Skip to main content

Advertisement

Log in

Contaminant exposure as an additional stressor to bats affected by white-nose syndrome: current evidence and knowledge gaps

  • Mini-Review
  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Bats are exposed to numerous threats including pollution and emerging diseases. In North America, the fungal disease white-nose syndrome (WNS) has caused declines in many bat species. While the mechanisms of WNS have received considerable research attention, possible influences of contaminants have not. Herein, we review what is known about contaminant exposure and toxicity for four species whose populations have been severely affected by WNS (Myotis sodalis, M. septentrionalis, M. lucifugus, and Perimyotis subflavus) and identify temporal and spatial data gaps. We determine that there is limited information about the effects of contaminants on bats, and many compounds that have been detected in these bat species have yet to be evaluated for toxicity. The four species examined were exposed to a wide variety of contaminants; however, large spatial and knowledge gaps limit our ability to evaluate if contaminants contribute to species-level declines and if contaminant exposure exacerbates infection by WNS.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Compiled data from publications are available in the Supplementary file.

References

  • Al-Jaibachi R, Cuthbert RN, Callaghan A (2018) Up and away: Ontogenic transference as a pathway for aerial dispersal of microplastics. Biol Lett 14:20180479

    Article  Google Scholar 

  • Anderson DM, Gilbert PM, Burkholder JM (2002) Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries 25:704–726

    Article  Google Scholar 

  • Atwood TC, Duncan C, Patyk KA, Nol P, Rhyan J, McCollum M, McKinney MA, Ramey AM, Cerqueira-Cézar CK, Kwok OCH, Dubey JP, Hennager S (2017) Environmental and behavioral changes may influence the exposure of an Arctic apex predator to pathogens and contaminants. Sci Rep. https://doi.org/10.1038/s41598-017-13496-9

  • Auteri GG, Knowles LL (2020) Decimated little brown bats show potential for adaptive change. Sci Rep 10:3023

    Article  CAS  Google Scholar 

  • Avena CV, Parfrey LW, Leff JE, Archer HM, Frick WF, Langwig KE, Kilpatrick AM, Powers KE, Foster JT, McKenzie VJ (2016) Deconstructing the bat skin microbiome: influences of the host and the environment. Microbiol 7:1753

    Google Scholar 

  • Baron LA, Sample BE, Suter II GW (1999) Ecological risk assessment in a large river-reservoir: Aerial insectivorous wildlife. Environ Toxicol Chem 18:621–627

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Becker DJ, Chumchal MM, Broders HG, Korstian JM, Clare EL, Rainwater TR, Plattm SG, Simmons NB, Fenton MB (2018) Mercury bioaccumulation in bats reflects dietary connectivity to aquatic food webs. Environ Pollut 233:1076–1085

    Article  CAS  Google Scholar 

  • Becker DJ, Speer KA, Korstian JM, Volokhov DV, Droke HF, Brown AM, Baijnauth CL, Padgett-Stewart T, Broders HG, Plowright RK, Rainwater TR, Fenton MB, Simmons NB, Chumbal MM (2021) Disentangling interactions among mercury, immunity, and infection in a Neotropical bat community. J Appl Ecol 58:879–889

    Article  CAS  Google Scholar 

  • Bergeson SM, Carter TC, Whitby MD (2015) Adaptive roosting gives little brown bats an advantage over Indiana bats. Am Midl Nat 174:321–330

    Article  Google Scholar 

  • Bernard RF, Willcox EV, Parise KL, Foster JT, McCracken GF (2017) White-nose syndrome fungus, Psuedogymnoascus destructans, on bats captured emerging from caves during winter in the southeastern United States. BMC Zool 2:1–11

    Article  Google Scholar 

  • Best TL, Jennings JB (1997) Myotis leibii. Mamm Species 547:1–6

    Google Scholar 

  • Blais JM, Macdonald RW, Mackay D, Webster E, Harvey C, Smol JP (2007) Biologically mediated transport of contaminants in aquatic systems. Environ Sci Technol 41:1075–1084

    Article  CAS  Google Scholar 

  • Bradney L, Wijesekara H, Palansooriya KN, Obadamudalige N, Bolan NS, Ok YS, Rinklebe J, Kim KH, Kirkham MB (2019) Particulate plastics as a vector for toxic trace-element uptake by aquatic and terrestrial organisms and human health risk. Environ Int 131:104937

