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Applications in Plant Sciences 2023Imaging technologies that capture three-dimensional (3D) variation in floral morphology at micro- and nano-resolutions are increasingly accessible. In herkogamous...
PREMISE
Imaging technologies that capture three-dimensional (3D) variation in floral morphology at micro- and nano-resolutions are increasingly accessible. In herkogamous flowers, such as those of , structural barriers between anthers and stigmas represent bottlenecks that restrict pollinator size and access to reproductive organs. To study the unresolved pollination biology of cacao, we present a novel application of micro-computed tomography (micro-CT) using floral dimensions to quantify pollinator functional size limits.
METHODS
We generated micro-CT data sets from field-collected flowers and museum specimens of potential pollinators. To compare floral variation, we used 3D Slicer to place landmarks on the surface models and performed a geometric morphometric (GMM) analysis using geomorph R. We identified the petal side door (an opening between the petal hoods and filament) as the main bottleneck for pollinator access. We compared its mean dimensions with proposed pollinators to identify viable candidates.
RESULTS
We identified three levels of likelihood for putative pollinators based on the number of morphological (body) dimensions that fit through the petal side door. We also found floral reward microstructures whose presence and location were previously unclear.
DISCUSSION
Using micro-CT and GMM to study the 3D pollination biology of cacao provides new evidence for predicting unknown pollinators. Incorporating geometry and floral rewards will strengthen plant-pollinator trait matching models for cacao and other species.
PubMed: 37915432
DOI: 10.1002/aps3.11549 -
Ecology and Evolution Jul 2023Mason bees ( spp.) are efficient fruit tree pollinators that can be encouraged to occupy and breed in artificial nesting material. In sweet cherry orchards, they are...
Mason bees ( spp.) are efficient fruit tree pollinators that can be encouraged to occupy and breed in artificial nesting material. In sweet cherry orchards, they are occasionally used as an alternative managed pollinator as a replacement for or in addition to honey bees (). Yet, the lack of practical guidelines on management practices, for example optimal stocking rates, for both mason bee nesting material and honey bees might compromise pollination service provision. In this study, we assessed the relationship between stocking rates (honey bee hives and mason bee nesting material) and the abundance of honey bees and mason bees in 17 sweet cherry () orchards in Central Germany. We furthermore performed a pollination experiment to explore the interactive effect of mason bees and honey bees on sweet cherry fruit set. In the orchards, both honey bee and mason bee abundance increased with increasing stocking rates of hives or nesting material, respectively. Honey bee abundance increased linearly with stocking rates. In contrast, mason bee abundance asymptoted at 2-3 nesting boxes per ha, beyond which more boxes resulted in little increase in visitation rate. Our pollination experiment demonstrated that orchards were pollen limited, with only 28% of insect-pollinated flowers setting fruit versus 39% of optimally hand-pollinated flowers. Honey bees and mason bees enhanced sweet cherry fruit set, but only when both were present and not when either was present alone in an orchard. Our findings demonstrate that offering nesting material for mason bees and employing honey bee hives can enhance bee abundance in sweet cherry orchards. By increasing honey bee abundance in combination with enhanced mason bee abundance, farmers can substantially boost fruit set and potentially sweet cherry yield. To enhance pollination services, farmers should consider the benefits of increasing pollinator biodiversity as an immediate benefit to improve crop yields.
PubMed: 37435028
DOI: 10.1002/ece3.10289 -
Annals of Botany Oct 2023Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive....
BACKGROUND AND AIMS
Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus allows testing for specialization to pollination vectors in the absence of this feature.
METHODS
We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion.
KEY RESULTS
Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny, whereas longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively.
CONCLUSIONS
Although detectable suites of integrated floral traits across Thalictrum were correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying the evolution of pollination mode in Thalictrum, presumably via different paths from an ancestral mixed pollination state.
