Plant–animal communication: past, present and future
Communication between plants and their animal partners underlies some of the planet’s most ecologically and economically important mutualisms. Study of communication in this context offers many opportunities to address fundamental questions about the costs and benefits of signal production, signal honesty, and receiver cognition. In this special issue, contributors highlight several key areas of current research, including how multiple receivers affect floral signaling, and how signaling may be related across different phases of reproduction. Visual signals are a particular emphasis, including how learning can mediate pollinator preferences, and the evolution of conspicuousness. In light of these focal areas, we summarize current trends towards the study of greater complexity both in terms of floral phenotypes and signaling/interaction networks.
KeywordsCommunication Floral signals Plant–animal interactions Pollination Herbivory Seed dispersal
In “Discovery of the Secret of Nature in the Structure and Fertilization of Flowers”, Sprengel (1793) amassed evidence to support the idea that plants reward animals with nectar in exchange for the transfer of pollen. Beyond identifying the key elements of pollination mutualisms (and, in passing, those of seed dispersal), this text is also remarkable for its coverage of how floral and fruit signals mediate relationships between plants and their partners. Here, Sprengel famously coined the term nectar guide (Saftmal) to describe floral patterns that direct pollinators towards both rewards and reproductive structures. His careful description of these signals laments, “nobody has recognized what I call nectar covers and nectar guides for what they are, although everyone has seen them.”
What purpose does the nectar of this or that flower serve? What is the particularly colored spot on it meant for? What connection do all parts of the flower have, and what relationships do they have to the fruit which should originate from the flower? And how does everything which we see and notice in a flower throughout its complete flowering period unite into a single beautiful whole? Sprengel (1793)
To be both seen and recognized remains a theme of research on plant–animal communication more than two centuries later. After all, many questions about how plants “speak” to their mutualistic partners can be addressed in species and locales not much more exotic than those available to an average eighteenth century naturalist. To cite an example from our own work: even the most casual of gardeners would agree that flowers are often both colorful and scented. Yet, researchers have barely begun to understand why plants produce such sensorially complex floral displays (Leonard et al. 2012), much less how pollinators process these multimodal signals (Leonard and Masek 2014). In this case, the critical first step was to identify an interesting question about signal evolution essentially hiding in plain sight.
To achieve a holistic understanding of plant–animal communication, that first step must be followed by a willingness to grapple with the perspectives of both sender and receiver, from proximate and ultimate points of view. Researchers must not only consider the drivers of signal production (e.g. the biochemistry and reproductive biology of the plant) but also the mechanisms and consequences of signal reception (e.g. the sensory and behavioral ecology of the animal). Thus, disciplinary boundaries and a growing emphasis on early-career specialization are challenges to the growth of “Plant–Animal Communication” as a focal area. Beyond the obvious divisions between what students learn in animal communication versus plant ecology courses, parallel trajectories in the literature can yield insights in the absence of discourse. For example, the same plant species could in principle be studied quite separately for its interactions with herbivores versus pollinators versus seed dispersers; the same flower or fruit for its color versus scent; the same receiver for its visual versus olfactory responses to a given plant structure.
For those inclined to bridge these divisions, plant–animal interactions offer an unparalleled testing ground for broader ideas about the evolution of communication. What keeps signals honest? How does conspicuousness evolve or coevolve in relation to sensory systems? What abiotic forces and antagonists shape signal evolution? Is signal form shaped by developmental or phylogenetic constraint? How much does it cost to produce a signal, and what is its fitness benefit? Indeed, as plant behavior goes mainstream (Bradbury and Vehrencamp 2011; Schaefer and Ruxton 2011; Karban 2015), interest in understanding plants’ interactions with animals through the lens of signaling theory will continue to grow. In contrast to many systems of animal communication, here is a case where we can often both easily quantify the signal and connect it indirectly or even directly to fitness. The list of fundamental questions about communication ideally suited to explore in plant–animal systems will likely spiral beyond the few examples noted here.
