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Ancestral pollinator state reconstruction for the Vriesea radiation from the Atlantic Rainforests of eastern Brazil showing repeated shifts between bat and hummingbird pollination. For this analysis, we used the phylogenetic tree of Gomes-da-Silva & Souza-Chies (2018) and collected information of pollinator groups from the literature for >50% of the species (for references see Supporting Information, Table S1). For species lacking pollinator information, we applied the concept of pollination syndromes based on floral morphology (Fӕgri & van der Pijl 1979). We categorized groups either as hummingbird-, hummingbird-/bat-or bat-pollinated and reconstructed ancestral pollinator states applying a Bayesian Markov chain Monte Carlo (MCMC) analysis in RASP version2.1 beta (Yu, Harris & He, 2012). Using the Jukes-Cantor + G model, sampling each of 100 generations, we ran the MCMC analysis for 50 000 generations and allowed all character combinations. We chose the MCMC approach because it offers the opportunity to code hummingbird/bat pollination as an intermediate stage.
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At least half of the 3600 species of Bromeliaceae are pollinated by hummingbirds. There is little doubt that the four to 12 evolutionary shifts towards and c. 32 shifts away from hummingbird pollination opened new evolutionary spaces for bromeliad diversification, and that hummingbird pollination has led to increased bromeliad diversification rates...
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Context 1
... depending on sample size and methodology of the ancestral state reconstruction Aguilar-Rodríguez et al., 2019). By plotting pollinator information on the phylogenetic tree for Vriesea of Gomes-da-Silva & Souza-Chies (2018), we here document one additional shift from bat to hummingbird pollination in V. thyrsoidea Mez (for details see legend to Fig. 3 and Supporting Information, Table S1). There are probably a number of additional, still undetected gains of hummingbird pollination, although most of these will involve only a few species. An example of a species not yet included in a phylogenetic analysis is Fosterella spectabilis H.Luther, the only species with a bird pollination ...
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... the larger genera of Bromeliaceae reveals that in fact there were many more switches from hummingbird to insect or bat pollination. For instance, by plotting pollinator information on the above-mentioned phylogenetic tree for Vriesea (containing 69 out of 214 species), we here document three additional shifts from hummingbird to bat pollination (Fig. 3). Furthermore, studies on the reproductive ecology of Pitcairnia ( Wendt et al., 2001Wendt et al., , 2002) in combination with the phylogenetic analysis of Saraiva, Mantovani & Forzza (2015) indicate that at least one switch from hummingbird to insect pollination and one switch to bat pollination has occurred in Pitcairnia. ...
Context 3
... depending on sample size and methodology of the ancestral state reconstruction Aguilar-Rodríguez et al., 2019). By plotting pollinator information on the phylogenetic tree for Vriesea of Gomes-da-Silva & Souza-Chies (2018), we here document one additional shift from bat to hummingbird pollination in V. thyrsoidea Mez (for details see legend to Fig. 3 and Supporting Information, Table S1). There are probably a number of additional, still undetected gains of hummingbird pollination, although most of these will involve only a few species. An example of a species not yet included in a phylogenetic analysis is Fosterella spectabilis H.Luther, the only species with a bird pollination ...
Context 4
... the larger genera of Bromeliaceae reveals that in fact there were many more switches from hummingbird to insect or bat pollination. For instance, by plotting pollinator information on the above-mentioned phylogenetic tree for Vriesea (containing 69 out of 214 species), we here document three additional shifts from hummingbird to bat pollination (Fig. 3). Furthermore, studies on the reproductive ecology of Pitcairnia ( Wendt et al., 2001Wendt et al., , 2002) in combination with the phylogenetic analysis of Saraiva, Mantovani & Forzza (2015) indicate that at least one switch from hummingbird to insect pollination and one switch to bat pollination has occurred in Pitcairnia. ...
