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The biogeography of plant-animal interactions is a novel topic on which many disciplines converge (e.g., reproductive biology, biogeography, and evolutionary biology). Narrative reviews have indicated that tropical columnar cacti and agaves have highly specialized pollination systems, while extratropical species have generalized systems. However, t...
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... In particular, for columnar cacti, the GDH was originally proposed for pollination mediated by bats that are year-round residents in the tropics but migratory in the temperate deserts of North America (Valiente-Banuet et al., 1996). The predictions of the GDH in cacti, however, have only been formally tested in two studies (Arzabe et al., 2018;Munguía-Rosas et al., 2009). Both studies seemed to support the hypothesis somehow. ...
... Both studies seemed to support the hypothesis somehow. Munguía-Rosas et al. (2009) mainly investigated Northern Hemisphere cacti species from Mexico and the south-west United States. This meta-analysis study focused on three pollination systems (diurnal, nocturnal, and hand cross-pollination) and suggested that they increase with latitude even when phylogenetic relatedness is taken into account. ...
Aim: The geographical dichotomy hypothesis (GDH) states several flowering plant groups have specialized pollination systems in tropical areas where resources are more reliable and pollinator communities tend to be more stable, than in extratropi-cal areas. Our main goal was to understand the scope of the GDH and/or gradual environmental variation considering the evolutionary history of the pollination traits.
Location: Neotropical tropics and adjacent extratropics.
Major taxa studied: Columnar cacti.
Methods: Using a database composed of ~54 columnar cacti species (31.7% of the global columnar cactus species), four complex traits were analysed: pollination syndromes , reproductive systems, type of anthesis, and duration of anthesis. We conducted generalized linear models (GLMs), phylogenetic regressions, evolutionary trait optimization, and multivariate models with 19 bioclimatic variables and potential evapotranspiration.
Results: Weak phylogenetic signal was detected for all traits, giving consistent results between GLMs and phylogenetic regression analysis. The pollination syndrome and duration of anthesis varied with latitude, in contrast to the reproductive system and the type of anthesis. In the Southern Hemisphere, the pollinators were more diverse and the duration of anthesis was longer. Different evolutionary paths between hemispheres were detected and optimization showed a complex pattern in the evolution of traits, suggesting high homoplasy with multiple transformations by convergence and/ or parallelism. The environmental models showed thermic seasonality may be at the core of the latitudinal variation of the pollination system.
Main conclusions: We did not detect a geographical dichotomy in pollination systems of the cacti, but rather a gradual change in different pollination attributes. Therefore, instead of a GDH, we propose an environmental gradient hypothesis (EGH). Environmental variables may be explaining the variation detected in pollination system traits by conditioning floral properties (morphology, phenology), diversity and distribution of pollinators, and/or coevolution occurrence. The complexity implied in these traits is consistent with high homoplasy levels and a differential evolutionary history between the hemispheres.
... Mixed pollination systems with both diurnal and nocturnal pollinators have been documented in many species of flowering plants, and the contribution to fruit set and seed production by diurnal versus nocturnal pollinators varies among species (Munguia-Rosas et al., 2009;Cruz-Neto et al., 2015;Prieto-Benitez et al., 2015). In our H. dentata population, pollinium removal and deposition rates by diurnal butterflies did not differ significantly from crepuscular hawkmoths, and pollination efficiency of butterflies did not differ significantly from crepuscular visitors. ...