Multiple agents shape floral signaling
Plant–animal interactions offer ample opportunities to understand how a complex network of interactants can influence communication in a given context. In the most commonly-studied scenario, herbivores perturb interactions between plants and pollinators via their direct effects on floral displays (e.g. McCall and Irwin 2006) or by inducing defenses that alter the chemistry of floral signals and rewards (e.g. Kessler and Halitschke 2009). In this issue, Hoffmeister and Junker (2016) ask how simulated herbivory affects bees’ responses to not only the flowers of Vicia faba, but also to the visual and olfactory signals of its extrafloral nectaries (EFNs). They outline an indirect pathway by which antagonists might alter interactions with pollinators: increases in EFN activity induced by herbivory can attract the attention of not only natural enemies, but also pollinators. Extrafloral nectar might be a useful resource for the bumblebees in this study, but their visits to these structures do not transfer pollen, and potentially deplete the resources available to antagonists of herbivores.
Signals are linked across reproductive phases
Beyond the herbivore–plant–pollinator triad described above, connections may also exist between the signals targeting pollinators and seed dispersers. This is not obvious from the literature: flowers and fruits represent two phases of plant reproduction usually studied quite independently of each other. This separation may partly reflect the taxonomic divide between the receivers commonly studied in each context (e.g. insects vs. mammals; hummingbirds vs. other avian species). Nonetheless, both pollination and seed dispersal biologists ask similar questions about signaling, and new findings suggest that, just as these two life history stages are invariably linked, communication in each context may be related.
As a first step towards greater integration, Valenta et al. (2016) review how traits associated with both fruits and flowers mediate interactions with pollinators and seed dispersers. The authors suggest several ways in which findings in each context could be brought together to yield a broader understanding of how communication contributes to plant fitness. For example, a researcher interested in the function of multimodal floral signals might find much to discuss with researchers asking similar questions about fruit traits. Likewise, recent discoveries about mimetic fruits raise new opportunities for researchers broadly interested in deceptive signaling.
Learning mediates the functional consequences of floral visual signals
Despite more than two centuries of research on floral visual displays, many basic aspects of their function and evolutionary history remain obscure. Even familiar nectar guides hold some surprises: although popularly assumed to be beneficial to both plants and pollinators, we have found that their presence may tip the balance of the interaction towards pollen transfer at the expense of nectar collection (Leonard and Papaj 2011). They may even help defend against nectar robbing, by incentivizing “legitimate” flower handling (Leonard et al. 2013). In this issue, de Jager et al. (2016) further unravel the details of how common components of floral patterns (rings and spots) manifest on the continuum of interactions ranging from mutualism to exploitation (Bronstein 1994). In this case, pollinator learning, visual properties of the pattern, and ecological context seem likely to guide these dynamics. This lab-based study is an important first step towards understanding the role of pollinator cognition in mediating visual pattern signaling by real floral phenotypes.
New modeling approaches reveal convergence towards conspicuousness
Visual modeling techniques (e.g. Chittka 1992; Vorobyev and Osorio 1998; Endler and Mielke 2005) can open a window into the sensory world of receivers, helping us predict the detectability and discriminability of flower or fruit signals. As animals vary in their visual sensitivity, color space models can also be used to understand how sensory systems might exert similar or different selection pressures on the displays of plant species. These models are also useful for shifting the focus away from our anthropocentric instincts about the function of a visual display. In this special issue, two contributions show how visual modeling can reveal aspects of floral signaling otherwise hidden from view.
Combining computer simulations, behavioral assays, and floral reflectance measurements, Bukovac et al. (2016) tackle a mysterious broad-scale pattern in the visual properties of bee-pollinated flowers. Namely, they find that a spectral “signature” (sharp changes in reflectance at 420–480 nm) rarely found in bee-pollinated flowers is also one which color space models predict should be difficult for bees to detect. Because some bird-pollianted flowers exhibit this visual property, its relative rarity among bee-pollinated plants may indicate pollinator-mediated selection, rather than a production constraint. Despite the utility of visual modeling, the authors also highlight uncertainties associated with key assumptions of these models, including gaps in our understanding of visual processing that might enhance the ability of these tools to explain large-scale patterns in floral signaling.
