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Inflorescence (a) and pollinators, Halictidae sp. (b), Frieseomelitta doederleini (c), and Trigona spinipes (d) of Rhynchospora ciliata, at the Jardim Botânico do Recife, in Pernambuco, Brazil
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In typically anemophilous families, there are species, such as Rhynchospora ciliata (Cyperaceae), in which both wind and insects have been registered as pollen vectors (ambophily). However, the contribution of each vector to pollination of ambophilous species can change under different environmental conditions. Therefore, this study aimed to determ...
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... This mixed pollination system involving animals and the wind is often considered a transitional system from zoophily (animal pollination) to anemophily (wind pollination) or vice versa (Culley et al. 2002;Costa and Machado 2012). Ambophily depends on both plant morphology and environmental factors that allow both animal and wind pollen transfer (Costa et al. 2018). Because it has an abiotic component, usually the wind, ambophily is expected to occur in open areas, encompassing flowers with exposed anthers and stigma, which allow pollen to be dispersed and captured by wind (Stelleman 1984;Friedman and Barrett 2009). ...
... In the first year, only one individual out of the eight sampled produced fruits and seeds, and in the second period four out of five individuals. These data reinforce the temporal variation nature of each vector's contribution in ambophilous systems (Lázaro and Traveset 2005;Costa et al. 2018). The variation in wind contribution among individuals can occur either by phenotypic characteristics of the individuals or by local microhabitat characteristics. ...
Some plant species have a kind of mixed pollination system—ambophily—which rely both on biotic and abiotic (most commonly wind) as pollen vectors. Ambophily remains poorly addressed in the pollination literature and may have been overlooked because existing studies do not quantify the wind contribution in animal-pollinated species. After observing pollen transport by the wind in an Orobanchaceae species with ornithophilous floral phenotype, we hypothesize that this species could be ambophilous. Esterhazya eitenorum Barringer is a (sub-)shrub endemic to a high-altitude grassland (campos de altitude) area in southeastern Brazil. Pollinated mainly by hummingbirds and secondarily by large bees, it presents features generally associated with ornithophily. Bird-pollinated species are not expected to be ambophilous, due to their high resource investment in floral construction and maintenance. However, here we detect ambophily in E. eitenorum by testing the potential for pollen export by the wind as well as seed set after floral visitor exclusion and spontaneous self-pollination treatments, and comparing these with natural conditions. Esterhazya eitenorum has an ambophilous pollination system, with effect size analyses between floral visitor exclusion treatments and natural conditions revealing significant contributions from both abiotic and biotic components. Although its floral phenotype corresponds to the main pollinator, the occurrence of ambophily in E. eitenorum underscores the need for an independent approach to the association of floral phenotypes with pollination vectors, in particular for the detection and better understanding of the evolution of mixed pollination systems.
... However, floral diversity is not restricted to zoophilous species. Groups considered mainly wind-pollinated, such as Cyperaceae and Poaceae, have a wide variation in the architecture of their inflorescences and the diversity of sexual systems (Goetghebeur 1998, Friedman and Harder 2004, Friedman and Barrett 2009b, Costa et al. 2018, Schulze-Albuquerque et al. 2020. ...
... In angiosperms, anemophily evolved from zoophily independently in different strains, possibly in response to the limitation of biotic vectors (Culley, Weller and Sakai 2002). In general, anemophilous species show cespitose growth and are more frequent at higher latitudes and in open areas (Culley et al. 2002, Costa et al. 2018). In addition, they are more abundant in temperate climates and rare in tropical forests, which is related to the lower humidity and rainfall rates that favour pollen transport (Culley et al. 2002). ...
... Experimental observations showed the occurrence of ambophily (pollination mediated by both biotic and abiotic vectors, see Abrahamczyk et al. 2022) in Cyperaceae, specifically in Cyperus L. (Wragg and Johnson 2011) and Rhynchospora Vahl (Costa and Machado 2012, Costa et al. 2018. In Eriophorum virginicum L., it was proposed that the wind would be an inefficient vector, with flies and bees playing a more significant role in cross-pollination (Meier and Wragg 2013). ...