Mixed pollination system with both diurnal and nocturnal visitors contributing to pollen transfer and seed set have been documented in many angiosperm species. The flowers of Habenaria species are usually green or white, with a long nectar secreting spur, and are usually interpreted as specialized for pollination by nocturnal moths. With a few exceptions, nocturnal moths and diurnal butterflies are both reported as pollinators of Habenaria species. However, the relative contributions made by moths versus butterflies to the reproductive success in the same orchid species has rarely been studied. We investigated the floral morphology, pollinators, pollination efficiency, and breeding system of Habenaria dentata in southern China. We showed that two species of diurnal swallowtail butterflies (Papilio helenus and Papilio memnon) and a species of crepuscular hawkmoth (Eupanacra mydon) were this orchid's effective pollinators. The pollinaria were attached to the eyes of these three insect species. Pollinator exclusion experiments showed that pollinarium removal and pollinium deposition rates on stigmas by butterflies (47.51% and 38.64% respectively) were not significantly different from those made by hawkmoths (50.70% and 34.47%, respectively), indicating that diurnal and crepuscular visits contributed equally to reproductive success. As natural rates of insect-mediated pollination of our population of H. dentata resulted in fruit set rates of 93.33%, rejected the prospect that this population was pollinator limited. Hand pollination experiments indicated that H. dentata was self-compatible but without autonomous self-pollination. The proportion of well-developed seeds with large embryos in self-pollinated fruits was significantly lower than in cross-pollinated fruits, suggesting natural selection favors xenogamy. Our results highlighted the importance of both butterflies and hawkmoths contributing to the reproductive success of a rare orchid with a mixed pollination system.
... First, species richness is generally considered a key driver of resource partitioning, with richer communities having higher resource partitioning and, hence, reduced niche overlap (Pianka, 1973). The higher array of available resources in richer communities can decrease niche overlap due to an asymmetry in the number of resources and resource exploiters (Armbruster, 2006;Munguía-Rosas et al., 2009). Higher species richness in pollination systems can also trigger the evolution of more generalist morphological traits and, therefore, a higher niche overlap at the community level (Schleuning et al., 2012). ...
Species interactions are one dimension of a niche. Niche overlap arises when two species share an interaction partner. In pollination systems, environmental and biotic factors affect niche overlap. Here, we explored the effects of climate seasonality, plant and bat richness, morphological traits, and phylogenetic distance in shaping the niche overlap of Neotropical bat–plant pollination networks. We examined a dataset of 22 bat–plant pollination networks in the Neotropical region. We measured niche overlap in bats and plants with the Morisita‐Horn index ( Ĉ H ) and used a SAR model to test the relationships between niche overlap and both abiotic and biotic factors. We found a lower niche overlap among bats in communities composed of phylogenetically distant bat species. Moreover, plant and bat overlap was lower in regions with higher precipitation seasonality. Our results indicate that climate seasonality and bat evolutionary history drive niche overlap in Neotropical bat–plant pollination interactions. These findings suggest that a higher precipitation seasonality promotes the emergence of temporal modules, which reduces niche overlap, likely due to seasonal species phenologies. Furthermore, the method used to record the interactions affects the degree of niche overlap. Interactions recorded with pollen samples tend to have higher niche overlap than direct observations. The responses of morphological traits and phylogenetic distances in bat niche overlap were uncoupled, suggesting an effect of historical processes independent of morphological traits. Our findings reinforce the importance of evolutionary history and ecological processes in imprinting patterns of interaction niche overlap.
Abstract in Portuguese is available with online material
... However, several studies have found no relationship between latitude and pollen limitation (e.g. Munguía-Rosas et al., 2009;Baer & Maron, 2018), including the findings of our investigation (Fig. S3b in Notes S4). Indeed, Vamosi et al. (2006) reported the opposite trend with greater pollen limitation in tropical than in temperate regions. ...
The length of time a flower remains open and functional – floral longevity – governs important reproductive processes influencing pollination and mating and varies considerably among angiosperm species. However, little is known about large‐scale biogeographic patterns and the correlates of floral longevity.
Using published data on floral longevity from 818 angiosperm species in 134 families and 472 locations world‐wide, we present the first global quantification of the latitudinal pattern of floral longevity and the relationships between floral longevity and a range of biotic and abiotic factors.
Floral longevity exhibited a significant phylogenetic signal and was longer at higher latitudes in both northern and southern hemispheres, even after accounting for elevation. This latitudinal variation was associated with several biotic and abiotic variables. The mean temperature of the flowering season had the highest predictive power for floral longevity, followed by pollen number per flower. Surprisingly, compatibility status, flower size, pollination mode, and growth form had no significant effects on flower longevity.
Our results suggest that physiological processes associated with floral maintenance play a key role in explaining latitudinal variation in floral longevity across global ecosystems, with potential implications for floral longevity under global climate change and species distributions.
