Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 31, pp 31762–31770 | Cite as

Mice exposure to haloxyfop-p-methyl ester at predicted environmentally relevant concentrations leads to anti-predatory response deficit

  • Bruna de Oliveira Mendes
  • Carlos Mesak
  • José Eduardo Dias CalixtoJr
  • Guilherme Malafaia
Short Research and Discussion Article

Abstract

Although the efficiency of haloxyfop-p-methyl ester (HPME) as selective herbicide is acknowledged, its impact on non-target organisms is poorly known. It is not known whether the short exposure of mammals to low HPME concentrations (consistent with a realistic contamination scenario) poses risks to these animals. Thus, the aim of the current study is to evaluate the effects of HPME on the anti-predatory behavior of female Swiss mice exposed to it. The animals were divided in groups: non-exposed (control) and exposed (route: i.p., for 2 days) to different herbicide concentrations (2.7 × 10−4 g/kg and 2.7 × 10−2 g/kg of body weight), which were considered environmentally relevant predicted concentrations. The animals were subjected to the open field and elevated plus-maze tests; results showed that the HPME did not lead to anxiolytic or anxiety behavior, or to locomotive changes in the tested animals, fact that was confirmed through the Basso Mouse Scale for locomotion scores. On the other hand, animals exposed to the herbicide were incapable of recognizing the snake as potential predator. Animals in the control group, exposed to a real snake (Pantherophis guttatus) remained longer in the safety zone of the test device, presented lower frequency of self-grooming behaviors for a shorter period-of-time, besides showing longer freezing time, which was not observed in animals exposed to HPME. Therefore, our study indicates the ecotoxicological potential of the herbicide, since anti-predatory behavior disorders may affect preys’ responses and population dynamics.

Keywords

Pesticides Mammals Environmental toxicology Behavioral biology 

Notes

Acknowledgments

The authors are grateful to the Brazilian National Council for Research (CNPq) (Brazilian research agency) (Proc. No 467801/2014-2) and to Instituto Federal Goiano for the financial support (Proc. No 23219000096/2018-93). Moreover, the authors are grateful to CAPES and FAPEG for granting the scholarship to the student who developed the current study.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All the herein adopted procedures were approved by the Ethics Committee on Animal Use of Goiano Federal Institute (Comissão de Ética no Uso de Animais do Instituto Federal Goiano), GO, Brazil (Protocol no. 6339041117). Meticulous efforts were made to assure that the animals suffered the least possible and to reduce external stress, pain, and discomfort sources. The current study did not exceed the number of animals necessary to produce trustworthy scientific data. The present article does not contain studies with human participants performed by any of the authors.

