Pollination Mutualism Research Articles

The Evolution of Resource Provisioning in Pollination Mutualisms.

AbstractResource dynamics influence the contemporary ecology of consumer-resource mutualisms. Suites of resource traits, such as floral nectar components, also evolve in response to different selective pressures, changing the ecological dynamics of the interacting species at the evolutionary equilibrium. Here we explore the evolution of resource-provisioning traits in a biotically pollinated plant that produces nectar as a resource for beneficial consumers. We develop a mathematical model describing natural selection on two quantitative nectar traits: maximum nectar production rate and maximum nectar reservoir volume. We use this model to examine how nectar production dynamics evolve under different ecological conditions that impose varying cost-benefit regimes on resource provisioning. The model results predict that natural selection favors higher nectar production when ecological factors limit the plant or pollinator's abundance (e.g., a lower productivity environment or a higher pollinator conversion efficiency). We also find that nectar traits evolve as a suite in which higher costs of producing one trait select for a compensatory increase in investment in the other trait. This empirically explicit approach to studying the evolution of consumer-resource mutualisms illustrates how natural selection acting via direct and indirect pathways of species interactions generates patterns of resource provisioning seen in natural systems.

Cycad-Weevil Pollination Symbiosis Is Characterized by Rapidly Evolving and Highly Specific Plant-Insect Chemical Communication.

Coevolution between plants and insects is thought to be responsible for generating biodiversity. Extensive research has focused largely on antagonistic herbivorous relationships, but mutualistic pollination systems also likely contribute to diversification. Here we describe an example of chemically-mediated mutualistic species interactions affecting trait evolution and lineage diversification. We show that volatile compounds produced by closely related species of Zamia cycads are more strikingly different from each other than are other phenotypic characters, and that two distantly related pollinating weevil species have specialized responses only to volatiles from their specific host Zamia species. Plant transcriptomes show that approximately a fifth of genes related to volatile production are evolving under positive selection, but we find no differences in the relative proportion of genes under positive selection in different categories. The importance of phenotypic divergence coupled with chemical communication for the maintenance of this obligate mutualism highlights chemical signaling as a key mechanism of coevolution between cycads and their weevil pollinators.

Unique chemistry associated with diversification in a tightly coupled cycad-thrips obligate pollination mutualism

Cycad cone thermogenesis and its associated volatiles are intimately involved in mediating the behavior of their obligate specialist pollinators. In eastern Australia, thrips in the Cycadothrips chadwicki species complex are the sole pollinators of many Macrozamia cycads. Further, they feed and reproduce entirely in the pollen cones. M. miquelii, found only in the northern range of this genus, is pollinated only by a C. chadwicki cryptic species that is the most distantly related to others in the complex. We examined the volatile profile from M. miquelii pollen and ovulate (receptive and non-receptive) cones to determine how this mediates pollination mechanistically, using GC-MS (gas chromatography-mass spectrometry) and behavioral tests. Monoterpenes comprise the bulk of M. miquelii volatile emissions, as in other Macrozamia species, but we also identified compounds not reported previously in any cycad, including three aliphatic esters (prenyl acetate and two of uncertain identity) and two aliphatic alcohols. The two unknown esters were confirmed as prenyl (3-methylbut-2-enyl) esters of butyric and crotonic ((E))-but-2-enoic) acids after chemical synthesis. Prenyl crotonate is a major component in emissions from pollen and receptive ovulate cones, is essentially absent from non-receptive cones, and has not been reported from any other natural source. In field bioassays, Cycadothrips were attracted only to those volatile treatments containing prenyl crotonate. We discuss M. miquelii cone odorants relative to those of other cycads, especially with respect to prenyl crotonate being a species-specific signal to this northern C. chadwicki cryptic species, and how this system may have diversified.

Proximity to crop relatives determines some patterns of natural selection in a wild sunflower.

