Abstract
Vegetated walls are common structures in urban environments, and aiming to test the hypothesis that the biogenic crusts and plant and animal communities inhabiting these vertical surfaces can be more reliable indicators of atmospheric metal deposition than plants or animals inhabiting urban soils, we analyzed the chemical composition of the wall crusts, moss cushions (Tortula muralis) and the shells, soft tissues and feces of the stonework snail Papillifera papillaris collected in three small towns in Tuscany (Central Italy). Crusts and mosses from the same stones or bricks indicated that Cd, Pb, and Zn are the main pollutants released by vehicular traffic, while Hg and Cu probably originate from other sources. The soft tissues of P. papillaris (purged of the gut contents) showed as well higher Cd, Pb, and Zn and lower Hg concentrations at more traffic-affected sites, while data from shells and feces suggested that this species probably ingests large amounts of Al, Cr, Fe, Mn, and Pb, and avoids eating mosses. Most lithophilic elements and Pb are scarcely absorbed in the snail digestive tract and soft tissues mainly accumulate Cd and essential elements such as Cu and Mn. This study definitively confirms the extraordinary Mn bioaccumulation in P. papillaris soft tissues and reports extraordinary Mn levels also in the shell. The shells also contain unusually high Cu, Fe, and Zn concentrations and this bioaccumulation likely remains after death, potentially providing a historical record of the snail exposure to metals over lifetime.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aleksander-Kwaterczak U, Gołas-Siarzewska M (2015) Comparative analysis of Helix pomatia L. shells found in soils with varying degrees of contamination (southern Poland). Geol Geophys Environ 41(4):299–309. https://doi.org/10.7494/geol.2015.41.4.299
ARPAT (2017) Annuario 2017 dei dati ambientali della Toscana - Provincia di Siena. Agenzia Regionale per la Protezione Ambientale della Toscana, Firenze, 38 pp. http://www.arpat.toscana.it/annuario. Last accessed 20 December 2017
Barbato D, Benocci A, Caruso T, Manganelli G (2017) The role of dispersal and local environment in urban land snail assemblages: an example of three cities in Central Italy. Urban Ecosyst 20(4):919–931. https://doi.org/10.1007/s11252-017-0643-8
Barca D, Comite V, Belfiore CM, Bonazza A, La Russa MF, Ruffolo SA, Crisci GM, Pezzino A, Sabbioni C (2014) Impact of air pollution in deterioration of carbonate building materials in Italian urban environments. Appl Geochem 48:122–131. https://doi.org/10.1016/j.apgeochem.2014.07.002
Bargagli R (1995) The elemental composition of vegetation and the possible incidence of soil contamination of samples. Sci Total Environ 176(1-3):121–128. https://doi.org/10.1016/0048-9697(95)04838-3
Bargagli R (1998) Trace elements in terrestrial plants: an ecophysiological approach to biomonitoring and biorecovery. Springer-Verlag, Berlin, p 324
Bargagli R (2016) Moss and lichen biomonitoring of atmospheric mercury: a review. Sci Total Environ 572:216–231. https://doi.org/10.1016/j.scitotenv.2016.07.202
Beeby A, Richmond L (2002) Evaluating Helix aspersa as a sentinel for mapping metal pollution. Ecol Indic 1(4):261–270. https://doi.org/10.1016/S1470-160X(02)00022-5
Berger B, Dallinger R (1993) Terrestrial snails as quantitative indicators of environmental metal pollution. Environ Monit Assess 25(1):65–84. https://doi.org/10.1007/BF00549793
Berger B, Dallinger R, Thomaser A (1995) Quantification of metallothionein as a biomarker for cadmium exposure in terrestrial gastropods. Environ Toxicol Chem 14(5):781–791. https://doi.org/10.1002/etc.5620140507
Bourgoin BP (1990) Mytilus edulis shell as a bioindicator of lead pollution. Considerations on bioavailability and variability. Mar Ecol Prog Ser 61:253–262. https://doi.org/10.3354/meps061253