    Article  CAS  Google Scholar 

  • Broders HG, Findlay CS, Zheng L (2004) Effects of clutter on echolocation call structure of Myotis septentrionalis and M. lucifugus. J Mammal 85:273–281

    Article  Google Scholar 

  • Brack Jr V, Johnson SA, Dunlap RK (2003) Wintering populations of bats in Indiana, with emphasis on the endangered Indiana Myotis, Myotis sodalis. Proc Indiana Acad Sci 112:61–74

    Google Scholar 

  • Brown SR, Flynn RW, Hoverman JT (2020) Perfluoroalkyl substances increase susceptibility of northern leopard frog tadpoles to trematode infection. Environ Toxicol Chem. https://doi.org/10.1002/etc.4678

  • Burton GV, Alley RJ, Rasmussen GL, Orton P, Cox V, Jones P, Graff D (1977) Mercury and behavior in wild mouse populations. Environ Res 14:30–34

    Article  CAS  Google Scholar 

  • Carter TC, Feldhamer GA (2005) Roost tree use by maternity colonies of Indiana bats and northern long-eared bats in southern Illinois. For Ecol and Manag 219:259–268

    Article  Google Scholar 

  • Cheng TL, Gerson A, Moore MS, Reichard JD, DeSimone J, Willis CKR, Frick WF, Kilpatrick AM (2019) Higher fat stores contribute to persistence of little brown bat populations with white-nose syndrome. J Anim Ecol 88:591–600

    Article  Google Scholar 

  • Cheng TL, Reichard JD, Coleman JTH, Weller TJ, Thogmartin WE, Reichert BE, Bennet AB, Broders HG, Campbell J, Etchison K, Feller DJ, Geboy R, Hemberger T, Herzog C, Hicks AC, Houghton S, Humber J, Kath JA, King RA, Loeb SC, Massé A, Morris KM, Niederriter H, Nordquist G, Perry RW, Reynolds RJ, Sasse DB, Scafini MR, Stark RC, Stihler CW, Thomas SC, Turner GG, Webb S, Westrich BJ, Frick WF (2021) The scope and severity of white-nose syndrome on hibernating bats in North America. Conserv Biol. https://doi.org/10.1111/cobi.13739

  • Chételat J, Hickey MBC, Poulain AJ, Dastoor A, Ryjkov A, McAlpine D, Vanderwolf K, Jung TS, Hale L, Cooke ELL, Hobson D, Jonasson K, Kaupas L, McCarthy S, McClelland C, Morningstar D, Norquay KJO, Novy R, Player D, Redford T, Simard A, Stamler S, Webber QMR, Yumvihoze E, Zanuttig M (2018) Spatial variation of mercury bioaccumulation in bats of Canada linked to atmospheric mercury deposition. Sci Total Environ 626:668–677

    Article  Google Scholar 

  • Chételat J, Ackerman JT, Eagles-Smith CA, Hebert CE (2020) Methylmercury exposure in wildlife: A review of the ecological and physiological processes affecting contaminant concentrations and their interpretation. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.135117

  • Clare EL, Barber BL, Sweeney BW, Hebert PDN, Fenton MB (2011) Eating local: influences of habitat on the diet of little brown bats (Myotis lucifugus). Mol Ecol 20:1772–1780

    Article  CAS  Google Scholar 

  • Clark Jr DR (1979) Lead concentrations: Bats vs. terrestrial small mammals collected near a major highway. Environ Sci Technol 13:338–341

    Article  CAS  Google Scholar 

  • Clark DR Jr (1986) Toxicity of methyl parathion to bats: Mortality and coordination loss Environ Toxicol Chem 5:191–195

    Article  CAS  Google Scholar 

  • Clark DRJr, Krynitsky A (1978) Organochlorine residues and reproduction in the little brown bat, Laurel, Maryland–1976. Pestic Monit J 12:113–116

    CAS  Google Scholar 

  • Clark DRJr, Prouty RM (1976) Organochlorine residues in three bat species from four localities in Maryland and West Virginia. Pestic Monit J 10:44–53

