Crabs tell the difference – Relating trace metal content with land use and landscape attributes

Chemosphere 144 (2016) 1377–1383

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Crabs tell the difference – Relating trace metal content with land use and landscape attributes Nuno V. Álvaro a,b,c,∗, Ana I. Neto a,b, Ruben P. Couto a, José M.N. Azevedo a,b, Armindo S. Rodrigues a,d a

University of the Azores, Department of Biology, Ponta Delgada, Azores, Portugal cE3c - ABG - Center for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Department of Biology, University of the Azores, 9501-801 Ponta Delgada, Portugal c Centro de Estudos do Clima, Meteorologia e Mudanças Globais, Pólo Universitário de Angra do Heroísmo, 9701-851 Angra do Heroísmo, Portugal d CVARG, Center for Volcanology and Evaluation of Geological Risks, Ponta Delgada, Portugal b

h i g h l i g h t s • • •

In volcanic islands different land uses have distinct heavy metal footprints. Heavy metals in Pachygrapsus marmoratus reflect its availability on the coast. The species is a potential monitoring tool for heavy metals in coastal areas.

a r t i c l e

i n f o

Article history: Received 13 July 2015 Received in revised form 21 September 2015 Accepted 3 October 2015 Available online 23 October 2015 Handling editor: James M. Lazorchak Keywords: Heavy metals Volcanic islands Decapods Indicators Coastal areas

a b s t r a c t Heavy metal concentration in a given locality depends upon its natural characteristics and level of anthropogenic pressure. Volcanic sites have a different heavy metal footprint from agriculture soils and both differ from urban centres. Different animal species absorb heavy metals differently according to their feeding behaviour and physiology. Depending on the capability to accumulate heavy metals, some species can be used in biomonitoring programs for the identification of disturbed areas. Crabs are included in these species and known to accumulate heavy metals. The present study investigates the potential of Pachygrapsus marmoratus (Fabricius, 1787), a small crab abundant in the Azores intertidal, as an indicator of the presence of heavy metals in Azorean coastal environments, comparing hydrothermal vent locations, urban centres and locations adjacent to agricultural activity. Specimens were collected in the same period and had their hepatopancreas removed, dried and analysed for heavy metals. Results revealed differences in concentration of the studied elements between all sampling sites, each one revealing a distinct heavy metal content. Fe, Cu, Mn, Zn and Cd are the metals responsible for separating the various sites. The concentration levels of the heavy metals recorded in the present study reflect the environmental available metals where the organisms live. This, associated to the large availability of P. marmoratus specimens in the Azores, and to the fact that these animals are easy to capture and handle, suggests this species as a potential bioindicator for heavy metal concentration in Azorean coastal areas, both humanized and naturally disturbed. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction Heavy metals are naturally present in the environment all over the world, usually in different concentrations depending on the ∗ Corresponding author. University of the Azores, Department of Biology, Ponta Delgada, Azores, Portugal. E-mail address: [email protected] (N.V. Álvaro).

http://dx.doi.org/10.1016/j.chemosphere.2015.10.022 0045-6535/© 2015 Elsevier Ltd. All rights reserved.

characteristics of each location. The prolonged exposure to heavy metals such as arsenic (As), cadmium (Cd) and chromium (Cr) is dangerous to animal and human health. Acute mercury (Hg) exposure originates lung damage, while chronic ingestion affects the neurologic development in foetuses, infants and children (Jarup, 2003). Lead (Pb) affects the central nervous system of animals and inhibits their ability to synthesize red blood cells. Long-term exposure to this element also promotes cancer and can result in

