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

Abstract

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...

Flexible responses to visual and olfactory stimuli by foragingManduca sexta: larval nutrition affects adult behaviour

“…On the other hand, M. sexta has consistently shown more significant responses to visual targets when olfactory stimuli were also provided (Raguso & Willis 2002;Goyret et al 2007;Riffell et al 2008). Here, the combined results from our behavioural experiments and spectroradiometric measurements support the hypothesis that naive M. sexta has difficulty recognizing an odourless visual target as a nectar source when their vision is impaired by suboptimal b-carotene intake during their larval stages.…”

Innate olfactory preferences in dung beetles

“…To what extent associative learning (association of new odours with an adequate substrate for feeding and reproduction) influences the apparent prevalence of innate olfactory preferences in dung beetles remains open to question. In many flower-visiting insects, adults commonly exhibit innate preferences for floral scents but can also learn to associate new floral cues with nectar rewards (Kelber, 2002;Cunningham et al, 2004;Riffell et al, 2008). The ability to learn is considered advantageous for insects facing scarce or changing resources.…”

“…In parasitoid species, learning of olfactory cues has been shown to result mainly from early adult experience (Turlings et al, 1993;Du et al, 1997) but learning during preimaginal stages has also been suspected (Smith and Cornell, 1979). In many flower-visiting species, foraging behaviour may proceed from a combination of innate preferences for certain flowers and learning abilities that guide insects towards new rewarding flower species (Kelber, 2002;Riffell et al, 2008). For example, floral odour learning by adults has been reported in hawkmoth species (Raguso and Willis, 2002;Cunningham et al, 2006) and bees (Giurfa, 2007;Wright et al, 2007;Riveros, 2009).…”

Insect eggs protected from high temperatures by limited homeothermy of plant leaves

“…In Arizona, M. sexta is active during the monsoon season from July to September (Riffell et al, 2008). Females attach eggs singly to the lower host leaf surface; eggs hatch after ~4days, and larvae typically develop through 5 or 6 instars (Kingsolver, 2007).…”