    CAS  Google Scholar 

  • Clark DR Jr, Prouty RM (1984) Disposition of dietary dieldrin in the little brown bat and correlation of skin levels with body burden Bull Environ Contam Toxicol 33:177–183

    Article  CAS  Google Scholar 

  • Clark DR Jr, Rattner BA (1987) Orthene toxicity to little brown bats (Myotis lucifugus): Acetylcholinesterase inhibition, coordination loss, and mortality Environ Toxicol Chem 6:705–708

    CAS  Google Scholar 

  • Clark DR Jr, Stafford CJ (1981) Effects of DDE and PCB on experimentally poisoned female little brown bats (Myotis lucifugus): Lethal brain concentrations J Toxicol Environ Health 7:925–934

    Article  CAS  Google Scholar 

  • Duchamp JE, Sparks DW, Swihart RK (2010) Exploring the “nutrient hot spot” hypothesis at trees used by bats. J Mammal 9:48–53

    Article  Google Scholar 

  • Edwards AE, Swall JL, Jagoe CH (2019) Mercury concentrations in bat guano from caves and bat houses in Florida and Georgia. Virginia J Sci 70:1–13

    Google Scholar 

  • Eidels RR, Whitaker Jr JO, Sparks DW (2007) Insecticide residues in bats and guano from Indiana. Proc Indiana Acad Sci 116:50–57

    CAS  Google Scholar 

  • Eidels RR, Whitaker Jr JO, Lydy MJ, Sparks DW (2013) Screening of insecticides in bats from Indiana. Proc Indiana Acad Sci 121:133–142

    Google Scholar 

  • Feirrera RL (2019) Guano communities. In: White WB, Culver DC, Pipan T (eds) Encyclopedia of Caves. Elsevier, pp. 357–364

  • Feldhamer GA, Carter TC, Whitaker Jr JO (2009) Prey consumed by eight species of insectivorous bats from southern Illinois. Am Midl Nat 162:43–51

    Article  Google Scholar 

  • Flache L, Becker NI, Kierdorf U, Czarnecki R, Düring A, Encarnaçao (2015) Hair samples as monitoring units for assessing metal exposure of bats: a new tool for risk assessment Mammal. Biol 80:178–181

    Google Scholar 

  • Flint S, Markle T, Thompson S, Wallace K (2012) Bisphenol A exposure, effects, and policy: a wildlife perspective. J Environ Manage 104:19–34

    Article  CAS  Google Scholar 

  • Francl KE, Ford WM, Sparks DW, Brack Jr V (2012) Capture and reproductive trends in summer bat communities in West Virginia: Assessing the impact of white-nose syndrome. J Fish Wildl Manage 3:33–42

    Article  Google Scholar 

  • Frick WF, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE, Foster JT, Barlow KE, Bartonicka T, Feller D, Haarsma AJ, Herzog C, Horácˇek I, van der Kooij J, Mulkens B, Petrov B, Reynolds R, Rodrigues L, Stihler CW, Turner GG, Kilpatrick AM (2015) Disease alters macroecological patterns of North American bats. Glob Ecol and Biogeogr 24:741–749

    Article  Google Scholar 

  • Frick WF, Puechmaille SJ, Willis CKR (2016) White-nose syndrome in bats. In: Voigt CC, Kingston T (eds) Bats in the anthropocene: Conservation of bats in a changing world. Springer International Publishing, Germany. pp. 245–262

  • Frick WF, Cheng TL, Langwig KE, Hoyt JR, Janicki AF, Parise KL, Kilpatrick AM (2017) Pathogen dynamics during invasion and establishment of white‐nose syndrome explain mechanisms of host persistence. Ecology 98:624–631

    Article  Google Scholar 

  • Frick WF, Kingston T, Flanders J (2019) A review of the major threats and challenges to global bat conservation. Ann NY Acad Sci. https://doi.org/10.1111/nyas.140451

  • Geluso KN, Altenbach JS, Wilson DE (1976) Bat mortality: pesticide poisoning and migratory stress. Science 194:184–186

    Article  CAS  Google Scholar 

  • Green K (2008) Migratory bogong moths (Agrotis infusa) transport arsenic and concentrate it to lethal effect by estivating gregariously in alpine regions of the snowy mountains of Australia. Arct Antarct Alp Res 40:74–80

