Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 16, pp 16865–16872 | Cite as

Phthalate pollution in an Amazonian rainforest

  • Alain Lenoir
  • Raphaël Boulay
  • Alain Dejean
  • Axel Touchard
  • Virginie Cuvillier-Hot
Short Research and Discussion Article

Abstract

Phthalates are ubiquitous contaminants and endocrine-disrupting chemicals that can become trapped in the cuticles of insects, including ants which were recognized as good bioindicators for such pollution. Because phthalates have been noted in developed countries and because they also have been found in the Arctic, a region isolated from direct anthropogenic influence, we hypothesized that they are widespread. So, we looked for their presence on the cuticle of ants gathered from isolated areas of the Amazonian rainforest and along an anthropogenic gradient of pollution (rainforest vs. road sides vs. cities in French Guiana). Phthalate pollution (mainly di(2-ethylhexyl) phthalate (DEHP)) was higher on ants gathered in cities and along road sides than on those collected in the pristine rainforest, indicating that it follows a human-mediated gradient of disturbance related to the use of plastics and many other products that contain phthalates in urban zones. Their presence varied with the ant species; the cuticle of Solenopsis saevissima traps higher amount of phthalates than that of compared species. However, the presence of phthalates in isolated areas of pristine rainforests suggests that they are associated both with atmospheric particles and in gaseous form and are transported over long distances by wind, resulting in a worldwide diffusion. These findings suggest that there is no such thing as a “pristine” zone.

Keywords

Phthalates Pollution Tropical rainforests Ants DEHP 

Notes

Acknowledgments

Financial support for this study was provided by a CNRS/Centre d’Études de la Biodiversité Amazonienne (CEBA) project entitled “Phthalate pollution in an Amazonian rainforest” (PPAR). We are grateful to Chloé Fasilleau and Chloé Moyse (École Polytechnique, Université de Tours, France) for the analysis of the data, to Jessica Pearce-Duvet and Andrea Yockey-Dejean for proofreading the manuscript, and to Jacques H. C. Delabie (Laboratório de Mirmecologia, CRC, Ilhéus, Bahia, Brazil) for the identification of the ants. We would like to thank the staff of the CNRS Nouragues research station and the Laboratoire Environnement de Petit-Saut for furnishing logistical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Supplementary material

11356_2016_7141_MOESM1_ESM.jpg (4.4 mb)
Suppl 1

(JPEG 4.40 mb)

11356_2016_7141_MOESM2_ESM.jpg (4 mb)
Suppl 2

(JPEG 4.02 mb)