Abiotic and biotic heterogeneity result in divergent patterns of natural selection in nature, with important consequences for fundamental evolutionary processes including local adaptation, speciation, and diversification. However, increasing amounts of the global terrestrial surface are homogenized by agriculture (which covers nearly 50% of terrestrial vegetated land surface) and other anthropogenic activities. Agricultural intensification leads to highly simplified biotic communities for many taxa, which may alter natural selection through biotic selective agents. In particular, the presence of crops may alter selection on traits of closely related wild relatives via shared mutualists and antagonists such as pollinators and herbivores. We asked how the presence of crop sunflowers (Helianthus annuus) alters natural selection on reproductive traits of wild sunflowers (Helianthus annuus texanus). Across two years and multiple sites, we planted replicated paired populations of wild H. a. texanus bordering sunflower crop fields versus approximately 2.5 km away. We measured fitness, floral traits, and interactions of the plants with insect pollinators and seed predators. We found limited evidence that proximity to crop sunflowers altered selection on individual traits, as total or direct selection differed by proximity for only three of eleven traits: ray length (a marginally significant effect), Isophrictis (Gelechiidae, moth) attack, and Neolasioptera (Cecidomyiidae, midge) attack. Direct (but not total) selection was significantly more heterogenous far from crop sunflowers relative to near crop sunflowers. Both mutualist pollinators and antagonist seed predators mediated differences in selection in some population‐pairs near versus far from crop sunflowers. Here, we demonstrate that agriculture can influence the evolution of wild species via altered selection arising from shared biotic interactions, complementing previously demonstrated evolutionary effects via hybridization.

Criteria to select vegetal species for restoration of plant-pollinator interactions in agricultural landscapes of the Pampa grassland (Argentina)

Ecological functions, including pollination services, can be successfully restored in degraded ecosystems. In this study we propose a procedure for selection of target species to be employed in the restoration of plant-pollinator interactions in agricultural landscapes, which is illustrated by a case study located in the Tandilia System, in the Southern Pampa grasslands of Argentina. Based on information from a large pollination network dataset of 12 hills, composed of 172 pollinators and 96 plants (metaweb), we identified the plant species playing a major role in the maintenance of pollination mutualisms. We obtained a ranking of interaction frequency for each of the 96 plant species of the metaweb, and selected native plants that received more than 100 individual flower visitors. The targeted species were evaluated using ten criteria related to ecological, technical and cultural characteristics, and then ranked according to their suitability for use in restoration projects (species rank, SR). From the total number of plant species (96) registered for all sampled hills, we identified a total of 24 plant species that represented 90% of the total interactions and 25% of the plant species recorded in the metaweb. Six of the 24 selected species were excluded since they were non-native, leaving 18 targeted native plant species. The SR value ranged between 2.68 and 8, with a mean of 4.63 ± 1.40. Two genera presented the highest SR values (Eryngium sp. and Baccharis sp.), and are recognized as potential candidates for restoration of other ecosystems. A rank that evaluates plant species capable of rehabilitating plant-pollinator interactions will form a solid basis for planning restoration projects, which are crucial for biodiversity rehabilitation and conservation.

Genomes of 12 fig wasps provide insights into the adaptation of pollinators to fig syconia

Figs and fig pollinators are one of the few classic textbook examples of obligate pollination mutualism. The specific dependence of fig pollinators on the relatively safe living environment with sufficient food sources in the enclosed fig syconia implies that they are vulnerable to habitat changes. However, there is still no extensive genomic evidence to reveal the evolutionary footprint of this long-term mutually beneficial symbiosis in fig pollinators. In fig syconia, there are also non-pollinator species. The non-pollinator species differ in their evolutionary and life histories from pollinators. We conducted comparative analyses on 11 newly sequenced fig wasp genomes and one previously published genome. The pollinators colonized the figs approximately 66.9 million years ago, consistent with the origin of host figs. Compared with non-pollinators, many more genes in pollinators were subject to relaxed selection. Seven genes were absent in pollinators in response to environmental stress and immune activation. Pollinators had more streamlined gene repertoires in the innate immune system, chemosensory toolbox, and detoxification system. Our results provide genomic evidence for the differentiation between pollinators and nonpollinators. The data suggest that owing to the long-term adaptation to the fig, some genes related to functions no longer required are absent in pollinators.

