Environmental Science and Pollution Research

, Volume 24, Issue 23, pp 19234–19248 | Cite as

Mice exposure to tannery effluents changes their olfactory capacity, and their response to predators and to the inhibitory avoidance test

  • Bruna de Oliveira Mendes
  • Letícia Martins Rabelo
  • Bianca Costa e Silva
  • Joyce Moreira de Souza
  • André Luis da Silva Castro
  • Anderson Rodrigo da Silva
  • Aline Sueli de Lima Rodrigues
  • Guilherme MalafaiaEmail author
Research Article


The current study has assessed whether the oral and/or dermal exposure of C57Bl/6 J mice to tannery effluent (a complex pollutant consisting of xenobiotic mixtures) could damage their olfactory functions, as well as whether it changes their aversive behavior in the inhibitory avoidance test. Accordingly, the animals were distributed in groups which were exposed or not to this xenobiotic through two different routes (oral and dermal), for 15 days. The effluent group subjected to oral exposure received drinking water containing 5% tannery effluent, whereas the animals in the dermal group were exposed to raw tannery effluent for 1 h/day. The animals dermally exposed to the tannery effluent (males and females) have shown the highest latency to find palatable food in the buried food test. The shortest time spent by the animals (orally or dermally) exposed to tannery effluent in the safety zone of the apparatus used in the predator exposure test, as well as the longest time spent by them in the aversive zone, have shown failures in their perception to the risk represented by the presence of the predator (cat). The passive avoidance test results have shown that the dermal exposure to tannery effluent led to partial memory deficit in male and female mice; therefore, the present study has confirmed the tannery effluent toxicity to mammals. Moreover, the present study was pioneer in demonstrating that the dermal exposure to this xenobiotic, even for a short period-of-time, can change the olfactory and cognitive functions of animals, as well as lead to harmful consequences to their health.


Agroindustrial wastes Xenobiotics Mammals Predation Cognition Behavior disruption 



The authors are grateful to the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No. 467801/2014-2) for granting scholarships to the students who developed this study; and to Instituto Federal Goiano for the financial support. In addition, the authors thank Dr. Boniek Gontijo Vaz for helpful chemical analysis.


