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Mean nectar values (A) mg of diluted sugar: dotted black line; (B) volume: black bars, sugar concentration: gray line; SD: vertical lines of the four bromeliad species studied: Pr: Pitcairnia recurvata, Pv: Pseudalcantarea viridiflora, Wno: Werauhia noctiflorens, Wnu: Werauhia nutans.
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Pollinators can be a limited resource and natural selection should favor differences in phenotypic characteristics to reduce competition among plants. Bats are important pollinators of many Neotropical plants, including the Bromeliaceae; however, the pre-pollination mechanisms for isolation among sympatric bat-pollinated bromeliads are unknown. Her...
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... varies highly among the four studied bromeliad species. The overall pattern shows that the highest nectar volume and concentration both occur in the early hours of the evening, following anthesis. Even in P. viridiflora and in both Werauhia species, which all open their flowers during the afternoon, nectar production is strictly nocturnal (Fig. 3). Although there are significant differences in the nectar traits among the four species (Table 2; see Supporting Information-Table S1), the overall values are broadly similar among most species. Pseudalcantarea viridiflora and W. noctiflorens produce nectar in similar quantity and of comparable quality, while P. recurvata shows values ...
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... updated) of epiphytic life-form and distributed mainly on the mountains of southern Central America (Costa Rica and Panama) (Grant, 1995;Morales, 2003). Previous studies in Werauhia indicate the presence of specialized pollination systems involving nocturnal nectarivorous bats (Aguilar-Rodríguez et al., 2019a) and hummingbirds (Lasso and Ackerman, 2004), as well as high selfing ability in W. gladioliflora (Cascante-Marín et al., 2005;Tschapka and von Helversen, 2007), W. nutans and W. noctiflorens (Aguilar-Rodríguez et al., 2019b), and W. sintenisii (Lasso and Ackerman, 2004). ...
... In spite of this, our evidence from camera traps suggests a low pollinator availability of nectar-feeding bats, with visitation ranging from none to 0.24 visits per night per plant. Data from other bat-pollinated bromeliads suggest varying but usually higher visitation rates; for instance, Aguilar-Rodríguez et al. (2019b) found no visitation to Werauhia nutans but up to 4.2 visits per flower per night in Pseudalcantarea viridiflora. While in W. gladioliflora, Tschapka and von Helversen (2007) observed 1-44 visits per flower per night. ...
... The mechanism of autonomous delayed selfing of the studied Werauhia was key to their reproductive success, representing 54-80% of the total fruit set. Recording the time of selfing in bromeliad pollination studies is not a common practice (Cascante-Marín and Núñez-Hidalgo 2023), but the few studies that have reported delayed selfing in bat-pollinated and highly autofertile bromeliads belong to Werauhia species (Cascante-Marín et al., 2005;Aguilar-Rodríguez et al., 2019b). However, these studies did not assess its contribution to reproductive success. ...
Plants with specialized pollination systems frequently exhibit adaptations for self-pollination, and this contradictory situation has been explained in terms of the reproductive assurance function of selfing. In the Neotropics, several plant lineages rely on specialized vertebrate pollinators for sexual reproduction, including the highly diverse Bromeliaceae family, which also displays a propensity for selfing. Thus far, the scarce evidence on the role of selfing in bromeliads and in other neotropical plant groups is inconclusive. To provide insights into the evolution and persistence of self-fertilization in the breeding systems of Bromeliaceae, we studied four sympatric epiphytic species from the genus Werauhia (Tillandsioideae) in Costa Rica. We documented their floral biology, pollination ecology, and breeding systems. We estimated the contribution of selfing by comparing the reproductive success between emasculated flowers requiring pollinator visits and unmanipulated flowers capable of selfing and exposed to open pollination across two flowering seasons. The studied species displayed specialized pollination by nectar-feeding bats as well as a high selfing ability (autofertility index values > 0.53), which was attained by a delayed selfing mechanism. Fruit set from natural cross-pollination was low (<26% in both years) and suggested limited pollinator visitation. In line with this, we found a very low bat visitation to flowers using video-camera recording, from 0 to 0.24 visits per plant per night. On the contrary, the contribution of selfing was comparatively significant since 54-80% of the fruit set from unmanipulated flowers can be attributed to autonomous self-pollination. We concluded that inadequate cross-pollination services diminished the reproductive success of the studied Werauhia, which was compensated for by a delayed selfing mechanism. The low negative effects of inbreeding on seed set and germination likely reinforce the persistence of selfing in this bromeliad group. These results suggest that selfing in bat-pollinated bromeliads may have evolved as a response to pollinator limitation.