Reproductive biology of the South American cycad Zamia boliviana, involving brood‐site pollination

AbstractBrood‐site pollination mutualisms represent extreme levels of reciprocal specialization between plants and insects. Several studies have revealed intimate associations between cycads and their insect pollinators across different continents. However, the reproductive biology of South American cycads is still poorly understood, with limited empirical data available. Here, we investigated the plant–pollinator interactions of Zamia boliviana (Cycadales, Zamiaceae), which is distributed on savanna patches in Brazil and Bolivia. Our aim was to examine reproductive biology (strobili development and their visitors) to identify potential pollinators from the perspective of dioecy and expectations of obligatory mutualism. We monitored reproductive cohorts and registered the strobiliʼs visitors. We classified the visitorsʼ activities and described the behavior of the most active and recurring ones in both reproductive structures to ascertain the potential pollinators and their relationship with the Z. boliviana. In situ experiments were used to demonstrate efficacy in seed production. Although other insects visit the strobili, only one Coleoptera (Erotylidae: Pharaxonotha) was present seasonally. Pharaxonotha cerradensis was the single species capable of transporting pollen and developing a life cycle associated with polleniferous strobili, while concomitantly visiting ovuliferous strobili. Experimental tests associated with observational evidence in the cycad indicated brood‐site pollination mutualism with the Erotylidae beetle, a potential pollinator of Z. boliviana. Our investigation confirmed a new case of obligatory mutualism between cycads and P. cerradensis in the New World. Future research on Zamia from South America should address pollination systems of this genus to better understand the ecology and evolution of plant–pollinator interactions.

Phosphorus fertilization induces nectar secretion for honeybee visitation and cross-pollination of almond trees.

Precise phosphorus (P) application requires a mechanistic understanding of mineral effects on crop biology and physiology. Photosynthate assimilation, metabolism, and transport require phosphorylation, and we postulated that P is critical for the bloom and fruit-set of almond trees that rely on stored carbohydrate reserves. Hence, we studied the growth, physiology and carbohydrate dynamics in 2-year-old almond trees irrigated with P concentrations between 1 mg l-1 and 20 mg l-1. Almond trees attained maximal photosynthesis, transpiration, and growth by 6 mg P l-1 irrigation. Nevertheless, almond trees continued to extract P in 10 mg P l-1 and 15 mg P l-1 irrigations, which corresponded to larger yields. We attributed the augmented productivity to increased fruit-set (59% between 6 mg P l-1 and 15 mg P l-1), caused by more frequent (29%) honeybee visits. High P improved pollinator visitation by enabling almond trees to utilize more of their starch reserves for nectar secretion (which increased by ~140% between 6 mg P l-1 and 15 mg P l-1). This work elucidates the benefits of P fertilization to plant-pollinator mutualism, critical to almond productivity, and reveals novel indices for optimal P application in almond orchards.

Genomic evidence of prevalent hybridization throughout the evolutionary history of the fig-wasp pollination mutualism

Ficus (figs) and their agaonid wasp pollinators present an ecologically important mutualism that also provides a rich comparative system for studying functional co-diversification throughout its coevolutionary history (~75 million years). We obtained entire nuclear, mitochondrial, and chloroplast genomes for 15 species representing all major clades of Ficus. Multiple analyses of these genomic data suggest that hybridization events have occurred throughout Ficus evolutionary history. Furthermore, cophylogenetic reconciliation analyses detect significant incongruence among all nuclear, chloroplast, and mitochondrial-based phylogenies, none of which correspond with any published phylogenies of the associated pollinator wasps. These findings are most consistent with frequent host-switching by the pollinators, leading to fig hybridization, even between distantly related clades. Here, we suggest that these pollinator host-switches and fig hybridization events are a dominant feature of fig/wasp coevolutionary history, and by generating novel genomic combinations in the figs have likely contributed to the remarkable diversity exhibited by this mutualism.

Multiple Attack to Inflorescences of an Annual Plant Does Not Interfere with the Attraction of Parasitoids and Pollinators

