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How do pesticides affect bats? – A brief review of recent publications

Como os pesticidas afetam os morcegos? - Uma breve revisão de publicações recentes

Abstract

Increased agricultural production has been increased use of pesticides worldwide, which poses a threat to both human and environmental health. Recent studies suggest that several non-target organisms, from bees to mammals, show a wide variety of toxic effects of pesticides exposure, including impaired behavior, development and reproduction. Among mammals, bats are usually a neglected taxon among ecotoxicological studies, although they play important ecological and economical roles in forest ecosystems and agriculture through to seed dispersal and insect population control. Considering their wide variety of food habits, bats are exposed to environmental pollutants through food or water contamination, or through direct skin contact in their roosting areas. In order to better understand the risk posed by pesticides to bats populations, we compiled studies that investigated the main toxicological effects of pesticides in bats, aiming at contributing to discussion about the environmental risks associated with the use of pesticides.

Keywords:
bioaccumulation; Chiroptera; ecotoxicology; eating habits; physiological changes

Resumo

O aumento da produção agrícola tem levado ao aumento do uso de pesticidas em todo o mundo, o que representa uma ameaça para a saúde humana e ambiental. Estudos recentes sugerem que vários organismos não-alvo, de abelhas a mamíferos, apresentam uma grande variedade de efeitos tóxicos após a exposição aos pesticidas a pesticidas, incluindo alterações de comportamento, no desenvolvimento e na reprodução. Entre os mamíferos, os morcegos geralmente são negligenciados entre os estudos ecotoxicológicos, embora desempenhem importantes papéis ecológicos e econômicos nos ecossistemas florestais e na agricultura por meio do controle de dispersão de sementes e de populações de insetos. Considerando sua ampla variedade de hábitos alimentares, eles estão expostos a poluentes ambientais através da contaminação de alimentos ou água, ou através do contato direto com a pele em suas áreas de descanso. Para entender melhor o risco que os agrotóxicos representam para as populações de morcegos, compilamos estudos que investigaram os principais efeitos toxicológicos de agrotóxicos em morcegos, visando à discussão sobre os riscos ambientais associados ao uso de agrotóxicos.

Palavras-chave:
bioacúmulo; chiroptera; ecotoxicologia; hábitos alimentares; alterações fisiológicas

1. Introduction

Environmental contamination is one of the main global concerns of the recent years, as an increasing number of studies are associating the exposure to various environmental pollutants with deleterious and often synergistic effects on living organisms (Cedergreen, 2014CEDERGREEN, N., 2014. Quantifying synergy: A systematic review of mixture toxicity studies within environmental toxicology. PLoS One, vol. 9, no. 5, pp. 96580. http://dx.doi.org/10.1371/journal.pone.0096580. PMid:24794244.
http://dx.doi.org/10.1371/journal.pone.0...
). Since the green revolution, there has been an increase in agricultural production accompanied by stagnation or a decline in crop yields. The increased population demand for food culminated with the increased use of pesticides, in order to improve crop productivity (Liu et al., 2015LIU, Y., PAN, X. and LI, J., 2015. A 1961-2010 record of fertilizer use, pesticide application and cereal yields: a review. Agronomy for Sustainable Development, vol. 35, no. 1, pp. 83-93. http://dx.doi.org/10.1007/s13593-014-0259-9.
http://dx.doi.org/10.1007/s13593-014-025...
).

Pesticides are chemical substances that act against any agent that can damage the production, storage, processing of agricultural products, pastures, and vectors. They contribute to agricultural production as they are used to protect crops and livestock from various pests, diseases, weeds, and parasites. Being an alternative to lower economic costs, pesticides help farmers to survive in a competitive market (Choudhary et al., 2018CHOUDHARY, S., YAMINI, RAHEJA, N., YADAV, S.K., KAMBOJ, M., SHARMA, A., 2018. A review: Pesticide residue: Cause of many animal health problems. Journal of Entomology and Zoology Studies, vol. 6, no. 3, pp. 330-333.).

While target organisms absorb a large proportion of the pesticides, a considerable amount is still disseminated in the environment by air and water, and is continuously found in soil, surface water, and groundwater. As several pesticides persist and accumulate in the environment, non-target organisms are continuously exposed through its residues or byproducts effects, including organisms that play key ecological roles in ecosystems (Aktar et al., 2009AKTAR, W., SENGUPTA, D. and CHOWDHURY, A., 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology, vol. 2, no. 1, pp. 1-12. http://dx.doi.org/10.2478/v10102-009-0001-7. PMid:21217838.
http://dx.doi.org/10.2478/v10102-009-000...
).

Bats comprise a wide variety of species inhabiting nearly the entire planet, exhibiting important ecological and economic roles as seed dispersers in natural ecosystems and insect populations control of agricultural pests (Boyles et al., 2011BOYLES, J.G., CRYAN, P.M., MCCRACKEN, G.F. and KUNZ, T.H., 2011. Economic importance of bats in agriculture. Science, vol. 332, no. 6025, pp. 41-42. http://dx.doi.org/10.1126/science.1201366. PMid:21454775.
http://dx.doi.org/10.1126/science.120136...
). However, only a few ecotoxicological studies addressed the effects of pesticides on any aspects of bats behavior, development or reproduction, and although studies are scarce, recent research articles have contributed to advance knowledge in this area. In this review, were compiled studies on the effects of pesticides in bats, aiming at contributing to the discussion about the environmental risks associated with the use of pesticides.

2. Effects of Pesticides in Non-Target Organisms

After the rise of pesticide use, several population declines of non-target organisms were associated with these compounds. Contamination of non-target organisms in the environment occurs through leaching, runoff, evaporation, erosion, and feeding (Köhler and Triebskorn, 2013KÖHLER, H.-R. and TRIEBSKORN, R., 2013. Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science, vol. 341, no. 6147, pp. 759-765. http://dx.doi.org/10.1126/science.1237591. PMid:23950533.
http://dx.doi.org/10.1126/science.123759...
). Volatile chemical components are rapidly transported to the atmosphere and can reach regions far from the application areas (Carvalho, 2017CARVALHO, F.P., 2017. Pesticides, environment, and food safety. Food and Energy Security, vol. 6, no. 2, pp. 48-60. http://dx.doi.org/10.1002/fes3.108.
http://dx.doi.org/10.1002/fes3.108...
). Dichlorodiphenyltrichloroethane (DDT) residues and their metabolites, for example, can be found in the soil, surface water, air and in tissues of wild animals such as fish, mammals, and birds (Köhler and Triebskorn, 2013KÖHLER, H.-R. and TRIEBSKORN, R., 2013. Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science, vol. 341, no. 6147, pp. 759-765. http://dx.doi.org/10.1126/science.1237591. PMid:23950533.
http://dx.doi.org/10.1126/science.123759...
).