    Article  Google Scholar 

  • Grisnik M, Bowers O, Moore AJ, Jones BF, Campbell JR, Walker DM(2020) The cutaneous microbiota of bats has in vitro antifungal activity against the white-nose pathogen. FEMS Microbiol Ecol 96:fiz193

    Article  CAS  Google Scholar 

  • Haas SE, Reeves MK, Pinkney AE, Johnson PTJ (2018) Continental-extent patterns in amphibian malformations linked to parasites, chemical contaminants, and their interactions. Glob Change Biol 24:e275–e288

    Article  Google Scholar 

  • Hallmann CA, Foppen RP, van Turnhout A, de Kroon H, Jongejans E (2014) Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511:341

    Article  CAS  Google Scholar 

  • Hanlon SM, Parris MJ (2013) The interactive effects of chytrid fungus, pesticides, and exposure on gray treefrog (Hyla versicolor) larvae. Environ Toxicol Chem 33:216–222

    Article  Google Scholar 

  • Hernout BV, McClean CJ, Arnold KE, Walls M, Baxter M, Boxall ABA (2016) Fur: A non-invasive approach to monitor metal exposure in bats. Chemosphere 147:376–381

    Article  CAS  Google Scholar 

  • Hickey MBC, Fenton MB, MacDonald KC, Soulliere C (2001) Trace elements in the fur of bats (Chiroptera: Vespertilionidae) from Ontario and Quebec, Canada. Bull Environ Contam Toxicol 66:699–706

    Article  CAS  Google Scholar 

  • Hoying KM, Kunz TH (2006) Variation in size at birth and post-natal growth in the insectivorous bat Pipistrellus subflavus (Chiroptera: Vespertilionidae). J Zool 245:15–27

    Article  Google Scholar 

  • Hoyt JR, Cheng TL, Langwig KE, Hee MM, Frick WF, Kilpatrick AM (2015) Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE 10:e0121329

    Article  Google Scholar 

  • Hurley S, Fenton MN (1980) Ineffectiveness of fenthion, zinc phosphide, DDT and two ultrasonic rodent repellers for control of populations of little brown bats (Myotis lucifugus). Bull Environ Contam Toxicol 25:503–507

    Article  CAS  Google Scholar 

  • Isidoro-Ayza M, Jones L, Dusek RJ, Lorch JM, Landsberg JH, Wilson P, Graham S (2019) Mortality of little brown bats (Myotis lucifugus carissima) naturally exposed to Microcystin-LR. J Wildl Dis 55:266–269

    Article  Google Scholar 

  • Jacobson SK, Rittenhouse TAG (2019) Deicing salts influence ranavirus outbreaks in wood frog (Lithobates sylvaticus) tadpoles. Honor Scholar Theses 618, University of Connecticut, Storrs, Connecticut, 32 pp

  • Jeschke P, Nauen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    Article  CAS  Google Scholar 

  • Langwig KE, Frick WF, R. Reynolds. KL, Johnson JS, Lacki MK, Thomas SC, Grider JF (2012) Frequent arousals from winter torpor in Rafinesque’s big-eared bat (Corynorhinus rafinesquii). PLoS ONE 7:e49754

    Article  Google Scholar 

  • Jonasson KA, Willis CKR (2011) Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome. PLoS ONE 6:e21061

    Article  CAS  Google Scholar 

  • Kalcounis-Rueppell MC, Payne VH, Huff SR, Boyko AL (2007) Effects of wastewater treatment plant effluent on bat foraging ecology in an urban stream system. Biol Conserv 138:120–130

    Article  Google Scholar 

  • Kannan K, Yun SE, 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 

  • Karouna-Renier NK, White C, Perkins CR, Schmerfeld JJ, Yates D (2014) Assessment of mitochondrial DNA damage in little brown bats (Myotis lucifugus) collected near a mercury contaminated river. Ecotoxicology 23:1419–1429

    Article  CAS  Google Scholar 

  • Kasso M, Balakrishnan M (2013) Ecological and economic importance of bats (Order Chiroptera). ISRN Biodivers. https://doi.org/10.1155/2013/187415

  • Kempuraj, D, Asadi S, Zhang B, Manola A, Hogan J, Peterson E, Theoharides TC (2010) Mercury induces inflammatory mediator release from human mast cells. J Neuroinflammation. https://doi.org/10.1186/1742-2094-7-20

