A sheep in wolf's clothing: do carrion and dung odours of flowers not only attract pollinators but also deter herbivores?

Carrion and dung odours of various flowers have traditionally been considered an adaptation for attracting the flies and beetles that pollinate them. While we accept the role of such odours in pollinator attraction, we propose that they may also have another, overlooked, anti‐herbivore defensive function. We suggest that such odours may deter mammalian herbivores, especially during the critical period of flowering. Carrion odour is a good predictor for two potential dangers to mammalian herbivores: (1) pathogenic microbes, (2) proximity of carnivores. Similarly, dung odour predicts faeces‐contaminated habitats that present high risks of parasitism. These are two new types of repulsive olfactory aposematic mimicry by plants: (1) olfactory feigning of carcass (thanatosis), a well‐known behavioural defensive strategy in animals, (2) olfactory mimicry of faeces, which also has a defensive visual parallel in animals.     

Omnivores as plant bodyguards—A model of the importance of plant quality

The importance of omnivores in ecological systems is increasingly being recognized, not least due to their intensified use as biocontrol agents in crop production. We model a simple plant–herbivore–omnivore (predator) system to explore the effects of plant suitability as food for omnivores on the outcome of omnivore–herbivore interactions. The model predicts that increasing plant suitability relative to herbivore suitability for the omnivore will catalyze the extinction of herbivores or omnivores, depending on the relative growth rate of omnivores feeding solely on plants or herbivores. When omnivore growth is higher on plants, either the omnivore or the herbivore goes extinct. When omnivore growth is higher on herbivores, the possible consequences are extinction, stable coexistence, and limit cycles, depending on the combination of species properties. Our results suggest that plants in some situations may evolve towards becoming more suitable to omnivores to escape detrimental herbivores and that breeders could manipulate crop suitability to omnivore species to reach a desired outcome of omnivore–herbivore interactions.     

Making the most of your pollinators: An epiphytic fig tree encourages its pollinators to roam between figs

Ficus species are characterized by their unusual enclosed inflorescences (figs) and their relationship with obligate pollinator fig wasps (Agaonidae). Fig trees have a variety of growth forms, but true epiphytes are rare, and one example is Ficus deltoidea of Southeast Asia. Presumably as an adaptation to epiphytism, inflorescence design in this species is exceptional, with very few flowers in female (seed‐producing) figs and unusually large seeds. Figs on male (pollinator offspring‐generating) trees have many more flowers. Many fig wasps pollinate one fig each, but because of the low number of flowers per fig, efficient utilization by F. deltoidea''s pollinators depends on pollinators entering several female figs. We hypothesized that it is in the interest of the plants to allow pollinators to re‐emerge from figs on both male and female trees and that selection favors pollinator roaming because it increases their own reproductive success. Our manipulations of Blastophaga sp. pollinators in a Malaysian oil palm plantation confirmed that individual pollinators do routinely enter several figs of both sexes. Entering additional figs generated more seeds per pollinator on female trees and more pollinator offspring on male trees. Offspring sex ratios in subsequently entered figs were often less female‐biased than in the first figs they entered, which reduced their immediate value to male trees because only female offspring carry their pollen. Small numbers of large seeds in female figs of epiphytic F. deltoidea may reflect constraints on overall female fig size, because pollinator exploitation depends on mutual mimicry between male and female figs.     

Direct and indirect effects of pollinators and seed predators to selection on plant and floral traits

