Skip to main content
SpringerLink
Log in

Low, Chronic Exposure to Endosulfan Induces Bioaccumulation and Decreased Carcass Total Fatty Acids in Neotropical Fruit Bats

  • Published:
Bulletin of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

We investigated the effects of the insecticide endosulfan on energy metabolism and its possible accumulation in fruit bats. Adult male bats (Artibeus lituratus) were exposed for 35 days, when they were offered fruit treated with endosulfan (E) and adhesive spreader (AS) in the following concentrations (g/L): 0.0; 0.0 (Control), 0.0; 0.015 (AS), 1.05; 0.015 (E1), 2.1; 0.015 (E2). Concentrations used were those recommended by the manufacturer for fruit crop application (E1) or twice this value (E2). E1 bats showed decreased plasma glucose concentration. Carcass fatty acids were decreased in E1 and E2 bats. Endosulfan bioaccumulation was observed in both liver and adipose tissues from E1 and E2 bats. These results indicate that the chronic exposure of fruit bats to environmentally relevant concentrations of endosulfan can lead to significant bioaccumulation beyond control and also decreased fatty acid content, which may impair the health of this important seed disperser in neotropical forests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Agbohessi TP, Toko II, N’tcha I, Geay F, Mandiki SNM, Kestemont P (2014) Exposure to agricultural pesticides impairs growth, feed utilization and energy budget in African Catfish Clarias gariepinus (Burchell, 1822) fingerlings. Int Aquat Res 6:229–243

  • Allinson G, Mispagel C, Kajiwara N, Anan Y, Hashimoto J, Laurenson L, Allinson M, Tanabe S (2006) Organochlorine and trace metal residues in adult southern bent-wing bat (Miniopterus schreibersii bassanii) in southeastern Australia. Chemosphere 64:1464–1471

    Article  CAS  Google Scholar 

  • Amaral TS, Carvalho TF, Barros MS, Picanço MC, Neves CA, Freitas MB (2012a) Short-term effects of spinosyn’s family insecticide on energy metabolism and liver morphology in frugivoros bats Artibeus lituratus (Olfers. 1818). Braz J of Biol 72(2):299–304

  • Amaral TS, Carvalho TF, Silva MC, Goulart LS, Barros MS, Picanço MC, Neves CA, Freitas MB (2012b) Metabolic and histopathological alterations in the fruit-eating bat Artibeus lituratus induced by the organophosphorous pesticide fenthion. Acta Chiropterol 14(1):225–232

  • Bayata S, Geiser F, Kristiansen P, Wilson SC (2014) Organic contaminants in bats: trends and new issues. Environ Int 63:40–52

    Article  Google Scholar 

  • Bennett BS, Thies ML (2007) Organochlorine pesticide residues in guano of Brazilian freetailed bats, Tadarida brasiliensis Saint-Hilaire, from east Texas. Bull Environ Contam Toxicol 78:191–194

    Article  CAS  Google Scholar 

  • Canlet C, Tremblay-Franco M, Gautier R, Molina J, Métais B, Blas-Y Estrada F, Gamet-Payrastre L (2013) Specific metabolic fingerprint of a dietary exposure to a very low dose of endosulfan. J Toxicol 2013:545802

    Article  Google Scholar 

  • Carneiro FF, Rigotto RM, Augusto LGDS, Friedrich K, Burigo AC (2015) Dossiê ABRASCO: um alerta sobre os impactos dos agrotóxicos na saúde.

  • Clark Jr. DR (2001) DDT and the decline of free-tailed bats (Tadarida brasiliensis) at Carlsbad Cavern, New Mexico. Arch Environ Contam Toxicol 40:537–543

    Article  CAS  Google Scholar 

  • Coats JR (1990) Mechanisms of toxic action and structure–activity relationships for organochlorine and synthetic pyrethroid insecticides. Environ Health Perspect 87:255–262

    Article  CAS  Google Scholar 

  • Dennis GC, Gartrell BD (2015) Nontarget mortality of New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone. J Wildl Dis 51:177–186

    Article  Google Scholar 

  • Folch J, Less M, Slorne SGHA (1957) A simple method for the isolation and purification of total lipids from animal tissue. J Biol Chem 226:226–497

