.7 13.9 3.12 3.69 21.7 20.9
± 1.69 ± 7.06 ± 10.5 ± 1.72 ± 4.91
0.36 0.29 0.03 0.03 0.56 0.08 0.01 0.01 0.16 0.10
Pb ± 0.20 ± 0.01 ± 2.40 ± 0.01 ± 0.20
6.70 0.35 0.19 0.12 2.04 0.54 0.44 0.19 0.15 0.08
Se ± 15.02 ± 0.17 ± 3.78 ± 0.74 ± 0.22
0.35 0.32 2.76 2.58 2.31 2.37 0.22 0.20 5.44 3.15
± 0.14 ± 0.85 ± 1.29 ± 0.08 ± 6.23
Zn
Mo
29.2 ± 14.1 26.9 152 ± 27.9 145 113 ± 89.4 85.8 1.01 ± 1.11 0.62 14.3 ± 12.1 10.2
nd nd 0.87 ± 1.13 0.52 nd nd
directly related to the presence on Yellow-legged gulls on the cliffs: high density > > low-intermediate density≥control (no gulls). The soils in the cliff areas where Yellow-legged gulls are present at high densities, such as Percha (Cíes Islands) and Centulo (Island of Ons) (Fig. 1), contain significantly higher concentrations of all of the trace elements, except Pb, than the soils in the control zone. The most abundant element found was Zn (164 mg kg−1), followed by Mo (28 mg kg−1), Pb and Cu (18 mg kg−1), As (14 mg kg−1), Cd (1.3 mg kg−1), Se (0.88 mg kg−1), Co (0.71 mg kg−1) and Hg (0.12 mg kg−1) (Table 3). These concentrations represent enrichment (relative to the control zone) of between 1.1 (for Pb) and 4 times (for As). Moreover, despite the diluting effect of the sand fraction, which mainly consists of quartz, on the trace element contents (see e.g. Jickells and Rae, 1997), the total concentrations of Cd, Cu, Mo, Zn and Hg were higher than the edaphogeochemical background levels reported for soils developed on granite (Macías and Calvo de Anta, 2008). The influence of seabirds on the abundance of trace elements in the soils is consistent with the findings of previous studies of ornithogenic soils (e.g. Otero, 1998; Liu et al., 2006; Brimble et al., 2009; Mallory et al., 2015; Espejo et al., 2017; Ziółek et al., 2017; Table 2). However, the mean concentrations of Zn and Mo obtained in the present study were much higher than those obtained in the previously mentioned studies (Tables 2, 3). The trace element content in the geochemical fractions varied substantially depending on the fraction and element considered. The trace element contents were lowest in fraction F1 (exchangeable) and were below 1 mg kg−1 for most elements, except Hg (fraction F2 < LD, LD Hg = 5 μg kg−1), (Fig. 2). The Zn, Pb, Cd and Co contents were higher in fraction F2 than in F3, while those of Cu, Se and Hg and were lower, and those of As and Mo were similar in both fractions (Fig. 2). Zinc was the most abundant element in fraction F2, (control zone: 9 ± 4, colonies: 12 ± 6–33 ± 9 mg kg−1), followed by Pb (control zone: 3.5 ± 1 mg kg−1
test for any differences in trace element concentrations between sites (control site, low-intermediate density of gulls, and high density of gulls). The level of significance used for all tests was 5%. All statistical analyses were carried out using SigmaStat 3.5 software. Faecal material (exc) and pellets (pel) showed higher concentrations of trace elements than other biomaterials, particularly of Zn, Cu, and As (Table 1). More specifically, the pellets and excrement contained the highest concentrations of Zn (pel: 150, exc: 113 mg kg−1), As (pel: 50, exc: 3,6 mg kg−1), Cu (pel: 20, exc: 18 mg kg−1), Cd (pel: 6.4, exc: 3.96 mg kg−1), Co (pel: 5.3, exc: 3.6 mg kg−1) and Hg (pel: 0.56, exc: 0.04). The feathers contained the highest concentrations of Pb (6.70 mg kg−1) and also high concentrations of As (2.48 mg kg−1) and Hg (0.36 mg kg−1). The egg membrane contained the highest mean concentrations of Se (5.44 mg kg−1) and Cu (21.7 mg kg−1), whereas the egg shell contained low concentrations of most of the trace elements considered. The concentration of Mo was only determined in the excrement samples (mean value, 0.87 mg kg−1) (Table 1). The concentrations of most of the trace elements were within the values