Although flowering traits are often assumed to be under strong selection by pollinators, significant variation in such traits remains the norm for most plant species. Thus, it is likely that the interactions among plants, mutualists, and other selective agents, such as antagonists, ultimately shape the evolution of floral and flowering traits. We examined the importance of pollination vs pre-dispersal seed predation to selection on plant and floral characters via female plant-reproductive success in Castilleja linariaefolia (Scrophulariaceae). C. linariaefolia is pollinated by hummingbirds and experiences high levels of pre-dispersal seed predation by plume moth and fly larvae in the Rocky Mountains of Colorado, USA, where this work was conducted. We first examined whether female reproduction in C. linariaefolia was limited by pollination. Supplemental pollination only marginally increased components of female reproduction, likely because seed predation masked, in part, the beneficial effects of pollen addition. In unmanipulated populations, we measured calyx length, flower production, and plant height and used path analysis combined with structural equation modeling to quantify their importance to relative seed set through pathways involving pollination vs seed predation. We found that the strength of selection on calyx length, flower production, and plant height was greater for seed predation pathways than for pollination pathways, and one character, calyx length, experienced opposing selection via pollination vs seed predation. These results suggest that the remarkable intraspecific variation in plant and floral characters exhibited by some flowering plants is likely the result of selection driven, at least in part, by pollinators in concert with antagonists, such as pre-dispersal seed predators. This work highlights the subtle but complex interactions that shape floral and vegetative design in natural ecosystems.     

Quantity versus quality: identifying the most effective pollinators of the hummingbird-pollinated Vriesea rodigasiana (Bromeliaceae)

Although hummingbirds are considered the major bromeliad pollinators, different species may contribute differently to pollination. This study analyses the importance of different hummingbirds to pollination of Vriesea rodigasiana (Bromeliaceae), based on visitation frequency (a quantity component) and germinated pollen load per visit (a quality component) in the Atlantic rainforest of southeastern Brazil. This bromeliad flowers for 3–4 months with a peak in March. Its yellow, tubular flowers last about 13 h and demonstrate approach herkogamy. During flowering peak, Thalurania glaucopis visited more flowers than Ramphodon naevius, whereas by the end of the flowering season the latter visited more. Differences in hummingbird bill length resulted in different pollen placement and stigma contact. The short-billed T. glaucopis received pollen on the top of its head, depositing it on the center of the stigma, while the long-billed R. naevius received it on the proximal part of its bill, depositing it on the lower lobe of the stigma. Flowers visited by T. glaucopis had six times more pollen tubes than those visited by R. naevius. Our results suggest that this functional group of hummingbirds may be split into even smaller groups, namely short-billed and long-billed hummingbirds, based on different sites of pollen placement. Although both species were pollen vectors of V. rodigasiana, the short-billed T. glaucopis was its most effective pollinator in the area supporting Stebbin’s principle, linking floral features and good pollinators.     

Mammal pollinators lured by the scent of a parasitic plant

To communicate with animals, plants use signals that are distinct from their surroundings. Animals generally learn to use these signals through associative conditioning; however, signals are most effective when they elicit innate behavioural responses. Many plant species have flowers specialized for pollination by ground-dwelling mammals, but the signals used to attract these pollinators have not been elucidated. Here, we demonstrate the chemical basis for attraction of mammal pollinators to flowers of the dioecious parasitic plant Cytinus visseri (Cytinaceae). Two aliphatic ketones dominate the scent of this species; 3-hexanone, which elicits strong innate attraction in rodents, and 1-hexen-3-one, which repels them in isolation, but not in combination with 3-hexanone. The aliphatic ketone-dominated scent of C. visseri contrasts with those of insect-pollinated plants, which are typically dominated by terpenoids, aromatic or non-ketone aliphatic compounds. 3-hexanone is also known from some bat-pollinated species, suggesting independent evolution of plant signals in derived, highly specialized mammal-pollination systems.     

Evidence for the recruitment of florivorous plant bugs as pollinators

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Beyond pollinator attraction: extra-floral displays deter herbivores in a Mediterranean annual plant

