Signals and Cues
“Signals” represent information shared between organisms for their mutual benefit, shaped by natural selection for the purpose of communication, whereas “cues” represent inadvertent or unavoidable information that could be utilized by an eavesdropper to their advantage.
Initially, our interest in the signal-cue distinction was more practical than conceptual. My students and I consistently found that when we performed Niko Tinbergen-esque experiments decoupling floral scent from visual display, our artificial flowers were never as attractive to hawkmoths as natural flowers were. We also realized that many flowers cross a threshold of dishonesty, when they remain turgid, colorful, and scented but no longer offer nectar or pollen as rewards, due to a recent pollinator visit. We began to wonder whether discerning pollinators might utilize other channels of floral information to forage more efficiently.
“Signals” represent information shared between organisms for their mutual benefit, shaped by natural selection for the purpose of communication, whereas “cues” represent inadvertent or unavoidable information that could be utilized by an eavesdropper to their advantage.
Initially, our interest in the signal-cue distinction was more practical than conceptual. My students and I consistently found that when we performed Niko Tinbergen-esque experiments decoupling floral scent from visual display, our artificial flowers were never as attractive to hawkmoths as natural flowers were. We also realized that many flowers cross a threshold of dishonesty, when they remain turgid, colorful, and scented but no longer offer nectar or pollen as rewards, due to a recent pollinator visit. We began to wonder whether discerning pollinators might utilize other channels of floral information to forage more efficiently.
This question led to a pair of NSF-funded collaborative projects with colleagues from the University of Arizona, one on the emission of CO2 by night-blooming flowers, and the other on the maintenance of humidity gradients in such flowers. We learned that many flowers produce ephemeral pulses of CO2 as they open, before pollinator visitation or nectar removal, and we confirmed that hawkmoths are sensitive to minute differences in CO2 plumes and prefer flowers thus endowed, but relax their preference when flowers are equally profitable. Joaquin Goyret and a summer REU student, Poppy Markwell, showed that male and female Manduca sexta moths differ in their responses, with males significantly preferring flowers with elevated CO2 but females only showing this preference when host plant (tomato foliage) odors are present, suggesting contextual differences in olfactory processing. Later, Martin von Arx measured modest, transient humidity gradients in the headspace of newly-opening Oenothera cespitosa flowers, linked them to passive evaporation of floral nectar and demonstrated that hawkmoths prefer such flowers to those with ambient humidity. Floral CO2 and humidity seemed like clear examples of cues that foraging moths could exploit to reduce visits to empty flowers, adding to a growing list of surprising sensory channels (heat, acoustic reflectance, static electrical charge) through which pollinators locate and handle flowers.
Goyret, J., P.M. Markwell, R.A. Raguso. 2008. Scale- and context-dependent effects of floral CO2 on nectar foraging by Manduca sexta. Proceedings of
the National Academy of Sciences, USA 105: 4565-4570. https://doi.org/10.1073/pnas.0708629105
von Arx, M., J. Goyret, G. Davidowitz, R.A. Raguso. 2012. Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths.
Proceedings of the National Academy of Sciences, USA 109: 9471-9476. https://doi.org/10.1073/pnas.1121624109
Goyret, J., P.M. Markwell, R.A. Raguso. 2008. Scale- and context-dependent effects of floral CO2 on nectar foraging by Manduca sexta. Proceedings of
the National Academy of Sciences, USA 105: 4565-4570. https://doi.org/10.1073/pnas.0708629105
von Arx, M., J. Goyret, G. Davidowitz, R.A. Raguso. 2012. Floral humidity as a reliable sensory cue for profitability assessment by nectar-foraging hawkmoths.
Proceedings of the National Academy of Sciences, USA 109: 9471-9476. https://doi.org/10.1073/pnas.1121624109
A follow-up study led by Ajinkya Dahake revealed something much different for the trumpet-shaped flowers of Datura wrightii. We were stunned to find steep floral humidity gradients, 10-fold higher than any previously measured, which persist in the face of wind and reconstitute quickly after nectar removal. Hawkmoths perceive humid air with specialized antennal sensilla, prefer humid flowers and perseverate even in the absence of nectar, such is the intensity of their sensory bias. In Datura, floral humidity is not an unavoidable by-product of nectar evaporation. It functions more like a signal than a cue, but unlike CO2, it rapidly degrades beyond the corolla limb and can only be perceived at the threshold of the flower. For smaller commensal insects and mites, such flowers constitute islands of humidity in the Sonoran Desert of southwestern North America.
Dahake, A., P. Jain, C. Vogt, W. Kandalaft, A. Strook, R.A. Raguso. 2022. A signal-like role for floral humidity in a nocturnal pollination system. Nature
Communications 13: 7773. https://doi.org/10.1038/s41467-022-35353-8
Raguso, R.A. 2023. Hidden worlds within flowers. Current Biology 33: R506-R512. https://doi.org/10.1016/j.cub.2023.04.054
Dahake, A., P. Jain, C. Vogt, W. Kandalaft, A. Strook, R.A. Raguso. 2022. A signal-like role for floral humidity in a nocturnal pollination system. Nature
Communications 13: 7773. https://doi.org/10.1038/s41467-022-35353-8
Raguso, R.A. 2023. Hidden worlds within flowers. Current Biology 33: R506-R512. https://doi.org/10.1016/j.cub.2023.04.054
In a recent study led by Shayla Salzman, we documented another example of a signal-like role for humidity gradients in an ancient nursery-pollination system between Zamia cycads and their weevil pollinators. Cycads are dioecious (male and female individual plants) gymnosperms, and the weevils breed in the male cones, thus pollination requires weevils to visit female cones against their interests. This is accomplished through a specific scent shared by male and female cones, and by the presence of steep humidity gradients where mature female cone scales crack open. Bioassays showed these features to be irresistible to the weevils, in a system in which there are no nectar rewards at all. Interestingly, high humidity is repellent in Australian cycads (Macrozamia) pollinated by thrips instead of weevils (work by Irene Terry), providing another example of context dependency, which appears to be the rule and not the exception in floral signal evolution.
Salzman, S., A. Dahake, W. Kandalaft, W. Valencia-Montoya, M. Calonje, C. D. Specht, R.A. Raguso. 2023. Cone humidity is a strong attractant in an obligate cycad
pollination system. Current Biology 33: 1-11. https://doi.org/10.1016/j.cub.2023.03.021
Dahake, A, R.A. Raguso, J. Goyret. 2023. Context and the functional use of sensory information in sensory ecology. Current Opinion in Insect Science 58: 101058
https://doi.org/10.1016/j.cois.2023.101058