Topics: Animals; Phylogeny; Pollination; Bayes Theorem; Flowers; Reproduction; Insecta; Thalictrum
PubMed: 37235981
DOI: 10.1093/aob/mcad069 -
Nature Communications Jul 2023Animal pollination supports the production of a wide range of food crops fundamental to maintaining diverse and nutritionally balanced diets. Here, we present a global... (Meta-Analysis)
Meta-Analysis
Animal pollination supports the production of a wide range of food crops fundamental to maintaining diverse and nutritionally balanced diets. Here, we present a global meta-analysis quantifying the contribution of pollination to multiple facets of crop quality, including both organoleptic and nutritional traits. In fruits and vegetables, pollinators strongly improve several commercially important attributes related to appearance and shelf life, whereas they have smaller effects on nutritional value. Pollination does not increase quality in stimulant crops, nuts, and spices. We report weak signals of a pollination deficit for organoleptic traits, which might indicate a potential service decline across agricultural landscapes. However, the deficit is small and non-significant at the α = 0.05 level, suggesting that pollen deposition from wild and/or managed pollinators is sufficient to maximise quality in most cases. As producing commercially suboptimal fruits can have multiple negative economic and environmental consequences, safeguarding pollination services is important to maintain food security.
Topics: Animals; Bees; Pollination; Crops, Agricultural; Fruit; Pollen; Vegetables; Ecosystem
PubMed: 37491349
DOI: 10.1038/s41467-023-40231-y -
American Journal of Botany Jul 2024Under pollinator limitations, specialized pollination syndromes may evolve toward contrasting responses: a generalized syndrome with increased pollinator attraction,...
PREMISE
Under pollinator limitations, specialized pollination syndromes may evolve toward contrasting responses: a generalized syndrome with increased pollinator attraction, pollinator reward, and pollen transfer capacity; or the selfing syndrome with increased self-pollen deposition, but reduced pollinator attraction and pollen transfer capacity. The buzz-pollination syndrome is specialized to explore female vibrating bees as pollinators. However, vibrating bees become less-active pollinators at montane areas of the Atlantic Forest (AF) domain. This study investigated whether the specialized buzz-pollination syndrome would evolve toward an alternative floral syndrome in montane areas of the AF domain, considering a generalized and the selfing syndromes as alternative responses.
METHODS
We utilized a lineage within the buzz-pollinated Miconia as study system, contrasting floral traits between montane AF-endemic and non-endemic species. We measured and validated floral traits that were proxies for pollinator attraction, reward access, pollen transfer capacity, and self-pollen deposition. We inferred the evolution of floral trait via phylogenetic comparative methods.
RESULTS
AF-endemic species have selectively evolved greater reward access and more frequently had generalist pollination. Nonetheless, AF-endemic species also have selectively evolved toward lower pollen transfer capacity and greater self pollination. These patterns indicated a complex evolutionary process that has jointly favored a generalized and the selfing syndromes.
CONCLUSIONS
The buzz pollination syndrome can undergo an evolutionary disruption in montane areas of the AF domain. This floral syndrome is likely more labile than often assumed, allowing buzz-pollinated plants to reproduce in environments where vibrating bees are less-reliable pollinators.
PubMed: 38956979
DOI: 10.1002/ajb2.16367 -
Molecular Phylogenetics and Evolution Sep 2023Pollination and seed dispersal of plants by animals are key mutualistic processes for the conservation of plant diversity and ecosystem functioning. Although different...
Pollination and seed dispersal of plants by animals are key mutualistic processes for the conservation of plant diversity and ecosystem functioning. Although different animals frequently act as pollinators or seed dispersers, some species can provide both functions, so-called 'double mutualists', suggesting that the evolution of pollination and seed dispersal may be linked. Here, we assess the macroevolution of mutualistic behaviours in lizards (Lacertilia) by applying comparative methods to a phylogeny comprising 2,838 species. We found that both flower visitation (potential pollination; recorded in 64 species [2.3% of total] across 9 families) and seed dispersal (recorded in 382 species [13,5% of total] across 26 families) have evolved repeatedly in Lacertilia. Furthermore, we found that seed dispersal activity pre-dated flower visitation and that the evolution of seed dispersal activity and flower visitation was correlated, illustrating a potential evolutionary mechanism behind the emergence of double mutualisms. Finally, we provide evidence that lineages with flower visitation or seed dispersal activity have higher diversification rates than lineages lacking these behaviours. Our study illustrates the repeated innovation of (double) mutualisms across Lacertilia and we argue that island settings may provide the ecological conditions under which (double) mutualisms persist over macroevolutionary timescales.