The evolution of several floral traits is thought to be driven by multiple selective agents, including pollinators and herbivores. Similar combinations of selection pressures may have shaped extra-floral traits. The conspicuous purple tufts of leaves (“flags”), which often terminate vertical inflorescences in the Mediterranean annual Salvia viridis, were shown to attract insect pollinators to the flowering patch. Here we test whether they also function as anti-herbivore signals. We determined the aposematic potential of S. viridis flags on three levels: concentrations of anthocyanins, suggested to function as aposematic visual signals, in leaves and flags; spectrometry to estimate whether the color-vision system of two common Mediterranean generalist herbivores (locusts and goats) can discriminate flags from leaves; and choice experiments to determine food preferences of the same herbivores. Anthocyanin concentrations in flags were >10-fold higher than in leaves. Flags exhibited peak reflectance at 450 and 700 nm wavelengths, while leaves reflected maximally at 550 nm. According to the Vorobyev-Osorio color vision model, these differences in color reflection are likely to allow visual discrimination by herbivores. Goats preferred feeding on clipped inflorescences over control inflorescences. Locusts preferred leaves over flags. To test whether this was due to deterrence from the flags’ coloration, we also offered them choice between leaves and a rare, white morph, of the flags. The locusts chose both equally immediately after presentation, but leaves attracted more individuals after 5 min of feeding. The locusts also preferred green cabbage over anthocyanin-rich red cabbage. These results support the function of colorful extra-floral displays as warning signals.     

A reassessment of the function of floral nectar in Croton suberosus (Euphorbiaceae): A reward for plant defenders and pollinators

Typically, plant-pollinator interactions are recognized as mutualistic relationships. Flower visitors, however, can potentially play multiple roles. The floral nectar in Croton suberosus has been proposed to operate as a reward for predators, especially the wasp Polistes instabilis (Vespidae), which kills herbivorous insects, while the plant has been thought to be mainly wind-pollinated. In this study, we reassessed the pollination mode of C. suberosus and the possible role of its flower visitors. Pollinator exclusion experiments demonstrated that C. suberosus should be considered a strictly entomophilous species. Inflorescences of C. suberosus were visited by a diverse entomofauna involving 28 taxa belonging to six orders; however, wasps and bees were the only visitors that carried C. suberosus pollen. The visitation rate of wasps was approximately four times that of bees. This observation, combined with the fact that the small size of bees makes effective contact of their bodies with the stigma difficult, strongly suggests that large wasps are responsible for most of the effective pollination of C. suberosus. Among the wasp visitors, P. instabilis seems to be one of the most important. These findings expose an unusual plant-insect interaction, in which the plant provides nectar and wasps pollinate and defend the plant.     

Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators

Plant populations often exist in spatially heterogeneous environments. Light level can directly affect plant reproductive success through resource availability or by altering pollinator behavior. It can also indirectly influence reproductive success by determining floral display size which may in turn influence pollinator attraction. We evaluated direct and indirect effects of light availability and measured phenotypic selection on phenological traits that may enhance pollen receipt in the insect-pollinated herb Campanulastrum americanum. In a natural population, plants in the sun had larger displays and received 7 times more visits than plants in the shade. Using experimental arrays to separate the direct effects of irradiance on insects from their response to display size, we found more visits to plants in the sun than in the shade, but no association between number of visits each flower received and display size. Plants in the sun were not pollen limited but pollen-augmented shade flowers produced 50% more seeds than open-pollinated flowers. Phenological traits, which may influence pollen receipt, were not under direct selection in the sun. However, earlier initiation and a longer duration of flowering were favored in the shade, which may enhance visitation in this pollen-limited habitat.     

Attracting pollinators and avoiding herbivores: insects influence plant traits within and across years

Perennial plants interact with herbivores and pollinators across multiple growing seasons, and thus may respond to herbivores and pollinators both within and across years. Joint effects of herbivores and pollinators influence plant traits, but while some of the potential interactions among herbivory, pollination, plant size, and plant reproductive traits have been well studied, others are poorly understood. This is particularly true for perennial plants where effects of herbivores and pollinators may manifest across years. Here, we describe two experiments addressing the reciprocal interactions of plant traits with herbivore damage and pollination across 2 years using the perennial plant Chamerion angustifolium. We measured (1) plant responses to manipulation of damage and pollination in the year of treatment and the subsequent season, (2) damage and pollination responses to manipulation of plant size and flowering traits in the year of treatment, and (3) plant-mediated indirect interactions between herbivores and pollinators. We found that plant traits had little effect on damage and pollination, but damage and pollination affected plant traits in both the treatment year and the subsequent year. We found evidence of indirect effects between leaf herbivores and pollinators in both directions; indirect effects of pollinators on leaf herbivores have not been previously demonstrated. Our results indicate that pollen receipt results in shorter plants with fewer stems but does not change flower number, while leaf herbivory results in taller plants with fewer flowers. Together, herbivory and pollination may contribute to intermediate plant height and plants with fewer stems and flowers in our system.     

