Deltamethrin reduces survival of non-target small mammals
Amanda R. Goldberg
A * , Dean E. Biggins B , Shantini Ramakrishnan C , Jonathan W. Bowser B , Courtney J. Conway D , David A. Eads B and Jeffrey Wimsatt E
+ Author Affiliations
- Author Affiliations
A Department of Biology, Colorado State University, Fort Collins, CO 80523, USA.
B US Geological Survey, Fort Collins Science Center, Fort Collins, CO 80526, USA.
C Conservation Science Center, New Mexico Forest and Watershed Restoration Institute, New Mexico Highlands University, Las Vegas, NM 87701, USA.
D US Geological Survey, Idaho Cooperative Fish and Wildlife Research Unit, University of Idaho, Moscow, ID 83844, USA.
E Department of Medicine, West Virginia University, Morgantown, WV 26506, USA.
Wildlife Research 49(8) 698-708 https://doi.org/10.1071/WR21153
Submitted: 23 October 2021 Accepted: 28 February 2022 Published: 25 May 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
Context: Vector-borne diseases have caused global pandemics and were responsible for more human deaths than all other causes combined in prior centuries. In the past 60 years, prevention and control programs have helped reduce human mortality from vector-borne diseases, but impacts of those control programs on wildlife populations are not well documented. Insecticides are used to reduce vector-borne diseases in several critically endangered animal populations. Although insecticides are often effective at controlling targeted vectors, their effects on non-target species have rarely been examined.
Aims: To evaluate the impact of deltamethrin (an insecticide) on sympatric non-target species in areas affected by sylvatic plague, a lethal flea-borne zoonosis.
Methods: We compared flea control and the effect of deltamethrin application on survival of non-target small mammals (Peromyscus maniculatus, Chaetodipus hispidus, Microtus spp., and Reithrodontomys megalotis) at three study locations in South Dakota, Colorado, and Idaho, USA.
Key results: Deltamethrin treatments were more effective in reducing fleas on P. maniculatus and Microtus spp. than C. hispidus. Following burrow, nest, and bait-station applications of deltamethrin dust, apparent small mammal survival was greater for non-treatment animals than for flea-reduction animals. However, the magnitude of the difference between treated and non-treated animals differed among host species, study location, time interval, and treatment application method.
Conclusions: Our results suggest that considering the impact of deltamethrin on co-occurring non-target species before widespread application in future insecticide applications is warranted.
Implications: Insecticide application methods warrant consideration when designing plague management actions.
Keywords: Chaetodipus, conservation, fleas, insecticide, management, Microtus, non-target, Peromyscus, Reithrodontomys, rodents, survival, Yersinia pestis.
References
Akaike, H (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.| A new look at the statistical model identification.Crossref | GoogleScholarGoogle Scholar |
Anderson Jr, GW, Heath, DG, Bolt, CR, Welkos, SL, and Friedlander, AM (1998). Short-and long-term efficacy of single-dose subunit vaccines against Yersinia pestis in mice. The American Journal of Tropical Medicine and Hygiene 58, 793–799.
| Short-and long-term efficacy of single-dose subunit vaccines against Yersinia pestis in mice.Crossref | GoogleScholarGoogle Scholar |
Barnes, AM, Ogden, LJ, and Campos, EG (1972). Control of the plague vector, Opisocrostis hirsutus, by treatment of prairie dog (Cynomys ludovicianus) burrows with 2% carbaryl dust. Journal of Medical Entomology 9, 330–333.
| Control of the plague vector, Opisocrostis hirsutus, by treatment of prairie dog (Cynomys ludovicianus) burrows with 2% carbaryl dust.Crossref | GoogleScholarGoogle Scholar | 4626587PubMed |
Biggins, DE, and Eads, DA (2021). Utah prairie dog population dynamics on the Awapa Plateau: precipitation, elevation, and plague. Journal of Mammalogy 102, 1289–1297.
| Utah prairie dog population dynamics on the Awapa Plateau: precipitation, elevation, and plague.Crossref | GoogleScholarGoogle Scholar |
Biggins, DE, and Kosoy, MY (2001). Influences of introduced plague on North American mammals: implications from ecology of plague in Asia. Journal of Mammalogy 82, 906–916.
