All plants synthesize a suite of several hundred terpenoid compounds with roles that include phytohormones, protein modification reagents, anti-oxidants, and more. Different plant lineages also ...synthesize hundreds of distinct terpenoids, with the total number of such specialized plant terpenoids estimated in the scores of thousands. Phylogenetically restricted terpenoids are implicated in defense or in the attraction of beneficial organisms. A popular hypothesis is that the ability of plants to synthesize new compounds arose incrementally by selection when, as a result of gradual changes in their biotic partners and enemies, the ‘old’ plant compounds were no longer effective, a process dubbed the ‘coevolutionary arms race’. Another hypothesis posits that often the sheer diversity of such compounds provides benefits that a single compound cannot. In this article, we review the unique features of the biosynthetic apparatus of terpenes in plants that facilitate the production of large numbers of distinct terpenoids in each species and how facile genetic and biochemical changes can lead to the further diversification of terpenoids. We then discuss evidence relating to the hypotheses that given ecological functions may be enhanced by the presence of mixtures of terpenes and that the acquisition of new functions by terpenoids may favor their retention once the original functions are lost.
•Linalool (3,7-dimethyl-1,6-octadien-3-ol) is a common floral volatile.•The two enantiomers of linalool have different biosynthetic sources and biological functions.•Insects have sophisticated ways ...to neutrally encode and behaviorally respond to these enantiomers.•Specific ratios of linalool or its derivatives can mediate highly specialized interactions.
Linalool (3,7-dimethyl-1,6-octadien-3-ol) is a common floral volatile with two distinct enantiomers and related metabolites involved in the full spectrum of plant–pollinator interactions. Recent studies reveal a complex interplay between pollinator attraction and plant defense mediated by linalool and its derivatives, from the smallest (Arabidopsis, Mitella) to the largest (Datura) flowers studied. Accordingly, fig wasps, fungus gnats and moths of all sizes show remarkable electrophysiological, neural and behavioral sensitivity to different enantiomers and quantitative ratios of linalool in floral bouquets. The diverse functions of linalool, ranging from toxin to long distance pollinator attractant are discussed in the broader context of floral volatile ecology and evolution.
Floral scent constitutes an ancient and important channel of communication between flowering plants, their pollinators, and enemies. Fragrance is a highly complex component of floral phenotype, with ...dynamic patterns of emission and chemical composition. The information content of specific volatile compounds is highly context dependent, and scent can function in direct and indirect ways from landscape to intrafloral scales. Floral scent promotes specialization in plant-pollinator relationships through private channels of unusual compounds, unique ratios of more widespread compounds, or through multicomponent floral filters. Floral scent also promotes outcrossing and reproductive isolation through floral constancy, via appetitive conditioning and discrimination on the basis of diverse mechanisms, including pheromone mimicry, odor intensity, complexity, composition, and synergy with visual stimuli. Finally, floral scent is a sexual signal and should be subject to the same selective pressures and modes of signal evolution as animal display, including signal honesty, sensory drive, and sensory exploitation.
The attention of the global pollination community has been drawn to food safety and other ecosystem services provided by pollinators, in light of decline in social bee populations. Despite ...intensified research on bees, recent studies have revealed important contributions of flies to pollination success, reproductive isolation and floral diversification. Diptera is a highly diverse insect order, comprising over 125,000 described species in 110 families and representing a broad spectrum of ecological niches beyond the well-known agricultural pests and blood-feeding vectors of human and animal diseases. Flies are most appreciated as generalized pollinators in alpine habitats (anthomyiids and tachinids) and as specialized pollinators in brood-site deceptive plants that mimic fungi (drosophilids), feces (muscids) or carrion (sarcophagids and calliphorids). Syrphid and bombyliid flies visit many of the same flowers as bees and butterflies do, but with different impacts on plant fitness. Guilds of South African plants have evolved specialized relationships with long-tongued nemestrinid and tabanid flies, thanks to geographic isolation and climatic stability. Studies in Japan highlight the evolution of another plant guild, pollinated by sciarid and mycetophilid fungus gnats, whereas
Zygothrica
flies (Drosophilidae) pollinate mushroom-like
Dracula
orchids in Andean cloud forests.