Crane flies and microlepidoptera also function as pollinators in Epidendrum (Orchidaceae: Laeliinae): the reproductive biology of E. avicula

Crane flies and microlepidoptera have been recorded as pollinators in unrelated orchid groups, but these insects have never been recorded in Epidendroideae, the most species‐rich orchid subfamily, which includes one of the most diverse genera among Orchidaceae, Epidendrum. Based on data on phenology, floral morpho‐anatomy, pollinators, pollination mechanisms and breeding system, the reproductive biology of E. avicula was studied in south‐eastern Brazil. Epidendrum avicula possess osmophores that produce a citric fragrance at night. The flowers attract Tipulidae flies and several families of microlepidoptera that drink the nectar produced in a tube formed by the adnation of the labellum and column. As is common in Epidendrum, after removing the pollinarium, both crane flies and micro‐moths get trapped by the proboscis, which frightens the insects and inhibits any possible intent to immediately visit another flower. The behavior of the pollinators on flowers, plus the retention of the anther cap by the pollinarium, results in a reduction in the occurrence of geitonogamy. Because E. avicula is self‐incompatible, the consequence of pollinator behavior and the floral mechanisms tend to reduce the pollen loss. As far as we know, this is the first study to report the reproductive biology of a species of Epidendroideae pollinated by crane flies and microlepidoptera. Based on more recent concepts of plant–pollinator interactions, although E. avicula is pollinated by several species belonging to two distinct orders, suggesting an unspecialized pollination system is involved, nectar‐seeking microlepidoptera and Tipulidae flies can be recognized as a single functional group.     

Scent chemistry and pollinators in the holoparasitic plant Cynomorium songaricum (Cynomoriaceae)

• Holoparasitic plants are interesting heterotrophic angiosperms. However, carrion‐ or faeces‐mimicking is rarely described for such plants. There is no information on the pollination biology of Cynomoriaceae, despite the fact that these plants are rare and vulnerable. This is the first study to reveal pollination in a member of this family, Cynomorium songaricum, a root holoparasite with a distinctive and putrid floral odour.
• From 2016 to 2018, we studied the floral volatiles, floral visitors and pollinators, behavioural responses of visitors to floral volatiles, breeding system, flowering phenology and floral biology of two wild populations of C. songaricum in Alxa, Inner Mongolia, China.
• A total of 42 volatiles were identified in inflorescences of C. songaricum. Among these volatiles are compounds known as typical carrion scents, such as p‐cresol, indole, dimethyl disulphide and 1‐octen‐3‐ol. C. songaricum is pollinated by various Diptera, such as Musca domestica, M. stabulans (Muscidae), Delia setigera, D. platura (Anthomyiidae), Lucilia sericata, L. caesar (Calliphoridae), Wohlfahrtia indigens, Sarcophaga noverca, S. crassipalpis and Sarcophila meridionalis (Sarcophagidae). The inflorescence scent of C. songaricum attracted these pollinators. The plants significantly benefit from insect pollination, although wind can be a pollen vector in the absence of pollinators. C. songaricum is a cross‐pollinated, self‐incompatible plant.
• Our findings suggest that C. songaricum releases malodorous volatiles to attract Diptera to achieve pollination. This new example lays the foundation for further comparative studies in other members of this plant group and contributes to a better understanding of fly‐pollinated, carrion mimicking plants.