| Influences of introduced plague on North American mammals: implications from ecology of plague in Asia.Crossref | GoogleScholarGoogle Scholar |
Biggins, DE, Godbey, JL, Gage, KL, Carter, LG, and Montenieri, JA (2010). Vector control improves survival of three species of prairie dogs (Cynomys) in areas considered enzootic for plague. Vector-Borne and Zoonotic Diseases 10, 17–26.
| Vector control improves survival of three species of prairie dogs (Cynomys) in areas considered enzootic for plague.Crossref | GoogleScholarGoogle Scholar | 20158328PubMed |
Biggins, DE, Godbey, JL, and Eads, DA (2021a). Epizootic Plague in Prairie Dogs: Correlates and Control with Deltamethrin. Vector-Borne and Zoonotic Diseases 21, 172–178.
| Epizootic Plague in Prairie Dogs: Correlates and Control with Deltamethrin.Crossref | GoogleScholarGoogle Scholar | 33481692PubMed |
Biggins, DE, Ramakrishnan, S, Rocke, TE, Williamson, JL, and Wimsatt, J (2021b). Enzootic plague reduces survival of Mexican woodrats (Neotoma mexicana) in Colorado. Ecosphere 12, e03371.
| Enzootic plague reduces survival of Mexican woodrats (Neotoma mexicana) in Colorado.Crossref | GoogleScholarGoogle Scholar |
Bourguet D, Guillemaud T (2016) The hidden and external costs of pesticide use. In ‘Sustainable Agriculture Reviews, vol 19’. (Ed. E Lichtfouse) pp. 35–120. (Springer: Cham, Switzerland)
| Crossref |
Brander, SM, Gabler, MK, Fowler, NL, Connon, RE, and Schlenk, D (2016). Pyrethroid pesticides as endocrine disruptors: Molecular mechanisms in vertebrates with a focus on fishes. Environmental Science and Technology 50, 8977–8992.
| Pyrethroid pesticides as endocrine disruptors: Molecular mechanisms in vertebrates with a focus on fishes.Crossref | GoogleScholarGoogle Scholar | 27464030PubMed |
Bronson, LR, and Smith, CR (2002). Use of liquid deltamethrin in modified, host-targeted bait tubes for control of fleas on sciurid rodents in northern California. Journal of Vector Ecology 27, 55–62.
| 12125873PubMed |
Burnham, KP, Anderson, DR, and Huyvaert, KP (2011). AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.
| AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons.Crossref | GoogleScholarGoogle Scholar |
Colman, RE, Brinkerhoff, RJ, Busch, JD, Ray, C, Doyle, A, Sahl, JW, Keim, P, Collinge, SK, and Wagner, DM (2021). No evidence for enzootic plague within black-tailed prairie dog (Cynomys ludovicianus) populations. Integrative Zoology 16, 834–851.
| No evidence for enzootic plague within black-tailed prairie dog (Cynomys ludovicianus) populations.Crossref | GoogleScholarGoogle Scholar | 33882192PubMed |
Dombro LM (2016) Ecological effects of deltamethrin insecticide in prairie dog colonies of western South Dakota. Auburn University Auburn, AL, USA.
Eads, DA, and Biggins, DE (2015). Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America. Conservation Biology 29, 1086–1093.
| Plague bacterium as a transformer species in prairie dogs and the grasslands of western North America.Crossref | GoogleScholarGoogle Scholar | 25817984PubMed |
Eads, DA, and Biggins, DE (2019). Plague management of prairie dog colonies: degree and duration of deltamethrin flea control. Journal of Vector Ecology 44, 40–47.
| Plague management of prairie dog colonies: degree and duration of deltamethrin flea control.Crossref | GoogleScholarGoogle Scholar | 31124240PubMed |
Eads, DA, Biggins, DE, Doherty Jr, PF, Gage, KL, Huyvaert, KP, Long, DH, and Antolin, MF (2013). Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: an example with fleas on prairie dogs. International Journal for Parasitology: Parasites and Wildlife 2, 246–256.
