Floral biology of Salvia stachydifolia, a species visited by bees and birds: connecting sexual phases, nectar dynamics and breeding system to visitors’ behaviour

Abstract Aims Adaptive convergence in floral phenotype among plants sharing a pollinator guild has been acknowledged in the concept of pollination syndrome. However, many plants display traits associated with a given syndrome, but are visited by multiple pollinators. This situation may indicate the beginning of a pollinator shift or may result in a stable situation with adaptations to different pollinators. In Salvia stachydifolia, a previous study suggested that flower shape is optimized to maximize the contribution to pollination of bees and hummingbirds. Here, we studied three additional aspects of its floral biology: sexual phases, nectar dynamics and breeding system, and examined their connection with pollinators’ behavior to explore the presence of adaptations to bee and/or hummingbird pollination. Methods Using a greenhouse population, we applied five pollination treatments to characterize breeding system. To determine sexual phases, we recorded flower opening, anther dehiscence, corolla fall and stigma receptivity. Additionally, we characterized nectar volume and concentration dynamics along the day. Finally, to determine pollinator assemblage and visitation patterns, we performed field observations and recorded pollinators’ behavior. Important findings Salvia stachydifolia was partially protandrous and self-compatible, but open-pollinated plants attained the highest reproductive success, suggesting that reproduction is mainly dependent on pollinator activity. Bombus opifex bumblebees were the most frequent visitors, but Sappho sparganura hummingbirds dominated visits early in the morning and at dusk. Nectar was typical of bumblebee-pollination. We suggest that the bee-hummingbird mixed visitation constitutes an unstable evolutionary situation, making S. stachydifolia an ideal system to understand the ecological circumstances in which pollination shifts occur.

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Pollination and floral biology of Adonis vernalis L. (Ranunculaceae) – a case study of threatened species

Acta Societatis Botanicorum Poloniae ◽

10.5586/asbp.2014.001 ◽

2014 ◽

Vol 83 (1) ◽

pp. 29-37 ◽

Cited By ~ 7

Author(s):

Bożena Denisow ◽

Małgorzata Wrzesień ◽

Anna Cwener

Keyword(s):

Threatened Species ◽

Breeding System ◽

Pollen Viability ◽

Management Strategies ◽

Reproductive Potential ◽

Floral Biology ◽

Pollination Syndrome ◽

Compact Range ◽

Pollen Vectors ◽

Pollination Systems

Although the knowledge of pollination systems of rare and threatened species is one of the principles for development of optimal conservation and management strategies, the data about their pollination requirements are scarce or incomplete. Different problems are listed (xerothermic habitat disappearance, overgrowing of patches, plant biology i.e., slow plant growth, problems with seed germination) among the possible causes of Adonis vernalis being threatened, but until now no consideration was given to the flowering biology and pollination.The observations of flowering biology of A. vernalis (Ranunculaceae), a clonal species, were conducted in an out-of-compact-range population, in the Lublin Upland, Poland (51°18'55" N, 22°38'21" E), in 2011–2013. The reproductive potential of A. vernalis is related to the population age structure, pollination syndrome, and breeding system. The flowers exhibit incomplete protogyny. The dichogamy function is supported by different (biological, morphological) mechanisms. Stigma receptivity occurred about one day before anthers started shedding self-pollen, and pollen viability was increasing gradually during the flower life-span (66.3% in distal anthers vs. 77.3% in proximal). The decrease in pollen production and in pollen viability coincided with the lowest degree of seed set, irrespective of the pollination treatment. Pollen vectors are necessary for efficient pollination, as the proportion of pistils setting fruits after open pollination (41–82.1%) was significantly higher compared to spontaneous self-pollination (only 5.5–12.3%). The pollination requirements together with pollen/ovule ratio (P/O = 501) indicate a facultative xenogamous breeding system in A. vernalis. Therefore, in the conditions of the global lack of pollinators, improper pollination may weaken the population by leading to a decrease in the proportion of recombinants, and in addition to other factors, may accelerate extinction of small A. vernalis populations.