Citations
... Bromeliads fascinate with their spectacular inflorescences, colorful bracts, and beautiful flowers, and increase their charm even more when we observe that they are visited by a hummingbird, bat, or an insect (Aguilar-Rodríguez et al., 2019;Kessler et al., 2020). However, there is a genus of the subfamily Bromelioideae that is somewhat shy because it is hardly possible to observe its hidden flowers with the naked eye as their inflorescences are not present on a conspicuous peduncle but located at the base of the leaves. ...
Bromeliads fascinate with their spectacular inflorescences, colorful bracts, and beautiful flowers, and increase their charm even more when we observe that they are visited by a hummingbird, bat, or an insect. However, there is a genus of the subfamily Bromelioideae that is somewhat shy because it is hardly possible to observe its hidden flowers with the naked eye as their inflorescences are not present on a conspicuous peduncle but located at the base of the leaves. The identity of its pollinators is also still a mystery and basically nothing is known about the sexual reproductive biology of this genus. We refer to Greigia Regel, whose large members have leaves arranged in a rosette pattern, more or less caulescent, of terrestrial and/or rupicolous habit, leaves with marginal spines, the flowers tubular, purple or white and borne in flattened inflorescences that are deeply arranged in the axils of the leaves. The inflorescences are usually covered by accumulated organic matter (e.g., leaf litter), so their presence is hardly visible. This is why its 36 unspectacular species, distributed mainly in humid montane forests from Mexico to Chile have gone largely unnoticed by botanists, resulting in few collections and a low number of herbarium specimens.
... The floral features of S. enigmaticus, i.e., red bracts and yellow perianth, exserted stamens and stigma, and diurnal anthesis, are unique in the genus Stigmatodon but common in Vriesea (Costa et al. 2014, Couto et al. 2022. These characteristics, associated with hummingbird pollination syndrome (ornithophily), seem to be the ancestral state among bromeliads, while bat pollination (chiropterophily) originated multiple times in the family as a whole (Aguillar-Rodríguez et al. 2019), as well as in Vriesea (Kessler et al. 2020;Neves et al. 2020), and is supported as an ancestral state in Stigmatodon species (Couto et al. 2022). All the 33 previously known species of Stigmatodon bear chiropterophilous flowers, therefore the floral features of S. enigmaticus could result from the retention of the ancestral state or a reversion to it, a hypothesis that needs to be tested with molecular phylogeny. ...
Stigmatodon enigmaticus is described and illustrated as a new lithophytic taxon from the quartzitic Campos Rupestres within the biodiversity hotspot of the Atlantic Forest, in Minas Gerais state, Southeastern Brazil. This puzzling new species presents floral features that are unique in the genus as they are associated with ornithophily, as in most Vriesea, contrasting with the chiropterous features of all previously known Stigmatodon species. It is assigned to the “S. limae group”, being most similar to S. vexatus, with which it is compared. Stigmatodon enigmaticus is a microendemic species and is here assessed as Critically Endangered due to its restricted habitat, reduced population size, and threats from invasive species. This finding adds to several others that reinforce the relevance of the currently unprotected Serra do Padre Ângelo as a priority for conservation.
... The family Bromeliaceae comprises about 3700 species of 79 genera (Butcher & Gouda et al. 2021), with half of the species epiphytic in habit (Zotz 2013). In this family, pollination mainly occurs through visits by the hummingbird (Kessler & Krömer 2000;Krömer et al. 2006;Kessler et al. 2020). However, the plants of some genera, especially those of the subfamily Tillandsioideae (e.g., Guzmania, Tillandsia and Vriesea), have evolved diverse floral characteristics that attract different pollinator groups such as insects, birds and bats (Benzing 2000;Kessler & Krömer 2000;Givnish et al. 2014;Aguilar-Rodríguez et al. 2016). ...
