Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides

In natural habitats, there is a strong evolutionary selection pressure on herbivorous insects to avoid danger and choose suitable host plants. Similar selection pressures may drive movement and choices of oviposition hosts by herbivorous insects living in agricultural cropping systems, in which inse...

Full description

Bibliographic Details
Main Authors: Purushottam Gyawali, Heather Kim, Delaney Ruth Vance, Haleh Khodaverdi, Anil Mantri, Christian Nansen
Format: Article
Language:English
Published: MDPI AG 2023-03-01
Series:Agriculture
Subjects:
Online Access:https://www.mdpi.com/2077-0472/13/3/723
_version_ 1797614046656069632
author Purushottam Gyawali
Heather Kim
Delaney Ruth Vance
Haleh Khodaverdi
Anil Mantri
Christian Nansen
author_facet Purushottam Gyawali
Heather Kim
Delaney Ruth Vance
Haleh Khodaverdi
Anil Mantri
Christian Nansen
author_sort Purushottam Gyawali
collection DOAJ
description In natural habitats, there is a strong evolutionary selection pressure on herbivorous insects to avoid danger and choose suitable host plants. Similar selection pressures may drive movement and choices of oviposition hosts by herbivorous insects living in agricultural cropping systems, in which insecticides are often used. In this study, we quantified movement responses and nymph emergence (collectively referred to as bio-responses) of western-tarnished plant bug (<i>Lygus hesperus</i> Knight (Hemiptera: Miridae)) individuals when exposed to environments associated with a perceived “risk” (experimental insecticide treatments and their corresponding controls). We introduce a novel analytical approach in which treatments (risk environments) are ranked in ascending order based on bio-responses (movement or nymph emergence). Consequently, linear regression coefficients were generated and used to interpret bio-responses of <i>Lygus</i> individuals in different life stages to risk environments. Initially, we predicted movement by <i>Lygus</i> individuals to be positively associated with environmental risk and nymph emergence to be negatively associated with environmental risk. Overall, based on a comprehensive combination of no- and two-choice bioassays, we found that: (1) In no-choice bioassays, movement parameters (both total distance moved and movement percentage) by all three life stages were lowest in low-risk environments and highest when <i>Lygus</i> individuals were exposed to either malathion or Grandevo. Accordingly, environments involving malathion or Grandevo were considered high-risk. (2) No-choice movement bioassays also revealed that <i>Lygus</i> males moved significantly more (based on comparison of regression intercepts) than other life stages, and that they responded significantly more (based on comparison of regression slopes) than conspecific females and nymphs. (3) In two-choice movement bioassays, neem elicited the most consistent movement responses by <i>Lygus</i> individuals, and adult life stages showed the strongest response. Two-choice movement bioassays also revealed that <i>Lygus</i> adults, compared to nymphs, were more likely to spend time in low-risk areas of the test arenas. (4) Nymph emergence was markedly lower in no-choice compared to two-choice bioassays, and in two-choice bioassays, Grandevo and malathion elicited especially biased nymph emergence from low-risk beans. To our knowledge, this is the first study in which movement bioassays have been used to quantify and characterize behavioral responses by <i>Lygus</i> life stages to environments associated with varying degrees of risk. The novel analytical approach presented in this study provides a high degree of complementarity to more traditional performance-testing methods used to evaluate responses to insecticides. Furthermore, we believe that this analytical approach can be of considerable relevance to studies of animal phenomics and behavioral studies of animals more broadly, in which adaptation and fitness parameters are examined in response to environmental risk and heterogeneity.
first_indexed 2024-03-11T07:04:07Z
format Article
id doaj.art-09a7c093627a4fecb3c1421452c99f3c
institution Directory Open Access Journal
issn 2077-0472
language English
last_indexed 2024-03-11T07:04:07Z
publishDate 2023-03-01
publisher MDPI AG
record_format Article
series Agriculture