Finally, a study by Gaskett et al. (2016) reinforces the idea that quantifying the conspicuousness of floral visual traits can shift our understanding of floral evolution. The authors explore signaling strategies in an assemblage of orchid species (representatives of Drakaea and Caladenia), which are pollinated by male thynnine wasps. The authors use a number of analytical techniques to compare the visual properties of floral structures and female wasps, including what may be the first application of color pattern geometry analysis to floral displays (an approach widely used in studies of animal signals: Endler and Mielke 2005; Endler 2012). Although these orchids are assumed to mimic female visual signals, this study returns evidence consistent with an alternative hypothesis: orchids from these two genera appear to have converged on patterns that succeed not via precise mimicry of female wasps, but because they are easy for male wasps to detect against the background. The authors discuss how this pollination strategy might have evolved along a pathway involving elements of both sensory exploitation and sexual deception.
The first axis (x) is that of floral complexity. This effort is already well underway regarding floral advertisements: in the past decade, interest has spiked in understanding how animals use multimodal signals to make decisions, and (relatedly) why plants might produce advertisements that span sensory modalities (Junker and Parachnowitsch 2015); (Fig. 1e). Dovetailing with these developments, we have also recently begun to study how animals forage for multiple reward types offered by their mutualist partners, as well as the reciprocal question of how a plant might benefit from offering a particular combination of resources (Francis et al. 2016); (Fig. 1d).
The second axis (y) represents interaction complexity. The push to expand beyond the classic plant–pollinator dyad is familiar, considering that the direct and indirect effects of plant–herbivore interactions on floral phenotypes have been studied for decades (e.g. Strauss et al. 1996; Johnson et al. 2015), and network approaches are now common in both studies of mutualistic interactions (Bascompte and Jordano 2007) and animal communication (McGregor 2005).
From these foundations, we highlight two areas where an interest in communication might yield unique insights into the ecology and evolution of plant–animal interactions:
Advertisement and decision-making in a community context
Angiosperms are not only partners in a mutualism with pollinators and seed dispersers, but also competitors in a marketplace for the services these animals provide. Fruit and flower traits such as color, luminance, pattern, size and scent can convey accurate information about the quality or quantity of reward available, and generalist pollinators or dispersers use this information to guide resource selection (e.g. Knauer and Schiestl 2015). Across plant species, however, no single trait seems to honestly signal the value of rewards to animals evaluating flowers or fruits. For one plant species, scent may be the best indicator of value; for another, color. To add to this complexity, rewards offered by competing plant species vary not only in quantity and quality but also type (e.g. co-flowering competitors might offer pollinators 2 μl vs. 8 μl of nectar; or alternately, 2 μl of nectar vs. 2 mg of pollen). These cognitive challenges are also relevant to seed dispersal, wherein the most useful signal can vary across plant species: for a non-ecological demonstration, consider the familiar quest to select the ripest avocado (via touch), banana (via vision), and melon (via scent). Consequently, a forager may often encounter relationships between signals and rewards that shift across the different plant species they visit (Fig. 1c). Animals’ interactions with a network of plant signalers thus offer an opportunity to address basic questions about how receivers compare co-signaling species that signal (1) across different sensory modalities and (2) with respect to multiple kinds of rewards.
Research on how pollinators learn and use floral signals might offer a starting point for the question of how animals cope with complex informational landscapes. Bees, for example, can clearly learn associations when signals convey information about different reward types (Muth et al. 2015) and discriminate among floral options using multiple sensory modalities (Leonard and Masek 2014). Understanding the efficacy of decision-making when signals or rewards vary within versus across categories is an obvious next step. Ideally, these scenarios would be inspired by studies establishing the diversity of signal-reward relationships facing foragers within a given plant community. Typically, such surveys focus on a single category (e.g. floral color or nectar volume); it would be more difficult to quantify floral communities along multiple axes (e.g. floral color + scent; nectar + pollen). Nevertheless, information from such field studies should inform the ecological realism of controlled experiments. Likewise, controlled experiments about animal decision-making might also allow us to make predictions regarding the signaling and reward strategies of co-flowering plants. For example, if a focal plant faces a strong visual competitor, would it more effectively boost visitation by investing in floral scent production? Such dynamics could be one driver of signal and reward diversity within a given floral community.
