Manduca sexta experience high parasitoid pressures in the field but minor fitness costs of consuming plant secondary compounds

1. Plant‐herbivore coevolutionary interactions have led to a range of plant defenses that minimize insect damage and a suite of counter adaptations that allow herbivores to feed on defended plants. Consuming plant secondary compounds results in herbivore growth and developmental costs but can have beneficial effects such as deterrence or harm of parasitoid enemies. Therefore, the role of secondary compounds on herbivore fitness must be considered in the context of the abundance and level of harm from natural enemies and the costs herbivores incur feeding on plant secondary compounds.
2. In this study, I combined field measurements of Cotesia congregata wasp parasitism pressure with detailed measurements of the costs of plant secondary compounds across developmental stages in the herbivore host, Manduca sexta.
3. I show that C. congregata parasitoids exert large negative selective pressures, killing 31%–57% of M. sexta larvae in the field. Manduca sexta developed fastest during instars most at risk for parasitoid oviposition but growth was slowed by consumption of plant secondary compounds. The negative effects of consuming plant secondary compounds as larvae influenced adult size traits but there were no immune, survival, or fecundity costs.
4. These results suggest that developmental costs experienced by M. sexta herbivores consuming defensive compounds are minor in comparison to the strong negative survival pressures from abundant parasitoid enemies.

     

Trichobaris weevils distinguish amongst toxic host plants by sensing volatiles that do not affect larval performance

Herbivorous insects use plant metabolites to inform their host plant selection for oviposition. These host‐selection behaviours are often consistent with the preference–performance hypothesis; females oviposit on hosts that maximize the performance of their offspring. However, the metabolites used for these oviposition choices and those responsible for differences in offspring performance remain unknown for ecologically relevant interactions. Here, we examined the host‐selection behaviours of two sympatric weevils, the Datura (Trichobaris compacta) and tobacco (T. mucorea) weevils in field and glasshouse experiments with transgenic host plants specifically altered in different components of their secondary metabolism. Adult females of both species strongly preferred to feed on D. wrightii rather than on N. attenuata leaves, but T. mucorea preferred to oviposit on N. attenuata, while T. compacta oviposited only on D. wrightii. These oviposition behaviours increased offspring performance: T. compacta larvae only survived in D. wrightii stems and T. mucorea larvae survived better in N. attenuata than in D. wrightii stems. Choice assays with nicotine‐free, JA‐impaired, and sesquiterpene‐over‐produced isogenic N. attenuata plants revealed that although half of the T. compacta larvae survived in nicotine‐free N. attenuata lines, nicotine did not influence the oviposition behaviours of both the nicotine‐adapted and nicotine‐sensitive species. JA‐induced sesquiterpene volatiles are key compounds influencing T. mucorea females’ oviposition choices, but these sesquiterpenes had no effect on larval performance. We conclude that adult females are able to choose the best host plant for their offspring and use chemicals different from those that influence larval performance to inform their oviposition decisions.     

Linkages between nectaring and oviposition preferences of Manduca sexta on two co‐blooming Datura species in the Sonoran Desert

1. The oviposition choices of phytophagous insects determine the environment that their offspring will experience, affecting both larval performance and host plant fitness. These choices, however, may be influenced by other activities, such as nectar foraging. 2. In the Sonoran Desert, Manduca sexta (Lepidoptera: Sphingidae) oviposits primarily on the perennial herb Datura wrightii. It has been reported to oviposit on the smaller‐flowered, co‐blooming, sympatric annual Datura discolor as well. Datura is also M. sexta's most important source of nectar in this region. Nectaring and oviposition decisions thus determine M. sexta's reproductive success, as well as the relative benefits (pollination) and costs (herbivory) that each Datura species derives from this interaction. 3. The nectaring and oviposition choices of adult M. sexta on these congeners were studied to investigate how nectar foraging influences oviposition. Larval performance on the two hosts was then assessed. 4. Nectaring and oviposition were behaviourally linked, with M. sexta preferring the perennial D. wrightii as both a nectar source and larval host when given a choice between the two species. This preference disappeared, however, when only D. discolor bore flowers. 5. In the laboratory, larvae developed at equal rates when fed D. wrightii or D. discolor leaves, but survival was higher on D. wrightii when larvae fed on intact plants. 6. These findings suggest that while female preferences match larval performance in most cases, the link between nectaring and oviposition may at times bias moths to lay eggs on inferior larval hosts.     