Studies about reproductive aspects of angiosperms rarely refer to herbaceous and anemophilous groups. Cyperaceae are cosmopolitan and diverse in terms of sexuality, inflorescence architecture, and pollination modes, such as anemophily, entomophily, and ambophily. Therefore, the evolution of reproductive traits can clarify some questions about the reproductive biology of angiosperms, especially regarding the transitions between biotic and abiotic pollination. This study was designed to investigate the evolution of reproductive traits in Cyperaceae through comparative phylogenetic methods, such as reconstruction of ancestral states and evolutionary correlation. If spicoids in Mapanioideae are indeed inflorescences, the bisexual flower in Cyperaceae would be derived, a rare case in angiosperms. In Cyperoideae, a decrease in the number of flowers and an increase in stamen loss events were observed. This result contradicts the hypothesized increase in reproductive structures in anemophilous species, in which a greater amount of pollen is produced to compensate for the waste generated by wind. Only one correlation was found: between the number of inflorescence branches and the number of reproductive units per inflorescence. Finally, the analyses showed the great diversity of reproductive biology in Cyperaceae and made evident the need to expand the theoretical studies to refine the discovery of correlated traits.
... For instance, typically anemophilous Cyperaceae includes so many species that the pollination systems for all of the species are probably not researched or known explicitly one by one in state of the art (e.g. da Costa et al. 2018). Plus, defining a mode of pollination for a given species needs remarkable efforts based on the full range of spatial and temporal occurrences (Culley et al. 2002). ...
Previous studies have discovered arboreal pollen in non-forested areas on the Tibetan Plateau, which are mostly anemophilous type and regarded as a result of the Asian summer monsoon. However, the relationship between the spatial distribution of wind-pollinated pollen and monsoon has seldom been illustrated quantitatively. Here, we used 676 surface samples (647 compiled, 29 new samples) to examine the characteristics of the spatial distribution patterns of 13 anemophilous pollen taxa on the southeastern Tibetan Plateau, by employing the spatial interpolation technique. Then, we quantified the correlation between the distributions of these taxa and monsoon wind via mantel test. The results show that the anemophilous pollen represents at least half percentage of the total pollen assemblages in most areas of the study region. Anemophilous tree pollen mainly distributes in the south and southeastern part, while anemophilous non-tree pollen does in the opposite and perpendicular direction. The distributional pattern of non-anemophilous pollen reflects that their corresponding plants most likely constitute the understory components of different forests or the minorities of non-forests communities. Mantel tests indicate that the anemophilous tree pollen has a highest correlation with the Asian summer monsoon. Anemophilous pollen, overall pollen assemblages and anemophilous pollen with air sacs have higher correlations with summer monsoon. Contrarily, non-anemophilous pollen has relatively weak correlation. Furthermore, we found that the relationships between various pollen groups or separate taxon and the Asian summer monsoon are dependent on sample types. The lake sediment surface samples had the strongest signal of the Asian summer monsoon among the different sample types. Our findings provide the strong evidence of the Asian summer monsoon influencing the pollen distribution patterns. More importantly, the quantification of this correlation between anemophilous tree pollen and the Asian summer monsoon offers the fundamentally theoretical basis of reconstructing paleo-monsoon by the proxy of windborne pollen taxa.
... Ambophily depends on both plant morphology and environmental factors that allow both animal and wind pollen transfer (Costa et al. 2018). Because it has an abiotic component, usually the wind, ambophily is expected to occur in open areas, encompassing owers with exposed anthers and stigma, which allow pollen to be dispersed and captured by wind (Stelleman 1984; Friedman and Barrett 2009). ...
Some plant species have a kind of mixed pollination system – ambophily – which rely both on biotic and abiotic (most commonly wind) as pollen vectors. Ambophily remains poorly addressed in the pollination literature and may have been overlooked because existing studies do not quantify the wind contribution in animal-pollinated species. Moreover, it is expected in species pollinated by different insect groups and generalist floral phenotype. Esterhazya eitenorum is a (sub-)shrub endemic to a high-altitude grassland ( campos de altitude ) area in southeastern Brazil. Pollinated mainly by hummingbirds and secondarily by large bees, it presents features generally associated with ornithophily. Bird-pollinated species are not expected to be ambophilous, due to their high resource investment in floral construction and maintenance. However, here we detect ambophily in E. eitenorum by testing the potential for pollen export by wind as well as seed set after floral visitor exclusion and spontaneous self-pollination treatments, and comparing these with natural conditions. Esterhazya eitenorum has an ambophilous pollination system, with effect size analyses between floral visitor exclusion treatments and natural conditions revealing significant contributions from both abiotic and biotic components. Although its floral phenotype corresponds to the main pollinator, the occurrence of ambophily in E. eitenorum underscores the need for an independent approach to the association of floral phenotypes with pollination vectors, in particular for the detection and better understanding of the evolution of mixed pollination systems.