  • Korstian JM, Chumchal MM, Bennett VJ, Hale AM (2017) Mercury contamination in bats from the central United States. Environ Toxicol Chem 37:160–165

    Article  Google Scholar 

  • Kraus JM, Schmidt TS, Walters DM, Wanty RB, Zuellig RE, Wolf RE (2014) Cross-ecosystem impacts of stream pollution reduce resource and contaminant flux to riparian food webs. Ecol Appl 24:235–243

    Article  Google Scholar 

  • Kraus JM (2019) Contaminants in linked aquatic–terrestrial ecosystems: Predicting effects of aquatic pollution on adult aquatic insects and terrestrial insectivores. Freshw Sci 38:919–927

    Article  Google Scholar 

  • Krümmel EM, Macdonald RW, Kimpe LE, Gregory-Eaves I, Demers MJ, Smol JP, Finney B, Blais M (2003) Delivery of pollutants by spawning salmon. Nature 425:255–256

    Article  Google Scholar 

  • Kunz TH, Anthony EL, Rumage III WT (1977) Mortality of little brown bats following multiple pesticide applications. J Wildl Manage 41:476–483

    Article  CAS  Google Scholar 

  • Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and fat in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5:8–17

    Article  Google Scholar 

  • Langwig KE, Frick WF, Bried JT, Hicks AC, Kunz TH, Kilpatrick AM (2012) Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett 15:1050–1057

    Article  Google Scholar 

  • Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Kilpatrick AM (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc B: Biol Sci 282:20142335

    Article  Google Scholar 

  • Lemieux-Labonté V, Simard A, Willis CK, Lapointe FJ (2017) Enrichment of beneficial bacteria in the skin microbiota of bats persisting with white-nose syndrome. Microbiome 5:115

    Article  Google Scholar 

  • Lewis CA, Cristol DA, Swaddle JP, Varian-Ramos CW, Zwollo P (2013) Decreased immune response in zebra finches exposed to sublethal doses of mercury. Arch Environ Contam Toxicol 64:327–336

    Article  CAS  Google Scholar 

  • Little ME, Burgess NM, Broders HG, Campbell LM (2015a) Distribution of mercury in archived fur from little brown bats across Atlantic Canada. Environ Pollut 207:52–58

    Article  CAS  Google Scholar 

  • Little ME, Burgess NM, Broders HG, Campbell LM (2015b) Mercury in little brown bat (Myotis lucifugus) maternity colonies and its correlation with freshwater acidity in Nova Scotia. Canada. Environ Sci Tech 49:2059–2065

    Article  CAS  Google Scholar 

  • Lorch JM, Meteyer CU, Behr MG, Boyles JG, Cryan PM, Hicks AC, Blehert DS (2011) Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature 480:376

    Article  CAS  Google Scholar 

  • Lorch JM, Palmer JM, Lindner DL, Ballmann AE, George KG, Griffin K, Knowles S, Huckabee JR, Haman KH, Anderson CD, Becker PA, Buchanan JB, Foster JT, Blehert DS (2016) First detection of bat white-nose syndrome in western North America. mSphere 1:e00148–16

    Article  CAS  Google Scholar 

  • McCracken GF, Westbrook JK, Brown VA, Eldridge M, Federico P, Kunz TH (2012) Bats track and exploit changes in insect pest populations. PLoS ONE 7:e43839

    Article  CAS  Google Scholar 

  • McFarland CA (1998) Potential agricultural insecticide exposure of Indiana bats (Myotis sodalis) in Missouri. Master Thesis, University of Missouri, Columbia, Missouri, 256 pp.

  • Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ, Gargas A, Behr MJ (2009) Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest 21:411–414

    Article  Google Scholar 

  • Meteyer CU, Barber D, Mandl JN (2012) Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. Virulence 3:583–588

    Article  Google Scholar 

  • Meyling NV, Arthur S, Pedersen KE, Dhakal S, Cedergreen N, Fredensborg BL (2018) Implications of sequence and timing of exposure for synergy between the pyrethroid insecticide alpha-cypermethrin and the entomopathogenic fungus Beauveria bassiana. Pest Manag Sci 74:2488–2495

    Article  CAS  Google Scholar 

  • Moosman PR, Warner DP, Hendren RH, Hosler MJ (2015) Potential for monitoring eastern small-footed bats on talus slopes. Northeast Nat 22:NENHC1–NENHC13

    Article  Google Scholar 

  • Moy NJ, Dodson J, Tassone SJ, Bukaveckas PA, Bulluck LP (2016) Biotransport of algal toxins to riparian food webs. Environ Sci Technol 50:10007–10014

    Article  CAS  Google Scholar 

  • Mwangi JN, Wang N, Ingersoll CG, Hardesty DK, Brunson EL, Li H, Deng B (2012) Toxicity of carbon nanotubes to freshwater aquatic invertebrates. Environ Toxicol Chem 31:1823–1830

    Article  CAS  Google Scholar 

  • Naidoo S, Vosloo D, Schoeman MC (2015) Pollutant exposure at wastewater treatment works affects the detoxification organs of an urban adapter, the banana bat. Environ Pollut 208:830–839

    Article  Google Scholar 

  • Nam D, Yates D, Ardapple P, Evers DC, Schmerfeld J, Basu N (2012) Elevated mercury exposure and neurochemical alterations in little brown bats (Myotis lucifugus) from a site with historical mercury contamination. Ecotoxicology 21:1094–1101

    Article  CAS  Google Scholar 

  • Naslund LC, Gerson JR, Brooks AC, Walters DM, Bernhardt ES (2020) Contaminant subsidies to riparian food webs in Appalachian streams impacted by mountaintop removal coal mining. Environ Sci Technol 54:3951–3959

    Article  CAS  Google Scholar 

  • Niemiller ML, Taylor SJ, Slay ME, Hobbs HH (2019) Biodiversity in the United States. In: White WB, Culver DC, Pipan T (eds) Encyclopedia of Caves. Elsevier, pp. 163–176

  • Noyes PD, McElwee MK, Miller HD, Clark BW, Van Tiem LA, Walcott KC, Erwin KN, Levin ED (2009) The toxicology of climate change: Environmental contaminants in a warming world. Environ Int 35:971–986

    Article  CAS  Google Scholar 

  • O’Keefe JM, Pettit JL, Loeb SC, Stiver WH (2019) White-nose syndrome dramatically altered the summer bat assemblage in a temperate Southern Appalachian forest. Mammal Biol 98:146–153

    Article  Google Scholar 

  • Oliveira JM, Destro ALF, Freitas MB, Oliveira LL (2021) How do pesticides affect bats? – A brief review of recent publications. Braz J of Biol 81:499–507

    Article  CAS  Google Scholar 

  • O’Rourke DR, Mangan MT, Mangan KE, Bokulich NA, MacManes MD, Foster JT (2021) Lord of the Diptera (and moths and spider): molecular diet analyses and foraging ecology of Indiana bats in Illinois. Front Ecol Evol. https://doi.org/10.3389/fevo.2021.623655

  • O’Shea TJ, Clark DR Jr (2002) An overview of contaminants and bats, with special reference to insecticides and the Indiana bat. In: Kurta A, Kennedy J (eds) The Indiana bat: biology and management of an endangered Species. Bat Conservational International, Austin, Texas, pp. 237–253

  • O’Shea TJ, Cryan PM, Hayman DTS, Plowright RK, Streicker DG (2016) Multiple mortality events in bats: a global review. Mammal Rev 46:175–190

    Article  Google Scholar 

  • Parise KL, Drees KP, Hoyt JR, Kilpatrick AM (2015) Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc B: Biol Sci 282:20142335

    Article  Google Scholar 

  • Paul KC, Jerrett M, Ritz B (2019) Type 2 diabetes mellitus and Alzheimer’s disease: overlapping biologic mechanisms and environmental risk factors. Curr Environ. Health Rep 5:44–58

    Google Scholar 

  • Perry RW, Jordan PN (2020) Survival and persistence of tri-colored bats hibernating in Arkansas mines. J Mammal 101:535–543

    Article  Google Scholar 

  • Pochini KM, Hoverman JT (2016) Reciprocal effects of pesticides and pathogens on amphibian hosts: The importance of exposure order and timing. Environ Pollut 221:359–366