| Using occupancy models to investigate the prevalence of ectoparasitic vectors on hosts: an example with fleas on prairie dogs.Crossref | GoogleScholarGoogle Scholar | 24533343PubMed |
Eads, DA, Biggins, DE, Bowser, J, McAllister, JC, Griebel, RL, Childers, E, Livieri, TM, Painter, C, Krank, LS, and Bly, K (2018). Resistance to deltamethrin in prairie dog (Cynomys ludovicianus) fleas in the field and in the laboratory. Journal of Wildlife Diseases 54, 745–754.
| Resistance to deltamethrin in prairie dog (Cynomys ludovicianus) fleas in the field and in the laboratory.Crossref | GoogleScholarGoogle Scholar | 29723100PubMed |
Eads, DA, Biggins, DE, and Gage, KL (2020). Ecology and management of plague in diverse communities of rodents and fleas. Vector-Borne and Zoonotic Diseases 20, 888–896.
| Ecology and management of plague in diverse communities of rodents and fleas.Crossref | GoogleScholarGoogle Scholar | 33074791PubMed |
Gage, KL, and Kosoy, MY (2005). Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology 50, 505–528.
| Natural history of plague: perspectives from more than a century of research.Crossref | GoogleScholarGoogle Scholar | 15471529PubMed |
Goldberg, AR, Conway, CJ, and Biggins, DE (2020). Flea sharing among sympatric rodent hosts: implications for potential plague effects on a threatened sciurid. Ecosphere 11, e93933.
| Flea sharing among sympatric rodent hosts: implications for potential plague effects on a threatened sciurid.Crossref | GoogleScholarGoogle Scholar |
Goldberg, AR, Conway, CJ, and Biggins, DE (2021a). Effects of experimental flea removal and plague vaccine treatments on survival of northern Idaho ground squirrels and two coexisting sciurids. Global Ecology and Conservation 26, e01489.
| Effects of experimental flea removal and plague vaccine treatments on survival of northern Idaho ground squirrels and two coexisting sciurids.Crossref | GoogleScholarGoogle Scholar |
Goldberg AR, Biggins DE, Ramakrishnan S, Bowser JW, Conway CJ, Eads DA, Wimsatt J (2021b) Effects of deltamethrin applications on non-target small mammal populations in South Dakota, Colorado, and Idaho, 2010–2017. U.S. Geological Survey data release.
Gregory, DA, Johnson, DL, and Thompson, BH (1993). The impact of bran baits treated with the insecticides carbaryl, chlorpyrifos and dimethoate on the survivorship and reproductive success of non-target mouse populations. Agriculture, Ecosystems & Environment 45, 95–103.
| The impact of bran baits treated with the insecticides carbaryl, chlorpyrifos and dimethoate on the survivorship and reproductive success of non-target mouse populations.Crossref | GoogleScholarGoogle Scholar |
Griffin, KA, Martin, DJ, Rosen, LE, Sirochman, MA, Walsh, DP, Wolfe, LL, and Miller, MW (2010). Detection of Yersinia pestis DNA in prairie dog–associated fleas by polymerase chain reaction assay of purified DNA. Journal of Wildlife Diseases 46, 636–643.
| Detection of Yersinia pestis DNA in prairie dog–associated fleas by polymerase chain reaction assay of purified DNA.Crossref | GoogleScholarGoogle Scholar | 20688665PubMed |
Heath, DG, Anderson Jr, GW, Mauro, JM, Welkos, SL, Andrews, GP, Adamovicz, J, and Friedlander, AM (1998). Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine. Vaccine 16, 1131–1137.
| Protection against experimental bubonic and pneumonic plague by a recombinant capsular F1-V antigen fusion protein vaccine.Crossref | GoogleScholarGoogle Scholar | 9682370PubMed |
Hoogland, JL, Davis, S, Benson-Amram, S, Labruna, D, Goossens, B, and Hoogland, MA (2004). Pyraperm kills fleas and halts plague among Utah prairie dogs. The Southwestern Naturalist 49, 376–383.
| Pyraperm kills fleas and halts plague among Utah prairie dogs.Crossref | GoogleScholarGoogle Scholar |
Hubbart, JA, Jachowski, DS, and Eads, DA (2011). Seasonal and among-site variation in the occurrence and abundance of fleas on California ground squirrels (Otospermophilus beecheyi). Journal of Vector Ecology 36, 117–123.
