Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta

Raguso, Robert A.; Willis, Mark A.

doi:10.1016/j.anbehav.2004.04.015

Cited by 260 publications

(311 citation statements)

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“…A combination of olfactory and visual cues are necessary for successful foraging behavior in many nocturnal and diurnal insects, including moths (10,14,15), solitary bees (26), beetles (27), and flies (28,29). Many of these nectarivores have innate preferences for a combination of odor and visible characteristics of plants for which they are pollinators (10,15,16) and can learn to associate new floral features with nectar rewards (10,30,31). This combination of innate preference and learning may represent ubiquitous cognitive processes that control foraging behavior in pollinators and possibly all insects.…”

Section: Discussionmentioning

confidence: 99%

“…A pollinator species that exhibits such behavioral flexibility is the hawkmoth, Manduca sexta (Sphingidae). M. sexta has a wide geographic range and typically feeds from a narrow range of moth-adapted flowers (13)(14)(15). In the semiarid grassland of Arizona, M. sexta is a frequent visitor to Datura wrightii (Solanaceae) (16).…”

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“…Hawkmoths may use multiple sensory modalities to learn to associate flowers and nectar rewards (14,15). To determine the strength of the association between the olfactory stimulus and the nectar resource, experiments were conducted by using paper flowers emitting D. wrightii and A. palmeri scents.…”

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Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Riffell

Alarcón

Abrell

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

170

159

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Spatiotemporal variability in floral resources can have ecological and evolutionary consequences for both plants and the pollinators on which they depend. Seldom, however, can patterns of flower abundance and visitation in the field be linked with the behavioral mechanisms that allow floral visitors to persist when a preferred resource is scarce. To explore these mechanisms better, we examined factors controlling floral preference in the hawkmoth Manduca sexta in the semiarid grassland of Arizona. Here, hawkmoths forage primarily on flowers of the bat-adapted agave, Agave palmeri, but shift to the moth-adapted flowers of their larval host plant, Datura wrightii, when these become abundant. Both plants emit similar concentrations of floral odor, but scent composition, nectar, and flower reflectance are distinct between the two species, and A. palmeri flowers provide six times as much chemical energy as flowers of D. wrightii. Behavioral experiments with both naïve and experienced moths revealed that hawkmoths learn to feed from agave flowers through olfactory conditioning but readily switch to D. wrightii flowers, for which they are the primary pollinator, based on an innate odor preference. Behavioral flexibility and the olfactory contrast between flowers permit the hawkmoths to persist within a dynamic environment, while at the same time to function as the major pollinator of one plant species.flower visitation ͉ foraging behavior ͉ moth ͉ pollination A bundance and composition of flower species are fundamental aspects of pollination biology, and both can change over a pollinator's lifetime. For any nectar or pollen forager, the ability to discriminate, learn, and switch among flowers in the face of an ever-changing environment is critically important. For example, availability of floral resources at a landscape scale can constrain the size (1) and behavior (2) of a population of floral visitors (3). Unfortunately, aside from research on social bees (e.g., Apis mellifera, Bombus spp.), our understanding of mechanisms controlling nectar foraging by pollinators is limited. Whereas observational studies of flower visitation (reviewed in ref. 4) and proportionally fewer studies of the effects of changing flower composition on foraging (5) have been conducted (6), the causal mechanisms controlling floral visitation remain unclear and seldom can be demonstrated from the observed correlations. Thus, there remains a fundamental gap between the processes that occur in the field and the underlying behavioral mechanisms mediating those interactions.Nectar foraging by insects involves a suite of behaviors, both innate and learned. Much of our understanding of flower choice and cognition comes from work with generalist honey bees (Apis mellifera) and bumble bees (Bombus spp.), for which learning is a critical component. For instance, honey bee workers exhibit innate color preferences, but when trained on flowers of alternative colors, the preference is extinguished (7). Learning permits individual bees the flexibility to fo...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Riffell

Alarcón

Abrell

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

170

159

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“…Floral CO 2 is a stimulus whose relevance to moth foraging behavior depends on the specific task at hand (e.g., oviposition) and the extent to which other floral information is available. In night-blooming plants such as D. wrightii, floral CO 2 might provide the most honest indication of nectar profitability to foraging moths because it decreases markedly within the first hour after anthesis (29), when nectar feeding by M. sexta is most intense (56,57), whereas floral odor and visual display remain unchanged after nectar has been drained from individual flowers (26,29). Future experiments should test the extent to which moths' foraging behavior in a natural setting reflects local differences in floral CO 2 , and whether females are capable of using such information at non-host nectar sources such as Oenothera caespitosa (Onagraceae) and Mirabilis longiflora (Nyctaginaceae).…”

Section: Context Dependence Of Female Responses In Binary-choice Assaysmentioning

confidence: 99%

Context- and scale-dependent effects of floral CO ₂ on nectar foraging by Manduca sexta

Goyret

Markwell²,

Raguso³

2008

Proc. Natl. Acad. Sci. U.S.A.