Intraspecific variation in floral traits, such as nectar, could lead to differences in the identity and pollinator effectiveness of visitors between populations of a flowering plant. We studied the bat-pollinated bromeliad species Pseudalcantarea viridiflora to determine whether there are differences in the identity of its pollinators and in its nectar traits between two study sites located at different latitudes in Veracruz, Mexico. We studied phenology and determined the volume, concentration and quantity of dissolved sugars in the nectar at both sites. The northern P. viridiflora population produced nectar that was more sugar-rich, leading to pollination by a larger species, Anoura geoffroyi, whereas the southern populations were visited mainly by Glossophaga mutica, a smaller pollinator. The most abundant nectarivorous bats at each site differ in terms of their efficiency as pollinators, and we suggest that this might affect their contribution to the fitness of the bromeliad.
Keywords:
Anoura; Bromeliaceae; chiropterophily; Glossophaga; Mexico; nectar traits; pollination; pollinator effectiveness
... In the Neotropics, the interactions with birds (hummingbirds) may have accelerated an extensive speciation in species rich families, e.g. Bromeliaceae (Givnish et al. 2014, Kessler et al. 2020. Stiles (1985) documented 50 plant species pollinated primarily by hummingbirds in a Costa Rican submontane forest. ...
Many tropical plants are pollinated by birds and several bird phylogenetical lineages have specialised to a nectar diet. The long-assumed, intimate ecological and evolutionary relationship between ornithophilous plants and phenotypically specialised nectarivorous birds has nevertheless been questioned in recent decades, where such plant–pollinator interactions have been shown to be highly generalised.
In our study, we analysed two extensive interaction datasets: bird–flower and insect–flower interactions, both collected on Mt Cameroon, west-central Africa. We tested if: 1) insects and birds interact with distinct groups of plants; 2) plants with a typical set of ornithophilous floral traits (i.e. bird pollination syndrome) interact mainly with birds; 3) birds favour plants with bird pollination syndrome and; 4) if and how the individual floral traits and plant level nectar production predict bird visitation.
Bird-visited plants were typically also visited by insects, while approximately half of the plants were visited by insects only. We confirmed the validity of the bird pollination syndrome hypothesis, as plants with bird-pollination syndrome traits were visited by birds at a higher rate and mostly hosted a lower frequency of visiting insects. However, these ornithophilous plants were not more attractive than the other plants for nectar-feeding birds. Nectar production per plant individual was a better predictor of bird visitation than any other floral trait traditionally related to the bird pollination syndrome. Our study thus demonstrated the highly asymmetrical relationship between ornithophilous plants and nectarivorous birds.
... We hypothesize that the association with hummingbirds and bats is a main biotic driver of Vriesea diversification. In addition, pollinator shifts can open new adaptive space for species diversification and distinct mechanisms may increase speciation within each main pollinator group (which seems to be where most diversification in the genus occurs), such as (i) floral specialization on specific pollinator species; (ii) efficiency of pollen transfer and deposition by specific pollinator species which affect connectivity among populations resulting in allopatric speciation; (iii) different flowering time and pollinator behaviour when foraging; and (iv) different pollinator species distribution along altitude and habitat types according to their physiological preferences (Aguilar-Rodriguez et al. 2019;Kessler et al. 2020). ...
... Studies comparing hummingbird-and bat-pollinated plant assemblages in the Atlantic Forest at different altitudinal ranges showed higher species diversity of both Vriesea and pollinators in the lowlands (Sazima et al. 1999;Buzato et al. 2000). For bromeliads in general, it has been argued that bat-pollinated species are more diverse at humid mid-elevations and lowlands, whereas hummingbird-pollinated species are more diverse in midelevation to highlands, which coincides with the physiological demands of the different groups of pollinators (see review of Kessler et al. 2020). In addition, these authors discuss the shifts among pollination syndromes to occur predominantly in transition zones at mid-elevation areas. ...
... The authors sampled only three Vriesea species (sensu Barfuss et al. 2016), but identified the genus as one of the most representative among the chiropterophilous in Bromeliaceae. Kessler et al. (2020) reported three shifts from hummingbird to bat and one shift from bat to hummingbird in Vriesea (sensu Gomes-da-Silva and Souza-Chies 2017). To properly track these shifts in pollination syndromes in Vriesea, a robust phylogeny resolved at the shallow phylogenetic relationships is needed. ...