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Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2013.0349 ◽

2014 ◽

Vol 369 (1648) ◽

pp. 20130349 ◽

Cited By ~ 37

Author(s):

Carolyn A. Wessinger ◽

Lena C. Hileman ◽

Mark D. Rausher

Keyword(s):

Quantitative Trait Loci ◽

Quantitative Trait ◽

Flower Colour ◽

Floral Traits ◽

Pollination Syndrome ◽

Pollination Syndromes ◽

Floral Trait ◽

Nectar Volume ◽

Hummingbird Pollination ◽

Trait Loci

Distinct floral pollination syndromes have emerged multiple times during the diversification of flowering plants. For example, in western North America, a hummingbird pollination syndrome has evolved more than 100 times, generally from within insect-pollinated lineages. The hummingbird syndrome is characterized by a suite of floral traits that attracts and facilitates pollen movement by hummingbirds, while at the same time discourages bee visitation. These floral traits generally include large nectar volume, red flower colour, elongated and narrow corolla tubes and reproductive organs that are exerted from the corolla. A handful of studies have examined the genetic architecture of hummingbird pollination syndrome evolution. These studies find that mutations of relatively large effect often explain increased nectar volume and transition to red flower colour. In addition, they suggest that adaptive suites of floral traits may often exhibit a high degree of genetic linkage, which could facilitate their fixation during pollination syndrome evolution. Here, we explore these emerging generalities by investigating the genetic basis of floral pollination syndrome divergence between two related Penstemon species with different pollination syndromes—bee-pollinated P. neomexicanus and closely related hummingbird-pollinated P. barbatus . In an F 2 mapping population derived from a cross between these two species, we characterized the effect size of genetic loci underlying floral trait divergence associated with the transition to bird pollination, as well as correlation structure of floral trait variation. We find the effect sizes of quantitative trait loci for adaptive floral traits are in line with patterns observed in previous studies, and find strong evidence that suites of floral traits are genetically linked. This linkage may be due to genetic proximity or pleiotropic effects of single causative loci. Interestingly, our data suggest that the evolution of floral traits critical for hummingbird pollination was not constrained by negative pleiotropy at loci that show co-localization for multiple traits.

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Within-day temporal isolation of two species of Iris (Iridaceae) sharing the same pollinator

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blaa032 ◽

2020 ◽

Vol 130 (3) ◽

pp. 447-457

Author(s):

Rong Liu ◽

Yike Gao ◽

Zhuping Fan ◽

Xinzi Wang ◽

Jianhua Xiao ◽

...

Keyword(s):

Reproductive Isolation ◽

Apis Cerana ◽

Floral Biology ◽

The Body ◽

Floral Colour ◽

Floral Structure ◽

Flower Opening ◽

Temporal Isolation ◽

Nectar Volume ◽

The Difference

Abstract Knowledge of factors driving reproductive isolation is essential to understand the process of speciation. To study the reproductive isolation of two closely related species with overlapping flowering seasons, Iris domestica and Iris dichotoma, we compared their reproductive system, floral biology and pollination biology. The results indicated that I. domestica was facultatively xenogamous, whereas I. dichotoma was facultatively autogamous. Although the two species differed significantly in floral colour, floral diameter, floral structure, nectar volume, flower opening and closing times, they shared the same diurnal pollinator, the honeybee Apis cerana. The frequency of pollination by A. cerana did not differ significantly between the two species, but honeybee pollination of I. domestica was more efficient compared with that of I. dichotoma. Despite the difference in floral structure between the two species, both species deposited pollen on the same parts of the body of honeybees. The temporal partitioning of within-day flowering times between I. domestica (from 07.15 to 08.15 h to 18.00 to 19.00 h) and I. dichotoma (from 15.45 to 16.15 h to 22.00 to 23.00 h), together with the time memory of honeybees, meant that the two species did not overlap in the time of their pollination, thus leading to temporal isolation as a major driver of reproductive isolation between the two species.

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Floral biology of dry rainforest in north Queensland and a comparison with adjacent savanna woodland

Australian Journal of Botany ◽

10.1071/bt00017 ◽

2001 ◽

Vol 49 (2) ◽

pp. 137 ◽

Cited By ~ 12

Author(s):

Dinah J. Hansman

Keyword(s):

Breeding System ◽

Flowering Phenology ◽

Floral Biology ◽

Pollination Syndrome ◽

Wind Pollination ◽

Floral Display ◽

Wet Season ◽

Savanna Woodland ◽

Canopy Trees ◽

Flower Diameter

In north Queensland, Australia, dry rainforest (deciduous and semi-evergreen vine thicket) occurs as patches within a matrix of savanna woodland. With floral morphology and pollen–ovule ratios as indicators of pollination syndrome and breeding system, the floral biology of dry rainforest was compared with that of adjacent savanna woodland and with rainforest elsewhere. Contingency tables and analysis of variance were used to examine and compare breeding system, flower diameter, floral display and putative pollination syndrome for 156 dry rainforest and 33 savanna woodland taxa. Most (91 of 97) dry rainforest species had pollen–ovule ratios indicating obligate outbreeding. Similar levels of dioecy (21%) and patterns of flowering phenology were observed to those reported for rainforests elsewhere. For dry rainforest canopy trees, flower diameter and morphology indicated pollination by small, generalist insects. Canopy trees tended to flower in the wet season and have low ovule numbers. Taxa assigned to the wind-pollination syndrome had the highest pollen–ovule ratios, suggesting less efficient pollen transfer. Sclerophyll savanna taxa (and some emergent dry rainforest trees) tended to flower in the dry season, have large flowers, high ovule numbers and a high level of floral display.