The effects of the alkaloid scopolamine on the performance and behavior of two caterpillar species

Plants have evolved many defenses against insect herbivores, including numerous chemicals that can reduce herbivore growth, performance, and fitness. One group of chemicals, the tropane alkaloids, is commonly found in the nightshade family (Solanaceae) and has been thought to reduce performance and fitness in insects. We examined the effects of the tropane alkaloid scopolamine, an alkaloid constituent of Datura wrightii, which is the most frequent host plant for the abundant and widespread insect herbivore Manduca sexta in the southwestern United States. We exposed caterpillars of two different species to scopolamine: M. sexta, which has a shared evolutionary history with Datura and other solanaceous plants, and Galleria mellonella, which does not. We showed that the addition of ecologically realistic levels of scopolamine to both the diet and the hemolymph of these two caterpillar species (M. sexta and G. mellonella) had no effect on the growth of either species. We also showed that M. sexta has no behavioral preference for or against scopolamine incorporated into an artificial diet. These results are contrary to other work showing marked differences in performance for other insect species when exposed to scopolamine, and provide evidence that scopolamine might not provide the broad-spectrum herbivore resistance typically attributed to it. It also helps to clarify the coevolutionary relationship between M. sexta and one of its main host plants, as well as the physiological mechanism of resistance against scopolamine.     

Plant volatiles and density-dependent conspecific female odors are used by Asian citrus psyllid to evaluate host suitability on a spatial scale

We investigated how chemical cues derived from female Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) and their host plants affect host acceptance choices by conspecifics. In four-choice cage and two-choice olfactometer assays, female psyllids avoided conspecific female cues in a density-dependent manner. However, odors from citrus plants actively damaged by psyllid feeding were attractive to conspecific females. When odors from feeding-damaged plants were presented simultaneously with odors from female D. citri, attraction of female conspecifics was no longer observed as compared with a clean air control in olfactometer assays. In subsequent experiments, D. citri females were released within arenas that contained actively feeding-damaged or non-damaged (control) citrus plants, each with previously psyllid-infested and uninfested young leaves. D. citri development is linked to the presence of these newly emerging leaves which is the only site of nymphal development. Female D. citri were initially attracted by the actively damaged plants as compared with non-damaged controls. After acceptance of plants that were actively damaged by feeding, D. citri females preferentially chose and settled on uninfested young leaves as compared with previously infested young leaves. A herbivore-induced plant volatile attractant and a female-specific odor repellent appear to be complementary foraging cues providing psyllids with information at two spatial scales: (1) the whole plant level for choosing a plant potentially harboring male conspecifics for mating, and (2) the within plant level to reduce intra-conspecific competition by identifying previously exploited resources.     

Behavioral evidence for contextual olfactory‐mediated avoidance of the ubiquitous phytopathogen Botrytis cinerea by Drosophila suzukii

Herbivorous insects may benefit from avoiding the smell produced by phytopathogens infecting plant host tissue if the infected tissue reduces insect fitness. However, in many cases the same species of phytopathogen can also infect host plant tissues that do not directly affect herbivore fitness. Thus, insects may benefit from differentiating between pathogen odors emanating from food and nonfood tissues. This is based on the hypothesis that unnecessarily staying attentive to pathogen odor from nonfood tissue may incur opportunity costs associated with not responding to other important survival functions. In this study adults of Drosophila suzukii Matsumura, an invasive larval frugivore, showed reduced attraction to the odor of raspberry fruit, a food tissue, when infected with Botrytis cinerea Pers., a ubiquitous phytopathogen, in favor of odors of uninfected raspberry fruit. Moreover, D. suzukii oviposited fewer eggs on infected raspberry fruit relative to uninfected raspberry fruit. Larval survival and adult size after eclosion were significantly reduced when reared on B. cinerea‐infected raspberry relative to uninfected fruit. Interestingly, when the behavioral choice experiment was repeated using Botrytis‐infected vs. ‐uninfected strawberry leaves, a nonfood tissue, in combination with fresh raspberry fruit, odor from B. cinerea‐infected leaves did not reduce D. suzukii attraction to raspberries relative to raspberries with uninfected leaves. These behavioral results illustrate the important role context can play in odor‐mediated interactions between insects, plants and microbes. We discuss implications of our findings for developing a repellent that can be useful for the management of D. suzukii.     