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fragrance ͉ odor ͉ olfaction ͉ pollination ͉ Sphingidae A nthophilous insects use information from a variety of sensory channels to locate flowers and feed from them (1). Thus, a crucial task for studying insect-plant interactions is to identify which components of the environment provide the sensory inputs used by insects, and to what extent context and scale affect their information content (2). Whereas flower colors and patterns (3, 4), whole-flower and nectar odors (5), and even corolla shape and texture are known features used by foraging insects and other nectivorous animals (6, 7), few studies have explicitly addressed the role of flower respiratory carbon dioxide (CO 2 ) as a stimulus involved in plant-pollinator interactions.Our knowledge of how insects use CO 2 as a sensory cue is derived primarily from studies of insects that vector diseases or attack crop plants. For example, many haematophagous insects use CO 2 to locate their animal hosts from a distance (8). Discontinuous CO 2 plumes modulate host-seeking behavior by mosquitoes (9, 10), suggesting that CO 2 acts as a long-range orientation stimulus (11). Tsetse flies and biting midges also use CO 2 as a long-range attractant that can synergize the attractiveness of other host odors (12, 13). However, CO 2 also functions as a close-range feeding stimulus (on the host's skin) for mosquitoes (8). CO 2 synergizes the attractiveness of some human skin odors to female yellow fever mosquitoes (14) and has been suggested to synergize triatomine bug responses to L(ϩ)-lactic acid (15).Some herbivorous insects show similar responses to CO 2 , although typically at closer range to its source than haematophagous insects. CO 2 alone is sufficient to guide Diabrotica virgifera beetle larvae toward corn roots (16), and larvae of noctuid (Helicoverpa armigera) (17) and pyralid (Elasmopalpus lignosellus) (18) moths orient to above-ambient CO 2 sources. Females of the pyralid moth Cactoblastis cactorum search for CO 2 sinks on photosynthetic stem surfaces of Opuntia stricta, as indicators of high carbon fixation activity (19). In this case, CO 2 gradients are used as close-range stimuli, as is true for tephritid flies that oviposit on fruit wounds, which provide a localized source of CO 2 and other olfactory oviposition stimulants (20). Finally, responses to CO 2 may be context-dependent. Tephritid flies respond to CO 2 when presented with a fruit-like visual stimulus (20). Within a certain concentration range, Drosophila melanogaster adults and larvae are repelled by CO 2 , and it has been suggested that these responses depend on the olfactory context (21).It is clear from the studies reviewed above that CO 2 may function alone or in concert with host odors, at a distance or at close range, via several behavioral mechanisms. Recent studies suggest that CO 2 may also contribute to the interactions between flowers and insect pollinators. Floral CO 2 is primarily associated with elevated respiratory activity in thermogenic flowers, including deceptive flowers that mim...

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“…While the simultaneous presence of attractive olfactory and visual stimuli is necessary to elicit nectar feeding in M. sexta (Raguso & Willis 2002, 2005, female moths rely primarily on olfactory cues to locate and identify host plants for oviposition (Sparks 1969(Sparks , 1973Ramaswamy 1988;Zhang et al 1999). In the laboratory, females oviposit on non-flowering D. wrightii, indicating that vegetative volatiles mediate recognition and acceptance of host plants.…”

Section: Introductionmentioning

confidence: 99%

Antagonistic effects of floral scent in an insect–plant interaction

et al. 2010

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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 (þ)-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 (þ)-and/or (2)-linalool were equally effective in mediating this behaviour. By contrast, females oviposited more on plants emitting (þ)-linalool (alone or in mixtures) over control plants, while plants emitting (2)-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.

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Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta

Cited by 260 publications

References 58 publications

Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Context- and scale-dependent effects of floral CO ₂ on nectar foraging by Manduca sexta

Antagonistic effects of floral scent in an insect–plant interaction

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Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta

Cited by 260 publications

References 58 publications

Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions

Context- and scale-dependent effects of floral CO 2 on nectar foraging by Manduca sexta

Antagonistic effects of floral scent in an insect–plant interaction

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Context- and scale-dependent effects of floral CO ₂ on nectar foraging by Manduca sexta