Pesticide residues have been associated with delays in the metamorphosis of anurans, bioaccumulation in wild birds and mammals, and reduction in bee and bird populations (Eqani et al., 2013EQANI, S. A. M. A. S., MALIK, R. N., CINCINELLI, A., ZHANG, G., MOHAMMAD, A., QADIR, A., and KATSOYIANNIS, A., 2013. Uptake of organochlorine pesticides (OCPs) and polychlorinated biphenyls (PCBs) by river water fish: The case of River Chenab. Science of the Total Environment, vol. 450-451, pp. 83-91. https://doi.org/10.1016/j.scitotenv.2013.01.052
https://doi.org/10.1016/j.scitotenv.2013...
; Freitas et al., 2017FREITAS, M.B., BROWN, C.T. and KARASOV, W.H., 2017. Warmer temperature modifies effects of polybrominated diphenyl ethers on hormone profiles in leopard frog tadpoles (Lithobates pipiens). Environmental Toxicology and Chemistry, vol. 36, no. 1, pp. 120-127. http://dx.doi.org/10.1002/etc.3506. PMid:27228472.
http://dx.doi.org/10.1002/etc.3506...
; Köhler and Triebskorn, 2013KÖHLER, H.-R. and TRIEBSKORN, R., 2013. Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science, vol. 341, no. 6147, pp. 759-765. http://dx.doi.org/10.1126/science.1237591. PMid:23950533.
http://dx.doi.org/10.1126/science.123759...
; Mullin et al., 2016MULLIN, C.A., FINE, J.D., REYNOLDS, R.D. and FRAZIER, M.T., 2016. Toxicological risks of agrochemical spray adjuvants: Organosilicone surfactants may not be safe. Frontiers in Public Health, vol. 4, pp. 1-8. http://dx.doi.org/10.3389/fpubh.2016.00092. PMid:27242985.
http://dx.doi.org/10.3389/fpubh.2016.000...
). The American Bald Eagle is a classic example of population decline induced by pesticides. The intensive use of DDT in the USA caused eggshell porosity and prevented the development of the offspring, leading to their premature death. This species entered the list of endangered animals and was only seen again 45 years after its use was banned in the country (Aktar et al., 2009AKTAR, W., SENGUPTA, D. and CHOWDHURY, A., 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology, vol. 2, no. 1, pp. 1-12. http://dx.doi.org/10.2478/v10102-009-0001-7. PMid:21217838.
http://dx.doi.org/10.2478/v10102-009-000...
; Banaszkiewicz, 2010BANASZKIEWICZ, T., 2010. Evolution of Pesticide Use. Contemporary Problems of Management and Environmental Protection, vol. 5, pp. 7-18.).

Recently, new molecules have emerged in the marked with the promise of lower toxicity. Currently there are in the worldwide approximately 2400 products commercially available, divided into 434 different active ingredients. These products are classified according to their chemical composition in organochlorines, organophosphates, pyrethroids, carbamates, neonicotinoids, chlorophenoxyacids, triazines and glycines. Within each chemical group are various types of commercial products with different purposes, such as insecticides (for the control of insects), acaricides (acarids), nematicides (nematodes, plant parasites), molluscicides and rodenticides (rodents). In addition, there are two separate chemical groups - the herbicides, whose purpose is controlling weeds, and the fungicides and bactericides, used to prevent fungal and bacterial diseases (Aktar et al., 2009AKTAR, W., SENGUPTA, D. and CHOWDHURY, A., 2009. Impact of pesticides use in agriculture: their benefits and hazards. Interdisciplinary Toxicology, vol. 2, no. 1, pp. 1-12. http://dx.doi.org/10.2478/v10102-009-0001-7. PMid:21217838.
http://dx.doi.org/10.2478/v10102-009-000...
; Banaszkiewicz, 2010BANASZKIEWICZ, T., 2010. Evolution of Pesticide Use. Contemporary Problems of Management and Environmental Protection, vol. 5, pp. 7-18.).

The global use of pesticides has reached large proportions, especially in developing countries (Figure 1) (FAO, 2019FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS – FAO. 2019. Pesticides Use. Rome, Italy: FAOSTAT.). Brazil, for example, has increased the use of pesticides in the last decade (Figure 2), and since 2008 is considered the largest consumer of pesticides in the world, (Albuquerque et al., 2016ALBUQUERQUE, A.F., RIBEIRO, J.S., KUMMROW, F., NOGUEIRA, A.J.A., MONTAGNER, C.C. and UMBUZEIRO, G.A., 2016. Pesticides in Brazilian freshwaters: A critical review. Environmental Science. Processes & Impacts, vol. 18, no. 7, pp. 779-787. http://dx.doi.org/10.1039/C6EM00268D. PMid:27367607.
http://dx.doi.org/10.1039/C6EM00268D...
) with emphasis on the use of herbicides (Figure 2) (FAO, 2019FOOD AND AGRICULTURE ORGANIZATION OF THE UNITED NATIONS – FAO. 2019. Pesticides Use. Rome, Italy: FAOSTAT.). Indiscriminate use and improper application are often observed in the crops, since frequency and recommended doses by manufacturers are not respected (Schiesari et al., 2013SCHIESARI, L., WAICHMAN, A., BROCK, T., ADAMS, C., and GRILLITSCH, B., 2013. Pesticide use and biodiversity conservation in the Amazonian agricultural frontier. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, vol. 368, no. 1619, pp. 1-9. https://doi.org/10.1098/rstb.2012.0378
https://doi.org/10.1098/rstb.2012.0378...
).

