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Timing of sub-lethal insecticide exposure determines parasite establishment success in an insect-helminth model

Published online by Cambridge University Press:  07 October 2019

Suraj Dhakal Open the ORCID record for Suraj Dhakal [Opens in a new window] ,
Nicolai Vitt Meyling ,
Kathrine Eggers Pedersen ,
Nina Cedergreen  and
Brian Lund Fredensborg
Suraj Dhakal*
Affiliation:
Section for Organismal Biology, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
Nicolai Vitt Meyling
Affiliation:
Section for Organismal Biology, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
Kathrine Eggers Pedersen
Affiliation:
Section for Environmental Chemistry and Physics, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871Frederiksberg C, Denmark
Nina Cedergreen
Affiliation:
Section for Environmental Chemistry and Physics, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871Frederiksberg C, Denmark
Brian Lund Fredensborg
Affiliation:
Section for Organismal Biology, Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen, Thorvaldsensvej 40, 1871 Frederiksberg C, Denmark
*
Author for correspondence: Suraj Dhakal, E-mail: sura@plen.ku.dk
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Abstract

Environmental toxicants are pervasive in nature, but sub-lethal effects on non-target organisms and their parasites are often overlooked. Particularly, studies on terrestrial hosts and their parasites exposed to agricultural toxicants are lacking. Here, we studied the effect of sequence and timing of sub-lethal exposures of the pyrethroid insecticide alpha-cypermethrin on parasite establishment using the tapeworm Hymenolepis diminuta and its intermediate insect host Tenebrio molitor as a model system. We exposed T. molitor to alpha-cypermethrin (LD20) before and after experimental H. diminuta infection and measured the establishment success of larval tapeworms. Also, we conducted in vitro studies quantifying the direct effect of the insecticide on parasite viability. Our results showed that there was no direct lethal effect of alpha-cypermethrin on H. diminuta cysticercoids at relevant concentrations (LD10 to LD90 of the intermediate host). However, we observed a significantly increased establishment of H. diminuta in beetles exposed to alpha-cypermethrin (LD20) after parasite infection. In contrast, parasite establishment was significantly lower in beetles exposed to the insecticide before parasite infection. Thus, our results indicate that environmental toxicants potentially impact host-parasite interactions in terrestrial systems, but that the outcome is context-dependent by enhancing or reducing parasite establishment depending on timing and sequence of exposure.

Keywords

Exposure timinginsecticidemultiple stressorsparasitesub-lethal effects
Type
Research Article
Information
Parasitology , Volume 147 , Issue 1 , January 2020 , pp. 120 - 125
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Copyright
Copyright © Cambridge University Press 2019