    Google Scholar 

  • Freitas MB, Welker AF, Pinheiro EC (2006) Seasonal variation and food deprivation in common vampire bats (Chiroptera: Phyllostomidae). Braz J Biol 66:1051–1055

    CAS  Google Scholar 

  • Gerell R, Lundeberg KG (1993) Decline of a bat Pipistrellus pipistrellus population in an industrialized area in south Sweden. Biol Conserv 65:153–157

    Article  Google Scholar 

  • Gorchov DL, Cornejo F, Ascorra C, Jaramillo M (1993) The role of seed dispersal in the natural regeneration of rain forest after strip-cutting in the Peruvian Amazon. In: Fleming TH and Estrada A (eds). Frugivory and seeddispersal: ecological and evolutionary aspects. W. Kluwer Academic Publishers, Dordrecht, pp 339–349

    Chapter  Google Scholar 

  • Howell GE, Meek E, Kilic J, Mohns M, Mulligan C, Chambers JE (2014) Exposure to p, p’-dichlorodiphenyldichloroethylene (DDE) induces fasting hyperglycemia without insulin resistance in male C57BL/6 H mice. Toxicology 5:6–14

    Article  Google Scholar 

  • Kalender S, Kalender Y, Ogutcu A, Uzunhisarcikli M, Durak D, Açikgoz F (2004) Endosulfan-induced cardiotoxicity and free radical metabolism in rats: the protective effect of vitamin E. Toxicology 202:227–235

    Article  CAS  Google Scholar 

  • Kannan K, Yun SH, Rudd RJ, Behr M (2010) High concentrations of persistent organic pollutants including PCBs, DDT, PBDEs and PFOS in little brown bats with white-nose syndrome in New York. USA. Chemosphere 80:613–618

    Article  CAS  Google Scholar 

  • Karami-Mohajeri S, Abdollahi M (2010) Toxic influence of organophosphate. carbamate. and organochlorine pesticides on cellular metabolism of lipids, proteins, and carbohydrates: a systematic review. Hum Exp Toxicol 30:1119–1140

    Article  Google Scholar 

  • Kuvarega AT, Taru P (2007) Accumulation of endosulfan in wild rat, Rattus norvegious as a result of application to soya bean in Mazoe (Zimbabwe). Environ Monit Assess 124:333–345

    Article  Google Scholar 

  • Lilley TM, Ruokolainen L, Meierjohann A, Kanerva M, Stauffe J, Laine VN, Atosuo J, Lilius EM, NIkinmaa (2013) Resistance to oxidative damage but not immunosuppression by organic tin compounds in natural populations of Daubenton’s bats (Myotis daubentonii). Comp Biochem Phys C 3:298–305

    Google Scholar 

  • Mazzetti MB, Taira MC, Lelli SM, Dascal E, Basabe JC, de Viale LC (2004) H exachlorobenzene impairs glucose metabolism in a rat modelo f porphyria cutanea tarda: a mechanistic approach. Arch Toxicol 78:25–33

    Article  CAS  Google Scholar 

  • Moore BJ, Olsen JL, Marks F, Brasel JA (1984) The effects of high fat feeding during one cycle of reproduction consisting of pregnancy, lactation and recovery on body composition and fat pad cellularity in the rat. J Nutr 114:1566–1573

    CAS  Google Scholar 

  • Naidoo S, Vosloo D, Schoeman MC (2015) Haematological and genotoxic responses in an urban adapter, the banana bat, foraging at wastewater treatment works. Ecotoxicol Environ Safe 114: 304–311

    Article  CAS  Google Scholar 

  • O’shea TJ, Everette AL, Ellison LE (2001) Cyclodiene insecticide DDE, DDT, Arsenic, and mercury contamination of big brown bats (Eptesicus fuscus) foraging at a Colorado Superfund site. Arch Environ Contam Toxicol 40:112–120

    Article  Google Scholar 

  • Oliveira JM (2013) Exposição Crônica a Baixas Concentrações do Inseticida Endosulfan Altera a Capacidade Antioxidante de Morcegos Frugívoros (Artibeus lituratus, OLFERS, 1818). Dissertation, Federal University of Viçosa.