Figure 1
Average consumption in ton of active ingredient of fungicides/bactericides, insecticides and herbicides used or sold in the World between 2005 and 2016. Compiled data from FAOSTAT (Food and Agriculture Organization of the United Nations).
Figure 2
Consumption in ton of active ingredient of fungicides/bactericides, insecticides, and herbicides used or sold in the agricultural sector for crops and seeds in Brazil. Compiled data from FAOSTAT.

On top of that, Brazil also does not have programs of adequate monitoring for the use of chemical components and pesticide residues in the environment, especially in freshwater (Barbosa et al., 2015BARBOSA, A.M.C., SOLANO, M. and UMBUZEIRO, G.A., 2015. Pesticides in drinking water - The brazilian monitoring program. Frontiers in Public Health, vol. 3, pp. 246. http://dx.doi.org/10.3389/fpubh.2015.00246. PMid:26581345.
http://dx.doi.org/10.3389/fpubh.2015.002...
). The monitoring is restricted to only five states, which show data with low credibility and high risk of bias (Albuquerque et al., 2016ALBUQUERQUE, A.F., RIBEIRO, J.S., KUMMROW, F., NOGUEIRA, A.J.A., MONTAGNER, C.C. and UMBUZEIRO, G.A., 2016. Pesticides in Brazilian freshwaters: A critical review. Environmental Science. Processes & Impacts, vol. 18, no. 7, pp. 779-787. http://dx.doi.org/10.1039/C6EM00268D. PMid:27367607.
http://dx.doi.org/10.1039/C6EM00268D...
). Another aggravating factor for the country is the use of pesticides that are proven toxic and are already banned in other regions of the world. Among the 50 best-selling commercial products in Brazil, 22 are banned in Europe, such as trichlorfon, 2,4-D, paraquat, and some triazine herbicides.

3. Bats and Pesticides Exposure

In order to assess the state of knowledge about the effects of bat exposure to pesticides, we performed a bibliographic search on the main search platforms (pubmed, scielo, scopus), using the several keywords (bats, toxicology, pesticides, organochlorine, ecotoxicology, insecticide, pyrethroid, fungicide, herbicide). We selected all articles that met the main criteria 1) written in English, 2) published between 1964-2019 and 3) studied the effects of pesticides on bats. Our main goal was to analyze the works published in this area, in each country, and which food guilds have been studied during these years. After compiling these data, we describe the main findings below.

Taken together, the main characteristics found were that, among the studies found (n = 28), most of them were about insectivorous bats (n = 19), followed by studies with fruit bats (n = 7). A few studies analyzed species richness and had no defined species (n = 2). The bat genuses most used in the studies were Pipistrellus (n = 6) and Artibeus (n = 6). The countries that carry out most of the studies are Brazil (n = 7) and the United States of America (n = 7), followed by United Kingdom (n = 3), South Africa (n = 2), Germany (n = 2), Australia (n = 1), France (n = 1), Spain (n = 1), Mexico (n = 1), Sweden (n = 1), Taiwan (n = 1), and Finland (n = 1). Among the main endpoints, the most described analysis were the quantification of pollutants in tissues such as liver and lipids (n = 18), biometric analyzes such as body weight, analysis of energy reserves, bioacoustics, plasma glucose, antioxidant enzymes, food consumption, genotoxicity tests, histology and others (Table 1).

Table 1
Description of papers with studied species, country of study, type of pollutant, and main outcomes.

Bats belong to the order Chiroptera, the second largest order in number of species among mammals. They represent 25% of existing mammal species (Altringham, 1996ALTRINGHAM, J.D. 1996. Bats: biology and behaviour. New York: Oxford University Press.). Occurring in all continents, there are currently approximately 1120 species described (Nowak et al., 1994NOWAK, R.M., WALKER, E.P. and ERNEST, P. 1994. Walker’s bats of the world. Baltimore, MD: Johns Hopkins University Press.).

Chiropterans are of great relevance to the ecosystems balance. Most species have developed morphological adaptations and eating habits that allowed them occupy different niches and a complex relationship of interdependence with the environment. The greatest variety of eating habits is found among microchiropterans, including hematophagous, fruit-eating, insect-eating bats, piscivorous, polinivoros, nectarivorous and omnivorous species (Nowak et al., 1994NOWAK, R.M., WALKER, E.P. and ERNEST, P. 1994. Walker’s bats of the world. Baltimore, MD: Johns Hopkins University Press.). This particular diversity allowed them to offer ecological services essential to ecosystems balance, such as insect control, seed dispersal and pollination.

Recent studies have been suggesting that bats may be at greater risk regarding pesticides exposure than previously expected. Pesticide exposure of bats can occur through food and water contamination or through skin contact in their roosting areas. Residues can bioaccumulate in their tissues and compromise their health. Low breeding rate and seasonal reduction in food availability are among the factors contributing to the vulnerability of bat species regarding exposure to pesticides (Stahlschmidt and Brühl, 2012STAHLSCHMIDT, P. and BRÜHL, C.A., 2012. Bats at risk? Bat activity and insecticide residue analysis of food items in an apple orchard. Environmental Toxicology and Chemistry, vol. 31, no. 7, pp. 1556-1563. http://dx.doi.org/10.1002/etc.1834. PMid:22505289.
http://dx.doi.org/10.1002/etc.1834...
; Stechert et al., 2014STECHERT, C., KOLB, M., BAHADIR, M., DJOSSA, B.A. and FAHR, J., 2014. Insecticide residues in bats along a land use-gradient dominated by cotton cultivation in northern Benin, West Africa. Environmental Science and Pollution Research International, vol. 21, no. 14, pp. 8812-8821. http://dx.doi.org/10.1007/s11356-014-2817-8. PMid:24756668.
http://dx.doi.org/10.1007/s11356-014-281...
). Moreover, we observed that the number of investigations that portray the effects of pesticides on bats still has several gaps and is concentrated in the temperate regions of the globe (Table 1). Central and South America present a great diversity of bat species, and although some countries from these regions consume a high amount of pesticides in the last 10 years (Figure 1), little is known about their effect on Neotropical bats populations.