Signaling across interaction contexts
Plant–animal systems may be ideal for understanding how the relative strength of temporally nested interactions impacts signaling, because of the ease with which one can collect longitudinal data during different stages of reproduction (Fig. 1a). As noted by Stournaras and Schaefer (2016), plant signaling traits may be more integrated across life history stages than disciplinary divisions would lead us to believe. Their study shows that abiotic stressors could drive the coloration of both leaves and reproductive structures, with consequences for the degree of visual contrast offered by both flowers and fruits. Besides the physical environment, in principle, biotic interactions might also connect fruit and flower signaling. Most simply, the vegetative coupling Stournaras and Schaefer (2016) describe makes it plausible that foliar herbivory might have related effects on the colors or scents of both fruits and flowers.
Perhaps more intriguingly, integration between flower and fruit signaling should also be impacted by temporal nestedness. Plant reproduction is an inherently hierarchical system where success in earlier contexts (vegetative production and pollination) can have cascading effects on the following context (seed dispersal). For example, the outcome of ineffective floral signaling (pollination failure) may impact both the importance and efficacy of signaling to dispersers as well as the opportunity to do so. Analogous scenarios have been established in other cross-context studies, e.g. those that show that intensity of florivory can alter pollinators’ impact on plant reproduction (Rodríguez-Rodríguez et al. 2015). A plant which has only half its flowers fertilized faces not only a potentially smaller display with which to attract dispersers, but also a scenario in which the efficacy of fruit signals is even more critical, as the dispersal fate of any single seed represents a greater proportion of total reproductive success. Given this, we might expect flexible allocation to fruit signals based upon the success of signaling in the preceding floral stage.
Effects of display size and density offer additional facets for consideration (Howe and Smallwood 1982). For example, when per capita seed dispersal increases with fruit crop (e.g. a plant has 80% of its seeds dispersed when it offers 100 fruits; 90% when it offers 200 fruits) we might expect floral signaling to pollinators to be a relatively stronger source of selection than fruit signaling. Alternatively, if per capita fruit dispersal is independent of crop size (i.e. 80 seeds are dispersed regardless if the crop is 100 or 200 fruits) selection on floral signals may be less important. These ideas could be tested by comparative studies assessing whether investment in floral signal production depends on the relationship between crop size and per capita dispersal.
Hints at a more direct mechanistic coupling between flowers and fruits can be found in agricultural systems, where pollination-associated differences in seed set appear to alter aspects of resulting fruit chemistry (Hogendoorn et al. 2010). Whether the effectiveness of plant–pollinator communication could alter the visual or chemical properties of fruits in a way meaningful to dispersers in natural systems seems to be an open question. However, just as herbivory can alter the chemistry of nectar rewards and floral displays (e.g. Adler et al. 2006), so too might pollinators have functionally-relevant effects on the signals or rewards associated with seed dispersal. If different directional selection regimes characterize signaling during fruit and flowering stages, such biosynthetic linkages could be a source of constraint worth further exploration.
Overall, the two axes of complexity discussed above present a varied landscape where fruit and flower traits may be under selection for their function as signals to mutualists and antagonists, their competitive advantage over simultaneous signalers, and their direct and pleiotropic effects on plants’ interactions with their abiotic environment. An obvious extension of these themes would be to explicitly account for spatial and temporal variation in signaling interactions (c.f. Schaefer and Ruxton 2011). There is obviously plenty of work to be done; given the potential that plant–animal systems offer for addressing these basic questions about the ecology and evolution of communication networks, we are excited about the findings and ideas presented in this special issue, and optimistic about the work they will inspire.
This work was supported by the National Science Foundation (Grant IOS-1257762 to A.S.L.; Graduate Research Fellowship to J.S.F). Thank you to D. Picklum, D.L. Moseley and F. Muth for comments.
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