    Article  Google Scholar 

  • Powell GVN (1983) Industrial effluents as a source of mercury contamination in terrestrial riparian vertebrates. Environ Pollut 5:51–57

    Article  CAS  Google Scholar 

  • Ramos-H D, Medellín RA, Morton-Mermea O (2020) Insectivorous bats as biomonitor of metal exposure in the megalopolis of Mexico and rural environments in Central Mexico. Environ Res 185:1–10

    Article  Google Scholar 

  • Reeder DM, Frank CL, Turner GG, Meteyer CU, Kurta A, Britzke ER, Vodzak ME, Darling SR, Stihler CW, Hicks AC, Jacob R, Grieneisen LE, Brownlee SA, Muller LK, Blehert DS (2012) Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS ONE 7:e38920

    Article  CAS  Google Scholar 

  • Reynolds RJ, Powers KE, Orndorff W, Ford WM, Hobson CS (2016) Changes in rates of capture and demographics of Myotis septentrionalis in West Virginia before and after onset of white-nose syndrome. Northeast Nat 23:195–204

    Article  Google Scholar 

  • Richmond EK, Rosi EJ, Walters DM, Fick J, Hamilton SK, Brodin T, Sundelin A, Grace MR (2018) A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nat Commun. https://doi.org/10.1038/s41467-018-06822-w

  • Ross PS, De Swart RL, Loveren HV, Osterhaus ADME, Vos JG (1996) The immunotoxicity of environmental contaminants to marine wildlife: a review. Annu Rev Fish Dis 6:151–165

    Article  Google Scholar 

  • Schmidt A, Brack Jr V, Rommé R, Tyrell K, Gehrt A (2000) Bioaccumulation of pesticide in bats from Missouri. In: Johnston JJ (ed) Pesticides and Wildlife. American Chemical Society, Washington DC, pp 8–21

    Chapter  Google Scholar 

  • Secord AL, Major A, Patnode K, Sparks DW (2015a) NY, MA, VT, NH, CT, PA, IN – Evaluation of the potential role of environmental contaminants in significant bat mortality conjunction with white-nose syndrome (WNS) in the Northeastern United States. Final Report 36 pp. https://www.fws.gov/northeast/nyfo/ec/files/5F44BatWNSECinvestigation-Final2015-noCECs.pdf. Accessed 12 Oct 2020

  • Secord AL, Patnode KA, Carter C, Redman E, Gefell DJ, Major AR, Sparks DW (2015b) Contaminants of emerging concern in bats from the northeastern United States. Arch Environ Contam Toxicol 69:411–421

    Article  CAS  Google Scholar 

  • Smallbone W, Cable J, Maceda-Veiga A (2016) Chronic nitrate enrichment decreases severity and induces protection against an infectious disease. Environ Int 91:265–270

    Article  CAS  Google Scholar 

  • Stansley W, Roscoe DE, Hawthorne E, Meyer R (2001) Food chain aspects of chlordane poisoning in birds and bats. Environ Contam and Toxicol 40:285–291

    Article  CAS  Google Scholar 

  • Syaripuddin K, Kumar A, Sing K, Hallim MA, Nursyereen M, Wilson J (2014) Mercury accumulation in bats near hydroelectric reservoirs in Peninsular Malaysia. Ecotoxicology 23:1164–1171

    Article  CAS  Google Scholar 

  • Torquetti CG, Guimaraes ATB, Soto-Blanco B (2021) Exposure to pesticides in bats. Sci Tot Environ. https://doi.org/10.1016/j.scitotenv.2020.142509

  • U.S. Geological Survey and U.S. Fish and Wildlife Service (2016) Environmental Contaminant Research Program In: Perry MC (ed) The history of Patuxent—America’s wildlife research story. U.S. Geological Survey Circular, pp 87–127

  • U.S. Fish and Wildlife Service (2016) 4(d) rule for northern long-eared bat (Myotis septentrionalis). Federal Register 81(9): 1900 https://www.fws.gov/Midwest/endangered/mammals/nleb/pdf/FRnlebFinal4dRule14Jan2016.pdf. Accessed 5 Oct 2020

  • Van Loveren H, Ross PS, Osterhaus ADME, Vos JG (2000) Contaminant-induced immunosuppression and mass mortalities among harbor seals. Toxicol Lett 112– 113:319–324

    Article  Google Scholar 

  • Veilleux JP, Whitaker Jr JO, Veilleux SL (2003) Tree-roosting ecology of reproductive female eastern pipistrelles, Pipistrellus subflavus, in Indiana. J Mammal 84:1068–1075

    Article  Google Scholar 

  • Verant ML, Meteyer CU, Speakman, JR, Cryan, PM, Lorch JM, Blehert, DS (2014) White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. BMC Physiol. https://doi.org/10.1186/s12899-014-0010-4.