Insect-eating bats are considered more susceptible to pesticides due to the fact that they are at the top of the food chain. Insect-eating bats help control insect populations, including vectors of diseases such as dengue, leishmaniosis, and malaria, as well as agriculture pests. Declines in insect-eating bats in North America represents a loss of billions of dollars in agricultural cultivation (Boyles et al., 2011BOYLES, J.G., CRYAN, P.M., MCCRACKEN, G.F. and KUNZ, T.H., 2011. Economic importance of bats in agriculture. Science, vol. 332, no. 6025, pp. 41-42. http://dx.doi.org/10.1126/science.1201366. PMid:21454775.
http://dx.doi.org/10.1126/science.120136...
; Cleveland et al., 2006CLEVELAND, C.J., BETKE, M., FEDERICO, P., FRANK, J.D., HALLAM, T.G., HORN, J. and KUNZ, T.H., 2006. Economic value of the pest control service provided by Brazilian free‐tailed bats in south‐central Texas. Frontiers in Ecology and the Environment, vol. 4, no. 5, pp. 238-243. http://dx.doi.org/10.1890/1540-9295(2006)004[0238:EVOTPC]2.0.CO;2.
http://dx.doi.org/10.1890/1540-9295(2006...
; López-Hoffman et al., 2014LÓPEZ-HOFFMAN, L., WIEDERHOLT, R., SANSONE, C., BAGSTAD, K.J., CRYAN, P., DIFFENDORFER, J.E. and SEMMENS, D., 2014. Market forces and technological substitutes cause fluctuations in the value of bat pest-control services for cotton. PLoS One, vol. 9, no. 2, pp. 87912. http://dx.doi.org/10.1371/journal.pone.0087912. PMid:24498400.
http://dx.doi.org/10.1371/journal.pone.0...
). When they feed on preys (insects, arthropods and others) contaminated with pesticides, insect-eating bats end up bioaccumulating residues in their tissues (Gerell and Gerell Lunderg, 1993GERELL, R. and GERELL LUNDERG, K., 1993. Decline of a bat Pipistrellus pipistrellus population in an industrialized area in south Sweden. Biological Conservation, vol. 65, no. 2, pp. 153-157. http://dx.doi.org/10.1016/0006-3207(93)90444-6.
http://dx.doi.org/10.1016/0006-3207(93)9...
; Stahlschmidt and Brühl, 2012STAHLSCHMIDT, P. and BRÜHL, C.A., 2012. Bats at risk? Bat activity and insecticide residue analysis of food items in an apple orchard. Environmental Toxicology and Chemistry, vol. 31, no. 7, pp. 1556-1563. http://dx.doi.org/10.1002/etc.1834. PMid:22505289.
http://dx.doi.org/10.1002/etc.1834...
). Residual concentrations of organochlorines, dieldrin, endosulfan, lindane, pyrethroids, organophosphates and carbamates were recorded in several tissues of insect-eating bats (Clark and Krynitsky, 1983CLARK, D.R. and KRYNITSKY, A.J., 1983. DDE in brown and white fat of hibernating bats. Environmental Pollution, vol. 31, Series A, pp. 287-299.; Eidels et al., 2016EIDELS, R.R., SPARKS, D.W., WHITAKER JUNIOR, J.O. and SPRAGUE, C.A., 2016. Sub-lethal Effects of Chlorpyrifos on Big Brown Bats (Eptesicus fuscus). Archives of Environmental Contamination and Toxicology, vol. 71, no. 3, pp. 322-335. http://dx.doi.org/10.1007/s00244-016-0307-3. PMid:27491870.
http://dx.doi.org/10.1007/s00244-016-030...
; Fernández et al., 1993FERNÁNDEZ, M.A., HERNÁNDEZ, L.M., IBÁNÑEZ, C., GONZÁLEZ, M.J., GUILLÉN, A. and PÉREZ, J.L., 1993. Congeners of PCBs in three bat species from Spain. Chemosphere, vol. 26, no. 6, pp. 1085-1097. http://dx.doi.org/10.1016/0045-6535(93)90197-D.
http://dx.doi.org/10.1016/0045-6535(93)9...
; Gerell and Gerell Lunderg, 1993GERELL, R. and GERELL LUNDERG, K., 1993. Decline of a bat Pipistrellus pipistrellus population in an industrialized area in south Sweden. Biological Conservation, vol. 65, no. 2, pp. 153-157. http://dx.doi.org/10.1016/0006-3207(93)90444-6.
http://dx.doi.org/10.1016/0006-3207(93)9...
; Kannan et al., 2010KANNAN, K., YUN, S.H., RUDD, R.J. and 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, vol. 80, no. 6, pp. 613-618. http://dx.doi.org/10.1016/j.chemosphere.2010.04.060. PMid:20493513.
http://dx.doi.org/10.1016/j.chemosphere....
; Lilley et al., 2013LILLEY, T.M., RUOKOLAINEN, L., MEIERJOHANN, A., KANERVA, M., STAUFFER, J., LAINE, V.N., ATOSUO, J., LILIUS, E.M. and NIKINMAA, M., 2013. Resistance to oxidative damage but not immunosuppression by organic tin compounds in natural populations of Daubenton’s bats (Myotis daubentonii). Comparative Biochemistry and Physiology. Toxicology & Pharmacology : CBP, vol. 157, no. 3, pp. 298-305. http://dx.doi.org/10.1016/j.cbpc.2013.01.003. PMid:23369694.
http://dx.doi.org/10.1016/j.cbpc.2013.01...
; Stechert et al., 2014STECHERT, C., KOLB, M., BAHADIR, M., DJOSSA, B.A. and FAHR, J., 2014. Insecticide residues in bats along a land use-gradient dominated by cotton cultivation in northern Benin, West Africa. Environmental Science and Pollution Research International, vol. 21, no. 14, pp. 8812-8821. http://dx.doi.org/10.1007/s11356-014-2817-8. PMid:24756668.
http://dx.doi.org/10.1007/s11356-014-281...
). We observe that insect-eating bats are the most studied (Table 1) and apparently accumulate more pesticides compared to bats with different eating habits. However, this information probably does not depict reality, since most surveys do not portray other food guilds (Table 1).