| Seasonal and among-site variation in the occurrence and abundance of fleas on California ground squirrels (Otospermophilus beecheyi).Crossref | GoogleScholarGoogle Scholar | 21635649PubMed |
Krasnov, BR, Burdelova, NV, Shenbrot, GI, and Khokhlova, IS (2002). Annual cycles of four flea species in the central Negev desert. Medical and Veterinary Entomology 16, 266–276.
| Annual cycles of four flea species in the central Negev desert.Crossref | GoogleScholarGoogle Scholar | 12243227PubMed |
Krasnov, BR, Spickett, A, Junker, K, Bugmyrin, SV, Ieshko, EP, Bespyatova, LA, Stanko, M, Khokhlova, IS, and Matthee, S (2021). Parasite counts or parasite incidences? Testing differences with four analyses of infracommunity modelling for seven parasite–host associations. Parasitology Research 120, 2569–2584.
| Parasite counts or parasite incidences? Testing differences with four analyses of infracommunity modelling for seven parasite–host associations.Crossref | GoogleScholarGoogle Scholar | 34137949PubMed |
Laake JL (2013) RMark: an R interface for analysis of capture-recapture data with MARK. Alaska Fisheries Science Centre processed report 2013-01. Alaska Fisheries Science Centre, Seattle, WA, USA.
Matchett, MR, Biggins, DE, Carlson, V, Powell, B, and Rocke, T (2010). Enzootic plague reduces black-footed ferret (Mustela nigripes) survival in Montana. Vector-Borne and Zoonotic Diseases 10, 27–35.
| Enzootic plague reduces black-footed ferret (Mustela nigripes) survival in Montana.Crossref | GoogleScholarGoogle Scholar | 20158329PubMed |
Matchett, MR, Stanley, TR, McCollister, MF, Eads, DA, Boulerice, JT, and Biggins, DE (2021). Oral Sylvatic Plague Vaccine Does Not Adequately Protect Prairie Dogs (Cynomys spp.) for Endangered Black-Footed Ferret (Mustela nigripes) Conservation. Vector-Borne and Zoonotic Diseases 21, 921–940.
| Oral Sylvatic Plague Vaccine Does Not Adequately Protect Prairie Dogs (Cynomys spp.) for Endangered Black-Footed Ferret (Mustela nigripes) Conservation.Crossref | GoogleScholarGoogle Scholar | 34757815PubMed |
Nieradko-Iwanicka, B, and Borzęcki, A (2015). Subacute poisoning of mice with deltamethrin produces memory impairment, reduced locomotor activity, liver damage and changes in blood morphology in the mechanism of oxidative stress. Pharmacological Reports 67, 535–541.
| Subacute poisoning of mice with deltamethrin produces memory impairment, reduced locomotor activity, liver damage and changes in blood morphology in the mechanism of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 25933966PubMed |
Ramakrishnan S (2017) Impact of enzootic plague on Neotoma mexicana in northern New Mexico. New Mexico Highlands University Las Vegas, NM, USA.
Rattner, BA, and Michael, SD (1985). Organophosphorus insecticide induced decrease in plasma luteinizing hormone concentration in white-footed mice. Toxicology Letters 24, 65–69.
| Organophosphorus insecticide induced decrease in plasma luteinizing hormone concentration in white-footed mice.Crossref | GoogleScholarGoogle Scholar | 3975930PubMed |
R Core Team (2017) ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at https://www.R-project.org
Rehman, H, Aziz, AT, Saggu, S, Abbas, ZK, Mohan, A, and Ansari, AA (2014). Systematic review on pyrethroid toxicity with special reference to deltamethrin. Journal of Entomology and Zoology Studies 2, 60–70.
Rocke, TE, Mencher, J, Smith, SR, Friedlander, AM, Andrews, GP, and Baeten, LA (2004). Recombinant F1-V fusion protein protects black-footed ferrets (Mustela nigripes) against virulent Yersinia pestis infection. Journal of Zoo and Wildlife Medicine 35, 142–146.
| Recombinant F1-V fusion protein protects black-footed ferrets (Mustela nigripes) against virulent Yersinia pestis infection.Crossref | GoogleScholarGoogle Scholar | 15305507PubMed |
Rocke, TE, Tripp, DW, Russell, RE, Abbott, RC, Richgels, KLD, Matchett, MR, Biggins, DE, Griebel, R, Schroeder, G, Grassel, SM, Pipkin, DR, Cordova, J, Kavalunas, A, Maxfield, B, Boulerice, J, and Miller, MW (2017). Sylvatic plague vaccine partially protects prairie dogs (Cynomys spp.) in field trials. Ecohealth 14, 438–450.