... A mixed wind and insect pollination system can be a stable system in which both pollen vectors can act in combination to increase the reproductive success of the species, so that the total fruit set is greater when both vectors are acting (Costa et al., 2017;Costa, Albuquerque, Thomas, & Machado, 2018;Costa & Machado, 2012;Culley et al., 2002;Schulze-Albuquerque et al., 2020;Villa-Machío et al., 2020;Wragg & Johnson, 2011). According to Linder (1998), in an ambophilous species, although flowers may be visited and pollinated by insects, a large amount of pollen also is dispersed by the wind, which may pollinate flowers. ...
... According to Linder (1998), in an ambophilous species, although flowers may be visited and pollinated by insects, a large amount of pollen also is dispersed by the wind, which may pollinate flowers. If environmental conditions are not suitable for wind pollination of ambophilous species, however, insect pollination can compensate for low fruit set by wind (Costa et al., 2018), or insects may also contribute by assisting in pollen dispersal by wind (see Schulze-Albuquerque et al., 2020). ...
... In the ambophilous Rhynchospora ciliata (Cyperaceae), wind and insects (bees, flies and wasps) contribute differently over time to plant reproduction. Fruit set in this species is determined by variation in pollen vectors due to the temporal variation in local environmental conditions, such as wind velocity and rainfall amount (Costa et al., 2018). ...
Ambophily (wind and insect pollination) has been reported for some genera of the typically wind‐pollinated family Cyperaceae, including the genus Rhynchospora . The significance of wind and insect pollination can vary, depending on local microclimatic conditions. Rhynchospora cephalotes is an ambophilous species that can grow under different environmental conditions, either along forest edges or inside forest fragments. This study, therefore, tests the hypothesis that (a) there is greater contribution by wind than insects to fruit set of the individuals at the forest edge and (b) there is greater contribution by insects than wind to fruit set of the individuals inside the forest. Field work was carried out in a fragment of Atlantic Forest in northeastern Brazil. We quantified the number of visits by insects, wind velocity and the reproductive success (fruit set) of R. cephalotes provided by wind and insects through exclusion experiments performed at the edge of and inside the forest. We observed a greater number of visits per day by pollinating bees to individuals inside the forest (36.83 ± 7.46) than to individuals at the edge (16.66 ± 6.53). The wind speed was significantly higher at the edge (1.71 ± 0.46 m/s) than inside the forest (0.97 ± 0.18 m/s). Bees and wind are both pollen vectors of R. cephalotes , but bees were the pollen vector that contributed most to fruit set (63.3%) for individuals inside the forest, whereas wind was the primary vector for individuals at the forest edge (76.6%). This seesaw in importance of each pollen vector in the two different environments guarantees high fruit set in R. cephalotes under different microclimatic conditions.
... (Larridon et al., 2018b). Although predominantly wind-pollinated, there are many transitions from wind to insect pollination in Cyperaceae ( Fig. 1F; Wragg & Johnson, 2011;Yano et al., 2015;Costa et al., 2018a;Villa-Machío et al., 2020). The sedge family is also physiologically diverse, with species using C 3 , C 4 , or C 3 -C 4 intermediate photosynthesis (Soros & Bruhl, 2000;Besnard et al., 2009). ...