Pollinators are important drivers of angiosperm diversification at both micro- and macroevolutionary scales. Both
hummingbirds and bats pollinate the species-rich and morphologically diverse genus Vriesea across its distribution in
the Brazilian Atlantic Forest. Here, we (i) determine if floral traits predict functional groups of pollinators as documented,
confirming the pollination syndromes in Vriesea and (ii) test if genetic structure in Vriesea is driven by geography (latitudinal
and altitudinal heterogeneity) or ecology (pollination syndromes). We analysed 11 floral traits of 58 Vriesea species and
performed a literature survey of Vriesea pollination biology. The genealogy of haplotypes was inferred and phylogenetic
analyses were performed using chloroplast (rps16-trnk and matK) and nuclear (PHYC) molecular markers. Floral traits
accurately predict functional groups of pollinators in Vriesea. Genetic groupings match the different pollination syndromes.
Species with intermediate position were found between the groups, which share haplotypes and differ morphologically
from the typical hummingbird- and bat-pollinated flowers of Vriesea. The phylogeny revealed moderately to well-supported
clades which may be interpreted as species complexes. Our results suggest a role of pollinators driving ecological isolation
in Vriesea clades. Incipient speciation and incomplete lineage sorting may explain the overall low genetic divergence within
and among morphologically defined species, precluding the identification of clear species boundaries. The intermediate
species with mixed floral types likely represent a window into shifts between pollinator syndromes. This study reports the
morphological-genetic continuum that may be typical of ongoing pollinator-driven speciation in biodiversity hotspots.
... Furthermore, the reduced nuclear gene flow among P. flammea populations (see Table S3) also suggests limited pollen dispersal and reduced ability of pollinating hummingbirds (Wendt et al. 2002) in maintaining gene exchange between rock outcrops, and ultimately promoting allopatric speciation, a key hypothesis raised for explaining diversification of this radiation family (Givnish et al. 2014;Kessler et al. 2020). In fact, reduced seed and/or pollen dispersal has likely promoted allopatric speciation in several Neotropical plants adapted to naturally fragmented habitats, such as inselberg (Alcantarea spp. ...
Geographic isolation and reduced population sizes can lead to local extinction, low efficacy of selection and decreased speciation. However, population differentiation is an essential step of biological diversification. In allopatric speciation, geographically isolated populations differentiate and persist until the evolution of reproductive isolation and ecological divergence completes the speciation process. Pitcairnia flammea allows us to study the evolutionary consequences of habitat fragmentation on naturally disjoint rock-outcrop species from the Brazilian Atlantic Rainforest (BAF). Our main results showed low-to-moderate genetic diversity within populations, and deep population structuring caused by limited gene flow, low connectivity, genetic drift and inbreeding of long-term isolation and persistence of rock-outcrop populations throughout Quaternary climatic oscillations. Bayesian phylogenetic and model-based clustering analyses found no clear northern and southern phylogeographic structure commonly reported for many BAF organisms. Although we found two main lineages diverging by ~2 Mya during the early Pleistocene, species’ delimitation analysis assigned most of the populations as independent evolving entities, suggesting an important role of disjoint rock outcrops in promoting high endemism in this rich biome. Lastly, we detected limited gene flow in sympatric populations although some hybridization and introgression were observed, suggesting a continuous speciation process in this species complex. Our data not only inform us about the extensive differentiation and limited gene flow found among Pitcairnia flammea species complex, but they also contain information about the mechanisms that shape the genetic architecture of small and fragmented populations of isolated rock outcrop of recently radiated plants.
... The absence of seeds in berries observed after flower maturation in plants we grew in greenhouse conditions suggests pollinator dependence, or some type of incompatibility. Septal nectaries occur in all Bromeliaceae (Bernadello et al., 1991;Sajo et al., 2004b), and the occurrence of septal nectaries and tubular corollas for nectar accumulation are considered to be adaptations to pollination by hummingbirds (Trochilidae) (Givnish et al., 2000; also see the review by Kessler, Abrahamczyk & Krömer, 2020, of the role of hummingbirds in the evolution and diversification of Bromeliaceae). ...