There is a growing realization that ecological interactions take place at many scales, from acorns to forests, and that formerly overlooked community members, particularly microbes, can play outsized ...ecological roles. Beyond their primary function as the reproductive organs of angiosperms, flowers constitute resource-rich, ephemeral habitats teeming with flower-loving symbionts, or ‘anthophiles’. The physical, chemical, and structural properties of flowers combine to create a habitat filter, selectively determining which anthophiles can reside there, and how, and when they interact. The microhabitats within flowers can provide shelter from predators or inclement weather, places to eat, sleep, thermoregulate, hunt, mate or reproduce. In turn, floral microhabitats contain the full range of mutualists, antagonists and apparent commensals, whose complex interactions impact how flowers look and smell, how profitable they are to foraging pollinators, and how selection feeds back upon the traits shaping those interactions. Recent studies suggest coevolutionary paths by which floral symbionts might be co-opted as mutualists and provide compelling examples in which ambush predators or florivores are recruited as floral allies. Unbiased studies that include the full roster of floral symbionts are likely to reveal novel links and additional nuance in the rich ecological communities hidden within flowers.
Raguso goes beyond the simplistic view of a flower as a pollinator attraction device, explaining how they function as micro habitats for diverse forms of life. The interactions between flowers and these organisms lie on a spectrum ranging from antagonistic to mutualistic and accounting for them will lead to greater insights into floral ecology.
In order to survive and reproduce, flowering plants must balance the conflicting selective pressures of herbivore avoidance and pollinator attraction. Links between herbivory and reproduction are ...often attributed to indirect effects of leaf damage on pollination via reductions in floral allocation, or increases in chemical defenses on herbivore-damaged plants. However, the impacts of herbivory on pollinators have the potential to extend beyond initial floral visits when plant defenses impact pollinator health, foraging behavior, and reproductive success. Here, we examine important but underexplored ways in which herbivory may alter floral phenotype and thus impact pollinators. First, we outline genetic and biochemical mechanisms predicted to underlie floral changes following herbivory, as they impact the floral resources (nectar and pollen) sought by pollinators. Next, we discuss how the consumption of secondary compounds might impact pollinator fitness, including carryover effects on subsequent foraging, mating success, and transgenerational effects on offspring. We consider how pollinator health, life history, and coevolutionary history might result in context-dependent impacts of plant defensive chemistry on pollinator fitness. Finally, we call for studies that measure the impact of herbivore-induced plant defenses on the full spectrum of flower visitors, and contrast case studies on conventional pollinators (for example, generalized bees) versus insects whose larvae are herbivores on the same plants that adults pollinate (such as several butterflies and moths). By linking these consequences of herbivory to fitness effects on both herbivores and pollinators, we will better understand how coevolution between plants, herbivores, and pollinators shapes both defensive and reproductive plant traits.
In order to survive and reproduce, flowering plants must balance the conflicting selective pressures of herbivore avoidance and pollinator attraction. Here, Jacobsen and Raguso examine the ways in which herbivory may alter floral phenotype and how the coevolution between plants, herbivores, and pollinators shapes both defensive and reproductive plant traits.
Abstract
Background and Aims
Flowers emit a wide range of volatile compounds which can be critically important to interactions with pollinators or herbivores. Yet most studies of how the environment ...influences plant volatiles focus on leaf emissions, with little known about abiotic sources of variation in floral volatiles. Understanding phenotypic plasticity in floral volatile emissions has become increasingly important with globally increasing temperatures and changes in drought frequency and severity. Here quantitative relationships of floral volatile emissions to soil water content were analysed.
Methods
Plants of the sub-alpine herb Ipomopsis aggregata and hybrids with its closest congener were subjected to a progressive dry down, mimicking the range of soil moistures experienced in the field. Floral volatiles and leaf gas exchange were measured at four time points during the drought.