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References

Alaux, C, Brunet, JL, Dussaubat, C, Mondet, F, Tchamitchan, S, Cousin, M, Brillard, J, Baldy, A, Belzunces, LP and Le Conte, Y (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environmental Microbiology 12, 774–782.CrossRefGoogle Scholar
Bradbury, SP and Coats, JR (1989) Comparative toxicology of the pyrethroid insecticides. In Ware, GW (ed.), Reviews of Environmental Contamination and Toxicology. New York, NY: Springer New York, pp. 133–177.CrossRefGoogle Scholar
Burt, MDB (1980) Aspects of the life history and systematics of Hymenolepis diminuta. In Arai, HP (ed.), Biology of the Tapeworm Hymenolepis Diminuta. United States: Academic Press, pp. 1–57.Google Scholar
Chin, HMH, Luong, LT and Shostak, AW (2017) Longitudinal study of parasite-induced mortality of a long-lived host: the importance of exposure to non-parasitic stressors. Parasitology 144, 1943–1955.CrossRefGoogle ScholarPubMed
Crofton, HD (1971) A quantitative approach to parasitism. Parasitology 62, 179–193.CrossRefGoogle Scholar
Dhakal, S, Meyling, NV, Williams, AR, Mueller-Harvey, I, Fryganas, C, Kapel, CMO and Fredensborg, BL (2015) Efficacy of condensed tannins against larval Hymenolepis diminuta (Cestoda) in vitro and in the intermediate host Tenebrio molitor (Coleoptera) in vivo. Veterinary Parasitology 207, 49–55.CrossRefGoogle ScholarPubMed
Dhakal, S, Micki Buss, S, Cassidy, EJ, Meyling, NV and Fredensborg, BL (2018) Establishment success of the beetle tapeworm Hymenolepis diminuta depends on dose and host body condition. Insects 9, 14.CrossRefGoogle ScholarPubMed
Doublet, V, Labarussias, M, Miranda, JR, Moritz, RFA and Paxton, RJ (2015) Bees under stress: sublethal doses of a neonicotinoid pesticide and pathogens interact to elevate honey bee mortality across the life cycle. Environmental Microbiology 17, 969–983.CrossRefGoogle ScholarPubMed
Furlong, MJ and Groden, E (2001) Evaluation of synergistic interactions between the Colorado potato beetle (Coleoptera: Chrysomelidae) pathogen Beauveria bassiana and the insecticides, imidacloprid, and cyromazine. Journal of Economic Entomology 94, 344–356.CrossRefGoogle ScholarPubMed
Goodchild, CG and Davis, BO (1972) Hymenolepis microstoma cysticercoid activation and excystation in vitro (Cestoda). The Journal of Parasitology 58, 735–741.CrossRefGoogle Scholar
Goulson, D (2013) REVIEW: an overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology 50, 977–987.CrossRefGoogle Scholar
Goulson, D (2014) Pesticides linked to bird declines. Nature 511, 295.CrossRefGoogle ScholarPubMed
Goulson, D, Nicholls, E, Botías, C and Rotheray, EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957.CrossRefGoogle ScholarPubMed
Guedes, RNC, Smagghe, G, Stark, JD and Desneux, N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annual Review of Entomology 61, 43–62.CrossRefGoogle ScholarPubMed
Hua, J, Buss, N, Kim, J, Orlofske, SA and Hoverman, JT (2016) Population-specific toxicity of six insecticides to the trematode Echinoparyphium sp. Parasitology 143, 542–550.CrossRefGoogle ScholarPubMed
IUPAC (2019) International union of pure and applied chemistry website. Available at https://sitem.herts.ac.uk/aeru/iupac/atoz.htm (Accessed 17 May 2019).Google Scholar
James, RR and Xu, J (2012) Mechanisms by which pesticides affect insect immunity. Journal of Invertebrate Pathology 109, 175–182.CrossRefGoogle ScholarPubMed
Jiang, X, Wang, Z, He, Q, Liu, Q, Li, X, Yu, L and Cao, H (2018) The effect of neonicotinoid insecticide and fungicide on sugar responsiveness and orientation behavior of honey bee (Apis mellifera) in semi field conditions. Insects 9, 130.CrossRefGoogle Scholar
Lackie, AM (1976) Evasion of the haemocytic defence reaction of certain insects by larvae of Hymenolepis diminuta (Cestoda). Parasitology 73, 97–107.CrossRefGoogle Scholar
Lalouette, L, Pottier, MA, Wycke, MA, Boitard, C, Bozzolan, F, Maria, A, Demondion, E, Chertemps, T, Lucas, P, Renault, D, Maibeche, M, Siaussat, DJES and Research, P (2016) Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environmental Science and Pollution Research 23, 3073–3085.CrossRefGoogle Scholar
Lethbridge, RC (1971) The hatching of Hymenolepis diminuta eggs and penetration of the hexacanths in Tenebrio molitor beetles. Parasitology 62, 445–456.CrossRefGoogle ScholarPubMed
Meyling, NV, Arthur, S, Pedersen, KE, Dhakal, S, Cedergreen, N and 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 Management Science 74, 2488–2495.CrossRefGoogle ScholarPubMed
Müller, T, Prosche, A and Müller, C (2017) Sublethal insecticide exposure affects reproduction, chemical phenotype as well as offspring development and antennae symmetry of a leaf beetle. Environmental Pollution 230, 709–717.CrossRefGoogle ScholarPubMed
O'Neal, ST, Anderson, TD and Wu-Smart, JY (2018) Interactions between pesticides and pathogen susceptibility in honey bees. Current Opinion in Insect Science 26, 57–62.CrossRefGoogle ScholarPubMed
Pettis, JS, vanEngelsdorp, D, Johnson, J and Dively, G (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99, 153–158.CrossRefGoogle ScholarPubMed
Pimentel, D (2009) Environmental and economic costs of the application of pesticides primarily in the United States. In Peshin, R, Dhawan, AK (eds), Integrated Pest Management: Innovation-Development Process: Volume 1. Dordrecht: Springer Netherlands, pp. 89–111.CrossRefGoogle Scholar
Pochini, KM and Hoverman, JT (2017) Reciprocal effects of pesticides and pathogens on amphibian hosts: the importance of exposure order and timing. Environmental Pollution 221, 359–366.CrossRefGoogle Scholar
Ratnieks, FLW and Carreck, NL (2010) Clarity on honey bee collapse? Science 327, 152.CrossRefGoogle ScholarPubMed
Raymann, K, Motta, EVS, Girard, C, Riddington, IM, Dinser, JA and Moran, NA (2018) Imidacloprid decreases honey bee survival rates but does not affect the gut microbiome. Applied and Environmental Microbiology 84, e00545–e00518.CrossRefGoogle Scholar
Rohr, JR, Raffel, TR, Sessions, SK and Hudson, PJ (2008) Understanding the net effects of pesticides on amphibian trematode infections. Ecological Applications 18, 1743–1753.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P (2005) Evolutionary ecology of insect immune defenses. Annual Reiview of Entomology 50, 529–551.CrossRefGoogle ScholarPubMed
Seid, AM, Fredensborg, BL, Steinwender, BM and Meyling, NV (2019) Temperature-dependent germination, growth and co-infection of Beauveria spp. isolates from different climatic regions. Biocontrol Science and Technology 29, 411–426.CrossRefGoogle Scholar
Shostak, AW (2012) Sequential and concurrent exposure of flour beetles (Tribolium confusum) to tapeworms (Hymenolepis diminuta) and pesticide (diatomaceous earth). Journal of Parasitology 98, 453–459.CrossRefGoogle Scholar
Shostak, AW (2014) Hymenolepis diminuta infections in Tenebrionid beetles as a model system for ecological interactions between helminth parasites and terrestrial intermediate hosts: a review and meta-analysis. Journal of Parasitology 100, 46–58.CrossRefGoogle ScholarPubMed
Shostak, AW, Van Buuren, KG and Cook, R (2015) Response of flour beetles to multiple stressors of parasitic (Hymenolepis diminuta), environmental (Diatomaceous Earth), and host (reproduction) origin. The Journal of Parasitology 101, 405–417.CrossRefGoogle ScholarPubMed
Soderlund, DM (2010) Toxicology and mode of action of pyrethroid insecticides. In Krieger, R (ed.), Hayes' Handbook of Pesticide Toxicology, 3rd Edn.New York: Academic Press, pp. 1665–1686.CrossRefGoogle Scholar