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reduced performance of the nervous system, weakness in fingers, wrists, or ankles, small increases in blood pressure and anaemia (Koller et al., 1985). Exposure to high Pb levels can severely damage the brain and kidneys and ultimately cause death (Tong et al., 2000; Martin and Griswold, 2009). Cd has also a disturbance effect in antioxidant enzymes of crabs and shrimps (Kang et al., 2012), affects lipid transport (Yang et al., 2013), and can inhibit calcium (Ca) uptake (Rainbow and Black, 2005). Heavy metals are strongly related with anthropogenic activities, e.g. industries of glass, textiles, herbicides, insecticides (Eisler, 1988; ECGSD, 1999). Harbours are also subjected to a large input of specific trace metals involved in human activities (Morillo et al., 2008). Duysak and Ersoy (2014) found higher concentration of zinc (Zn), Cd, copper (Cu) and Pb inside a fishing harbour in the coast of Turkey. They also found high levels of iron (Fe), cobalt (Co), nickel (Ni), manganese (Mn) and Cr in the gastropod Monodonta turbinata from a location close to Kaleköy, an urban centre with strong household waste discharges. Other sources of heavy metals are vehicle brake emissions (Cu), tire wear (Zn), and atmospheric emissions (Cd and Pb). All these elements are also present in construction materials such as bricks and painted wood (Davis et al., 2001). According to Spatari et al. (2002), each person in Europe uses approximately 8 kg/year of Cu in e.g. infrastructures, buildings, industries, and private households. About 40% of it is discarded into the environment. Cr is also present in many man-made materials such as: stainless steel and non-iron alloy production for plating metals; pigments; leather processing; production of catalysts; surface treatments; refractories (Jacobs and Testa, 2004). This element is a primary contaminant because of its toxicity to humans and to the environment. Ni is present in many artefacts such as brake linings, tires, stainless steel and metal alloys for engine parts (Paul and Meyer, 2001; Cempel and Nikel, 2006). Ni is usually transported via water streams like river and wastewater effluents in to oceanic waters (Cempel and Nikel, 2006). Heavy metals are also frequently associated with volcanism and (according to Adamo et al., 2003), volcanic soils have high metal retention properties that may play a key role in maintaining the element in soil for a long time. The exposure to volcanic emissions can last years after the end of the eruption and this may increase the chance of contamination and enlarge the percentage of occurrence of diseases caused by exposure to heavy metals (Amaral and Rodrigues, 2011). Volcanism is a natural contamination source for the coastal ecosystems of the Azores (Depledge et al., 1992). Investigations focussed on the effect of volcanic emissions on marine organisms in this region has revealed higher than normal concentrations of heavy metals on organisms living near littoral hydrothermal vents: (i) talitroidean amphipods collected in the Azores had higher Zn and Cu concentrations than its Scottish counterparts (Moore et al., 1995); (ii) the intertidal barnacle Chthamalus stellatus sampled in hydrothermal vents in São Miguel had more Zn and Cd than specimens collected in mainland Portugal and Southwest Spain (Weeks et al., 1995); (iii) the barnacle Megabalanus azoricus collected in the Azores had higher concentrations of rubidium (Rb) and selenium (Se), in comparison to several studies performed in other countries (Dionisio et al., 2013) and the concentrations of Cd and As greatly surpassed the EU consumer safety levels (Dionisio et al., 2013); (iv) patellid limpets collected in hydrothermal vents in São Miguel had more Mn, Rb, Fe, and Cu than specimens elsewhere (Cunha et al., 2008); macroalgae samples also collected in Azorean sites with hydrothermal activity had higher concentrations of Zn, Mn, and Rb than samples collected at non volcanic sites (Couto et al., 2010). Other potential sources of heavy metals in this region are human activities, e.g. extensive use of agrochemicals in agriculture