Lipoxygenase-mediated modification of insect elicitors: Generating chemical diversity on the leaf wound surface

Plants can distinguish mechanical damage from larval folivory through the recognition of specific constituents of larval oral secretions (OS) which are deposited on the surface of leaf wounds during feeding. Fatty acid-amino acid conjugates (FACs) are major constituents of the OS of Lepidopteran larvae and they are strong elicitors of herbivore-induced defense responses in several plant species, including the wild tobacco Nicotiana attenuata. When OS from Manduca sexta larvae is deposited on N. attenuata wounded leaves, the major FAC N-linolenoyl-glutamic acid (18:3-Glu) is modified within seconds by a heat labile process. Some of the major modified forms are oxygenated products derived from 13-lipoxygenase activity and one of these derivatives, 13-oxo-13:2-Glu, is an active elicitor of enhanced JA biosynthesis and differential monoterpene emission in N. attenuata leaves.Key words: lipoxygenase, plant-insect interactions, fatty acid-amino acid conjugates, FAC, fatty acid-amides, insect elicitor, jasmonic acid, volatiles, herbivore-associated-elicitors, HAEs     

The nutritional landscape of host plants for a specialist insect herbivore

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Fitness consequences of host plant choice: a field experiment

Determining the relative contributions of different ecological factors for herbivore fitness is one key to understanding the ecology and evolution of host plant choice by herbivores. Natural enemies are increasingly being recognized as an important factor: host plants of inferior quality for development may still be used by herbivores if they provide enemy‐free space (EFS). Here we used the tobacco hornworm, Manduca sexta, to experimentally disentangle the effects of natural enemies from the potentially confounding factors of host plant quality, competition and microhabitat. We explored the consequences for both individual components of fitness and total fitness of M. sexta feeding on a typical high quality host plant, tobacco Nicotiana tabacum and a novel, low quality host plant, devil's claw Proboscidea louisianica in an experimental field environment in the presence of a parasitoid natural enemy, Cotesia congregata. Although early larval survival, development and growth rates, final body size and fecundity were all reduced for M. sexta feeding on devil's claw, a high rate of parasitism on tobacco and an absence of parasitism on devil's claw contributed to similar total fitness (net reproductive rate, R₀) across the two host plant species. Our results suggest M. sexta has adopted a novel host plant (devil's claw) outside its typical host range because this host plant provides enemy free space. In addition, oviposition behavior of adult female M. sexta appears to be well suited to exploiting the enemy‐free space on devil's claw; oviposition by M. sexta on devil's claw appears to correspond with seasonal variation in parasitoid abundance.     

Multimodal Floral Signals and Moth Foraging Decisions

Background

Combinations of floral traits – which operate as attractive signals to pollinators – act on multiple sensory modalities. For Manduca sexta hawkmoths, how learning modifies foraging decisions in response to those traits remains untested, and the contribution of visual and olfactory floral displays on behavior remains unclear.

Methodology/Principal Findings

Using M. sexta and the floral traits of two important nectar resources in southwestern USA, Datura wrightii and Agave palmeri, we examined the relative importance of olfactory and visual signals. Natural visual and olfactory cues from D. wrightii and A. palmeri flowers permits testing the cues at their native intensities and composition – a contrast to many studies that have used artificial stimuli (essential oils, single odorants) that are less ecologically relevant. Results from a series of two-choice assays where the olfactory and visual floral displays were manipulated showed that naïve hawkmoths preferred flowers displaying both olfactory and visual cues. Furthermore, experiments using A. palmeri flowers – a species that is not very attractive to hawkmoths – showed that the visual and olfactory displays did not have synergistic effects. The combination of olfactory and visual display of D. wrightii, however – a flower that is highly attractive to naïve hawkmoths – did influence the time moths spent feeding from the flowers. The importance of the olfactory and visual signals were further demonstrated in learning experiments in which experienced moths, when exposed to uncoupled floral displays, ultimately chose flowers based on the previously experienced olfactory, and not visual, signals. These moths, however, had significantly longer decision times than moths exposed to coupled floral displays.