| Sylvatic plague vaccine partially protects prairie dogs (Cynomys spp.) in field trials.Crossref | GoogleScholarGoogle Scholar | 28643091PubMed |
Russell, RE, Tripp, DW, and Rocke, TE (2019). Differential plague susceptibility in species and populations of prairie dogs. Ecology and Evolution 9, 11962–11971.
| Differential plague susceptibility in species and populations of prairie dogs.Crossref | GoogleScholarGoogle Scholar | 31695901PubMed |
Sánchez-Bayo F (2011) Impacts of agricultural pesticides on terrestrial ecosystems. In ‘Ecological Impacts of Toxic Chemicals’. (Eds Sánchez-Bayo, PJ van den Brink, RM Mann) pp. 63–87. (Bentham Books: Sharjah, UAE)
| Crossref |
Seery, DB, Biggins, DE, Montenieri, JA, Enscore, RE, Tanda, DT, and Gage, KL (2003). Treatment of black-tailed prairie dog burrows with deltamethrin to control fleas (Insecta: Siphonaptera) and plague. Journal of Medical Entomology 40, 718–722.
| Treatment of black-tailed prairie dog burrows with deltamethrin to control fleas (Insecta: Siphonaptera) and plague.Crossref | GoogleScholarGoogle Scholar | 14596288PubMed |
Sheffield, SR, and Lochmiller, RL (2001). Effects of field exposure to diazinon on small mammals inhabiting a semienclosed prairie grassland ecosystem. I. Ecological and reproductive effects. Environmental Toxicology and Chemistry: An International Journal 20, 284–296.
| Effects of field exposure to diazinon on small mammals inhabiting a semienclosed prairie grassland ecosystem. I. Ecological and reproductive effects.Crossref | GoogleScholarGoogle Scholar |
Tripp, DW, Gage, KL, Montenieri, JA, and Antolin, MF (2009). Flea abundance on black-tailed prairie dogs (Cynomys ludovicianus) increases during plague epizootics. Vector-Borne and Zoonotic Diseases 9, 313–321.
| Flea abundance on black-tailed prairie dogs (Cynomys ludovicianus) increases during plague epizootics.Crossref | GoogleScholarGoogle Scholar | 19492944PubMed |
Tripp, DW, Streich, SP, Sack, DA, Martin, DJ, Griffin, KA, and Miller, MW (2016). Season of deltamethrin application affects flea and plague control in white-tailed prairie dog (Cynomys leucurus) colonies, Colorado, USA. Journal of Wildlife Diseases 52, 553–561.
| Season of deltamethrin application affects flea and plague control in white-tailed prairie dog (Cynomys leucurus) colonies, Colorado, USA.Crossref | GoogleScholarGoogle Scholar | 27195680PubMed |
Tripp, DW, Rocke, TE, Runge, JP, Abbott, RC, and Miller, MW (2017). Burrow dusting or oral vaccination prevents plague-associated prairie dog colony collapse. EcoHealth 14, 451–462.
| Burrow dusting or oral vaccination prevents plague-associated prairie dog colony collapse.Crossref | GoogleScholarGoogle Scholar | 28643090PubMed |
(2021). Endangered and threatened wildlife and plants; endangered species status for the Peñasco least chipmunk and designation of critical habitat. Federal Register 86, 54584–53609.
van den Berg, H, Zaim, M, Yadav, RS, Soares, A, Ameneshewa, B, Mnzava, A, Hii, J, Dash, AP, and Ejov, M (2012). Global trends in the use of insecticides to control vector-borne diseases. Environmental Health Perspectives 120, 577–582.
| Global trends in the use of insecticides to control vector-borne diseases.Crossref | GoogleScholarGoogle Scholar | 22251458PubMed |
White, GC, and Burnham, KP (1999). Program MARK: survival estimation from populations of marked animals. Bird Study 46, S120–S139.
| Program MARK: survival estimation from populations of marked animals.Crossref | GoogleScholarGoogle Scholar |