References

  1. Abe Y, Yamaguchi M, Mutsuga M, Hirahara Y, Kawamura Y (2012) Survey of plasticizers in polyvinyl chloride toys. Food Hyg Safe Sci 53:19–27CrossRefGoogle Scholar
  2. Ait Bamai Y, Shibata E, Saito I, Araki A, Kanazawa A, Morimoto K, Nakayama K, Tanaka M, Takigawa T, Yoshimura T, et al. (2014) Exposure to house dust phthalates in relation to asthma and allergies in both children and adults. Sci Total Environ 485–486:153–163CrossRefGoogle Scholar
  3. Alves C, Oliveira T, Pio C, Silvestre AJD, Fialho P, Barata F, Legrand M (2007) Characterisation of carbonaceous aerosols from the Azorean Island of Terceira. Atmos Environ 41:1359–1373CrossRefGoogle Scholar
  4. Babich MA, Osterhout CA (2010) Toxicity review of diisononyl phthalate (DINP). Bethesda, MD, p. 154 http://www.cpsc.gov/about/cpsia/toxicityDINP.pdf Google Scholar
  5. Barušić L, Galić A, Bošnir J, Baričević L, Mandić-Andačić I, Krivohlavek A, Mojsović Ćuić A, Đikić D (2015) Phthalate in children’s toys and childcare articles in Croatia. Curr Sci 109:1480–1486Google Scholar
  6. Basset Y, Cizek L, Cuénoud P, Didham RK, Novotny V, Ødegaard F, Roslin T, Tishechkin AK, Schmidl J, Winchester NN, et al. (2015) Arthropod distribution in a tropical rainforest: tackling a four dimensional puzzle. PLoS One 10:e0144110CrossRefGoogle Scholar
  7. Blanchard M, Teil M-J, Dargnat C, Alliot F, Chevreuil M (2013) Assessment of adult human exposure to phthalate esters in the urban Centre of Paris (France). Bull Environ Contam Toxicol 90:91–96CrossRefGoogle Scholar
  8. Blanchard O, Glorennec P, Mercier F, Bonvallot N, Chevrier C, Ramalho O, Mandin C, Le Bot B (2014) Semivolatile organic compounds in indoor air and settled dust in 30 French dwellings. Environ Sci Technol 48:3959–3969CrossRefGoogle Scholar
  9. Cao X-L (2008) Determination of phthalates and adipate in bottled water by headspace solid-phase microextraction and gas chromatography/mass spectrometry. J Chromato A 1178:231–238CrossRefGoogle Scholar
  10. Cavill GWK, Houghton E (1974) Volatile constituents of the Argentine ant, Iridomyrmex humilis. J Insect Physiol 20:2049–2059CrossRefGoogle Scholar
  11. Cecinato A, Balducci C, Mastroianni D, Perilli M (2012) Sampling and analytical methods for assessing the levels of organic pollutants in the atmosphere: PAH, phthalates and psychotropic substances: a short review. Environ Sci Pollut Res 19:1915–1926CrossRefGoogle Scholar
  12. Choi JK, Heo JB, Ban SJ, Yi SM, Zoh KD (2012) Chemical characteristics of PM2.5 aerosol in Incheon, Korea. Atmos Environ 60:583–592CrossRefGoogle Scholar
  13. Cuvillier-Hot V, Salin K, Devers S, Tasiemski A, Schaffner P, Boulay R, Lenoir A (2014) Impact of ecological doses of the most widespread phthalate on a terrestrial species, the ant Lasius niger. Environ Res 131:104–110CrossRefGoogle Scholar
  14. Dejean A, Céréghino R, Leponce M, Rossi V, Roux O, Compin A, Delabie JHC, Corbara B (2015) The fire ant Solenopsis saevissima and habitat disturbance alter ant communities. Biol Conserv 187:145–153CrossRefGoogle Scholar
  15. Desdoits-Lethimonier C, Albert O, Le Bizec B, Perdu E, Zalko D, Courant F, Lesné L, Guillé F, Dejucq-Rainsford N, Jégou B (2012) Human testis steroidogenesis is inhibited by phthalates. Hum Reprod 27:1451–1459CrossRefGoogle Scholar
  16. Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJB, Collen B (2014) Defaunation in the Anthropocene. Science 345:401–406CrossRefGoogle Scholar
  17. Doyle TJ, Bowman JL, Windell VL, McLean DJ, Kim KH (2013) Transgenerational effects of di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol Reprod 88:111–115CrossRefGoogle Scholar
  18. Gao D-W, Wen Z-D (2016) Phthalate esters in the environment: a critical review of their occurrence, biodegradation, and removal during wastewater treatment processes. Sci Total Environ 541:986–1001CrossRefGoogle Scholar