Cyperaceae (sedges) are the third largest monocot family and are of considerable economic and ecological importance. Sedges represent an ideal model family to study evolutionary biology because of their species richness, global distribution, large discrepancies in lineage diversity, broad range of ecological preferences, and adaptations including multiple origins of C4 photosynthesis and holocentric chromosomes. Goetghebeur’s seminal work on Cyperaceae published in 1998 provided the most recent complete classification at tribal and generic level, based on a morphological study of Cyperaceae inflorescence, spikelet, flower and embryo characters plus anatomical and other information. Since then, several family‐level molecular phylogenetic studies using Sanger sequence data have been published. Here, more than 20 years after the last comprehensive classification of the family, we present the first family‐wide phylogenomic study of Cyperaceae based on targeted sequencing using the Angiosperms353 probe kit sampling 311 accessions. Additionally, 62 accessions available from GenBank were mined for overlapping reads and included in the phylogenomic analyses. Informed by this backbone phylogeny, a new classification for the family at the tribal, subtribal and generic levels is proposed. The majority of previously recognized suprageneric groups are supported, and for the first time we establish support for tribe Cryptangieae as a clade including the genus Koyamaea. We provide a taxonomic treatment including identification keys and diagnoses for the 2 subfamilies, 24 tribes and 10 subtribes and basic information on the 95 genera. The classification includes five new subtribes in tribe Schoeneae: Anthelepidinae, Caustiinae, Gymnoschoeninae, Lepidospermatinae and Oreobolinae.
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... In anemophilous groups, reversal to entomophily can occur in some species and, in such cases, floral characteristics necessary to attract pollinators, such as colour and scent, have evolved (Leppik, 1955;Culley et al., 2002;Wragg & Johnson, 2011;Costa & Machado, 2012). In addition, both vectors (wind and insects) can act together in pollination (ambophily), which may be an intermediate condition in the process of reversal to entomophily or a stable condition, increasing reproductive success when compared to the reproductive success promoted by either of the vectors individually (Culley et al., 2002;Friedman & Barrett, 2009;Costa & Machado, 2012;Rech et al., 2014;Costa et al., 2018). ...
... Poaceae are a cosmopolitan family of monocotyledons usually considered to be anemophilous, but some recent studies have recorded visiting insects including bees (Bogdan, 1962;Soderstrom & Calderón, 1971;Adams, Perkins & Estes, 1981;Nadgauda, John & Mascarenhas, 1993;Seres & Ramírez, 1995;Guilherme & Ressel, 2001;Huang et al., 2002;Koshy, Harikumar & Narendran, 2011;Wolowski & Freitas, 2015;Ruiz-Sanchez et al., 2017;Saunders, 2018), flies (Soderstrom & Calderón, 1971;Seres & Ramírez, 1995;Guilherme & Ressel, 2001;Grombone-Guartini, do Nascimento & Santos-Gonçalves, 2011;Koshy et al., 2011;Wolowski & Freitas, 2015;Ruiz-Sanchez et al., 2017;Dórea et al., 2018;Saunders, 2018) and beetles (Soderstrom & Calderón, 1971;Seres & Ramírez, 1995;Guilherme & Ressel, 2001;Wolowski & Freitas, 2015). In addition, pollinating insects have been recorded in other families related to Poaceae, such as Cyperaceae (Magalhães et al., 2005;Wragg & Johnson, 2011;Wolowski & Freitas, 2015;Costa et al., 2017Costa et al., , 2018. These studies indicate that these animals can act as pollinators and, in some cases, the plants have an ambophilous pollination system. ...
... The insects contributed either directly to the transfer of pollen from one flower to another and/or indirectly through insectinduced wind pollination. This mixed pollination system allows species to have the advantage of ensuring pollination under different environmental conditions, so that pollen vectors contribute more or less to the formation of fruits depending on environmental conditions (Culley et al., 2002;Costa et al., 2018) as described for Rhynchospora ciliata Vahl (Cyperaceae) (Costa et al., 2018) and for Paspalum dilatatum Poir. (Poaceae) (Adams et al., 1981). ...
Usually considered anemophilous, grasses (Poaceae) have been the subject of few studies that recorded insects visiting their flowers. Such visitors, with wind, could act as pollen vectors in a possible ambophilous system. Since colour and scent are floral cues attracting pollinating insects, we aimed to provide the first insights into how these cues could be involved in the attraction of pollinators by grasses. Chloris barbata, Paspalum maritimum (with two morphotypes), P. millegrana and Urochloa plantaginea were studied. We determined the role of each pollen vector (wind and insect) and we registered the frequency of floral visitors. Also, we characterized the colour reflectance of glumes, anthers and stigmas and we determined the colour space in the bee colour hexagon and the chemical composition of floral scents. The floral structures of each species reflect colour differently and are perceived differently by pollinators. Furthermore, the volatile organic compounds detected are similar to those found in entomophilous species. In two of the grass species, we registered eight species of visitors, including bees, wasps and flies. Overall, wind was the most important vector for reproductive success. Insects, however, may induce wind pollination by creating pollen clouds when they visit inflorescences.