Fruit-eating bats, on the other hand, are large seed dispersers contributing to reforestation and forest conservation (Altringham, 1996ALTRINGHAM, J.D. 1996. Bats: biology and behaviour. New York: Oxford University Press.). These animals are also in constant exposure to environmental contaminants and their almost exclusive fruit diet makes them good indicators of the presence and magnitude of pesticide contamination (Valdespino and Sosa, 2017VALDESPINO, C. and SOSA, V.J., 2017. Effect of landscape tree cover, sex and season on the bioaccumulation of persistent organochlorine pesticides in fruit bats of riparian corridors in eastern Mexico. Chemosphere, vol. 175, pp. 373-382. http://dx.doi.org/10.1016/j.chemosphere.2017.02.071. PMid:28236707.
http://dx.doi.org/10.1016/j.chemosphere....
). Nevertheless, from 1964 to 2019 research on bioaccumulation and the effect of pesticides on fruit-eating bats is still scarce (Table 1).

Besides food, water is another route of exposure of bats to pesticides. Contamination can occur directly through drinking water, or indirectly when feeding on insects. In addition, water quality is a selective factor for the species, since some may prefer to forage in places with less polluted water than others (Korine et al., 2015KORINE, C., ADAMS, A.M., SHAMIR, U. and GROSS, A., 2015. Effect of water quality on species richness and activity of desert-dwelling bats. Mammalian Biology, vol. 80, no. 3, pp. 185-190. http://dx.doi.org/10.1016/j.mambio.2015.03.009.
http://dx.doi.org/10.1016/j.mambio.2015....
). Despite the importance of water quality for the species, to our knowledge, no studies show a direct association of pesticide residues in water bodies and its bioaccumulation in bat tissues, although studies involving heavy metals managed to prove this direct relashionship (Hill et al., 2016HILL, K., VAN ASWEGEN, S., SCHOEMAN, M.C., CLAASSENS, S., JANSEN VAN RENSBURG, P., NAIDOO, S. and VOSLOO, D., 2016. Foraging at wastewater treatment works affects brown adipose tissue fatty acid profiles in banana bats. Biology Open, vol. 5, no. 2, pp. 92-99. http://dx.doi.org/10.1242/bio.013524. PMid:26740572.
http://dx.doi.org/10.1242/bio.013524...
; José Zocche et al., 2010JOSÉ ZOCCHE, J., DIMER LEFFA, D., PAGANINI DAMIANI, A., CARVALHO, F., AVILA MENDONÇA, R., DOS SANTOS, C.E.I. and DE ANDRADE, V.M., 2010. Heavy metals and DNA damage in blood cells of insectivore bats in coal mining areas of Catarinense coal basin, Brazil. Environmental Research, vol. 110, no. 7, pp. 684-691. http://dx.doi.org/10.1016/j.envres.2010.06.003. PMid:20655518.
http://dx.doi.org/10.1016/j.envres.2010....
; Naidoo et al., 2015NAIDOO, S., VOSLOO, D. and SCHOEMAN, M.C., 2015. Haematological and genotoxic responses in an urban adapter, the banana bat, foraging at wastewater treatment works. Ecotoxicology and Environmental Safety, vol. 114, pp. 304-311. http://dx.doi.org/10.1016/j.ecoenv.2014.04.043. PMid:24953517.
http://dx.doi.org/10.1016/j.ecoenv.2014....
, 2016NAIDOO, S., VOSLOO, D., and SCHOEMAN, M.C., 2016. Pollutant exposure at wastewater treatment works affects the detoxification organs of an urban adapter, the Banana Bat. Environmental Pollution, vol. 208, pp. 830-839. https://doi.org/10.1016/j.envpol.2015.09.056
https://doi.org/10.1016/j.envpol.2015.09...
).

Bat populations have been declining in some regions of the world, and some authors are associating this decline with the bioaccumulation of pesticides in their tissues (Bennett and Thies, 2007BENNETT, B.S. and THIES, M.L., 2007. Organochlorine pesticide residues in guano of Brazilian free-tailed bats, Tadarida brasiliensis Saint-Hilaire, from East Texas. Bulletin of Environmental Contamination and Toxicology, vol. 78, no. 3–4, pp. 191-194. http://dx.doi.org/10.1007/s00128-007-9089-7. PMid:17476450.
http://dx.doi.org/10.1007/s00128-007-908...
; Dennis and Gartrell, 2015DENNIS, G.C. and GARTRELL, B.D., 2015. Nontarget mortality of New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone. Journal of Wildlife Diseases, vol. 51, no. 1, pp. 177-186. http://dx.doi.org/10.7589/2013-07-160. PMid:25375946.
http://dx.doi.org/10.7589/2013-07-160...
). In New Zealand and Spain, analysis of bats carcasses found in their roosting areas reveled high concentrations of pesticides (Dennis and Gartrell, 2015DENNIS, G.C. and GARTRELL, B.D., 2015. Nontarget mortality of New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone. Journal of Wildlife Diseases, vol. 51, no. 1, pp. 177-186. http://dx.doi.org/10.7589/2013-07-160. PMid:25375946.
http://dx.doi.org/10.7589/2013-07-160...
; Fernández et al., 1993FERNÁNDEZ, M.A., HERNÁNDEZ, L.M., IBÁNÑEZ, C., GONZÁLEZ, M.J., GUILLÉN, A. and PÉREZ, J.L., 1993. Congeners of PCBs in three bat species from Spain. Chemosphere, vol. 26, no. 6, pp. 1085-1097. http://dx.doi.org/10.1016/0045-6535(93)90197-D.
http://dx.doi.org/10.1016/0045-6535(93)9...
). In the United States, forty years after the pesticide DDT was banned due to its persistence and adverse effects on the environment, a large group of insect-eating bats was found dead and a high concentration of DDT was reported in their brain, kidneys, and liver (Buchweitz et al., 2018BUCHWEITZ, J.P., CARSON, K., REBOLLOSO, S. and LEHNER, A., 2018. DDT poisoning of big brown bats, Eptesicus fuscus, in Hamilton, Montana. Chemosphere, vol. 201, pp. 1-5. http://dx.doi.org/10.1016/j.chemosphere.2018.02.152. PMid:29505918.
http://dx.doi.org/10.1016/j.chemosphere....
).

