Title: Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore
Background: Exotic plant species represent a novel resource for invertebrates and many herbivorous insects have incorporated exotic plants into their diet. Using a new host plant can have physiological repercussions for these herbivores that may be beneficial or detrimental. In this study, we compared how using an exotic versus native host plant affected the immune system response and feeding efficiency of a specialist lepidopteran, the common buckeye ( Junonia coenia : Nymphalidae, Hübner 1822). Materials and Methods: In a lab experiment, larvae were reared on either the exotic host plant, Plantago lanceolata (Plantaginaceae), or the native host plant, Mimulus guttatus (Phrymaceae). Beginning at second instar feeding efficiency data were collected every 2 days until fifth instar when immune assays were performed. Immune assays consisted of standing phenoloxidase activity, total phenoloxidase activity, and melanization. Results: Interestingly, we found that all three immune system parameters were higher on the exotic host plant compared to the native host plant. The exotic host plant also supported higher pupal weights, faster development time, greater consumption, and more efficient approximate digestibility. In contrast, the native host plant supported higher efficiency of conversion of ingested and digested food. The relationship between immunity and feeding efficiency was more complex but showed a large positive effect of greater host plant consumption on all immune parameters, particularly for the exotic host plant. While not as strong, the efficiency of conversion of digested food tended to show a negative effect on the three immune parameters. Conclusion: Overall, the exotic host plant proved to be beneficial for this specialist insect with regard to immunity and many of the feeding efficiency parameters and continued use of this host plant is predicted for populations already using it. more »« less
Yoon, Su’ad A.; Harrison, Joshua G.; Smilanich, Angela M.; Forister, Matthew L.(
, Functional Ecology)
Abstract
Maternally transmitted microbes are ubiquitous. In insects, maternal microbes can play a role in mediating the insect immune response. Less is known about how ecological factors, such as resource use, interact with maternal microbes to affect immunity.
In the context of a recent colonization of a novel host plant by the Melissa blue butterflyLycaeides melissa, we investigated the interaction between host plant use and vertically transmitted, extracellular egg‐associated microbes in determining the strength of the insect immune response.
We reared larvae on two different host plant species: a native hostAstragalus canadensisand a novel hostMedicago sativa. Egg‐associated microbes were removed through a series of antimicrobial egg washes prior to hatching. Immune response was measured through three assays: standing phenoloxidase (PO), total PO and melanization.
We detected strong effects of microbial removal. Egg washing resulted in larvae with an increased immune response as measured by total PO—contrary to reports from other taxa. The effect of washing was especially strong for larvae consuming the native host plant.
This result may explain why consumption of the egg casing is not a universal behaviour in insects, due to negative effects on larval immunity.
Read the freePlain Language Summaryfor this article on the Journal blog.
Muchoney, Nadya D.; Bowers, M. Deane; Carper, Adrian L.; Mason, Peri A.; Teglas, Mike B.; Smilanich, Angela M.(
, Ecology and Evolution)
Abstract
Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly,Euphydryas phaeton(Nymphalidae), have recently incorporated an exotic plant,Plantago lanceolata(Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus,Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using eitherP.lanceolataor a native plant,Chelone glabra(Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.
Decker, Leslie E.; Jeffrey, Christopher S.; Ochsenrider, Kaitlin M.; Potts, Abigail S.; de Roode, Jacobus C.; Smilanich, Angela M.; Hunter, Mark D.; Ardia, ed., Daniel(
, Journal of Animal Ecology)
Abstract
Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterfliesDanaus plexippus, consistently experience infection by a virulent parasiteOphryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity.
We investigated plant‐mediated influences of elevated CO2(eCO2) on endogenous immune responses of monarch larvae to infection byO. elektroscirrha. Recently, transcriptomics have revealed that infection byO. elektroscirrhadoes not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2alter the balance between exogenous and endogenous sources of immunity remains unknown.
We fed monarchs two species of milkweed;A. curassavica(medicinal) andA. incarnata(non‐medicinal) grown under ambient CO2(aCO2) or eCO2. We then measured endogenous immune responses (phenoloxidase activity, haemocyte concentration and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions.
The melanization response of late‐instar larvae was reduced on medicinal milkweed in comparison to non‐medicinal milkweed. Moreover, the endogenous immune responses of early‐instar larvae to infection byO. elektroscirrhawere generally lower in larvae reared on foliage from aCO2plants and higher in larvae reared on foliage from eCO2plants. When grown under eCO2, milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2results in increased endogenous immune function.
Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.