... Evolving a mixed pollination system might be a response to the unpredictability of a single pollination vector, e.g. low pollinator density, or low wind (Ríos et al. 2014 and references therein;da Costa et al. 2018). ...
An increasing number of double mutualisms (i.e. two interacting species benefiting each other in two different functions, e.g. pollination and seed dispersal) have been reported, mainly from island ecosystems, although we still lack much information on how effective such species are in both processes. Here, we assessed the pollination effectiveness of a double mutualism between an ancient Mediterranean gymnosperm, Ephedra fragilis, and a lizard, Podarcis lilfordi. On the one hand, we assessed the lizard contribution to different fitness measures (seed set and germination success), relative to that of insects and the wind effect; on the other, we determined the lizards' seed removal rate (i.e. the quantity component of seed dispersal effectiveness). In both processes, we further tested for differences in their contributions among male, female and juvenile lizards. Ephedra fragilis showed to be mostly anemophilous, lizards and insects playing only a minor role on seed set. However, lizards qualitatively contributed to pollination success, as seeds coming from lizard-pollinated cones germinated at higher rates than those pollinated by wind or insects, although this was detected only for small seeds (<8 mg). The plant produced a low seed set (c. 23 %), which was compensated by a high seed germinability (c. 70 %). Adult male lizards were those most implicated in pollination, quantitatively more important than insects, and in seed dispersal. This work, thus, reports the importance of a lizard species in one of the few double mutualisms found in the World involving a gymnosperm, and it represents the first documentation of a double mutualism in the Mediterranean region. Our findings further contribute to highlight the role of both inter-and intraspecific differences in the effectiveness of mutualistic interactions.
... According to the definition criteria of the comprehensive equilibrium of compulsory education resource allocation as defined in Table 1, the equilibrium allocation of compulsory education resources in a single region can be judged accordingly (Costa, Albuquerque, Thomas & Machado, 2018;Sardenne et al., 2017;Liu, Shen, Meng & Sun, 2018;Bengtsson-Palme, Kristiansson & Larsson, 2018;Wu et al., 2017). ...
Based on the reality of the Chinese government's promotion of the integration of urban and rural compulsory education, this paper proposes the concept of the compulsory education resource allocation Gini coefficient and comprehensive balance of compulsory education resource allocation and defined that the balance of compulsory education resource allocation can be reflected through the comprehensive equilibrium of compulsory education resource allocation. This paper proposes a compulsory education resource allocation balance measurement index system of two parts, which are a mandatory indicator system and a control index system, with the former being the minimum standard that must be met. Based on the PSR theory, a control index system consisting of 3 dimensions and 12 indicators is constructed from three aspects: pressure, state, and corresponding dimensions. This paper proposes a method of measuring the Gini coefficient of compulsory education resource allocation and the allocation balance of compulsory education resources, and verifying the feasibility of theoretical research through cases.
Stingless bees are major flower visitors in the tropics, but their foraging preferences and behavior are still poorly understood. Studying stingless bee interactions with angiosperms is methodologically challenging due to the high tropical plant diversity and inaccessibility of upper canopy flowers in forested habitats. Pollen DNA metabarcoding offers an opportunity of assessing floral visitation efficiently and was applied here to understand stingless bee floral resources spectra and foraging behavior. We analyzed pollen and honey from nests of three distantly related stingless bee species, with different body size and social behavior: Melipona rufiventris, Scaptotrigona postica and Tetragonisca angustula. Simultaneously, we evaluate the local floristic components through seventeen rapid botanical surveys conducted at different distances from the nests. We discovered a broad set of explored floral sources, with 46.3 plant species per bee species in honey samples and 53.67 in pollen samples. Plant families Myrtaceae, Asteraceae, Euphorbiaceae, Melastomataceae and Malpighiaceae dominated the records, indicating stingless bee preferences for abundant resources that flowers of these families provide in the region. Results also reinforce the preference of stingless bees for forest trees, even if only available at long distances. Our high-resolution results encourage future bee-plant studies using pollen and honey metabarcoding in hyper-diverse tropical environments.