Topics: Animals; Ecosystem; Lizards; Phylogeny; Plants; Seeds; Pollination; Symbiosis; Seed Dispersal
PubMed: 37290582
DOI: 10.1016/j.ympev.2023.107839 -
American Journal of Botany Apr 2024Barriers at different reproductive stages contribute to reproductive isolation. Self-incompatibility (SI) systems that prevent self-pollination could also act to control...
PREMISE
Barriers at different reproductive stages contribute to reproductive isolation. Self-incompatibility (SI) systems that prevent self-pollination could also act to control interspecific pollination and contribute to reproductive isolation, preventing hybridization. Here we evaluated whether SI contributes to reproductive isolation among four co-occurring Opuntia species that flower at similar times and may hybridize with each other.
METHODS
We assessed whether Opuntia cantabrigiensis, O. robusta, O. streptacantha, and O. tomentosa, were self-compatible and formed hybrid seeds in five manipulation treatments to achieve self-pollination, intraspecific cross-pollination, open pollination (control), interspecific crosses or apomixis, then recorded flowering phenology and synchrony.
RESULTS
All species flowered in the spring with a degree of synchrony, so that two pairs of species were predisposed to interspecific pollination (O. cantabrigiensis with O. robusta, O. streptacantha with O. tomentosa). All species had distinct reproductive systems: Opuntia cantabrigiensis is self-incompatible and did not produce hybrid seeds as an interspecific pollen recipient; O. robusta is a dioecious species, which formed a low proportion of hybrid seeds; O. streptacantha and O. tomentosa are self-compatible and produced hybrid seeds.
CONCLUSIONS
Opuntia cantabrigiensis had a strong pollen-pistil barrier, likely due to its self-incompatibility. Opuntia robusta, the dioecious species, is an obligate outcrosser and probably partially lost its ability to prevent interspecific pollen germination. Given that the self-compatible species can set hybrid seeds, we conclude that pollen-pistil interaction and high flowering synchrony represent weak barriers; whether reproductive isolation occurs later in their life cycle (e.g., germination or seedling survival) needs to be determined.
Topics: Hybridization, Genetic; Sympatry; Pollination; Self-Incompatibility in Flowering Plants; Reproductive Isolation; Flowers; Seeds; Opuntia; Reproduction; Pollen; Species Specificity; Apomixis
PubMed: 38584339
DOI: 10.1002/ajb2.16309 -
PloS One 2023Forest products derived from woody trees, such as fruits, seeds, honey, wood and others, are important resources for supporting rural livelihoods. However, little is...
Forest products derived from woody trees, such as fruits, seeds, honey, wood and others, are important resources for supporting rural livelihoods. However, little is known about the breeding systems or floral visitors of trees that provide these resources, often due to the difficulty of accessing tree canopies. This study addresses key knowledge gaps from a data poor region, providing information on the breeding systems and contribution of biotic pollination to two trees abundant in south-central Africa, that provide forest product supports for rural livelihoods: Julbernardia paniculata (Benth.) Troupin and Syzygium guineense (Willd.) subsp. barotsense F. White (Fabaceae and Myrtaceae respectively). The breeding systems of these species were assessed by conducting controlled pollination experiments, and then measuring the effects on reproductive success to determine the degree of self-compatibility and pollen limitation. Floral visitors and their behaviour were observed to provide preliminary information on possible pollinator groups. S. guineense appeared to be self-compatible, while J. paniculata showed signs of both self-incompatibility and pollen limitation. Floral visitors of both species were dominated by bees, with native honeybees (Apis mellifera) providing the highest visitation rates. These insights provide the first steps for understanding the reproductive ecology of these key tree species and can help to inform sustained management and conservation aimed at protecting forests and supporting rural livelihoods, as well as broaden the understanding of the floral visitors, and contribution of biotic pollination to forest tree reproductive success.