Comune di Siena (2005) SMaS, Schema Metropolitano dell'area Senese, Scenario 2005. http://maps1.ldpgis.it/siena/?q=smas. Last accessed 20 December 2017
Cravo A, Bebianno MJ, Foster P (2004) Partitioning of trace metals between soft tissues and shells of Patella aspera. Environ Int 30(1):87–98. https://doi.org/10.1016/S0160-4120(03)00154-5
Davidson A, Harborne JB, Longton RE (1990) The acceptability of mosses as food for generalist herbivores, slugs in the Arionidae. Bot J Linn Soc 104(1-3):99–113. https://doi.org/10.1111/j.1095-8339.1990.tb02213.x
Focardi S, Loiselle SA, Mazzuoli S, Bracchini L, Dattilo AM, Rossi C (2008) Satellite-based indices in the analysis of land cover for municipalities in the province of Siena, Italy. J Environ Management 86(2):383–389. https://doi.org/10.1016/j.jenvman.2006.08.011
Förstner U, Wittmann GTW (1981) Metal pollution in the aquatic environment. Springer-Verlag, Berlin, p 486. https://doi.org/10.1007/978-3-642-69385-4
Francis RA (2010) Wall ecology: a frontier for urban biodiversity and ecological engineering. Prog Phys Geogr 35:43–63
Garcia DA (2017) Green areas management and bioengineering techniques for improving urban ecological sustainability. Sustain Cities Soc 30:108–117. https://doi.org/10.1016/j.scs.2017.01.008
Gerdol R, Bragazza L, Marchesini R, Medici A, Pedrini P, Benedetti S, Bovolenta A, Coppi S (2002) Use of moss (Tortulas muralis Hedw.) for monitoring organic and inorganic air pollution in urban and rural sites in northern Italy. Atmos Environ 36(25):4069–4075. https://doi.org/10.1016/S1352-2310(02)00298-4
Gerdol R, Marchesini R, Iacumin P, Brancaleoni L (2014) Monitoring temporal trends of air pollution in an urban area using mosses and lichens as biomonitors. Chemosphere 108:388–395. https://doi.org/10.1016/j.chemosphere.2014.02.035
Giordano S, Adamo P, Spagnuolo V, Tretiach M, Bargagli R (2013) Accumulation of airborne trace elements in mosses, lichens and synthetic materials exposed at urban monitoring stations: towards a harmonisation of the moss-bag technique. Chemosphere 90(2):292–299. https://doi.org/10.1016/j.chemosphere.2012.07.006
Girod A (2011) Land snails from Late Glacial and Early Holocene Italian sites. Quat Int 244(1):105–116. https://doi.org/10.1016/j.quaint.2011.04.025
Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electro 4:1–9
IUCN (2013) Italy’s biodiversity at risk. A call for action. IUCN, Brussels, Belgium
Jim CY, Chen WY (2010) Habitat effect on vegetation ecology and occurrence on urban masonry walls. Urban For Urban Green 9(3):169–178. https://doi.org/10.1016/j.ufug.2010.02.004
Jordaens K, De Wolf H, Vandecasteele B, Blust R, Backljau T (2006) Associations between shell strength, shell morphology and heavy metals in the land snail Cepaea nemoralis (Gastropoda, Helicidae). Sci Total Environ 363(1-3):285–293. https://doi.org/10.1016/j.scitotenv.2005.12.002
Koide M, Soo Lee D, Goldberg ED (1982) Metal and transuranic records in mussel shells, byssal threads and tissues. Estuar Coast Shelf Sci 15(6):679–695. https://doi.org/10.1016/0272-7714(82)90079-8
Kosior G, Prell M, Samecka-Cymerman A, Stankiewicz A, Kolon K, Kryza R, Brudzińska-Kosior A, Frontasyeva M, Kempers AJ (2015) Metals in Tortula muralis from sandstone buildings in an urban agglomeration. Ecol Indic 58:122–131. https://doi.org/10.1016/j.ecolind.2015.05.051
Lisci M, Pacini E (1993) Plants growing on the walls of Italian towns. I. Sites and distribution. Phyton 33:5–26
Maravelaki-Kalaitzaki P (2005) Black crusts and patinas on Pentelic marble from the Parthenon and Erechtheum (Acropolis, Athens): characterization and origin. Anal Chim Acta 532(2):187–198. https://doi.org/10.1016/j.aca.2004.10.065