reported for biomaterials generated by other seabirds (feathers, eggs, excrement) (Table 2), although the concentrations of some elements were much higher in the Yellow-legged gull (i.e. Pb and As in the feathers and Co in excrement). Previous studies have examined the macro-remains (i.e. spines, scales, shells, etc.) in seabird excrement with the aim of determining the diets of different species (Bearhop et al., 2001; Votier et al., 2003; Munilla et al., 2014). However, there is no information available regarding the trace element contents of seabird excrement. The diet of the Yellow-legged gull in the study area mainly consists of the crab Polybius henslowii and intertidal invertebrates such as Pollycipes cornucopia and Mytilus galloprovincialis (Munilla et al., 2014; Fig. 1). The total concentration of trace elements in the soil was generally
Table 2 Total concentration (mean ± SD and median values in brackets, mg kg−1) of trace elements in biomaterials and ornitogenic soils of seabirds from previous works. Biomaterial
As
Cd
Faecal materials
nd
Feathers
0.18 ± 0.10 (0.14) 0.19 ± 0.15 (0.16) nd
24.1 ± (12.5) 0.10 ± (0.07) 0.19 ± (0.07) 1.48 ± (0.28)
Eggshells Soils
Co
Cu
Hg
0.07
1.50 ± 1.56 (0.80) nd
36.9 ± 21.2 (24.9) nd
0.25
< ld
1.99
29.9 ± 22.8 (29.90)
0.85 ± 0.21 (0.85) 37.5 ± 36.7 (22.94)
1.88 ± (1.88) 2.90 ± (1.94) 0.87 ± (0.20) 0.16 ± (0.16)
25.0
1.40 2.85 1.55 0.06
Pb
Se
Zn
Mo
Referencia
17.6 ± 19.4 (8.30) 0.83 ± 0.37 (0.85) 0.18 ± 0.11 (0.20) 100 ± 130 (39.50)
nd
185 ± 105 (162) ND
nd
1–8
nd
3,9–22
nd
3,23–41
0.12
3,42–47
2.18 ± 1.76 (1.05) 2.34 ± 0.88 (2.05) nd
14.5 ± 1.91 (14.55) 115 ± 71.1 (91.40)
ND: no determined. ld: limit detection. Faecal materials: 1. Otero and Mouriño, 2002; 2. Otero, 1998; 3. Liu et al., 2006, 4. Rial et al., 2016; 5. Shatova et al., 2017; 6. Signa et al., 2013; 7. Wing et al., 2014; 8. Wing et al., 2017. Feathers: 9. Becker et al., 2016; 10. Bond and Diamond, 2009; 11. Burger and Gochfeld, 2000; 12. Burger and Gochfeld, 2009; 13. Burger et al., 2009; 14. Calle et al., 2015; 15. Espín et al., 2012; 16. Fort et al., 2016; 17. Furness and Camphuysen, 1997; 18. Goutner et al., 2000; 19. Mallory et al., 2015; 20. Monteiro et al., 1998; 21. Szumiło-Pilarska et al., 2017; 22. Thompson et al., 1993. Eggshells: 23. Barrett et al., 1996; 24. Barrett et al., 1985; 25. Braune et al., 2001; 26. Braune et al., 2002; 27. Braune et al., 2016; 28. Burger, 2002; 29. Burger et al., 2009; 30. Ceyca et al., 2016; 31. Christopher et al., 2002; 32. Day et al., 2006; 33. Day et al., 2012; 34. de Moreno et al., 1997; 35. Fimreite et al., 1974; 36. Jarman et al., 1996; 37. Mallory and Braune, 2012; 38. Mallory et al., 2015; 39. Peck et al., 2016; 40. Sanpera et al., 2000; 41. Sydeman and Jarman, 1998. Soils: 42. García et al., 2002a; 43. García et al., 2002b; 44. Otero, 1998; 45. Rajakaruna, 2009; 46. Wojtun et al., 2013; 47. Ziółek et al., 2017. 146
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Table 3 Total concentration (mean ± SD and median values in brackets) of trace elements in soils (mg kg−1). For each element, different letters indicate sites with significantly different means. Site
As
Cd
Co
Cu
Hg
Pb
Se
Zn
Mo
Control site
4.37 ± 1.0a (4.12) 7.94 ± 3.4b 8.05 14.0 ± 5.4b 13.30
0.57 ± 0.10a 0.55 0.60 ± 0.15a 0.57 1.31b ± 0.4b 1.35
0.45 ± 0.1a 0.46 0.60 ± 0.1b 0.59 0.71 ± 0.2b 0.65
9.01a ± 2.9a 8.39 13.2 ± 5.8ab 12.35 18.2 ± 6.0b 19.5
0.07 ± 0.04a 0.06 0.08 ± 0.04b 0.07 0.12 ± 0.04c 0.11
16.1 ± 1.5a 16.14 14.8 ± 5.9a 13.85 18.2 ± 5.8a18.9
0.26 ± 0.1a 0.22 0.61 ± 0.3b 0.57 0.88 ± 0.3c 0.90
108 ± 16a 105 75 ± 15a 73.2 164 ± 83b 154
11.2 ± 7.6a 9.67 10.2 ± 6.8a 8.77 28 ± 22b 19.4
L-I. influence High influence