(Parelho et al., 2014) and general activities related with urban centres. However, to our knowledge, there is no research comparing these potential different sources of heavy metals in the Azorean coastal systems. The present study investigates the potential of Pachygrapsus marmoratus (Fabricius, 1787) as an indicator of the presence of heavy metals in Azorean coastal environments by comparing locations near hydrothermal vents, urban centres and agricultural fields. P. marmoratus was chosen because it is consumed in the Azores, abundant in the rocky intertidal and man-made structures such as harbours, marinas and sea walls (N.V. Álvaro personal observation), and previously referred as a bioindicator for metal accumulation. Fratini et al. (2008), in samples from Italy, found bioaccumulation levels of As, Cd, Pb and Cu that reflected with accuracy the levels of pollution in their immediate environment. Mouneyrac et al. (2001) reported high concentrations of Cd, Cu, Zn in the gill and hepatopancreas of samples from the Gironde estuary (France). The species is present in the Mediterranean basin, East Atlantic between the Normandy coast of France and Morocco, the Azores, Madeira and the Canary Islands (Poupin et al., 2005). Being an intertidal species it is naturally resilient to daily environmental changes. Furthermore it is an omnivorous species (Cannicci et al., 2002, 2007) and the diversity in food consumption permits the absorption of different elements at various concentrations depending on the food source. This paper will therefore contribute to evaluate if sites with different land uses have distinct heavy metal footprints, and if P. marmoratus can be considered a potential monitoring tool for heavy metals in coastal areas. 2. Material and methods 2.1. Sampling Samples of P. marmoratus approximately of the same size (around 1.6 mm mean size of carapace length) were obtained, in one sampling occasion during the first semester of 2014, from the urban sites Cais da Sardinha (CDS) and Lagoa (LAG), the hydrothermal vent location Ladeira da Velha (LDV), and from Negrito (NEG), a location adjacent to agricultural activity (Fig. 1). Urban sites are located in São Miguel, the most populated island of the archipelago (around 137 thousand people, about half of the population in the Azores). CDS is located inside the commercial harbour of Ponta Delgada, the largest Azorean city in the archipelago. It is subject to the pollution associated with the harbour traffic and to the effect of different pollution sources associated with urban activities. LAG is located near the wastewater treatment plant of Lagoa, a small city in the south of the island of São Miguel with few small industries. LDV is also located on São Miguel Island but on the north coast, away from any urban outflows and characterized by the presence of volcanic hydrothermal vents, in the vicinity of which the samples were taken. NEG is located on the south of Terceira Island near a recreational bathing area in a location dominated by agriculture, pasture fields, and vineyard sites. There are also two streams that flow in to sea near the sampling location. 2.2. Laboratory procedures After collection, specimens were sexed, measured (carapace length) and weighted. A subsample of 16 adult animals (1.6 mm mean size, 2.86 g mean weight), respecting sex ratio, was selected per sample and their hepatopancreas removed and dried (60 °C for eight days), following the work by Mouneyrac et al. (2001)

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Fig. 1. Sampling locations: CDS – Cais da Sardinha; LAG – Lagoa; LDV – Ladeira da Velha; NEG – Negrito.

and Fratini et al. (2008) that confirmed its storing capacity for heavy metals accumulation. Nineteen samples of 0.5 g of dried hepatopancreas were obtained, respectively six from CDS, three from LAG, six from LDV and four from NEG. These samples were made by adding the dried hepatopancreas of several individual of each location according to their availability. After drying, a portion was removed and digested using hydrofluoric acid, a mixture of nitric and perchloric acids, and a mixture of nitric and hydrochloric acids and then analysed for trace metals content using Inductively Coupled Plasma Mass Spectrometry (ICP-MS). Quality control was tested against two certified reference materials for trace metals (DOLT-3 and DORM-2). The elements analysed in the present study were As, Cd, Co, Cr, Cu, Fe, Hg, Mn, Ni, Pb, Rb, Se, and Zn. 2.3. Data analysis A similarity matrix (normalized Euclidean distances) was constructed with the resulting data, and locations were compared with an ANOSIM test and a cluster analysis. A SIMPER analysis was performed to evaluate metals responsible for the observed differences. The software Primer-E v.5 (Clarke, 1993) was used for this analysis. 3. Results The average concentration of the heavy metals analysed in the present study is presented in Table 1. The more abundant metals were Fe, Cu, Zn and Mn, listed for all sites, but with their concentration varying according to the sampling location.