Monaci F, Moni F, Lanciotti E, Grechi D, Bargagli R (2000) Biomonitoring of airborne metals in urban environments: new tracers of vehicle emission, in place of lead. Environ Poll 107(3):321–327. https://doi.org/10.1016/S0269-7491(99)00175-X
Morillas H, Maguregui M, García-Florentino C, Carrero JA, Salcedo I, Madariaga JM (2016) The cauliflower-like black crusts on sandstones: a natural passive sampler to evaluate the surrounding environmental pollution. Environ Res 147:218–232. https://doi.org/10.1016/j.envres.2016.02.015
Naszradi T, Badacsonyi A, Keresztényi I, Podar D, Csintalan Z, Tuba Z (2007) Comparison of two metal surveys by moss Tortula muralis in Budapest, Hungary. Environ Monit Assess 134(1-3):279–285. https://doi.org/10.1007/s10661-007-9617-2
Notten MJ, Oosthoek AJP, Rozema J, Aerts R (2005) Heavy metal concentrations in a soil-plant-snail food chain along a terrestrial soil pollution gradient. Environ Pollut 138(1):178–190. https://doi.org/10.1016/j.envpol.2005.01.011
Oehlmann J, Schulte-Oehlmann U (2003) Molluscs as bioindicators. In: Markert BA, Breure AM, Zechmeister HG (eds), Bioindicators & Biomonitors: principles, concepts and applications. Elsevier Sci BV, pp 577-635
Ondina P, Hermida J, Outeiro A, Mato S (2004) Relationships between terrestrial gastropod distribution and soil properties in Galicia (NW Spain). Appl Soil Ecol 26(1):1–9. https://doi.org/10.1016/j.apsoil.2003.10.008
Ridot-Sharpe J (2010) Papillifera papillaris: a second colony is discovered in England. Archaeo+Malacol Group Newsl 18:4–6
Rota E, Barbato D, Ancora S, Bianchi N, Bargagli R (2016) Papillifera papillaris (O.F. Müller), a small snail living on stones and monuments, as indicator of metal deposition and bioavailability in urban environments. Ecol Indic 69:360–367
Ruffolo SA, Comite V, La Russa MF, Belfiore CM, Barca D, Bonazza A, Crisci GM, Pezzino A, Sabbioni C (2015) An analysis of the black crusts from Seville Cathedral: a challenge to deepen the understanding of the relationships among microstructure, microchemical features and pollution sources. Sci Total Environ 502:157–166. https://doi.org/10.1016/j.scitotenv.2014.09.023
Scheifler R, de Vaufleury A, Coeurdassier M, Crini N, Badot P-M (2006) Transfer of Cd, Cu, Ni, Pb, and Zn in a soil-plant-invertebrate food chain: a microcosm study. Environ Toxicol Chem 25(3):815–822. https://doi.org/10.1897/04-675R.1
Simkiss K, Watkins B (1991) Differences in zinc uptake between snails (Helix aspersa (Muller)) from metal- and bacteria-polluted sites. Funct Ecol 5(6):787–794. https://doi.org/10.2307/2389542
Tynan S, Eggins S, Kinsely L, Welch SA, Kirste D (2005) Mussel shells as environmental tracers: an example from the Loveday Basin. In: Roach IC (ed) Regolith 2005—ten years of CRC LEME, CRC LEME, pp 314–317
de Vaufleury A (2015) Landsnail for ecotoxicological assessment of chemicals and soil contamination—ecotoxicological assessment of chemicals and contaminated soils using the terrestrial snail, Helix aspersa, at various stage of its life cycle: a review. In: Armon RH, Hänninen O (eds) Environmental indicators. Springer, Netherlands, pp 365–391
Yap CK, Ismail A, Tan SG, Abdul Rahim I (2003) Can the shell of the green-lipped mussel Perna viridis from the west coast of Peninsular Malaysia be a potential biomonitoring material for Cd, Pb and Zn? Estuar Coast Shelf Sci 57(4):623–630. https://doi.org/10.1016/S0272-7714(02)00401-8
Acknowledgements
We wish to thank Nicola Bianchi for his expertise and assistance in analytical procedures.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Rota, E., Braccino, B., Dei, R. et al. Organisms in wall ecosystems as biomonitors of metal deposition and bioavailability in urban environments. Environ Sci Pollut Res 25, 10946–10955 (2018). https://doi.org/10.1007/s11356-017-1170-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-017-1170-0