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Pollination biology and reproduction of Seemannia sylvatica (Kunth) Hanstein (Gesneriaceae) in the Serra da Bodoquena National Park, Mato Grosso do Sul

Biota Neotropica ◽

10.1590/s1676-06032011000400013 ◽

2011 ◽

Vol 11 (4) ◽

pp. 125-130 ◽

Cited By ~ 11

Author(s):

Eduardo Camargo ◽

Licléia da Cruz Rodrigues ◽

Andréa Cardoso Araujo

Keyword(s):

Breeding System ◽

Fruit Set ◽

Riparian Forest ◽

Floral Biology ◽

Nectar Production ◽

Mato Grosso ◽

Nectar Volume ◽

Cross Pollination ◽

Self Pollination ◽

Different Ages

In Brazil, the family Gesneriaceae is represented by 23 genera and approximately 200 species. Seemannia sylvatica is an herb that occurs in dense populations in the riverbeds at Serra da Bodoquena. Goals of this study were to report the floral biology (on the first five days of anthesis), as well as to determine the breeding system and the pollinators of S. sylvatica. Data collection was conducted from June 2005 to July 2006 through monthly field trips, lasting for five days. Data on floral biology, breeding system and on the floral visitors were taken from individuals located along a track 2500 m long, in riparian forest of Salobrinha river. Flowers of S. sylvatica are tubular, red, with no perceptive odor and lasted more than five days (ca. 10 - 20 days in individuals transferred to an urban garden and kept in vases). Seemania sylvatica is protandrous, and the male phase occurred between the first and the fourth days of anthesis, while the female one started in the fifth day. Mean nectar volume secreted was 4.77 ± 3.2 µl, with a significative variation among flowers of different ages. Otherwise, nectar concentration average was 9.71 ± 4.41%, and did not varied significantly in flowers of different ages. The flowers of S. sylvatica were pollinated mainly by the hummingbirds Phaethornis pretrei and Thalurania furcata, and pierced by the bee Ceratina chloris. The butterfly Parides anchises orbygnianus was considered an occasional pollinator of these flowers. Seemannia sylvatica is self-compatible, since fruit set occurred on the experiments of spontaneous self-pollination, manual self-pollination, cross-pollination and open pollination (control). The protandry, coupled with the pattern of nectar production, characterized by low volume and solute concentration, which induces the pollinators to visit different flowers in a given circuit foraging, act maximizing the likelihood of cross-pollination in S. sylvatica. Moreover, the high proportion of fruit set by autogamy is an important strategy considering that S. sylvatica is visited by few species, being pollinated mainly by P. pretrei. Therefore, in the absence of these visitors, the formation of fruits may be achieved.

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Pollination ecology of Caryocar brasiliense (Caryocaraceae) in Central Brazil cerrado vegetation

Journal of Tropical Ecology ◽

10.1017/s0266467400007173 ◽

1993 ◽

Vol 9 (2) ◽

pp. 199-211 ◽

Cited By ~ 55

Author(s):

Rogério Gribel ◽

John D. Hay

Keyword(s):

Breeding System ◽

Fruit Set ◽

Seed Set ◽

Floral Biology ◽

Cerrado Vegetation ◽

Central Brazil ◽

Glossophaga Soricina ◽

Caryocar Brasiliense ◽

Anoura Geoffroyi ◽

Phyllostomus Discolor

ABSTRACTThe floral biology, breeding system and pollination of Caryocar brasiliense were studied in the cerrado vegetation of Central Brazil. The large, yellowish-cream, brush-like flowers are pollinated mainly by glossophagine bats (Glossophaga soricina and Anoura geoffroyi). Three non-glossophagine bats (Phyllostomus discolor, Vampyrops lineatus and Carollia perspicillata) and two short probosisced hawk moths (Erinyis ello and Pseudosphinx tetrio) may also act as occasional pollinators. Caryocar brasiliense is self-compatible although it sets significantly more fruits when crossed than when selfed. The natural fruit set (fruit/flower ratio) and seed set (seed/ovule ratio) are 3.1% and 1.0% respectively. Most of the fruits and seeds are formed through the action of the flower visitors, despite the fact that about 20% of the non-visited flowers receive self pollen on at least one stigma.