Plants in the flowering stage need to ensure reproduction by protecting themselves from attack and by preserving interactions with mutualist pollinators. When different plant mutualists are using the same type of cues, such as volatile compounds, attraction of parasitoids and pollinators may trade off. To explore this, we compared volatile emission of Brassica nigra plants in response to single or dual attack on their inflorescences. Additionally, we recorded flower visitation by pollinators and the attraction of parasitoids in the greenhouse and/or field. Brassica nigra were exposed in the flowering stage to one or two of the following three attackers: Brevicoryne brassicae aphids, Pieris brassicae caterpillars, and Xanthomonas campestris pv. raphani bacteria. We found that single attack by caterpillars, and dual attack by caterpillars plus aphids, induced the strongest changes in plant volatile emission. The caterpillars’ parasitoid C. glomerata did not exhibit preference for plants exposed to caterpillars only vs. plants exposed to caterpillars plus aphids or plus bacteria. However, the composition of the pollinator community associated with flowers of B. nigra was affected by plant exposure to the attackers, but the total number of pollinators visiting the plants did not change upon attack. We conclude that, when B. nigra were exposed to single or dual attack on their inflorescences, the plants maintained interactions with natural enemies of the insect attackers and with pollinators. We discuss how chemical diversity may contribute to plant resilience upon attack.

The Scent of Life: Phoretic Nematodes Use Wasp Volatiles and Carbon Dioxide to Choose Functional Vehicles for Dispersal.

Hitchhikers (phoretic organisms) need vehicles to disperse out of unsuitable habitats. Therefore, finding vehicles with the right functional attributes is essential for phoretic organisms. To locate these vehicles, phoretic organisms employ cues within modalities, ranging from visual to chemical senses. However, how hitchhikers discriminate between individual vehicles has rarely been investigated. Using a phoretic nematode community associated with an obligate fig-fig wasp pollination mutualism, we had earlier established that hitchhiking nematodes make decisions based on vehicle species identity and number of conspecific hitchhikers already present on the vehicle. Here we investigate if hitchhikers can differentiate between physiological states of vehicles. We asked whether phoretic nematodes choose between live or dead vehicles present in a chemically crowded environment and we investigated the basis for any discrimination. We conducted two-choice and single-choice behavioral assays using single nematodes and found that plant- and animal-parasitic nematodes preferred live over dead vehicles and used volatiles as a sensory cue to make this decision. However, in single-choice assays, animal-parasitic nematodes were also attracted towards naturally dead or freeze-killed wasps. The volatile profile of the wasps was dominated by terpenes and spiroketals. We examined the volatile blend emitted by the different wasp physiological states and determined a set of volatiles that the phoretic nematodes might use to discriminate between these states which is likely coupled with respired CO2. We determined that CO2 levels emitted by single wasps are sufficient to attract nematodes, demonstrating the high sensitivity of nematodes to this metabolic product.

Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms.

Hitchhikers (phoretic organisms) identify their vehicles using species-specific visual, chemical and vibrational cues. However, what factors influence their choice between vehicles of the same species has rarely been investigated. Hitchhikers must not only avoid overcrowded vehicles but may also need to travel with conspecifics to ensure mates at their destination. Hence, a trade-off between overcrowding and presence of conspecifics likely determines the choice of a vehicle especially when destination sites are distant, ephemeral and unique. Here, we investigate whether a trade-off between the presence of conspecifics versus overcrowding by conspecifics or heterospecifics on a vehicle affects hitchhiker choice. We also investigate the sensory modality responsible for this choice. We experimentally examine these questions using a phoretic nematode community (containing plant- and animal-parasitic taxa) obligately associated with a brood-site pollination mutualism. In this model system, nematodes co-travel with conspecifics and heterospecifics on pollinators as vehicles, between ephemeral plant brood sites to complete their developmental life cycle. In this system, hitchhiker overcrowding has proven negative impacts on vehicle and plant fitness. We expected nematodes to respond to conspecifics and heterospecific density on offered vehicles when making their choice. We found that animal-parasitic nematodes preferred vehicles containing some conspecifics within a certain density range. However, plant-parasitic nematodes preferentially boarded vehicles that were devoid of conspecifics or had few conspecifics. Plant parasites that preferred empty vehicles likely hitchhiked in pairs. Both nematode types employed volatile cues to discriminate between vehicles with different conspecific nematode densities. Our results suggest that vehicle overcrowding by conspecifics, most likely, guaranteed access to mates at the destination determined hitchhiker choice. Surprisingly, and contrary to our expectations, plant- and animal-parasitic nematodes did not respond to heterospecific crowding on vehicles and did not discriminate between vehicles with different heterospecific nematode densities. The reason for this lack of response to heterospecific presence is unknown. This study not only shows that phoretic organisms use different strategies while choosing a vehicle but also confirms that density-dependent effects can ensure the stability and persistence of phoretic interactions in a mutualism by balancing overcrowding against reproductive assurance.