... In addition to different nectar compositions, the species also differ in flower color, flower morphology, types of inflorescences, as well as flowering time (day flowering versus night flowering), and these traits are associated with different pollinator types. The pollinators are diverse, mainly hummingbirds and bats, but they are also other bird and insect species [38][39][40][41]. ...
Floral nectar contains sugars and numerous other compounds, including amino acids, but little is known about their function and origin in nectar. Therefore, the amino acid, sugar, and inorganic ion concentrations, as well as the activity of alanine aminotransferase (AlaAT) and glutamine synthetase (GS) in nectar, nectaries, and leaves were analyzed in 30 Pitcairnia species. These data were compared with various floral traits, the pollinator type, and the phylogenetic relationships of the species to find possible causes for the high amino acid concentrations in the nectar of some species. The highest concentrations of amino acids (especially alanine) in nectar were found in species with reddish flowers. Furthermore, the concentration of amino acids in nectar and nectaries is determined through analyzing flower color/pollination type rather than phylogenetic relations. This study provides new insights into the origin of amino acids in nectar. The presence of almost all amino acids in nectar is mainly due to their transport in the phloem to the nectaries, with the exception of alanine, which is partially produced in nectaries. In addition, active regulatory mechanisms are required in nectaries that retain most of the amino acids and allow the selective secretion of specific amino acids, such as alanine.
... We hypothesize that if both species have a high probability of pollination, a strong morphological correspondence between heads and cranium traits of bats and flower traits will be found, as it has been documented in other plant-pollinator systems (Barrios et al., 2016;Ings et al., 2009). Likewise, we expect that if both bat species have a high probability of pollination, pollen grains of N. tetetzo will be either the only or the main component found in their pollen loads as it has been documented for other species (Aguilar-Rodríguez et al., 2019;Borkent & Schlinger, 2008;Fisogni et al., 2018). ...
Neobuxbaumia tetetzo is a columnar cactus whose flowers are visited by the bat species Choeronycteris mexicana and Leptonycteris yerbabuenae. Although both bat species are considered the pollinators of N. tetetzo, the probability of pollination of each bat species has not been estimated. In this study, we determine the relative importance of C. mexicana and L. yerbabuenae as pollinators of N. tetetzo. The probability of pollination was estimated using two different approaches: (i) morphological correspondence between head (linear traits [total head length, snout length, and face height and width]) and cranial traits (shape traits) of bats and flower traits (linear [internal floral tube length including and excluding the nectary, corolla diameter, stamen length, style length, and corolla tube diameter] and shape traits), and (ii) pollen load analyses to estimate the percentage of occurrence (PO) and the pollination probability index (PPI). Our results showed a lack of a significant correspondence between both head and cranial traits of C. mexicana and the flowers of N. tetetzo, and linear morphological correspondence between total head length of L. yerbabuenae and flower length. Pollen loads of C. mexicana were composed by seven different pollen types, its PO and PPI were 41.87 ± 9.53% and 0.29, respectively. Leptonycteris yerbabuenae pollen loads were composed by three pollen types, with a PO of 78.29 ± 13.67% and a PPI of 0.67. Our results suggest that whereas C. mexicana has a low constancy to the flowers of N. tetetzo, L. yerbabuenae has a higher probability of pollination. The study evaluates the relative importance of two bat species (Choeronycteris mexicana and Leptonycteris yerbabuenae) as pollinators of Neobuxbaumia tetetzo (Cactaceae). Our results suggest that whereas C. mexicana has a low constancy to the flowers of N. tetetzo, L. yerbabuenae has a high probability of pollinating it.