Topics: Bees; Animals; Flowers; Plant Breeding; Pollination; Reproduction; Forests; Trees; Fabaceae
PubMed: 37856431
DOI: 10.1371/journal.pone.0292929 -
American Journal of Botany Oct 2023The interaction between ecological and evolutionary processes has been recognized as an important factor shaping the evolutionary history of species. Some authors have...
PREMISE
The interaction between ecological and evolutionary processes has been recognized as an important factor shaping the evolutionary history of species. Some authors have proposed different ecological and evolutionary hypotheses concerning the relationships between plants and their pollinators; a special case is the interaction and suspected coevolution among Agave spp. and their main pollinators, the Leptonycteris bats. Agave spp. have, in general, a pollination syndrome compatible with chiropterophily including floral shape and size, nocturnal nectar production, and nectar quality and sugar concentration. Our goal was to analyze the interaction Agave-Leptonycteris and its dynamics during three different climate scenarios.
METHODS
We modeled the Agave-Leptonycteris interaction in its spatial and temporal components during the Pleistocene using Ecological Niche Models (ENMs) and three climate scenarios: Current, Last Glacial Maximum (LGM), and Last InterGlacial (LIG). Furthermore, we analyzed the geographic correlation between 96 Agave spp. and two of the Mexican Tequila bats, genus Leptonycteris.
RESULTS
We found that Leptonycteris spp. interact with different Agave spp. over their migratory routes. We propose an interaction refuge in Metztitlán and Tehuacán-Cuicatlán areas, where Agave- Leptonycteris interaction has probably remained active. During the nonmigratory season, both bat species consume nectar of almost the same Agave spp., suggesting the possibility of a diffuse coevolution among Agave and Leptonycteris bats.
CONCLUSIONS
We propose that in the areas related to migratory bat movements, each bat species interacts with different Agave spp., whereas in the areas occupied by nonmigrant individuals, both bat species consume nectar of almost the same Agave taxa.
Topics: Humans; Animals; Plant Nectar; Chiroptera; Agave; Pollination; Biological Evolution
PubMed: 37561648
DOI: 10.1002/ajb2.16222 -
Die Naturwissenschaften Sep 2023This study characterizes the osmophores and corolla traits in 18 species of Bignonieae Dumort., a Bignoniaceae tribe occurring in the Cerrado, a neotropical savanna in...
This study characterizes the osmophores and corolla traits in 18 species of Bignonieae Dumort., a Bignoniaceae tribe occurring in the Cerrado, a neotropical savanna in Brazil. To detect osmophore distribution, whole, newly opened flowers were immersed in Neutral Red Solution. Samples from the corolla tube and lobes were also fixed and analyzed micromorphologically, anatomically, and histochemically. The osmophores showed six markedly different distribution patterns that were not clearly associated with histological features. In most species, osmophores comprised papillose secretory epidermises and a few layers of subepidermal parenchyma. Starch grains, lipid droplets, and terpenes were detected in osmophores. An ornamented cuticle, cuticular folds, glandular and non-glandular trichomes, raised stomata and epicuticular wax granules are common traits in the species studied and may be useful in determining the taxonomy of the group. We found that 94% of the species visited by bees had papillose epidermises while the single hummingbird-pollinated species presented a flattened epidermis. Variations in osmophore pattern among species visited by bees, including variations within the same plant genus, are novel finding. Additionally, the Bignonieae species visited by bees presented a textured corolla surface, which has been reported as facilitating bee attachment and movement towards the floral resource. Future studies with a greater number of Bignonieae species and more detailed pollinator behavioral assays may help in the interpretation of the variations in corolla traits and functional relationships between flowers and pollinators.
Topics: Animals; Bees; Bignoniaceae; Brazil; Flowers; Phenotype; Terpenes
PubMed: 37682350
DOI: 10.1007/s00114-023-01873-6