  • Paulino MG, Benze TP, Sadauskas-Henrique H, Sakuragui MM, Fernandes JB, Fernandes MN (2014) The impact of organochlorines and metals on wild fish living in a tropical hydroelectric reservoir: bioaccumulation and histopathological biomarkers. Sci Total Environ 497–498:293–306

    Article  Google Scholar 

  • Rezg R, Mornagui B, El-Fazaa S, Gharbi N (2007) Biochemical evaluation of hepatic damage in subchronic exposure to malathion in rats: effect on superoxide dismutase and catalase activities using native PAGE. C R Biol 331:655–662

    Article  Google Scholar 

  • Saiyed H, Dewan A, Bhatnagar V, Shenoy U, Shenoy R, Rajmohan H, Patel K, Kashyap R, Kushyap R, Kulkarni P, Rajan B, Lakkad B (2003) Effect of Endosulfan on male reproductive development. Environ Health Perspect 111:1958–1962

    Article  CAS  Google Scholar 

  • Singh SK, Pandey RS (1990) Effect of sub-chronic endosulfan exposures on plasma gonadotrophins, testosterone, testicular testosterone and enzymes of androgen biosynthesis in rat. Indian J Exp Biol 10:953–956

    Google Scholar 

  • Sjörgren B, Noerdenskjöld T, Holmgeen H, Mollerstrom J (1938) Beitrag zur Kenntnis der Leberrhythmik (glycogen, Phosphor und Calcium in der Kaninchenleber). Pflugers Arch EJP 240:427–448

    Article  Google Scholar 

  • Stechert C, Kolb M, Bahadir M, Djossa BA, Fahr B (2014) Insecticide residues in bats along a land use-gradient dominated by cotton cultivation in northern Benin, West Africa. Environ Sci Pollut Res 21:8812–8821

    Article  CAS  Google Scholar 

  • Swanepoel RE, Racey PA, Shore RF, Speakman JR (1999) Energetic effects of sublethal exposure to lindane on pipistrelle bats (Pipistrellus pipistrellus). Environ Pollut 104:169–177

    Article  CAS  Google Scholar 

  • Thangavel P, Sumathiral K, Maheswari S, Rita S, Ramaswamy M (2010) Hormone profile of an edible, freshwater teleost, Sarotherodon mossambicus (Peters) under endosulfan toxicity. Pestic Biochem Physiol 97:229–234

    Article  CAS  Google Scholar 

  • Tomlin CDS (ed) (2006) A world compendium: the pesticide manual, 14th edn. BCPC, Hampshire

    Google Scholar 

  • Van Dyk JS, Pletschke B (2011) Review on the use of enzymes for the detection of organochlorine, organophosphate and carbamate pesticides in the environment. Chemosphere 82:291–307

  • Vizzotto LD, Taddei VA (1973) Chave para determinação de quirópteros brasileiros. Universidade Estadual Paulista, São José do Rio Preto.

    Google Scholar 

Download references

Acknowledgments

We thank the National Counsel of Technological and Scientific Development (CNPq, Brazil) for supporting this research.

Author information

Authors and Affiliations

  1. Federal University of Viçosa, Vicosa, Brazil

    Alessandro Brinati, Jerusa Maria Oliveira, Viviane Silva Oliveira, Mirlaine Soares Barros, Bruno Marques Carvalho, Luciane Silva Oliveira, Maria Eliana Lopes Queiroz, Sérgio Luiz Pinto Matta & Mariella Bontempo Freitas

Authors
  1. Alessandro Brinati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jerusa Maria Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Viviane Silva Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mirlaine Soares Barros
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruno Marques Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Luciane Silva Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maria Eliana Lopes Queiroz
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sérgio Luiz Pinto Matta
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Mariella Bontempo Freitas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jerusa Maria Oliveira.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 711 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brinati, A., Oliveira, J.M., Oliveira, V.S. et al. Low, Chronic Exposure to Endosulfan Induces Bioaccumulation and Decreased Carcass Total Fatty Acids in Neotropical Fruit Bats. Bull Environ Contam Toxicol 97, 626–631 (2016). https://doi.org/10.1007/s00128-016-1910-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00128-016-1910-8

Keywords

Search

Navigation