Conclusions/Significance

These results highlight the importance of specific sensory modalities for foraging hawkmoths while also suggesting that they learn the floral displays as combinatorial signals and use the integrated floral traits from their memory traces to mediate future foraging decisions.     

Observational evidence of herbivore‐specific associational effects between neighboring conspecifics in natural,dimorphic populations of Datura wrightii

Associational effects—in which the vulnerability of a plant to herbivores is influenced by its neighbors—have been widely implicated in mediating plant–herbivore interactions. Studies of associational effects typically focus on interspecific interactions or pest–crop dynamics. However, associational effects may also be important for species with intraspecific variation in defensive traits. In this study, we observed hundreds of Datura wrightii—which exhibits dimorphism in its trichome phenotype—from over 30 dimorphic populations across California. Our aim was to determine whether a relationship existed between the trichome phenotype of neighboring conspecifics and the likelihood of being damaged by four species of herbivorous insects. We visited plants at three timepoints to assess how these effects vary both within and between growing seasons. We hypothesized that the pattern of associational effects would provide rare morphs (i.e., focal plants that are a different morph than their neighbors) with an advantage in the form of reduced herbivory, thereby contributing to the negative frequency‐dependent selection previously documented in this system. We found the best predictor of herbivory/herbivore presence on focal plants was the phenotype of the focal plant. However, we also found some important neighborhood effects. The total number of plants near a focal individual predicted the likelihood and/or magnitude of herbivory by Tupiochoris notatus, Lema daturaphila, and Manduca sexta. We also found that velvety focal plants with primarily sticky neighbors are more susceptible to infestation by Tupiochoris notatus and Lema daturaphila. This does not align with the hypothesis that associational effects at the near‐neighbor scale contribute to a rare‐morph advantage in this system. Overall, the results of our study show that the number and trichome‐morph composition of neighboring conspecifics impact interactions between D. wrightii and insect herbivores.     

Transplant Antennae and Host Brain Interact to Shape Odor Perceptual Space in Male Moths

Behavioral responses to odors rely first upon their accurate detection by peripheral sensory organs followed by subsequent processing within the brain’s olfactory system and higher centers. These processes allow the animal to form a unified impression of the odor environment and recognize combinations of odorants as single entities. To investigate how interactions between peripheral and central olfactory pathways shape odor perception, we transplanted antennal imaginal discs between larval males of two species of moth Heliothis virescens and Heliothis subflexa that utilize distinct pheromone blends. During metamorphic development olfactory receptor neurons originating from transplanted discs formed connections with host brain neurons within olfactory glomeruli of the adult antennal lobe. The normal antennal receptor repertoire exhibited by males of each species reflects the differences in the pheromone blends that these species employ. Behavioral assays of adult transplant males revealed high response levels to two odor blends that were dissimilar from those that attract normal males of either species. Neurophysiological analyses of peripheral receptor neurons and central olfactory neurons revealed that these behavioral responses were a result of: 1. the specificity of H. virescens donor olfactory receptor neurons for odorants unique to the donor pheromone blend and, 2. central odor recognition by the H. subflexa host brain, which typically requires peripheral receptor input across 3 distinct odor channels in order to elicit behavioral responses.     

Complex Odor from Plants under Attack: Herbivore's Enemies React to the Whole, Not Its Parts

Background

Insect herbivory induces plant odors that attract herbivores'' natural enemies. Assuming this attraction emerges from individual compounds, genetic control over odor emission of crops may provide a rationale for manipulating the distribution of predators used for pest control. However, studies on odor perception in vertebrates and invertebrates suggest that olfactory information processing of mixtures results in odor percepts that are a synthetic whole and not a set of components that could function as recognizable individual attractants. Here, we ask if predators respond to herbivore-induced attractants in odor mixtures or to odor mixture as a whole.