  1. Almeida SF, Rabelo LM, Souza JM, Ferreira RO, Guimarães ATB, Pereira CCO, Rodrigues ASL, Malafaia G (2016) Behavioral changes in female Swiss mice exposed to tannery effluents. Revista Ambiente Água 11(3):519–534CrossRefGoogle Scholar
  2. American Public Health Association (APHA) (1997) Standard methods for the examination of water and wastewater, 20th edn. APHA, AWWA, WPCR, New York, p 1194Google Scholar
  3. Basso DM, Fisher LC, Anderson AJ, Jakeman LB, McTigue DM, Popovich PG (2006) Basso mouse scale for locomotion detects differences in recovery after spinal cord injury in five common mouse strains. J Neurotrauma 23:635–659. doi: 10.1089/neu.2006.23.635 CrossRefGoogle Scholar
  4. Borba Filho GL, Zenki KC, Kalinine E, Baggio S, Pettenuzzo L, Zimmer ER, Weis SN, Calcagnotto ME, Onofre de Souza D (2015) A new device for step-down inhibitory avoidance task—effects of low and high frequency in a novel device for passive inhibitory avoidance task that avoids bioimpedance variations. PLoS One 10(2):e0116000. doi: 10.1371/journal.pone.0116000.eCollection 2015 CrossRefGoogle Scholar
  5. Brandão ML, Anseloni VZ, Pandóssio JE, De Araújo JE, Castilho VM (1999) Neurochemical mechanisms of the defensive behavior in the dorsal midbrain. Neurosci Biobehav Rev 23:863–875. doi: 10.1016/S0149-7634(99)00038-X CrossRefGoogle Scholar
  6. Buck L, Axel R (1991) A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65:175–187. doi: 10.1016/0092-8674(91)90418-X CrossRefGoogle Scholar
  7. Caito S, Aschner M (2015) Neurotoxicity of metals. Handb Clin Neurol 131:169–189. doi: 10.1016/B978-0-444-62627-1.00011-1 CrossRefGoogle Scholar
  8. Campos KFC, Amaral VCS, Rico JL, Miguel TT, Nunes-de-Souza RL (2013) Ethopharmacological evaluation of the rat exposure test: a prey-predator interaction test. Behav Brain Res 240:160–170. doi: 10.1016/j.bbr.2012.11.023 CrossRefGoogle Scholar
  9. Cocheo V (1990) Environmental impact of tanning industry. Med Lav 81:230–241Google Scholar
  10. Crisanto KO, Andrade WMG, Silva KDA, Lima RH, Costa MSMO, Cavalcante JS, Lima RRM, Nascimento ES Jr, Cavalcante JC (2015) The differential mice response to cat and snake odor. Physiol Beh 152:272–279. doi: 10.1016/j.physbeh.2015.10.013 CrossRefGoogle Scholar
  11. Gray A, McNaughton N (2000) Fundamentals of the septo-hippocampal system. In: Gray JA, McNaughton N (eds) The neuropsychology of anxiety: an enquiry into the functions of septo-hippocampal system, 2nd edn. Oxford University Press, Oxford, pp 204–232Google Scholar
  12. Gross CT, Canteras NS (2012) The many paths to fear. Nat Rev Neurosci 13:651–658. doi: 10.1038/nrn3301 CrossRefGoogle Scholar
  13. Guimarães AT, de Oliveira FR, de Souza JM, da Silva WA, da Silva AR, Rodrigues ASL, de Melo e Silva D, Costa RM, da Silva Castro AL, Malafaia G (2016) Anxiety and memory deficits induced by tannery effluent in C57BL/6J female mice. Environ Sci Pollut Res Int 23:25323–25334. doi: 10.1007/s11356-016-7746-2 CrossRefGoogle Scholar
  14. Heydel JM, Coelho A, Thiebaud N, Legendre A, Le Bon AM, Faure P, Neiers F, Artur Y, Golebiowski J, Briand L (2013) Odorant-binding proteins and xenobiotic metabolizing enzymes: implications in olfactory perireceptor events. Anat Rec 296:1333–1345. doi: 10.1002/ar.22735 CrossRefGoogle Scholar
  15. Holahan MR, Smith CA (2015) Phthalates and neurotoxic effects on hippocampal network plasticity. Neurotoxicology 48:21–34. doi: 10.1016/j.neuro.2015.02.008 CrossRefGoogle Scholar
  16. Hu J, Xiao Z, Zhou R, Deng W, Xang M, Ma S (2011) Ecological utilization of leather tannery waste with circular economy model. J Clean Prod 19:221–228. doi: 10.1016/j.jclepro.2010.09.018 CrossRefGoogle Scholar
  17. Mendes BO, Guimarães ATB, Castro ACF, Silva BC, Barbosa CC, Barbosa JJ, Souza JM, Rabelo LM, Souza MR, Moreira MG, Mazzei ND, Santos JÁ, Ferreira RO, Silva WAM, Malafaia G (2016) Dermal exposure to tannery effluent did not alter predictive behavior for depression in male Swiss mice. JSM Axiety Depress 1:1011Google Scholar
  18. Miyake M, Ito Y, Sawada M, Sakai K, Suzuki H, Sakamoto T, Sawamoto K, Kamijima M (2016) Subchronic inhalation exposure to 2-ethyl-1-hexanol impairs the mouse olfactory bulb via injury and subsequent repair of the nasal olfactory epithelium. Arch Toxicol 90:1949–1958. doi: 10.1007/s00204-016-1699-6 CrossRefGoogle Scholar
  19. Moysés FS (2014) Efeito da exposição ao efluente de curtume em diferentes modelos animais. Tese de Doutorado. Universidade Federal do Rio Grande do Sul, Instituto de Ciências Básicas da SaúdeGoogle Scholar
  20. Moysés FS, Bertoldi K, Spindler C, Sanches EF, Elsner VR, Rodrigues MA, Siqueira IR (2014) Exposition to tannery wastewater did not alter behavioral and biochemical parameters in Wistar rats. Physiol Behav 129:160–166. doi: 10.1016/j.physbeh.2014.02.022 CrossRefGoogle Scholar
  21. Oral R, Meriç S, De Nicola E, Petruzzelli D, Della RC, Pagano G (2005) Multi-species toxicity evaluation of a chromium-based leather tannery wastewater. Desalination 211:48–57. doi: 10.1016/j.desal.2006.02.084 CrossRefGoogle Scholar