4. Main Effects of Pesticides in Bats

Once ingested, xenobiotics are metabolically converted to more water-soluble compounds, easier to excrete. This biotransformation may alter the chemical´s pharmacodynamic or toxic effect. Some metabolites derived from the original compounds can also bioaccumulate in tissues and induce immunotoxicity, oxidative stress, endocrine disruption and reproductive failure in wild animals even after the exposure period (Berny, 2007BERNY, P., 2007. Pesticides and the intoxication of wild animals. Journal of Veterinary Pharmacology and Therapeutics, vol. 30, no. 2, pp. 93-100. http://dx.doi.org/10.1111/j.1365-2885.2007.00836.x. PMid:17348893.
http://dx.doi.org/10.1111/j.1365-2885.20...
).

The highest concentrations of pesticides in bats are found in the adipose tissue, followed by the liver and the brain. Bats can be 30 times more sensitive to pesticide bioaccumulation than exposed rats (Shore et al., 1996SHORE, R.F., MYHILL, D.G. and WRIGHT, J., 1996. A comparison of the toxicity to laboratory mice and pipistrelle bats Pipistrellus pipistrellus of exposure to remedially-treated timber. Environmental Toxicology and Pharmacology, vol. 2, no. 2–3, pp. 125-129. http://dx.doi.org/10.1016/S1382-6689(96)00042-7. PMid:21781714.
http://dx.doi.org/10.1016/S1382-6689(96)...
).

In several bat species, organochlorines were found to increase the basal metabolic rate with a consequent reduction in body energy reserves (Brinati et al., 2016BRINATI, A., OLIVEIRA, J.M., OLIVEIRA, V.S., BARROS, M.S., CARVALHO, B.M., OLIVEIRA, L.S., QUEIROZ, M.E., MATTA, S.L. and FREITAS, M.B., 2016. Low, chronic exposure to endosulfan induces bioaccumulation and decreased carcass total fatty acids in neotropical fruit bats. Bulletin of Environmental Contamination and Toxicology, vol. 97, no. 5, pp. 626-631. http://dx.doi.org/10.1007/s00128-016-1910-8. PMid:27592102.
http://dx.doi.org/10.1007/s00128-016-191...
; Kannan et al., 2010KANNAN, K., YUN, S.H., RUDD, R.J. and 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, vol. 80, no. 6, pp. 613-618. http://dx.doi.org/10.1016/j.chemosphere.2010.04.060. PMid:20493513.
http://dx.doi.org/10.1016/j.chemosphere....
; Swanepoel et al., 1999SWANEPOEL, R., RACEY, P., SHORE, R. and SPEAKMAN, J., 1999. Energetic effects of sublethal exposure to lindane on pipistrelle bats (Pipistrellus pipistrellus). Environmental Pollution, vol. 104, no. 2, pp. 169-177. http://dx.doi.org/10.1016/S0269-7491(98)00196-1. PMid:15093044.
http://dx.doi.org/10.1016/S0269-7491(98)...
). Energy reserves mobilization, especially from lipids, increases blood concentration of pesticides, which increases its effects in more sensitive tissues, such as liver and brain (Boyd et al., 1988BOYD, I.L., MYHILL, D.G., and MITCHELL-JONES, A.J., 1988. Uptake of gamma-HCH (Lindane) by pipistrelle bats and its effect on survival. Environmental Pollution, vol. 51, no. 2, pp. 95-111.). In the brain, organochlorines can compromise the regulation of several processes such as hibernation (Chen et al., 2008CHEN, J., YUAN, L., SUN, M., ZHANG, L. and ZHANG, S., 2008. Screening of hibernation-related genes in the brain of Rhinolophus ferrumequinum during hibernation. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, vol. 149, no. 2, pp. 388-393. http://dx.doi.org/10.1016/j.cbpb.2007.10.011. PMid:18055242.
http://dx.doi.org/10.1016/j.cbpb.2007.10...
) and prey capture during flight (Schwartz and Smotherman, 2011SCHWARTZ, C.P. and SMOTHERMAN, M.S., 2011. Mapping vocalization-related immediate early gene expression in echolocating bats. Behavioural Brain Research, vol. 224, no. 2, pp. 358-368. http://dx.doi.org/10.1016/j.bbr.2011.06.023. PMid:21726584.
http://dx.doi.org/10.1016/j.bbr.2011.06....
; Wenstrup and Portfors, 2011WENSTRUP, J.J. and PORTFORS, C.V., 2011. Neural processing of target distance by echolocating bats: functional roles of the auditory midbrain. Neuroscience and Biobehavioral Reviews, vol. 35, no. 10, pp. 2073-2083. http://dx.doi.org/10.1016/j.neubiorev.2010.12.015. PMid:21238485.
http://dx.doi.org/10.1016/j.neubiorev.20...
). In the liver, this class of pesticide can compromise the detoxifying ability (Hill et al., 2016HILL, K., VAN ASWEGEN, S., SCHOEMAN, M.C., CLAASSENS, S., JANSEN VAN RENSBURG, P., NAIDOO, S. and VOSLOO, D., 2016. Foraging at wastewater treatment works affects brown adipose tissue fatty acid profiles in banana bats. Biology Open, vol. 5, no. 2, pp. 92-99. http://dx.doi.org/10.1242/bio.013524. PMid:26740572.
http://dx.doi.org/10.1242/bio.013524...
). Moreover, the reduction of energy reserves may also impair reproductive processes, especially in females, and makes awakening of torpor difficult (Eidels et al., 2016EIDELS, R.R., SPARKS, D.W., WHITAKER JUNIOR, J.O. and SPRAGUE, C.A., 2016. Sub-lethal Effects of Chlorpyrifos on Big Brown Bats (Eptesicus fuscus). Archives of Environmental Contamination and Toxicology, vol. 71, no. 3, pp. 322-335. http://dx.doi.org/10.1007/s00244-016-0307-3. PMid:27491870.
http://dx.doi.org/10.1007/s00244-016-030...
). Decreased energy reserves also may induce an increase in foraging time, which involves a higher energy expenditure and make individuals more susceptible to predation (Allinson et al., 2006ALLINSON, G., MISPAGEL, C., KAJIWARA, N., ANAN, Y., HASHIMOTO, J., LAURENSON, L., ALLINSON, M. and TANABE, S., 2006. Organochlorine and trace metal residues in adult southern bent-wing bat (Miniopterus schreibersii bassanii) in southeastern Australia. Chemosphere, vol. 64, no. 9, pp. 1464-1471. http://dx.doi.org/10.1016/j.chemosphere.2005.12.067. PMid:16527329.
http://dx.doi.org/10.1016/j.chemosphere....
; Swanepoel et al., 1999SWANEPOEL, R., RACEY, P., SHORE, R. and SPEAKMAN, J., 1999. Energetic effects of sublethal exposure to lindane on pipistrelle bats (Pipistrellus pipistrellus). Environmental Pollution, vol. 104, no. 2, pp. 169-177. http://dx.doi.org/10.1016/S0269-7491(98)00196-1. PMid:15093044.
http://dx.doi.org/10.1016/S0269-7491(98)...
).