... Speciation can be viewed as a fundamental process of biodiversity that is determined by the evolution of reproductive isolation between previously interbreeding populations [1][2][3][4][5]. The emergence of new species and their maintenance depends largely on a wide range of reproductive barriers [6][7][8][9][10]. The process of speciation is constrained by the barriers contributing to reproductive isolation and how natural selection acts on the formation of reproductively isolated populations from different populations to discrete species [11,12]. ...
... Several studies have documented that the contribution of pre-pollination barriers to total isolation is stronger than that of post-zygotic barriers [10,11,21,53]. Among pre-zygotic barriers, microhabitat isolation and pollinator isolation were the main mechanisms contributing to the total reproductive isolation in these two species. ...
Evaluation of multiple barriers contributing to reproductive isolation between sympatric plant species is key to understanding the mechanism of their coexistence; however, such investigations in biodiversity hotspots are still rare. In this study, we investigated and compared geography, microhabitat, phenology, flora, and pollinators, in addition to pollen–pistil interactions, seed production, and seed germination of the closely related sympatric Salvia digitaloides and S. flava on Yulong Snow Mountain, Southwestern Yunnan, China. The geographic distribution of these species overlapped, but their adaptation to physical and chemical properties of soil microhabitats differed. They shared the same flowering time but differed in flower size, style length, nectar volume, sugar concentration, and flower longevity. Both species shared bumblebees as effective pollinators, but flower constancy for the two species was relatively strong. Pollen tube growth, seed production, and seed germination were lower in interspecific than in intraspecific crosses. Our study suggested that microhabitat and pollinator isolation acted as the most important isolating barriers in maintaining the coexistence of the two Salvia species. Our study also highlighted that post-pollination barriers play an important role in preventing the gene flow between these two Salvia species.
... Speciation can be viewed as a fundamental process of biodiversity that is determined by the evolution of reproductive isolation between previously interbreeding populations [1][2][3][4][5]. The emergence of new species and their maintenance depends largely on a wide range of reproductive barriers [6][7][8][9][10]. The process of speciation is constrained by the barriers contributing to reproductive isolation and how natural selection acts on the formation of reproductively isolated populations from different populations to discrete species [11,12]. ...
... Several studies have documented that the contribution of pre-pollination barriers to total isolation is stronger than that of post-zygotic barriers [10,11,21,53]. Among pre-zygotic barriers, microhabitat isolation and pollinator isolation were the main mechanisms contributing to the total reproductive isolation in these two species. ...
Evaluation of multiple barriers contributing to reproductive isolation between sympatric
plant species is key to understanding the mechanism of their coexistence; however, such investigations in biodiversity hotspots are still rare. In this study, we investigated and compared geography,
microhabitat, phenology, flora, and pollinators, in addition to pollen–pistil interactions, seed production, and seed germination of the closely related sympatric Salvia digitaloides and S. flava on
Yulong Snow Mountain, Southwestern Yunnan, China. The geographic distribution of these species
overlapped, but their adaptation to physical and chemical properties of soil microhabitats differed.
They shared the same flowering time but differed in flower size, style length, nectar volume, sugar
concentration, and flower longevity. Both species shared bumblebees as effective pollinators, but
flower constancy for the two species was relatively strong. Pollen tube growth, seed production, and
seed germination were lower in interspecific than in intraspecific crosses. Our study suggested that
microhabitat and pollinator isolation acted as the most important isolating barriers in maintaining
the coexistence of the two Salvia species. Our study also highlighted that post-pollination barriers
play an important role in preventing the gene flow between these two Salvia species
... In other cases, plants can partition the temporal niche at finer scales, such as by using different anthesis/ receptivity periods during the day (Armbruster & Herzig, 1984;Stone et al., 1996;Aguilar-Rodríguez et al., 2019;Liu et al., 2020). ...