The nonmetric multidimensional scale plot (Fig. 2A) shows a clear separation between the four sampling sites as well as a larger proximity between each site’s replicates, which is supported by the cluster analysis (Fig. 2B) that separated samples in four main clusters, according to their provenance. At a higher level, LDV (volcanic environment) separated from the remaining sampling sites; a second division separated CDS (commercial harbour) from the less impacted sites (LAG and NEG). These differences were significant (see Table 2, global R was 0.953 with a significance level of sample statistics of 0.05). Metals responsible for separating the various sites were Fe, Cu, Mn, Zn and Cd (see SIMPER analysis in Table 3). From these, the more abundant metals were Fe and Cu (see Table 1). Fe had the higher concentration in LDV and was responsible for separating this site from the remaining. Cu concentration was higher in the two urban centres (CDS, LAG) and comparatively low in NEG and LDV (about 10% of its concentration in CDS). 4. Discussion Each site revealed a distinct heavy metal footprint as shown by the cluster analysis. Metals responsible for separating LDV from the other locations (Fe, Cu, Mn and Zn) are, in fact, known to increase in active volcanic areas. For example, a 0.2 nM increase of Fe concentration was recorded by Achterberg et al. (2013) for the Iceland basin after an eruption of the Eyjafjallajökull volcano. Couto et al. (2010) reported higher concentrations of Mn and Zn in the calcareous alga Corallina elongata from a hydrothermal site in the southwest coast of São Miguel than in samples collected from locations non-exposed to heavy metal natural emissions. Cunha et al. (2008) also reported a higher concentration of the above two elements and Cu in limpets from two shallow water hydrothermal

7 – – – 0.0055 – – – – 0.907 – – –

–

6 – – – 0.131 – – 0.055 – – – 0.08 –

–

5 9.33 – – 5.27 – – – – 0.873 0.6 0.39 –

–

5 12.92 – – 3.29 – – – – 0.856 0.47 0.35 –

–

1 2 3 4 168 ± 4.7 40.4 146.56 5.00 2.3 ± 0.2 0.8 8.23 0.37 3.87 ± 0.1 5.2 ± 0.1 5.95 6.69 – 0.12 ± 0 – – 5.6 2.82 ± 0.9 – – 1.75 65.67 ± 9.8 6.76 7.28 15.2 0.09 ± 0.1 – – 0.13 1683.33 ± 0.1 – – – 44.57 ± 2.2 5.2 5.63 29.18 7.02 ± 3.9 – – – 0.6 ± 0.1 2.75 36.89 0.08 34.53 ± 2.5 – – 0.75

LDV Azores Azores Ado-Ekiti, Nigeria Lagos, Nigeria (♂) Lagos, Nigeria (♀) Florida, USA Southern Gulf of Mexico

0.82 ± 0.5 – – –

112.67 ± 2.1 144.25 ± 11.8 159.83 ± 5.8 2 ± 0.1 2.48 ± 0.1 2.62 ± 0.4 2.6 ± 0.1 3.18 ± 0.1 – – 0.63 ± 0 6.33 ± 0.1 5.08 ± 0.5 8.02 ± 1.7 28.67 ± 21.5 23 ± 9 28.33 ± 3.9 0.07 ± 0 0.05 ± 0 0.09 ± 0.1 197.67 ± 5 32.23 ± 2.4 417.17 ± 21.9 7.57 ± 1.2 7.23 ± 3 4.12 ± 0.8 0.6 ± 0 3.48 ± 0.5 0,2 ± 2.8 25.93 ± 0.5 33.15 ± 2.9 34.73 ± 3,1 LAG NEG CDS

0.43 ± 0.05 0.28 ± 0.04 0.7 ± 0

Cr Co Cd As

Location

Metal concentration in body (dry weight, μg g−1 )

Cu

Fe

300 ± 0 450 ± 0 200 ± 0

Hg

Mn

Ni

Pb

Rb

Se

Zn

1 1 1

Source

N.V. Álvaro et al. / Chemosphere 144 (2016) 1377–1383 Table 1 Average (+SD) concentration of heavy metals in decapod crustaceans (μg g−1 ). 1- this study (LAG – Lagoa; NEG – Negrito; CDS – Cais da Sardinha; LDV – Ladeira da Velha); 2- Cunha et al. (2008); 3- Dionisio et al. (2013); 4Falusi and Olanipekun (2007); 5- Olusegun et al. (2008); 6- Adams and Engel (2014); 7- Castañeda-Chavez et al. (2014).