  19. Gaudin R, Marsan P, Ndaw S, Robert A, Ducos P (2011) Biological monitoring of exposure to di(2-ethylhexyl) phthalate in six French factories: a field study. Int Arch Occup Environ Health 84:523–531CrossRefGoogle Scholar
  20. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108CrossRefGoogle Scholar
  21. Gómez-Ramos MM, García-Valcárcel AI, Tadeo JL, Fernández-Alba AR, Hernando MD (2016) Screening of environmental contaminants in honey bee wax comb using gas chromatography–high-resolution time-of-flight mass spectrometry. Environ Sci Pollut Res 23:4609–4620CrossRefGoogle Scholar
  22. Holmstrup M, Bindesbøl A-M, Oostingh GJ, Duschl A, Scheil V, Köhler H-R, Loureiro S, Soares AMVM, Ferreira ALG, Kienle C, et al. (2010) Interactions between effects of environmental chemicals and natural stressors: a review. Sci Total Environ 408:3746–3762CrossRefGoogle Scholar
  23. Huang J, Nkrumah PN, Li Y, Appiah-Sefah G (2013) Chemical behavior of phthalates under abiotic conditions in landfills. Rev Environ Contam Toxicol 224:39–52Google Scholar
  24. Jensen J, van Langevelde J, Pritzl G, Krogh PH (2001) Effects of di(2-ethylhexyl) phthalate and dibutyl phthalate on the collembolan Folsomia fimetaria. Environ Toxicol Chem 20:1085–1091CrossRefGoogle Scholar
  25. Kampa M, Castanas E (2008) Human health effects of air pollution. Environ Pollut 151:362–367CrossRefGoogle Scholar
  26. Kather R, Drijfhout F, Martin S (2011) Task group differences in cuticular lipids in the honey bee Apis mellifera. J Chem Ecol 37:205–212CrossRefGoogle Scholar
  27. Kristensen TN, Pertoldi C, Pedersen LD, Andersen DH, Bach LA, Loeschcke V (2004) The increase of fluctuating asymmetry in a monoclonal strain of collembolans after chemical exposure-discussing a new method for estimating the environmental variance. Ecol Indic 4:73–81CrossRefGoogle Scholar
  28. Lenoir A, Cuvillier-Hot V, Devers S, Christidès J-P, Montigny F (2012) Ant cuticles: a trap for atmospheric phthalate contaminants. Sci Total Environ 441:209–212CrossRefGoogle Scholar
  29. Lenoir A, Devers S, Touchard A, Dejean A (2016) The Guianese population of the fire ant Solenopsis saevissima is unicolonial. Insect Sci doi: 10.1111/1744-7917.12232 Google Scholar
  30. Lenoir A, Touchard A, Devers S, Christides J-P, Boulay R, Cuvillier-Hot V (2014) Ant cuticular response to phthalate pollution. Environ Sci Pollut Res 21:13446–13451CrossRefGoogle Scholar
  31. Longino JT, Branstetter MG, Colwell RK (2014) How ants drop out: ant abundance on tropical mountains. PLoS One 9:e104030CrossRefGoogle Scholar
  32. Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK (2013) Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One 8:e55387CrossRefGoogle Scholar
  33. Manzetti S, van der Spoel ER, van der Spoel D (2014) Chemical properties, environmental fate, and degradation of seven classes of pollutants. Chem Res Toxicol 27:713–737CrossRefGoogle Scholar
  34. Martin JM, Roux O, Groc S, Dejean A (2011) A type of unicoloniality within the native range of the fire ant Solenopsis saevissima. C R Biol 334:307–310CrossRefGoogle Scholar
  35. Rastogi SC (1998) Gas chromatographic analysis of the phthalate esters in plastic toys. Chromatographia 47:724–726CrossRefGoogle Scholar
  36. Rhind SM (2009) Anthropogenic pollutants: a threat to ecosystem sustainability? Philos Trans R Soc Lond B 364:3391–3401CrossRefGoogle Scholar
  37. Rissman EF, Adli M (2014) Transgenerational epigenetic inheritance: focus on endocrine disrupting compounds. Endocrinology 155:2770–2780CrossRefGoogle Scholar
  38. Saillenfait A-M, Laudet-Hesbert A (2005a) Phtalates. EMC-Toxicol Pathol 2:1–13CrossRefGoogle Scholar