Abstract An important goal of disease ecology is to understand trophic interactions influencing the host–pathogen relationship. This study focused on the effects of diet and immunity on the outcome of viral infection for the polyphagous butterfly, Vanessa cardui Linnaeus (Lepidoptera: Nymphalidae) (painted lady). Specifically, we aimed to understand the role that larval host plants play when fighting a viral pathogen. Larvae were orally inoculated with the entomopathogenic virus, Junonia coenia densovirus (JcDV) (Family Parvoviridae, subfamily Densovirinae, genus Protoambidensovirus, species Lepidopteran protoambidensovirus 1) and reared on two different host plants (Lupinus albifrons Bentham (Fabales: Fabaceae) or Plantago lanceolata Linnaeus (Lamiales: Plantaginaceae)). Following viral infection, the immune response (i.e., phenoloxidase [PO] activity), survival to adulthood, and viral load were measured for individuals on each host plant. We found that the interaction between the immune response and survival of the viral infection was host plant dependent. The likelihood of survival was lowest for infected larvae exhibiting suppressed PO activity and feeding on P. lanceolata, providing some evidence that PO activity may be an important defense against viral infection. However, for individuals reared on L. albifrons, the viral infection had a negligible effect on the immune response, and these individuals also had higher survival and lower viral load when infected with the pathogen compared to the controls. Therefore, we suggest that host plant modifies the effects of JcDV infection and influences caterpillars’ response when infected with the virus. Overall, we conclude that the outcome of viral infection is highly dependent upon diet, and that certain host plants can provide protection from pathogens regardless of immunity.
Hahn, Philip G.; Cammarano, Joseph H.(
, Journal of Applied Ecology)
Abstract
Crop diversification offers a promising solution to meet expanding global food demands while maintaining ecosystem services. Diversification strategies that use mixed planting to reduce pest damage (e.g. intercropping), termed ‘associational effects’ (AE) in the ecological literature, can decrease (associational resistance) or increase (associational susceptibility) herbivore abundance on a focal plant. While application of AE to agroecosystems typically reduces pest abundance, the range of outcomes varies widely.
We conducted a meta‐analysis using 272 estimates of insect herbivore abundance on crops neighbored by a conspecific or heterospecific from 44 studies undertaken on six continents. We focus on four agricultural crops well represented from sites across the globe to test hypotheses related to understanding how herbivore traits (diet breadth, feeding guild, origin), plant traits (crop type, phylogenetic distance to neighbour) and environmental context (climate, experimental design) contribute to variation in the outcomes of AE.
Overall, bicultures provided a strong reduction of insect abundance on the focal crop. Climate and interactions between herbivore traits, particularly diet breadth and origin, and plant traits or environmental context mediated the strength of AE.
Bicultures provided the strongest reductions in insect abundance at low latitudes, and this effect decreased at higher latitudes but only for insects with certain traits. Abundance of generalist herbivores and globally distributed pests tended to be most strongly negatively affected by bicultures, under certain contexts, whereas specialist herbivores and native pests were less affected by neighbours.
Synthesis and application. This meta‐analysis highlights that crop diversification schemes have an overall strongly beneficial effect of reducing pest abundance. However, there was also variability in the outcomes that is determined in part by the interactive effects of herbivore traits and environmental context. The results provide guidance for incorporating beneficial ecological interactions into integrated pest management strategies.
Mo, Carmen, and Smilanich, Angela M. Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore. Retrieved from https://par.nsf.gov/biblio/10454178. Frontiers in Physiology 14. Web. doi:10.3389/fphys.2023.1127670.
Mo, Carmen, & Smilanich, Angela M. Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore. Frontiers in Physiology, 14 (). Retrieved from https://par.nsf.gov/biblio/10454178. https://doi.org/10.3389/fphys.2023.1127670
Mo, Carmen, and Smilanich, Angela M.
"Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore". Frontiers in Physiology 14 (). Country unknown/Code not available. https://doi.org/10.3389/fphys.2023.1127670.https://par.nsf.gov/biblio/10454178.
@article{osti_10454178,
place = {Country unknown/Code not available},
title = {Feeding on an exotic host plant enhances plasma levels of phenoloxidase by modulating feeding efficiency in a specialist insect herbivore},
url = {https://par.nsf.gov/biblio/10454178},
DOI = {10.3389/fphys.2023.1127670},
abstractNote = {Background: Exotic plant species represent a novel resource for invertebrates and many herbivorous insects have incorporated exotic plants into their diet. Using a new host plant can have physiological repercussions for these herbivores that may be beneficial or detrimental. In this study, we compared how using an exotic versus native host plant affected the immune system response and feeding efficiency of a specialist lepidopteran, the common buckeye ( Junonia coenia : Nymphalidae, Hübner 1822). Materials and Methods: In a lab experiment, larvae were reared on either the exotic host plant, Plantago lanceolata (Plantaginaceae), or the native host plant, Mimulus guttatus (Phrymaceae). Beginning at second instar feeding efficiency data were collected every 2 days until fifth instar when immune assays were performed. Immune assays consisted of standing phenoloxidase activity, total phenoloxidase activity, and melanization. Results: Interestingly, we found that all three immune system parameters were higher on the exotic host plant compared to the native host plant. The exotic host plant also supported higher pupal weights, faster development time, greater consumption, and more efficient approximate digestibility. In contrast, the native host plant supported higher efficiency of conversion of ingested and digested food. The relationship between immunity and feeding efficiency was more complex but showed a large positive effect of greater host plant consumption on all immune parameters, particularly for the exotic host plant. While not as strong, the efficiency of conversion of digested food tended to show a negative effect on the three immune parameters. Conclusion: Overall, the exotic host plant proved to be beneficial for this specialist insect with regard to immunity and many of the feeding efficiency parameters and continued use of this host plant is predicted for populations already using it.},
journal = {Frontiers in Physiology},
volume = {14},
author = {Mo, Carmen and Smilanich, Angela M.},
}
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