Morphological niche partitioning between related syntopic plants that are distylous (with short- and long-styled morphs) is complex. Owing to differences in the heights of stigmas and anthers, each floral morph must place pollen onto two distinct parts of the body of the pollinator. This led us to hypothesize that such partitioning should be more accurate among distylous syntopic species in comparison to combinations with other related plants that do not co-occur. We tested these assumptions using a set of Palicourea (Rubiaceae) species as a model system. We compared the distribution, flowering phenology, floral measurements and reciprocity of sexual organ heights of two syntopic species (Palicourea rigida and Palicourea coriacea) and one non-syntopic congener (Palicourea marcgravii). The three species overlapped in their distributions and flowering periods. The position of sexual organs was, in most cases, partitioned between syntopic populations, with low overlap in anther and stigma heights. However, we found a higher overlap involving the non-syntopic species, especially between Palicourea rigida and Palicourea marcgravii. Additionally, reciprocity of sexual organs was more accurate in intraspecific inter-morph combinations (i.e. legitimate organ correspondence) in comparison to intraspecific intra-morph, interspecific syntopic and interspecific non-syntopic combinations. The partitioning of morphological traits between syntopic species might facilitate the differential placement of pollen on the body of the pollinator and reduce the chances of interspecific interference.
... They produce hexose-rich nectar, suggesting pollination by bats (Krömer et al. 2008). In this genus, pollination by bats has been reported previously in P. macropetala (Aguilar-Rodríguez et al. 2014) and in P. viridiflora (Aguilar-Rodríguez et al. 2019b), while preliminary information pertaining to P. grandis suggests that it is also a chiropterophilous species (P. A. Aguilar-Rodríguez unpublished data). ...
... We compared the data obtained in the first site (Rancho Viejo) with the information collected previously in a second locality (hereafter, Los Tuxtlas; Aguilar-Rodríguez et al. 2019b). This second study site is located in the southeastern region of the state, in the ejido of Adolfo Ruiz Cortines (18°32ʼ3.55ʼʼN, ...
... Pseudalcantarea viridiflora is distributed in Mexico, Guatemala, Honduras and Nicaragua (Espejo-Serna et al. 2005). This species, at least in the south of Veracruz state, is pollinated by nectarivorous bats (Aguilar-Rodríguez et al. 2019b). Plants used in this study were collected with the permission of the Secretaría del Medio Ambiente y Recursos Naturales (permit No. 02405/14 granted to MCMG). ...
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
... The uropatagium is also useful when carrying pups during the reproductive season and its manipulation is largely controlled by the calcaneus (Adams & Thibault, 1999). Also, it has been proposed that nectar-eating bats uropatagium serves to transport pollen from one flower to another (Aguilar-Rodríguez et al., 2019). ...
New World bats are involved in key ecological processes and are good indicators of environmental changes. Recently, trait-based approaches have been used in several taxa to better understand mechanisms underlying species assemblages, biotic interactions, environmental relationships and ecosystem functions. However, despite the relevance of bats on ecosystem dynamics, so far, there is no conceptual framework that relies on the measurement of bat traits to address functional studies. Here, we present a set of 50 bat biological traits, which are suitable to assess environmental stressors and can potentially affect ecological processes. Several examples were provided to show the applicability of this framework in the study of Neotropical bat ecology. We suggest some considerations regarding trait-based approach including the importance of intraspecific variation, correlations between traits, response-effect framework, global dataset, and future directions to assess the reliability of functional relations across species and Neotropical regions by using traits. This could be helpful in tackling ecological questions associated with community assembly and habitat filtering, species diversity patterns along environmental gradients, and ecological processes. We envision this paper as a first step toward an integrative bat functional trait protocol held up with solid evidence.
Bat pollination at the range margin in the southwestern Neotropics has been largely unexplored. We provide for the first time direct evidence on bat pollination, visitation rate, and efficiency for three species of the Southern Andean Yungas. These interactions are valuable targets for future conservation efforts in this endangered ecosystem.
Abstract in Spanish is available with online material.