     

Virulence not only costs but also benefits the transmission of a fungal virus

Current theory suggests that cost-benefit relationships govern the evolution of parasite virulence. The cost of virulence is expected to be high for fungal viruses, which are obligate parasites and completely dependent on their hosts. The majority of fungal viruses infect their hosts without any apparent symptoms. Cryphonectria hypovirus 1 (CHV-1), in contrast, is virulent and debilitates its host, Cryphonectria parasitica. However, the virulence of CHV-1 is associated with high costs for virus transmission, such as an attenuated fungal growth and reduced production of the fungal spores spreading the virus. In this study, we tested the hypothesis that virulence may not only have costs but also benefits for transmitting CHV-1 across vegetative incompatibility barriers between fungi. We investigated viruses with low, medium, and high virulence, and determined their transmission rate per host-to-host contact (transmissibility). The average transmission rate across all combinations tested was 53% for the most virulent virus, 37% for the virus with intermediate virulence, and 20% for the virus with lowest virulence. These results showed that increased virulence was strongly correlated with increased transmissibility, potentially counterbalancing virulence costs. This association of virulence and transmissibility may explain why CHV-1 spread widely and evolved higher virulence than most other fungal viruses.     

Strike while the ionome is hot: making the most of plant genomic advances

Research into plant nutrition focuses on how plants maintain elemental differences from the surrounding environment. Classic genetic analysis has been hindered because it is not possible to accurately screen for perturbations in this disequilibrium. Recent work by Lahner and colleagues has enabled efficient screening and identification of plants that have altered elemental profiles.     

The indirect benefits of mating with attractive males outweigh the direct costs

The fitness consequences of mate choice are a source of ongoing debate in evolutionary biology. Recent theory predicts that indirect benefits of female choice due to offspring inheriting superior genes are likely to be negated when there are direct costs associated with choice, including any costs of mating with attractive males. To estimate the fitness consequences of mating with males of varying attractiveness, we housed female house crickets, Acheta domesticus, with either attractive or unattractive males and measured a variety of direct and indirect fitness components. These fitness components were combined to give relative estimates of the number of grandchildren produced and the intrinsic rate of increase (relative net fitness). We found that females mated to attractive males incur a substantial survival cost. However, these costs are cancelled out and may be outweighed by the benefits of having offspring with elevated fitness. This benefit is due predominantly, but not exclusively, to the effect of an increase in sons' attractiveness. Our results suggest that the direct costs that females experience when mating with attractive males can be outweighed by indirect benefits. They also reveal the value of estimating the net fitness consequences of a mating strategy by including measures of offspring quality in estimates of fitness.     

Precipitation and predation risk alter the diversity and behavior of pollinators and reduce plant fitness

Biotic and abiotic factors may individually or interactively disrupt plant–pollinator interactions, influencing plant fitness. Although variations in temperature and precipitation are expected to modify the overall impact of predators on plant–pollinator interactions, few empirical studies have assessed if these weather conditions influence anti-predator behaviors and how this context-dependent response may cascade down to plant fitness. To answer this question, we manipulated predation risk (using artificial spiders) in different years to investigate how natural variation in temperature and precipitation may affect diversity (richness and composition) and behavioral (visitation) responses of flower-visiting insects to predation risk, and how these effects influence plant fitness. Our findings indicate that predation risk and an increase in precipitation independently reduced plant fitness (i.e., seed set) by decreasing flower visitation. Predation risk reduced pollinator visitation and richness, and altered species composition of pollinators. Additionally, an increase in precipitation was associated with lower flower visitation and pollinator richness but did not alter pollinator species composition. However, maximum daily temperature did not affect any component of the pollinator assemblage or plant fitness. Our results indicate that biotic and abiotic drivers have different impacts on pollinator behavior and diversity with consequences for plant fitness components. Even small variation in precipitation conditions promotes complex and substantial cascading effects on plants by affecting both pollinator communities and the outcome of plant–pollinator interactions. Tropical communities are expected to be highly susceptible to climatic changes, and these changes may have drastic consequences for biotic interactions in the tropics.