Increase in humidity widens heat tolerance range of tropical Ceratosolen fig wasps

1. Fig wasps are the obligate mutualistic pollinators of fig trees, which are important components of tropical forests. The stability of these species interactions, in the face of environmental changes, relies heavily on the thermal tolerance of these wasps.2. This study determined the upper thermal limits of three tropical Ceratosolen fig wasp species. Humidity levels and collection season were varied to determine the effect of water availability on heat tolerance.3. Wasps were placed in incubators to simulate different temperature regimes (30–45 °C) with varying humidity conditions. Wasp populations from either the dry or wet seasons were tested. Upper lethal temperature was determined by recording wasp survival.4. All factors (temperature, humidity, season, wasp species, and their interactions) significantly affected wasp longevity. Exposure to high temperatures resulted in a significant decrease in wasp longevity: longest at 30 °C and the ratio decreased rapidly at 40 and 45 °C. An increase in temperature from 30 to 35 °C caused at least a two‐fold reduction in wasp lifespan. More surprisingly, humid conditions allowed survival for two to six times longer than non‐humid conditions in high temperatures (40–45 °C). Wasps obtained during the wet season also survived longer than those from the dry season. Increased water availability (i.e. during wet season and with high humidity conditions) thus increased wasp upper thermal limits.5. Relative humidity was a strong limiting factor in the heat tolerance of tropical wasps. Persistence of insect species that are narrowly‐distributed will depend on the presence of intact, high‐humidity habitats.

Formica francoeuri responds to pheromones and defensive chemical cues of social bees

Insects must detect and respond to diverse chemical cues in a complex chemical landscape. Intraspecific and intraguild communication have received a lot of attention, especially among bee taxa. However, little is known about interspecific chemical communication in general and in non-bees in particular. Ants, such as Formica francoeuri, also are opportunistic floral visitors who seek the carbohydrate-rich rewards of flowers. Thus, these ants likely encounter aggressive competitors for nectar, such as bees. Here, we performed a series of experiments to examine how ant foragers respond to bee pheromones, venom and sting glands in the context of foraging. Understanding how ants utilize non-target chemical cues will identify previously cryptic interactions and provide new insights into the hidden mechanisms governing foraging decisions. As the foraging decisions by floral visitors have a direct impact on the pollination mutualism, studies such as this will help us build better predictive models of plant–pollinator networks and develop hypotheses as to how these interaction networks may change with shifts in the floral visitor community.

Behaviors and Interactions of Insects in Mid-Mesozoic Ecosystems of Northeastern China

During the past 20 years, more than 1,600 species of well-preserved fossil insects, including members of over 270 families within 24 orders, have been described from the Middle Jurassic Yanliao Entomofauna and Early Cretaceous Jehol Entomofauna in Northeastern China. Diversified fossil insects not only document the origin, systematics, and early evolution of many lineages, but also reveal these lineages' behaviors and interactions with coexisting plants, vertebrates, and other insects in their ecosystems. Fossil evidence has been documented, for example, regarding insects' feeding and pollination mutualism with gymnosperms; ectoparasitic feeding on blood of vertebrates; camouflage, mimicry of gymnosperm plants, and eyespot warning; sound stridulation for attracting potential mates; and sexual display, mating, egg-laying, and parental care. In this article, we review the diverse taxonomy of mid-Mesozoic insects of Northeastern China and elucidate their behaviors and interactions within their ecosystems, which have impacted their early evolution and development into extant insects.

An early gall-inducing parasitic wasp adversely affects the fitness of its host Ficus tree but not the pollinator

The fig tree-fig pollinator mutualism is one of the most tightly knit symbiotic systems. The research on the ecology of non-pollinators which exploit the mutualism without providing services to the host is very limited and conclusions about the role they play in the maintenance of this mutualism are full of contradictions. The non-pollinating fig wasps species are highly diverse in their feeding habit and ecological function, which may result in different consequences on the mutualism. Sycophaga testacea is an early-ovipositing galler hosted by Ficus racemosa, which is a potencial competitor to the pollinators as they use the same female flowers in the fig as their ovipositing sites. In this study, we investigate the effect of S. testacea on the production of both pollinator and fig tree with a field control experiment. Seed production is decreased significantly when the figs were parasitized, while the offspring production of the pollinator is not significantly affected, which indicates that this galler species has a harmful effect on the fitness of its host fig tree but not the pollinator. The overall development ratio of the galls is decreased significantly when the figs were parasitized, and we found that the intrinsic low development ratio of S. testacea is responsible for the decrease in the overall development ratio.