Organochlorines typically interfere with acetylcholinesterase activity, which may impair their echolocation performance (Eidels et al., 2016EIDELS, R.R., SPARKS, D.W., WHITAKER JUNIOR, J.O. and SPRAGUE, C.A., 2016. Sub-lethal Effects of Chlorpyrifos on Big Brown Bats (Eptesicus fuscus). Archives of Environmental Contamination and Toxicology, vol. 71, no. 3, pp. 322-335. http://dx.doi.org/10.1007/s00244-016-0307-3. PMid:27491870.
http://dx.doi.org/10.1007/s00244-016-030...
; Hsiao et al., 2016HSIAO, C.-J., LIN, C.-L., LIN, T.-Y., WANG, S.-E. and WU, C.-H., 2016. Imidacloprid toxicity impairs spatial memory of echolocation bats through neural apoptosis in hippocampal CA1 and medial entorhinal cortex areas. Neuroreport, vol. 27, no. 6, pp. 462-468. http://dx.doi.org/10.1097/WNR.0000000000000562. PMid:26966783.
http://dx.doi.org/10.1097/WNR.0000000000...
). Considering the importance of this feature for bats navigation, this single effect can impair a wide variety of their nocturnal activities. In fact, among insect-eating bats bat species monitored in agricultural areas with different degrees of herbicide exposure, populations observed foraging in organic crop areas showed a higher foraging time and a greater species richness when compared to those found in areas near crops treated with pesticides (Barré et al., 2018BARRÉ, K., LE VIOL, I., JULLIARD, R., CHIRON, F. and KERBIRIOU, C., 2018. Tillage and herbicide reduction mitigate the gap between conventional and organic farming effects on foraging activity of insectivorous bats. Ecology and Evolution, vol. 8, no. 3, pp. 1496-1506. http://dx.doi.org/10.1002/ece3.3688. PMid:29435227.
http://dx.doi.org/10.1002/ece3.3688...
).

Exposure to organochlorines also caused several pathologies in bats’ liver, such as vacuolization, necrosis and apoptosis (Amaral et al., 2012aAMARAL, T.S., CARVALHO, T.F., SILVA, M.C., BARROS, M.S., PICANÇO, M.C., NEVES, C.A., and FREITAS, M.B., 2012a. Short-term effects of a spinosyn’s family insecticide on energy metabolism and liver morphology in frugivorous bats Artibeus lituratus (Olfers, 1818). Brazilian Journal of Biology = Revista Brasleira de Biologia, vol. 72, no. 2, pp. 299-304., bAMARAL, T.S., CARVALHO, T.F., SILVA, M.C., GOULART, L.S., BARROS, M.S., PICANÇO, M.C., NEVES, C.A. and FREITAS, M.B., 2012b. Metabolic and histopathological alterations in the fruit-eating bat Artibeus lituratus induced by the organophosphorous pesticide fenthion. Acta Chiropterologica, vol. 14, no. 1, pp. 225-232. http://dx.doi.org/10.3161/150811012X654420.
http://dx.doi.org/10.3161/150811012X6544...
; Oliveira et al., 2017OLIVEIRA, J.M., BRINATI, A., MIRANDA, L.D.L., MORAIS, D.B., ZANUNCIO, J.C., GONÇALVES, R.V. and FREITAS, M.B., 2017. Exposure to the insecticide endosulfan induces liver morphology alterations and oxidative stress in fruit-eating bats (Artibeus lituratus). International Journal of Experimental Pathology, vol. 98, no. 1, pp. 17-25. http://dx.doi.org/10.1111/iep.12223. PMid:28449369.
http://dx.doi.org/10.1111/iep.12223...
). In addition, they induced oxidative stress (Oliveira et al., 2018OLIVEIRA, J.M., LOSANO, N.F., CONDESSA, S.S., DE FREITAS, R.M.P., CARDOSO, S.A., FREITAS, M.B. and DE OLIVEIRA, L.L., 2018. Exposure to deltamethrin induces oxidative stress and decreases of energy reserve in tissues of the Neotropical fruit-eating bat Artibeus lituratus. Ecotoxicology and Environmental Safety, vol. 148, pp. 648-692. http://dx.doi.org/10.1016/j.ecoenv.2017.11.024. PMid:29172149.
http://dx.doi.org/10.1016/j.ecoenv.2017....
) and decreased the total hepatic antioxidant capacity (Oliveira et al., 2017OLIVEIRA, J.M., BRINATI, A., MIRANDA, L.D.L., MORAIS, D.B., ZANUNCIO, J.C., GONÇALVES, R.V. and FREITAS, M.B., 2017. Exposure to the insecticide endosulfan induces liver morphology alterations and oxidative stress in fruit-eating bats (Artibeus lituratus). International Journal of Experimental Pathology, vol. 98, no. 1, pp. 17-25. http://dx.doi.org/10.1111/iep.12223. PMid:28449369.
http://dx.doi.org/10.1111/iep.12223...
), which, depending on the severity of the liver lesions, can cause death (Dennis and Gartrell, 2015DENNIS, G.C. and GARTRELL, B.D., 2015. Nontarget mortality of New Zealand lesser short-tailed bats (Mystacina tuberculata) caused by diphacinone. Journal of Wildlife Diseases, vol. 51, no. 1, pp. 177-186. http://dx.doi.org/10.7589/2013-07-160. PMid:25375946.
http://dx.doi.org/10.7589/2013-07-160...
).