  22. Panda RC, Rai CL, Sivakumar V, Mandal AB (2012) Odour removal in leather tannery. Adv Chem Eng Sci 2:199–203. doi: 10.4236/aces.2012.22024 CrossRefGoogle Scholar
  23. Rabelo LM, Silva BC, Almeida SF, Silva WAM, Mendes BO, Guimarães ATB, Silva AR, Castro ALS, Rodrigues ASL, Malafaia G (2016) Memory deficit in Swiss mice exposed to tannery effluent. Neurotoxicol Teratol 55:45–49. doi: 10.1016/
  24. Rastogi SK, Pandey A, Tripathi S (2008) Occupational health risks among the workers employed in leather tanneries at Kanpur. Indian J Occup Environ Med 12:132–135. doi: 10.4103/0019-5278.44695 CrossRefGoogle Scholar
  25. Schoenig GP, Osimitz TG, Gabriel KL, Hartnagel R, Gill MW, Goldenthal EI (1999) Evaluation of the chronic toxicity and oncogenicity of N,N-diethyl-m-toluamide (DEET). Toxicol Sci 47:99–109CrossRefGoogle Scholar
  26. Silva WAM, Mendes BO, Guimarães ATB, Rabelo LM, Ferreira RO, Silva BC, Souza JM, Menezes IPP, Rodrigues ASL, Malafaia G (2016) Dermal exposure to tannery effluent causes neurobehavioral changes in C57Bl/6J and Swiss mice. Chemosphere 160:237–243. doi: 10.1016/j.chemosphere.2016.06.083 CrossRefGoogle Scholar
  27. Siqueira IR, Vanzella C, Bianchetti P, Rodrigues MAS, Stülp S (2011) Anxiety-like behaviour in mice exposed to tannery wastewater: the effect of photoelectrooxidation treatment. Neurotoxicol Teratol 33:481–484. doi: 10.1016/ CrossRefGoogle Scholar
  28. Soto AM, Calabro JM, Precht NV, Yau AU, Orlando EF, Daxenberger A, Kolok AS, Guillette JL, Bizec BL, Lange IG, Sonnenschein C (2004) Androgenic and estrogenic activity in water bodies receiving cattle feedlot effluent in Eastern Nebraska, USA. Environ Health Perspect 112:346–352CrossRefGoogle Scholar
  29. Souza JM, Guimarães ATB, Silva WAM, Pereira CCO, Menezes IPP, Malafaia G (2016a) Tannery effluent effects on vertebrates: lessons from experimental animals. Int J Curr Res 8:39902–39914Google Scholar
  30. Souza JM, da Silva WA, de Oliveira MB, Guimarães AT, de Lima Rodrigues AS, Montalvão MF, da Costa ED, da Silva AR, Malafaia G (2016b) Inbred mice strain shows neurobehavioral changes when exposed to tannery effluent. Environ Sci Pollut Res Int. doi: 10.1007/s11356-016-7949-6
  31. Steinbrecht RA (1998) Odorant-binding proteins: expression and function. Ann N Y Acad Sci 855:323–332. doi: 10.1111/j.1749-6632.1998.tb10591.x CrossRefGoogle Scholar
  32. Suderman FW (2001) Nasal toxicity, carcinogenicity, and olfactory uptake of metals. Ann Clin Lab Sci 31:3–24Google Scholar
  33. Tagliari KC, Cecchini R, Rocha JAV, Vargas VMF (2004) Mutagenicity of sediment and biomarkers of oxidative stress in fish from aquatic environments under the influence of tanneries. Mutat Res 561:101–117. doi: 10.1016/j.mrgentox.2004.04.001 CrossRefGoogle Scholar
  34. Taju G, Majeed S, Nambi K, Sarath BV, Vimal S (2012) Comparison of in vitro and in vivo acute toxicity assays in Etroplus suratensis (Bloch, 1790) and its three cell lines in relation to tannery effluent. Chemosphere 87:55–61. doi: 10.1016/j.chemosphere.2011.11.056 CrossRefGoogle Scholar
  35. Takeuchi H, Sakano H (2014) Neural map formation in the mouse olfactory system. Cell Mol Life Sci 71:3049–3057. doi: 10.1007/s00018-014-1597-0 CrossRefGoogle Scholar
  36. Thiebaud N, Veloso Da Silva S, Jakob I, Sicard G, Chevalier J, Ménétrier F, Berdeaux O, Artur Y, Heydel JM, Le Bon AM (2013) Odorant metabolism catalyzed by olfactory mucosal enzymes influences peripheral olfactory responses in rats. PLoS One 8:e59547. doi: 10.1371/journal.pone.0059547 CrossRefGoogle Scholar
  37. Tigini V, Giansanti P, Mangiavillano A, Pannocchia A, Varese G (2011) Evaluation of toxicity, genotoxicity and environmental risk of simulated textile and tannery wastewaters with a battery of biotests. Ecotoxicol Environ Saf 74:866–873. doi: 10.1016/j.ecoenv.2010.12.001 CrossRefGoogle Scholar
  38. Wang L, Chen IZ, Lin D (2015) Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85:1344–1358. doi: 10.1016/j.neuron.2014.12.025 CrossRefGoogle Scholar
  39. Yang M, Crawley JN (2009) Simple behavioral assessment of mouse olfaction. Curr Protoc Neurosci Chapter 8:Unit 8.24. doi:10.1002/0471142301.ns0824s48Google Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Bruna de Oliveira Mendes
    • 1
  • Letícia Martins Rabelo
    • 1
  • Bianca Costa e Silva
    • 1
  • Joyce Moreira de Souza
    • 1
  • André Luis da Silva Castro
    • 2
  • Anderson Rodrigo da Silva
    • 3
  • Aline Sueli de Lima Rodrigues
    • 2
  • Guilherme Malafaia
    • 1
    • 2
    • 4
    Email author
  1. 1.Laboratório de Pesquisas BiológicasInstituto Federal Goiano–Campus UrutaíUrutaíBrazil
  2. 2.Departamento de Ciências Biológicas, Programa de Pós-Graduação em Conservação de Recursos Naturais do CerradoInstituto Federal Goiano–Campus UrutaíUrutaíBrazil
  3. 3.Laboratório de Estatística ExperimentalInstituto Federal Goiano–Câmpus UrutaíUrutaíBrazil
  4. 4.Programa de Pós-Graduação em Biodiversidade AnimalUniversidade Federal de Goiás–Campus SamambaiaGoiâniaBrazil

Personalised recommendations