Reduced Water Negatively Impacts Social Bee Survival and Productivity Via Shifts in Floral Nutrition.

Pollinators provide a key ecosystem service vital for the survival and stability of the biosphere. Identifying factors influencing the plant–pollinator mutualism and pollinator management is necessary for maintaining a healthy ecosystem. Since healthy beehives require substantial amounts of carbohydrates (nectar) and protein (pollen) from forage plants such as clover, we must assess how resources offered by plants change under limited water conditions in order to fully understand how drought modifies the pollination mutualism. Here we document how reduced water availability leads to decreased nectar quality and quantity and decreased protein quality of pollen. Furthermore, we provide conclusive evidence that these lower quality resources lead to decreased survival and productivity in both developing honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae). The results emphasize the importance of the nutritional effects of reduced water on bees when predicting shifts of pollination mutualisms under climate change.

Sweet Flag Flowers Act as Cradles for Tiny Beetle Pollinators

Sweet flag, Acorus calamus, is one of the basal-most monocots and is commonly found in wetlands of the Northern Hemisphere. Although sweet flag has long been considered insect-pollinated, the pollinators of this plant have never been reported. We found that two species of tiny beetle, Platamartus jakowlewi and Sibirhelus corpulentus (Kateretidae), carried pollen grains of sweet flag in Japan. These beetles oviposit on the inflorescences, and the hatched larvae feed on pollen and other plant tissues of inflorescences. Our results suggest that the basal-most monocot A. calamus is pollinated by specialized beetles that use the inflorescences as a breeding site. These photographs illustrate the article “Entomophily in Acorus calamus: implications for brood-site pollination mutualism in basal-most monocots” by Daichi Funamoto, Tomoyuki Suzuki, and Shinji Sugiura published in Ecology. https://doi.org/10.1002/ecy.3089

Chemical signal is in the blend: bases of plant-pollinator encounter in a highly specialized interaction

In several highly specialized plant-insect interactions, scent-mediated specificity of pollinator attraction is directed by the emission and detection of volatile organic compounds (VOCs). Although some plants engaged in such interactions emit singular compounds, others emit mixtures of VOCs commonly emitted by plants. We investigated the chemical ecological bases of host plant recognition in the nursery pollination mutualism between the dioecious Ficus carica and its specific pollinator Blastophaga psenes. Using Y-tube olfactometer tests, we show that B. psenes females are attracted by VOCs of receptive figs of both sexes and do not exhibit preference for VOCs of either male or female figs. Electrophysiological tests and chemical analysis revealed that of all the VOCs emitted by receptive figs, only five were found to be active on female antennae. Behavioural tests show that, in contrast to VOCs presented alone, only a blend with a particular proportion of four of these VOCs is as attractive as the odour of receptive figs, and that if there is a very small change in this blend proportion, the pollinator is no longer attracted. This study revealed that in highly specialized mutualistic interactions specificity could be mediated by a particular blend of common compounds emitted by plants.

The ecological consequences of herbivore-induced plant responses on plant-pollinator interactions.

Plant induced responses to herbivory have long been found to function as plant direct and indirect defenses and to be major drivers of herbivore community and population dynamics. While induced defenses are generally understood as cost-saving strategies that allow plants to allocate valuable resources into defense expression, it recently became clear that, in particular, induced metabolic changes can come with significant ecological costs. In particular, interactions with mutualist pollinators can be significantly compromised by herbivore-induced changes in floral morphology and metabolism. We review recent findings on the evidence for ecological conflict between defending against herbivores and attracting pollinators while using similar modes of information transfer (e.g. visual, olfactory, tactile). Specifically, we discuss plant traits and mechanisms through which plants mediate interactions between antagonists and mutualist and present functional hypotheses for how plants can overcome the resulting conflicts.