Besides the effects of pesticides in cells and tissues, some chemicals also interfere with the endocrine system of non-target organisms, impairing hormone secretion, transportation and/or biding to target cells. Several organochlorine and pyrethroid insecticides are considered endocrine disrupters, altering the reproduction axis mediated by testosterone in rats (Thies and McBee, 1994THIES, M.L. and MCBEE, K., 1994. Cross-placental transfer of organochlorine pesticides in mexican free-tailed bats from Oklahoma and New Mexico. Archives of Environmental Contamination and Toxicology, vol. 27, no. 2, pp. 239-242. http://dx.doi.org/10.1007/BF00214268. PMid:8060168.
http://dx.doi.org/10.1007/BF00214268...
; Thies et al., 1996THIES, M.L., THIES, K. and MCBEE, K., 1996. Organochlorine pesticide accumulation and genotoxicity in Mexican free-tailed bats from Oklahoma and New Mexico. Archives of Environmental Contamination and Toxicology, vol. 30, no. 2, pp. 178-187. http://dx.doi.org/10.1007/BF00215796. PMid:8593080.
http://dx.doi.org/10.1007/BF00215796...
). In bats, only a few studies have been contributing to this important area, including the reported incidence of several testicular and epididymal pathologies followed by the exposure to the fungicide tebuconazole in Neotropical fruit-eating bats (Machado-Neves et al., 2018MACHADO-NEVES, M., NETO, M.J.O., MIRANDA, D.C., SOUZA, A.C.F., CASTRO, M.M., SERTORIO, M.N. and FREITAS, M.B., 2018. Dietary exposure to tebuconazole affects testicular and epididymal histomorphometry in frugivorous bats. Bulletin of Environmental Contamination and Toxicology, vol. 101, no. 2, pp. 197-204. http://dx.doi.org/10.1007/s00128-018-2377-6. PMid:29881942.
http://dx.doi.org/10.1007/s00128-018-237...
).

Immunotoxicological effects of pesticides are also a neglected area regarding studies with bats, although the white-nose syndrome has been killing millions of bats in temperate regions. Pesticides toxicity leads to immunosuppression and makes the individual more susceptible to infections by pathogenic organisms (Afonso et al., 2016AFONSO, E., TOURNANT, P., FOLTÊTE, J.-C., GIRAUDOUX, P., BAURAND, P.-E., ROUÉ, S. and SCHEIFLER, R., 2016. Is the lesser horseshoe bat (Rhinolophus hipposideros) exposed to causes that may have contributed to its decline? A non-invasive approach. Global Ecology and Conservation, vol. 8, pp. 123-137. http://dx.doi.org/10.1016/j.gecco.2016.09.002.
http://dx.doi.org/10.1016/j.gecco.2016.0...
). A direct association to pesticides exposure was suggested by Kannan et al. (2010)KANNAN, K., YUN, S.H., RUDD, R.J. and 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, vol. 80, no. 6, pp. 613-618. http://dx.doi.org/10.1016/j.chemosphere.2010.04.060. PMid:20493513.
http://dx.doi.org/10.1016/j.chemosphere....
, which reported a reduced complement system activity induced by organochlorine bioaccumulation in insect-eating bats (Kannan et al., 2010KANNAN, K., YUN, S.H., RUDD, R.J. and 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, vol. 80, no. 6, pp. 613-618. http://dx.doi.org/10.1016/j.chemosphere.2010.04.060. PMid:20493513.
http://dx.doi.org/10.1016/j.chemosphere....
) (Lilley et al., 2013LILLEY, T.M., RUOKOLAINEN, L., MEIERJOHANN, A., KANERVA, M., STAUFFER, J., LAINE, V.N., ATOSUO, J., LILIUS, E.M. and NIKINMAA, M., 2013. Resistance to oxidative damage but not immunosuppression by organic tin compounds in natural populations of Daubenton’s bats (Myotis daubentonii). Comparative Biochemistry and Physiology. Toxicology & Pharmacology : CBP, vol. 157, no. 3, pp. 298-305. http://dx.doi.org/10.1016/j.cbpc.2013.01.003. PMid:23369694.
http://dx.doi.org/10.1016/j.cbpc.2013.01...
). Insect-eating bats were found to have more ectoparasites when foraging under polluted waters (Korine et al., 2015KORINE, C., ADAMS, A.M., SHAMIR, U. and GROSS, A., 2015. Effect of water quality on species richness and activity of desert-dwelling bats. Mammalian Biology, vol. 80, no. 3, pp. 185-190. http://dx.doi.org/10.1016/j.mambio.2015.03.009.
http://dx.doi.org/10.1016/j.mambio.2015....
). The main endpoints observed are summarized in Figure 3.

Figure 3
Major endpoints of the consequences of bats exposure to pesticides.

Given the aspects afore mentioned, we conclude that bats are sensitive to pesticide exposure and may act as a model for pesticide risk assessment programs (Stahlschmidt and Brühl 2012STAHLSCHMIDT, P. and BRÜHL, C.A., 2012. Bats at risk? Bat activity and insecticide residue analysis of food items in an apple orchard. Environmental Toxicology and Chemistry, vol. 31, no. 7, pp. 1556-1563. http://dx.doi.org/10.1002/etc.1834. PMid:22505289.
http://dx.doi.org/10.1002/etc.1834...
). Specific characteristics such as high metabolic rate, high longevity and high oxygen consumption contribute to the importance of evaluating pesticides effects in key bat species.

5. Conclusion

Many studies have yet to be done to know the degree and exactly how pesticides act in the physiology of bats, but impacts are high for these animals and may reduce populations' survival capacity, resulting in large losses for both conservation and economy efforts. Future research is needed for increasing the conservational effort of this taxon.

  • (With 3 figures)

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Publication Dates

  • Publication in this collection
    15 May 2020
  • Date of issue
    Mar-May 2021

History

  • Received
    17 June 2019
  • Accepted
    17 Dec 2019
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