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FLORAL BIOLOGY AND BREEDING SYSTEM IN CARDIOCRINUM GIGANTEUM (LILIACEAE), A PERENNIAL BULBIFEROUS HERB IN YUNNAN PROVINCE IN CHINA

Acta Horticulturae ◽

10.17660/actahortic.2013.977.14 ◽

2013 ◽

pp. 133-142

Author(s):

W.L. Guan ◽

Y.F. Li ◽

X. Chen ◽

S.F. Li ◽

J. Song

Keyword(s):

Breeding System ◽

Yunnan Province ◽

Floral Biology

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Solitary bee pollinators adjust pollen foraging to the unpredictable flower opening of a species of Petunia (Solanaceae)

Biological Journal of the Linnean Society ◽

10.1093/biolinnean/blz193 ◽

2019 ◽

Vol 129 (2) ◽

pp. 273-287

Author(s):

Fernanda Figueiredo De Araujo ◽

Reisla Oliveira ◽

Theo Mota ◽

João Renato Stehmann ◽

Clemens Schlindwein

Keyword(s):

Floral Biology ◽

Floral Resources ◽

Pollen Foraging ◽

Flower Opening ◽

Foraging Patterns ◽

Social Species ◽

Pollen Presentation ◽

Total Pollen ◽

Flower Visiting ◽

Effective Pollinators

Abstract Details of the foraging patterns of solitary bees are much less well known than those of social species, and these patterns are often adjusted to exploit floral resources of one or only a few species. The specialized flower-visiting bees of Petunia are good models for investigating such foraging patterns. Here we analysed the floral biology and pollen presentation schedule of the endangered Petunia mantiqueirensis in mixed Araucaria forests of Serra da Mantiqueira, Brazil. Pollinators and their pollen foraging behaviour and food specialization were determined through analyses of scopa pollen loads. Flowers opened throughout the day and presented all their pollen resources within the first 30 min of anthesis, thus providing their pollen resources in an asynchronous fashion in one-flower packages throughout the day. Females of Pseudagapostemon fluminensis were the most frequent flower visitors, contacting stigmas in 96% of their visits, and were the unique effective pollinators of Petunia mantiqueirensis. These pollinators were responsible for the first three visits to 115 individually monitored flowers at any daylight hour, removing ~86% of a flower’s total pollen supply during the first visit. Although female bees harvest the majority of pollen resources of Petunia mantiqueirensis, analyses of scopa loads revealed that most of them also collect pollen from plants of other families while foraging for pollen in Petunia flowers.

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Adaptive response of extreme epiphyte Tillandsia species (Bromeliaceae) is demonstrated by different sexual reproduction strategies in the Brazilian Chaco

Botanical Journal of the Linnean Society ◽

10.1093/botlinnean/boz104 ◽

2019 ◽

Vol 192 (4) ◽

pp. 840-854

Author(s):

Aline C Gomes ◽

Bruno H S Ferreira ◽

Camila S Souza ◽

Luan M M Arakaki ◽

Camila Aoki ◽

...

Keyword(s):

Breeding System ◽

Reproductive Strategies ◽

Extreme Environments ◽

Extreme Environment ◽

Floral Biology ◽

Reproduction Strategies ◽

Pollen Vectors ◽

Self Compatibility ◽

Floral Visitors ◽

Selection For

Abstract Some epiphytes are adapted to extreme environments with the ability to survive drought as a result of their morphological (xeromorphism), anatomical (foliar trichomes or scales) and physiological features. In contrast to vegetative features, they may have diverse sexual reproductive strategies. Here we compared the flowering morphology, floral biology, breeding system and pollinators of Tillandsia duratii, T. loliacea and T. recurvifolia (Bromeliaceae) adapted to an extreme environment, the Brazilian Chaco. Tillandsia duratii and T. recurvifolia flower for 5–6 months, whereas T. loliaceae flowers for 11 months, mainly in the dry season, with low to high flowering overlap between them. Although these species generally show similar flowering morphology, they differ in size, colour, odour and/or floral functionality, suggesting non-sharing of pollinators among them. Bimodal pollination occurs in T. duratii (bees, moths other than hawkmoths) and T. recurvifolia (butterflies, hummingbirds); in T. loliacea, we recorded no floral visitors. Tillandsia recurvifolia is self-incompatible, has flowers which approach herkogamy and protandry, and depends on pollen vectors for fruit set. The other two species show reverse herkogamy, autonomous self-pollination and self-compatibility (mixed breeding system); therefore, pollinators are not required. The disparity in reproductive strategies among the three species suggests the possibility of selection for diverse modes of reproduction.

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