spelling doaj.art-09a7c093627a4fecb3c1421452c99f3c2023-11-17T09:02:37ZengMDPI AGAgriculture2077-04722023-03-0113372310.3390/agriculture13030723Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to InsecticidesPurushottam Gyawali0Heather Kim1Delaney Ruth Vance2Haleh Khodaverdi3Anil Mantri4Christian Nansen5Department of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USADepartment of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USADepartment of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USADepartment of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USADepartment of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USADepartment of Entomology and Nematology, University of California, Davis, One Shields Avenue, Davis, CA 95616, USAIn natural habitats, there is a strong evolutionary selection pressure on herbivorous insects to avoid danger and choose suitable host plants. Similar selection pressures may drive movement and choices of oviposition hosts by herbivorous insects living in agricultural cropping systems, in which insecticides are often used. In this study, we quantified movement responses and nymph emergence (collectively referred to as bio-responses) of western-tarnished plant bug (<i>Lygus hesperus</i> Knight (Hemiptera: Miridae)) individuals when exposed to environments associated with a perceived “risk” (experimental insecticide treatments and their corresponding controls). We introduce a novel analytical approach in which treatments (risk environments) are ranked in ascending order based on bio-responses (movement or nymph emergence). Consequently, linear regression coefficients were generated and used to interpret bio-responses of <i>Lygus</i> individuals in different life stages to risk environments. Initially, we predicted movement by <i>Lygus</i> individuals to be positively associated with environmental risk and nymph emergence to be negatively associated with environmental risk. Overall, based on a comprehensive combination of no- and two-choice bioassays, we found that: (1) In no-choice bioassays, movement parameters (both total distance moved and movement percentage) by all three life stages were lowest in low-risk environments and highest when <i>Lygus</i> individuals were exposed to either malathion or Grandevo. Accordingly, environments involving malathion or Grandevo were considered high-risk. (2) No-choice movement bioassays also revealed that <i>Lygus</i> males moved significantly more (based on comparison of regression intercepts) than other life stages, and that they responded significantly more (based on comparison of regression slopes) than conspecific females and nymphs. (3) In two-choice movement bioassays, neem elicited the most consistent movement responses by <i>Lygus</i> individuals, and adult life stages showed the strongest response. Two-choice movement bioassays also revealed that <i>Lygus</i> adults, compared to nymphs, were more likely to spend time in low-risk areas of the test arenas. (4) Nymph emergence was markedly lower in no-choice compared to two-choice bioassays, and in two-choice bioassays, Grandevo and malathion elicited especially biased nymph emergence from low-risk beans. To our knowledge, this is the first study in which movement bioassays have been used to quantify and characterize behavioral responses by <i>Lygus</i> life stages to environments associated with varying degrees of risk. The novel analytical approach presented in this study provides a high degree of complementarity to more traditional performance-testing methods used to evaluate responses to insecticides. Furthermore, we believe that this analytical approach can be of considerable relevance to studies of animal phenomics and behavioral studies of animals more broadly, in which adaptation and fitness parameters are examined in response to environmental risk and heterogeneity.https://www.mdpi.com/2077-0472/13/3/723host selection<i>Lygus hesperus</i>preferenceavoidanceinsect behavior
spellingShingle Purushottam Gyawali
Heather Kim
Delaney Ruth Vance
Haleh Khodaverdi
Anil Mantri
Christian Nansen
Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
Agriculture
host selection
<i>Lygus hesperus</i>
preference
avoidance
insect behavior
title Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
title_full Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
title_fullStr Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
title_full_unstemmed Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
title_short Can Insects Assess Environmental Risk? Movement Responses and Nymph Emergence in Response to Insecticides
title_sort can insects assess environmental risk movement responses and nymph emergence in response to insecticides
topic host selection
<i>Lygus hesperus</i>
preference
avoidance
insect behavior
url https://www.mdpi.com/2077-0472/13/3/723
work_keys_str_mv AT purushottamgyawali caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides
AT heatherkim caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides
AT delaneyruthvance caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides
AT halehkhodaverdi caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides
AT anilmantri caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides
AT christiannansen caninsectsassessenvironmentalriskmovementresponsesandnymphemergenceinresponsetoinsecticides