References

  1. Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaiee A (2004) Pesticides and oxidative stress: a review. Med Sci Monit 10:144–147Google Scholar
  2. Banaś A, Johansson I, Stenlid G, Stymne S (1993) Investigation of the mode of action of the herbicide haloxyfop. Zesz Nauk Wyższ Szk Roln P Siedlce Ser Nauki Przyrodnicze 34:1–19Google 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 23:635–659CrossRefGoogle Scholar
  4. Blanchard DC, Li CI, Hubbard D, Markham CM, Yang M, Takahashi LK, Blanchard RJ (2003) Dorsal premammillary nucleus differentially modulates defensive behaviors induced by different threat stimuli in rats. Neurosci Lett 345(3):145–148CrossRefGoogle Scholar
  5. Cardoso LS, Estrela FN, Chagas TQ, da Silva WAM, Costa DRO, Pereira I, Vaz BG, Rodrigues ASL, Malafaia G (2018) The exposure to water with cigarette residue changes the anti-predator response in female Swiss albino mice. Environ Sci Pollut Res 25(9):8592–8607CrossRefGoogle Scholar
  6. Carpender SE, Caraco NF, Correll DL, Howarth RW, Sharpley AN, Smith VH (1998) Nonpoint pollution of surface waters with phosphorus and nitrogen. Ecol Appl 8(3):559–568CrossRefGoogle Scholar
  7. Crist E, Mora C, Engelman R (2017) The interaction of human population, food production, and biodiversity protection. Science 356(6335):260–264CrossRefGoogle Scholar
  8. Estrela DC, da Silva WA, Guimarães AT, de Oliveira Mendes B, da Silva Castro AL, da Silva Torres IL, Malafaia G (2015) Predictive behaviors for anxiety and depression in female Wistar rats subjected to cafeteria diet and stress. Physiol Behav 151:252–263CrossRefGoogle Scholar
  9. European Food Safety Authority (2014) Reasoned opinion on the review of the existing maximum residue levels (MRLs) for haloxyfop-P. EFSA J 12:3861–3921CrossRefGoogle Scholar
  10. Fernández-Teruel A, Estanislau C (2016) Meanings of self-grooming depend on an inverted U-shaped function with aversiveness. Nat Rev Neurosci 17:591CrossRefGoogle Scholar
  11. Frings H, Frings M, Kivert A. Behavior patterns of the laboratory mouse under auditory stress. J. Mammal., 32 (1951), pp. 60–76CrossRefGoogle Scholar
  12. Glinka ME, Samuels BA, Diodato A, Teillon J, Feng Mei D, Shykind BM, Hen R, Fleischmann A (2012) Olfactory deficits cause anxiety-like behaviors in mice. J Neurosci 32(19):6718–6725CrossRefGoogle Scholar
  13. Hansen NC, Gupta SC, Moncrief JF (2000) Herbicide banding and tillage effects on runoff, sediment, and phosphorus losses. J Environ Qual 29:1555–1560CrossRefGoogle Scholar
  14. Janssens L, Stoks R (2003) Predation risk causes oxidative damage in prey. Biol Lett 9(4):20130350CrossRefGoogle Scholar
  15. Janssens L, Stoks R (2014) Chronic predation risk reduces escape speed by increasing oxidative damage: a deadly cost of an adaptive antipredator response. PLoS One 9(6):e101273CrossRefGoogle Scholar
  16. Kalueff AV, Tuohimaa P (2005) Mouse grooming microstructure is a reliable anxiety marker bidirectionally sensitive to GABAergic drugs. Eur J Pharmacol 508:147–153CrossRefGoogle Scholar
  17. Kalueff AV, Stewart AM, Song C, Berridge KC, Graybiel AM, Fentress JC (2016) Neurobiology of rodent self-grooming and its value for translational neuroscience. Nat Rev Neurosci 17(1):45–59CrossRefGoogle Scholar
  18. Kavaliers M, Choleris E (2001) Antipredator responses and defensive behavior: ecological and ethological approaches for the neurosciences. Neurosci Biobehav Rev 5(7–8):577–586CrossRefGoogle Scholar
  19. Korte SM (2001) Corticosteroids in relation to fear, anxiety and psychopathology. Neurosci Biobehav Rev. 25(2):117–42CrossRefGoogle Scholar
  20. Kunwar P, Zelikowky M, Remedios R, Cai H, Yilmaz M, Meister M, Anderson DJ (2015) Ventromedial hypothalamic neurons control a defensive emotion state. eLife 4:e06633CrossRefGoogle Scholar
  21. Martinez RCR, Carvalho-Netto EF, Amaral VCS, Nunes-de-Souza RL, Canteras NS (2008) Investigation of the hypothalamic defensive system in the mouse. Behav Brain Res 192:185–190CrossRefGoogle Scholar
  22. Mendes BO, Rabelo LM, E Silva BC, de Souza JM, da Silva Castro AL, da Silva AR, de Lima Rodrigues AS, Malafaia G (2017) Mice exposure to tannery effluents changes their olfactory capacity, and their response to predators and to the inhibitory avoidance test. Environ Sci Pollut Res 24(23):19234–19248CrossRefGoogle Scholar
  23. Olayinka ET, Ore A (2015) Hepatotoxicity, nephrotoxicity and oxidative stress in rat testis following exposure to haloxyfop-p-methyl ester, an aryloxyphenoxypropionate herbicide. Toxics 3(4):373–389CrossRefGoogle Scholar
  24. Ore A, Olayinka ET (2017) Fluazifop- p-butyl, an aryloxyphenoxypropionate herbicide, diminishes renal and hepatic functions and triggers testicular oxidative stress in orally exposed rats. Toxicol Ind Health 33(5):406–415.  https://doi.org/10.1177/0748233716657763 CrossRefGoogle Scholar
  25. Pereira FCM, Alves PLCA (2015) Herbicides for weed control in eucalypt. Revista Brasileira de Herbicidas 14(4):333–347CrossRefGoogle Scholar
  26. Quintão TC, Rabelo LM, Alvarez TGS, Guimarães AT, Rodrigues ASL, Cardoso LS, Ferreira RO, Malafaia G (2018) Precopulatory sexual behavior of male mice is changed by the exposure to tannery effluent. Chemosphere 195:312–324CrossRefGoogle Scholar
  27. Ramankutty N, Mehrabi Z, Waha K, Jarvis L, Kremen C, Herrero M, Rieseberg LH (2018) Trends in global agricultural land use: implications for environmental health and food security. Ann Rev Plant Biol.  https://doi.org/10.1146/annurev-arplant-042817-040256 CrossRefGoogle Scholar
  28. Ramos A (2008) Animal models of anxiety: do I need multiple tests? Trends Pharmacol Sci 39(10):493–498CrossRefGoogle Scholar
  29. Souza JM, Rabelo LM, de Faria DBG, Guimarães ATB, da Silva WAM, Rocha TL, Estrela FN, Chagas TQ, de Oliveira Mendes B, Malafaia G (2018) The intake of water containing a mix of pollutants at environmentally relevant concentrations leads to defensive response deficit in male C57Bl/6J mice. Sci Total Environ 628-629:186–197CrossRefGoogle Scholar
  30. Takahashi LK (2014) Olfactory systems and neural circuits that modulate predator odor fear. Front Behav Neurosci 11(8):72Google Scholar
  31. Tiffany PB, Mollenauer S, Plotnik R, White M (1979) Olfactory bulbectomy: emotional behavior and defense responses in the rat. Physiol Behav 47(1):311–317CrossRefGoogle Scholar
  32. Wang L, Chen IZ, Lin D (2015) Collateral pathways from the ventromedial hypothalamus mediate defensive behaviors. Neuron 85:1344–1358CrossRefGoogle Scholar
  33. Zahid HJ, Robinson E, Kelly RL (2016) Agriculture, population growth, and statistical analysis of the radiocarbon record. Proc Natl Acad Sci 113(4):931–935CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Bruna de Oliveira Mendes
    • 1
  • Carlos Mesak
    • 1
  • José Eduardo Dias CalixtoJr
    • 2
  • Guilherme Malafaia
    • 1
    • 3
  1. 1.Post-Graduation Program in Conservation of Cerrado Natural Resources – Biological Research LaboratoryInstituto Federal Goiano –Campus UrutaíUrutaíBrazil
  2. 2.Post-Graduation Program in Forest SciencesUniversidade de BrasíliaBrasíliaBrazil
  3. 3.Laboratório de Pesquisas BiológicasInstituto Federal Goiano –Campus UrutaíUrutaíBrazil

Personalised recommendations