  • Woller-Skar MM, Jones DN, Luttenton MR, Russell AL (2015) Microcystin detected in little brown bats (Myotis lucifugus). Am Midl Nat 174:331–334

    Article  Google Scholar 

  • Wagner CA (2007) Metabolic acidosis: new insights from mouse models. Curr Opin Nephrol Hy 16:471–476

    Article  CAS  Google Scholar 

  • Walters DM, Fritz KM, Otter RR (2008) The dark side of subsidies: adult stream insects export organic contaminants to riparian predators. Ecol App 18:1835–1841

    Article  Google Scholar 

  • Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CKR (2012) Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci 109:6999–7003

    Article  CAS  Google Scholar 

  • Warnecke L, Turner JM, Bollinger TK, Misra V, Cryan PM, Blehert DS, Wibbelt G, Willis CKR (2013) Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol Lett 9:20130177

    Article  Google Scholar 

  • Warren RW, Hall DB, Gregor PD (2014) Radionuclides in bats using a contaminated pond on the Nevada National Security Site, USA. J Environ Radioact 129:86–93

    Article  CAS  Google Scholar 

  • Welden NAC, Cowie PR (2016) Long-term microplastic retention causes reduced body condition in the langoustine, Nephrops norvegicus. Environ Pollut 218:895–900

    Article  CAS  Google Scholar 

  • White DH, Krynitsky AJ (1986) Wildlife in some areas of New Mexico and Texas accumulate elevated DDE residues, 1983. Arch Environ Contam Toxicol 15:149–157

    Article  CAS  Google Scholar 

  • Wilkinson GS, South JM (2002) Life history, ecology, and longevity in bats. Aging Cell 1:124–131

    Article  CAS  Google Scholar 

  • Wray AK, Jusino MA, Banik MT, Palmer JM, Kaarakka H, White JP, Lindner DL, Gratton C, Peery MZ (2018) Incidence and taxonomic richness of mosquitoes in the diets of little brown and big brown bats. J Mammal 99:668–674

    Article  Google Scholar 

  • Yamamuro M, Komuro T, Kamiya H, Kato T, Hasegawa H, Kameda Y (2019) Neonicotinoids disrupt aquatic food webs and decrease fishery yields. Science 366:620–623

    Article  CAS  Google Scholar 

  • Yates D, Adams EM, Angelo SE, Evers DC, Schmerfeld J, Moore MS, Kunz TH, Divoll T, Edmonds ST, Perkins C, Taylor R, O’Driscoll NJ (2014) Mercury in bats from the Northeastern United States. Ecotoxicology 23:45–55

    Article  CAS  Google Scholar 

  • Zukal J, Pikula J, Bandouchova H(2015) Bats as bioindicators of heavy metal pollution: History and prospect Mammal Biol 80:220–27

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank the anonymous reviewers and Riley Bernard for providing feedback that greatly improved the manuscript. CL was supported by the Nancy Gore Hunger Professorship in Environmental Studies at the University of Tennessee.

Author contributions

AC, EW, and CL developed the idea for and content of the review article. AC conducted literature searches and wrote the review article. AC, EW, and CL revised all versions of the article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Emma V. Willcox.

Ethics declarations

Conflict of interest

Although Christy Leppanen is an FDA/CTP employee, this work was not done as part of her official duties. This publication reflects the views of the author and should not be construed to reflect the FDA/CTP’s views or policies.

Consent to Publish

All authors consent to publication of this manuscript.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cable, A.B., Willcox, E.V. & Leppanen, C. Contaminant exposure as an additional stressor to bats affected by white-nose syndrome: current evidence and knowledge gaps. Ecotoxicology 31, 12–23 (2022). https://doi.org/10.1007/s10646-021-02475-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-021-02475-6

Keywords

Navigation