colonies: 4.2 ± 2–5.2 ± 1.4 mg kg−1) and Mo (control zone: 1.0 ± 2 mg kg−1 colonies: 1.3 ± 0.4–1.6 ± 67 mg kg−1), whereas the other elements were found at much lower concentrations (< 1 mg kg−1). High concentrations of Cu were detected in fraction 3, varying from 4 mg kg−1, obtained in the control zone, to 8.3 mg kg−1 in the sub-colonies with high densities of the gulls, representing > 90% of the Cu extracted in all three fractions together. These results are consistent with the strong affinity between Cu and the soil organic matter, thus differentiating Cu from most other
trace metals, which show high affinity for Fe/Mn oxyhydroxides (Adriano, 2001). Selenium is also mainly associated with the oxidizable fraction. Previous studies indicate that in soil Se is mainly associated with the organic matter or occurs as the zerovalent form (Se0), which will be extracted in the F3 fraction (Martens and Suarez, 1998; Adriano, 2001). Although to a lesser than the previous elements, high proportions of Co, Hg and Pb (siderophile elements) were associated with organic matter. The sandy texture (> 70% sand) of the soils under study resulted in a low concentration of amorphous
Fig. 2. Mean ( ± standard error) concentrations of the trace element fractions in the control site and sub-colony soils: CS: control site (n = 11); L-I: low-intermediate density of gulls (n = 11) and H: high density of gulls (n = 17). Note that different scales are used in the graphs in the upper (mg kg−1) and lower (μg kg−1) parts of the figure. For each element and the same geochemical fraction (F1: exchangeable and carbonate fraction; F2: easy reducible fraction; or F3: oxidizable fraction), different letters indicate significant differences among sampling sites at p < 5%. 147
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Fe oxyhydroxides (Fe/Al soluble in ammonium oxalate < 0.1%; Otero et al., 2015), which limits the importance of this fraction in the adsorption and coprecipitation of trace elements. By contrast, the mean organic C content was high (control zone: 9.3 ± 2%; colonies 7–14%; Otero et al., 2015), which may explain the importance of the organic matter fraction of the colony soils in retaining elements (see also Otero and Fernández-Sanjurjo, 2000). The results of the sequential extraction also contributed to distinguishing the control zone from the areas most strongly affected by the presence of the Yellow-legged gull. Thus, the total contents of Pb and Cd in the colony soils were not significantly different from those in the control zone. However, the mean concentrations of Cd and Pb and of most of the trace elements considered were significantly higher for some of the geochemical fractions extracted, mainly fraction F3 (Fig. 2). In addition, the sum of the three fractions represented > 60% of the total content, whereas in the control zone, the corresponding proportion was 50%, except for Se (78%) and Pb (60%). These results support the previously suggested idea that the presence of seabirds contributes to increasing the concentration of the most reactive geochemical fractions in the surrounding soil (Otero, 1998: Otero and FernándezSanjurjo, 2000). In conclusion, the biomaterials (in particular the excrement and pellets) generated by the Yellow-legged gull in the seabird colonies in the Atlantic Islands National Park contains high concentrations of trace elements. The colony soils, even in the recently established colony with a low-intermediate density of gulls, are thus clearly enriched in trace elements relative to the control zone. The enrichment is especially high in the most labile soil fractions (i.e. organic matter, Fe oxyhydroxides). Finally, due to the low content of Fe/Al oxyhydroxides in the soils under study, the organic matter is the soil component that plays the most important role in retaining trace elements.
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