Methodology/Principal Findings

We studied a system consisting of Lima bean, the herbivorous mite Tetranychus urticae and the predatory mite Phytoseiulus persimilis. We found that four herbivore-induced bean volatiles are not attractive in pure form while a fifth, methyl salicylate (MeSA), is. Several reduced mixtures deficient in one component compared to the full spider-mite induced blend were not attractive despite the presence of MeSA indicating that the predators cannot detect this component in these odor mixtures. A mixture of all five HIPV is most attractive, when offered together with the non-induced odor of Lima bean. Odors that elicit no response in their pure form were essential components of the attractive mixture.

Conclusions/Significance

We conclude that the predatory mites perceive odors as a synthetic whole and that the hypothesis that predatory mites recognize attractive HIPV in odor mixtures is unsupported.     

Aboveground herbivory induced jasmonates disproportionately reduce plant reproductive potential by facilitating root nematode infestation

Different plant feeders, including insects and parasitic nematodes, can influence each other by triggering systemic changes in their shared host plants. In most cases, however, the underlying mechanisms are unclear, and the consequences for plant fitness are not well understood. We studied the interaction between leaf feeding Manduca sexta caterpillars and root parasitic nematodes in Nicotiana attenuata. Simulated M. sexta attack increased the abundance of root parasitic nematodes in the field and facilitated Meloidogyne incognita reproduction in the glasshouse. Intact jasmonate biosynthesis was found to be required for both effects. Flower counts revealed that the jasmonate‐dependent facilitation of nematode infestation following simulated leaf attack reduces the plant's reproductive potential to a greater degree than would be expected from the additive effects of the individual stresses. This work reveals that jasmonates mediate the interaction between a leaf herbivore and root parasitic nematodes and illustrates how plant‐mediated interactions can alter plant's reproductive potential. The selection pressure resulting from the demonstrated fitness effects is likely to influence the evolution of plant defense traits in nature.     

Antagonistic effects of floral scent in an insect–plant interaction

In southwestern USA, the jimsonweed Datura wrightii and the nocturnal moth Manduca sexta form a pollinator–plant and herbivore–plant association. Because the floral scent is probably important in mediating this interaction, we investigated the floral volatiles that might attract M. sexta for feeding and oviposition. We found that flower volatiles increase oviposition and include small amounts of both enantiomers of linalool, a common component of the scent of hawkmoth-pollinated flowers. Because (+)-linalool is processed in a female-specific glomerulus in the primary olfactory centre of M. sexta, we hypothesized that the enantiomers of linalool differentially modulate feeding and oviposition. Using a synthetic mixture that mimics the D. wrightii floral scent, we found that the presence of linalool was not necessary to evoke feeding and that mixtures containing (+)- and/or (−)-linalool were equally effective in mediating this behaviour. By contrast, females oviposited more on plants emitting (+)-linalool (alone or in mixtures) over control plants, while plants emitting (−)-linalool (alone or in mixtures) were less preferred than control plants. Together with our previous investigations, these results show that linalool has differential effects in feeding and oviposition through two neural pathways: one that is sexually isomorphic and non-enantioselective, and another that is female-specific and enantioselective.     

Olfactory Associative Learning of the Pupal Parasitoid Pimpla luctuosa Smith (Hymenoptera: Ichneumonidae)

Laboratory experiments were conducted to determine the role of learning in olfactory host searching by the ichneumonid pupal parasitoid, Pimpla luctuosa Smith. Females learned to associate novel odors such as vanilla and strawberry with hosts when they oviposited in at least several hosts with the odors. Repeated experiences of hosts with an odor increased the response of the experienced odor, and females that had experienced host odor seven times responded to the experienced odors 90% of the time. Although the response by females to a learned odor gradually decreased with increasing host-deprivation time, 60% of the females that had experienced host odor 7 days earlier still responded to the experienced odor. Females also learned two separate odors associated with hosts at a time and responded to both odors without a preference for one odor over the other. When trained two separate odors with hosts, females learned the second odor more quickly than the first odor. After females experienced several stings in simulated hosts with the previously learned odor, they ceased to respond to the learned odor, suggesting that repeated unrewarding experiences cause females to cease to respond to the learned odors.