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vents (São Miguel, Azores) compared to limpets from sites without hydrothermalism. The higher concentration of Cu found in the two urban locations (CDS, LAG) is in agreement with other published information that indicates this element as abundant in urban areas (Davis et al., 2001; Gobel et al., 2007), where it is known to have a low recycling capacity (Spatari et al., 2002). Our results however do not agree with the work of Olusegun et al. (2008) that recorded low values of Cu in samples of the decapod Callinectes amnicola from an estuary area with a large concentration of trace metals due to human pollution in Nigeria. Also in Nigeria, Falusi and Olanipekun (2007) reported low values of Cu for the decapod Carcinus sp. from a river with city wastewater effluents. Another element known to be abundant in urban centres, where the consumption of fossil fuels is higher, is Ni (Barałkiewicz and Siepak, 1999). In the present study, this element had also higher concentration in the two urban sites. Present results for Zn also agree with literature since this metal is indicated as common in urban areas due to its inclusion in automobile tires (Li et al., 2001; Kennedy and Sutherland, 2008) and also in areas with hydrothermal vents (Hsu-Kim et al., 2008). However in Nigeria, Falusi and Olanipekun (2007) reported for the decapod Carcinus sp. lower values of Zn from a river with city wastewater effluents. The higher concentration of Cd in NEG is probably related to the location of this site in the proximity of rural areas dominated by fields with conventional farming that use chemical pesticides and fertilizers, known to have Cd in their composition (Abollino et al., 2002; Aydinalp and Marinova, 2003; Dœlsch et al., 2006; Parelho et al., 2014). Also the two proximal stream outfalls may carry part of the agrochemicals from the upstream agriculture fields, enhancing the concentration of this element in NEG. The higher concentration of Cd in this location may also be related to the entrance of fresh water in Negrito bay which may locally reduce the water salinity and increase the rate of Cd and Zn uptake by the species, as suggested by several authors (Wright, 1977; Rainbow, 1997; Rainbow and Black, 2005). The lower values of Cd obtained in the present study for the non-rural sites are in agreement with the work of Castañeda-Chavez et al. (2014) and Adams and Engel (2014) that reported low values of this element for the decapod Callinectes sapidus in, respectively, heavy metal polluted lagoon systems of the Southern Gulf of Mexico and in an estuary area in Florida with a known history of ecological disturbance. These results also agree with the ones reported by Falusi and Olanipekun (2007) for the decapod Carcinus sp. from a river with city wastewater effluents in Nigeria. On the other hand, our results differ from Dionisio et al. (2013) that found a much higher concentration of Cd in the barnacle Megabalanus azoricus in hydrothermal vent sites in the Azores. Worth considering that these animals are suspension feeders, which may explain these results. Low concentrations of Hg obtained in the studied samples are in agreement with the ones reported by Cunha et al. (2008) for limpets living in two shallow water hydrothermal vents in São Miguel and may indicate that the Hg content in Azorean coasts is low, even in volcanic environments. Worth considering also, in this respect, is the role of selenium in the prevention and inhibition of mercury toxicity reported for several marine organisms (Storelli et al., 2002; Torres et al., 2014a, 2014b). This may also be a reason for the low concentrations found in the present study as Se was commonly present in the studied crabs and in similar concentrations in the specimens collected in the four sampling sites. Higher Pb values obtained in CDS may be related with the location of this sampling site in a harbour with commercial, fishing and recreational vessels that use paints containing led and copper in their composition (Almeida et al., 2007).

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Fig. 2. A. Nonmetric multidimensional scale plot; and B. cluster analysis (group average) dendogram using the complete set of samples: CDS – Cais da Sardinha; LAG – Lagoa; LDV – Ladeira da Velha; NEG – Negrito.