Aechmea (Bromeliaceae) is a large genus with controversial systematics and distinct flower shapes and pollinators. We explored floral anatomy and development in two Aechmea spp. belonging to different subgenera to contribute useful information on reproductive biology and taxonomy. We examined floral buds using scanning electron and light microscopy to characterize the development of septal nectaries, petal appendages, ovules, stamens and carpels. In A. gamosepala, we confirmed that the petal appendages develop late, whereas in A. correia-araujoi they develop earlier during floral development. Petal appendage formation included positional changes, possibly affecting floral attributes and visitation by insects, rather than vertebrates. Nectar is released through three basal orifices distally on the ovary, and here we document the link between the nectary region, through discrete canals, upward to the conduplicate lobes of the wet stigma. Improved understanding of the floral development and morphology of Aechmea may help to explain the existence of polymorphic flowers in this genus and may have implications for studies on interactions with pollinators and systematics.
... The first of these papers, following on from, for example, Magalhães et al. (2018), is a timely review by Kessler, Abrahamczyk & Krömer (2020; Fig. 1) of the role of hummingbird pollination in the diversification of Bromeliaceae. The authors present various potential and non-exclusive mechanisms that may increase diversification rates of hummingbird-pollinated clades of Bromeliaceae and discuss the challenges in testing such hypotheses due to a lack of available data. ...
The ancestors of Bromeliaceae originated in the Guayana Shield c. 100 Mya. However, most of the current taxa started to diversify in South America just after the main orogenic changes associated with the beginning of the uplift of the Andes during the Miocene (c. 20 Mya; Givnish et al., 2007, 2011). Since then, impressive diversifications of several functional and ecological adaptations have allowed bromeliads to occupy a range of extreme habitats in almost all of tropical and subtropical South America, and currently species occur from northern Patagonia to the southern USA (Florida); there is also a single species in West Africa (Benzing, 2000; Christenhusz & Chase, 2013). Species from this wonderful monocot family are good models for understanding how the interplay among microevolutionary processes such as gene flow, genetic drift and natural selection influence species-level patterns of macroevolution (i.e. speciation and extinction rates) in the Neotropics.
A fundamental question in evolutionary biology is how clades of organisms exert influence on one another. The evolution of the flower and subsequent plant/pollinator coevolution are major innovations that have operated in flowering plants to promote species radiations at a variety of taxonomic levels in the Neotropics. Here we test the hypothesis that pollination by Neotropical endemic hummingbirds drove the evolution of two unique stigma traits in correlation with other floral traits in New World Salvia (Lamiaceae). We examined morphometric shapes of stigma lobing across 400 Salvia spp., scored presence and absence of a stigma brush across Salvia, and used a suite of phylogenetic comparative methods to detect shape regime shifts, correlation of trait shifts with BayesTraits and phylogenetic generalized least square regressions, and the influence of scored pollinators on trait evolution using OUwie. We found that a major Neotropical clade of Salvia evolved a correlated set of stigma features, with a longer upper stigma lobe and stigmatic brush, following an early shift to hummingbird pollination. Evolutionary constraint is evident as subsequent shifts to bee pollination largely retained these two features. Our results support the hypothesis that hummingbirds guided the correlative shifts in corolla, anther connective, style and stigma shape in Neotropical Salvia, despite repeated shifts back to bee pollination.
Este estudio proporciona una lista comentada de las especies de Puya (Bromeliaceae) registradas en el departamento de Lambayeque, Perú. Se reportan un total de cinco especies, de las cuales cuatro se registran por primera vez y una de ellas se confirma como endemismo de los Andes del Departamento. Las ecorregiones donde se encuentran corresponden al Bosque Seco estacional (BSe), la transición Matorral Desértico-Bosque Seco (MD-BS) y Jalca (JA). Se presenta una clave para las especies reportadas y se discuten las razones de los endemismos, amenazas y sus criterios de categorización.