Key Results
As the soil dried, floral volatile emissions increased overall and changed in composition, from more 1,3-octadiene and benzyl alcohol to higher representation of some terpenes. Emissions of individual compounds were not linearly related to volumetric water content in the soil. The dominant compound, the monoterpene α-pinene, made up the highest percentage of the scent mixture when soil moisture was intermediate. In contrast, emission of the sesquiterpene (E,E)-α-farnesene accelerated as the drought became more intense. Changes in floral volatiles did not track the time course of changes in photosynthetic rate or stomatal conductance.
Conclusions
This study shows responses of specific floral volatile organic compounds to soil moisture. The non-linear responses furthermore suggest that extreme droughts may have impacts that are not predictable from milder droughts. Floral volatiles are likely to change seasonally with early summer droughts in the Rocky Mountains, as well as over years as snowmelt becomes progressively earlier. Changes in water availability may have impacts on plant–animal interactions that are mediated through non-linear changes in floral volatiles.
Despite recent interest in the non-sugar components of floral nectar, nearly nothing is known about the ecological importance and phylogenetic distribution of scented nectar. If present, the scent of ...nectar would provide an honest signal to nectar-feeding animals. Nectar odors may directly impact plant reproductive fitness, through pollinator attraction or deterrence of nectar robbers and florivores. In addition, nectar odors may indirectly impact plant fitness through antimicrobial activity, pleiotropic interactions with plant defense, and communication with predators and parasitoids. The literature provides only circumstantial evidence for scented nectar, through the study of bee honey odors. Here I confirm the presence of scent in the nectar of four out of seven angiosperm species sampled with solid-phase micro-extraction and gas chromatography-mass spectrometry. In Abelia x grandiflora and Hedychium coronarium, nectar odors are a hydrophilic subset of the compounds emitted by surrounding floral tissues, suggesting passive absorption by the nectar standing crop. Sucrose solution applied to the petals of a nectarless flower, Magnolia grandiflora, absorbed a hydrophilic subset of scent compounds after one hour, lending support to this hypothesis. Nectar from Oenothera primiveris and Agave palmeri contained unique scent compounds compared to the floral tissues. The presence of fermentation volatiles in A. palmeri nectar suggests a dynamic role for yeast in its floral biology. These data highlight the need for systematic studies on the distribution and mechanistic importance of scented floral nectar to plant-animal interactions.
Unrelated organisms that share similar niches often exhibit patterns of convergent evolution in functional traits. Based on bimodal distributions of hawkmoth tongue lengths and tubular white flowers ...in Africa, this study hypothesized that long-tongued hawkmoths comprise a pollination niche (ecological opportunity) that is distinct from that of shorter-tongued hawkmoths.
Field observations, light trapping, camera surveillance and pollen load analysis were used to identify pollinators of plant species with very long-tubed (>8 cm) flowers. The nectar properties and spectral reflectance of these flowers were also measured. The frequency distributions of proboscis length for all captured hawkmoths and floral tube length for a representative sample of night-blooming plant species were determined. The geographical distributions of both native and introduced plant species with very long floral tubes were mapped.
The convolvulus hawkmoth Agrius convolvuli is identified as the most important pollinator of African plants with very long-tubed flowers. Plants pollinated by this hawkmoth species tend to have a very long (approx. 10 cm) and narrow flower tube or spur, white flowers and large volumes of dilute nectar. It is estimated that >70 grassland and savanna plant species in Africa belong to the Agrius pollination guild. In South Africa, at least 23 native species have very long floral tubes, and pollination by A. convolvuli or, rarely, by the closely related hawkmoth Coelonia fulvinotata, has been confirmed for 11 of these species. The guild is strikingly absent from the species-rich Cape floral region and now includes at least four non-native invasive species with long-tubed flowers that are pre-adapted for pollination by A. convolvuli.
This study highlights the value of a niche perspective on pollination, which provides a framework for making predictions about the ecological importance of keystone pollinators, and for understanding patterns of convergent evolution and the role of floral traits in plant colonization.
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