  39. Saillenfait A-M, Laudet-Hesbert A (2005b) Phtalates (II). EMC-Toxicol Pathol 2:137–150CrossRefGoogle Scholar
  40. Salapasidou M, Samara C, Voutsa D (2011) Endocrine disrupting compounds in the atmosphere of the urban area of Thessaloniki, Greece. Atmos Environ 45:3720–3729CrossRefGoogle Scholar
  41. Saravanabhavan, GMJ (2012) Human biological monitoring of diisononyl phthalate and diisodecyl phthalate: a review. J Environ Pub Health 2012:ID 810501Google Scholar
  42. Schwindt AR, Winkelman DL, Keteles K,  Murphy M, Vajda AM (2014) An environmental oestrogen disrupts fish population dynamics through direct and transgenerational effects on survival and fecundity. J Appl Ecol 51:582–591. doi: 10.1111/1365-2664.12237
  43. Staples CA, Peterson DR, Parkerton TF, Adams WJ (1997) The environmental fate of phthalate esters: a literature review. Chemosphere 35:667–749CrossRefGoogle Scholar
  44. Teil M-J, Blanchard M, Chevreuil M (2006) Atmospheric fate of phthalate esters in an urban area (Paris, France). Sci Total Environ 354:212–223CrossRefGoogle Scholar
  45. Teil M-J, Moreau-Guigon E, Blanchard M, Alliot F, Gasperi J, Cladière M, Mandin C, Moukhtar S, Chevreuil M (2016) Endocrine disrupting compounds in gaseous and particulate outdoor air phases according to environmental factors. Chemosphere 146:94–104CrossRefGoogle Scholar
  46. Tomar RS, Budroe JD, Cendak R (2013) Evidence on the carcinogenicity of the diisononyl phthalate (DINP). California Environmental Protection Agency. http://oehha.ca.gov/prop65/hazard_ident/pdf_zip/DINP_HID100413.pdf
  47. Valton AS, Serre-Dargnat C, Blanchard M, Alliot F, Chevreuil M, Teil M (2014) Determination of phthalates and their by-products in tissues of roach (Rutilus rutilus) from the Orge river (France). Environ Sci Pollut Res 21:12723–12730CrossRefGoogle Scholar
  48. Vidau C, Diogon M, Aufauvre J, Fontbonne R, Viguès B, Brunet J-L, Texier C, Biron DG, Blot N, El Alaoui H, et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS One 6:e21550CrossRefGoogle Scholar
  49. Vienne C, Soroker V, Hefetz A (1995) Congruency of hydrocarbon patterns in heterospecific groups of ants: transfer and/or biosynthesis? Insect Soc 42:267–277CrossRefGoogle Scholar
  50. Williams BJ, Goldstein AH, Kreisberg NM, Hering SV (2010) In situ measurements of gas/particle-phase transitions for atmospheric semivolatile organic compounds. Proc Natl Acad Sc 107:6676–6681CrossRefGoogle Scholar
  51. Xie ZY, Ebinghaus R, Temme C, Caba A, Ruck W (2005) Atmospheric concentrations and air–sea exchanges of phthalates in the North Sea (German bight). Atmos Environ 39:3209–3219CrossRefGoogle Scholar
  52. Xie ZY, Ebinghaus R, Temme C, Lohmann R, Caba A, Ruck W (2007) Occurrence and air-sea exchange of phthalates in the arctic. Environ Sci Technol 41:4555–4560CrossRefGoogle Scholar
  53. Yuan S-Y, Huang IC, Chang B-V (2010) Biodegradation of dibutyl phthalate and di-(2-ethylhexyl) phthalate and microbial community changes in mangrove sediment. J Hazard Mater 184:826–831CrossRefGoogle Scholar
  54. Zhou QH, Wu ZB, Cheng SP, He F, Fu GP (2005) Enzymatic activities in constructed wetlands and di-n-butyl phthalate (DBP) biodegradation. Soil Biol Biochem 37:1454–1459CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Alain Lenoir
    • 1
  • Raphaël Boulay
    • 1
  • Alain Dejean
    • 2
    • 3
  • Axel Touchard
    • 3
  • Virginie Cuvillier-Hot
    • 4
  1. 1.IRBI, Institut de Recherche sur la Biologie de l’InsecteCNRS UMR 7261, Université de ToursToursFrance
  2. 2.Ecolab, Université de Toulouse, CNRS, INPT, UPSToulouseFrance
  3. 3.CNRS, UMR EcoFoG, AgroParisTech, Cirad, INRAUniversité des Antilles, Université de GuyaneKourouFrance
  4. 4.CNRS; UMR 8198, Unité Évolution, Écologie et PaléontologieUniversité de LilleLilleFrance

Personalised recommendations