Table 2 ANOSIM comparison of heavy metal concentration between sampling sites. Asterisc and bold indicate significant differences (P ≤ 0.05). CDS – Cais da Sardinha; LAG – Lagoa; LDV – Ladeira da Velha; NEG – Negrito. Sampling sites

R statistic

Significance level(P)

Actual permutations

Possible permutations

Global∗ LDV/LAG LDV/NEG∗ LDV/CDS∗ CDS/LAG CDS/NEG∗ NEG/LAG

1.0 1.0 1.0 1.0 1.0 1.0 1.0

0.001∗ 0.012 0.005∗ 0.002∗ 0.012 0.005∗ 0.029

999 84 210 462 84 210 35

814773960 84 210 462 84 210 35

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Table 3 Main elements contributing to the differences between sites (SIMPER analysis): CDS – Cais da Sardinha; LAG – Lagoa; LDV – Ladeira da Velha; NEG – Negrito. Sampling sites

Element

Average dissimilarity

Contribution %

LDV/LAG

Fe Cu Mn Zn Fe Mn Fe Cu Cu Fe Zn Mn Cu Fe Cd Cu Fe Mn Zn Cd

14.96 5.17 2.23 1.65 12.54 2.41 15.94 9.13 4.89 1.98 1.56 1.43 11.48 4.99 1.1 6.95 4.83 1.59 1.14 0.9

56.2 19.42 8.39 6.19 65.58 12.62 53.73 30.78 38.16 15.43 12.16 11.19 54.03 23.48 5.18 40.67 28.27 9.29 6.69 5.27

LDVNEG LDV/CDS CDS/LAG

CDS/NEG

NEG/LAG

5. Conclusions The concentration levels of heavy metals in P. marmoratus reported in the present study reflect the environmental bioavailability of elements where the organisms live. Each one of the chosen sites had different characteristics and that was revealed by its heavy metal content. This feature, associated to the large availability of P. marmoratus specimens, and to the fact that these animals are easy to capture and to handle, suggests this species as a potential bioindicator for heavy metal concentration monitoring in Azorean coastal areas. Acknowledgements The authors thank the help of Sergio Fernandez Navarrete in the collection and sorting of the animals in the field and laboratory work. This research was partially supported by the European Regional Development Fund (ERDF) through the COMPETE - Operational Competitiveness Programme and national funds through FCT – Foundation for Science and Technology, under the project “PEst-C/MAR/LA0015/2013, by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020 and by cE3c funding (Ref: UID/BIA/00329/2013). It was also partly supported by CIRN (Centro de Investigação de Recursos Naturais, University of the Azores), and CIIMAR (Interdisciplinary Centre of Marine and Environmental, Porto, Portugal). Nuno V. Álvaro was funded by Fundo Regional de Ciência, Governo Regional dos Açores (M3.1.2/F/015/2011). References Abollino, O., Aceto, M., Malandrino, M., Mentasti, E., Sarzanini, C., Petrella, F., 2002. Heavy metals in agricultural soils from Piedmont, Italy. Distribution, speciation and chemometric data treatment. Chemosphere 49, 545–557. http://dx.doi.org/ 10.1016/S0045-6535(02)00352-1. Achterberg, E.P., Moore, C.M., Henson, S.A., Steigenberger, S., Stohl, A., Eckhardt, S., Avendano, L.C., Cassidy, M., Hembury, D., Klar, J.K., Lucas, M.I., Macey, A.I., Marsay, C.M., Ryan-Keogh, T.J., 2013. Natural iron fertilization by the Eyjafjallajökull volcanic eruption. Geophys. Res. Lett. 40, 921–926. http://dx.doi.org/10. 1002/grl.50221. Adamo, P., Denaix, L., Terribile, F., Zampella, M., 2003. Characterization of heavy metals in contaminated volcanic soils of the Solofrana river valley (southern Italy). Geoderma 117, 347–366. http://dx.doi.org/10.1016/s0016-7061(03) 00133-2.

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