... In order to evaluate if this dichotomy translates into a specialization latitudinal gradient, Mungu ıa-Rosas et al. (2009) carried out a meta-analysis that included North American and also a few South American cacti species. These authors found evidence of a latitudinal gradient, but the effect of latitude was not significant when they added a phylogenetic control (Mungu ıa-Rosas et al., 2009). Later studies showed that species from extra-tropical South America also have generalized pollination systems (Walter, 2010;Ortega-Baes et al., 2011;Ossa & Medel, 2011;Alonso-Pedano & Ortega-Baes, 2012;Ortega-Baes & Gorostiague, 2013;Gorostiague & Ortega-Baes, 2017). ...
... studies in which pollinator effectiveness was not tested and the role of floral visitors was inferred from their behaviour. This approach does not consider the relative importance of each pollinator, assuming that they are all equally important, and previous studies have demonstrated that this is not true for some cacti (Valiente-Banuet et al., 1996;Mungu ıa-Rosas et al., 2009). In this sense, the conclusion that species possessed ecologically specialized pollination systems should be taken with caution, since the latter was not experimentally demonstrated for all of them. ...
Biotic interactions are said to be more specialized in the tropics, and this was also proposed for the pollination systems of columnar cacti from North America. However, this has not yet been tested for a wider set of cactus species. Here, we use the available information about pollination in the Cactaceae to explore the geographic patterns of this mutualistic interaction, and test if there is a latitudinal gradient in its degree of specialization.
We performed a bibliographic search of all publications on the pollination of cacti species and summarized the information to build a database. We used generalized linear models to evaluate if the degree of specialization in cacti pollination systems is affected by latitude, using two different measures: the number of pollinator guilds (functional specialization) and the number of pollinator species (ecological specialization).
Our database contained information about the pollination of 148 species. The most frequent pollinator guilds were bees, birds, moths and bats. There was no apparent effect of latitude on the number of guilds that pollinate a cactus species. However, latitude had a small but significant effect on the number of pollinator species that service a given cactus species.
Bees are found as pollinators of most cactus species, along a wide latitudinal gradient. Bat and bird pollination is more common in the tropics than in the extra‐tropics. The available information suggests that cacti pollination systems are slightly more ecologically specialized in the tropics, but it does not support any trend with regard to functional specialization.
... Los murciélagos frugívoros y varias especies vegetales han coevolucionado, el murciélago una vez que consume la pulpa de la fruta madura, dispersa a la planta durante el vuelo mediante una lluvia de semillas, esto trae otros beneficios como la reforestación pasiva de selvas y bosques (Saldaña-Vázquez et al. 2019). Los murciélagos nectarívoros funcionan como reguladores de la diversidad genética para especies de cactáceas, cuyo grado de dependencia varía a lo largo de la distribución geográfica y de la habilidad alimenticia de los murciélagos para complementar alguna fase de su ciclo reproductivo (Munguía-Rosas et al. 2009). Los murciélagos carnívoros y hematófagos (tres especies con distribución en México) cumplen una relación antagónica con otras especies, al fungir como depredadores (Marques-Dracxler y Kissling 2021) y muestran un potencial para la salud humana como la saliva del murciélago vampiro Desmodus rotundus, que contiene un anticoagulante eficaz para el tratamiento de padecimientos del sistema vasodilatador (Kakumanu et al. 2019). ...
Los cambios en la riqueza, abundancia y composición de gremios tróficos de la comunidad de murciélagos son una respuesta ante el impacto de la fragmentación y perturbación del hábitat; su evaluación es necesaria para entender la adaptación o extinción local de los murciélagos debido a los cambios en la estructura del paisaje original del bosque mesófilo de montaña (BMM). El objetivo del estudio fue evaluar la riqueza, abundancia, los gremios tróficos y la respuesta a la fragmentación de una comunidad de murciélagos en fragmentos de BMM con distinto grado de perturbación. Durante un periodo de siete meses de monitoreo, se usaron redes de niebla para la captura de murciélagos, colocadas en cuatro unidades de muestreo (UM) con distinta condición de perturbación; la diversidad de murciélagos se describió con base en el número efectivo de especies y sus respectivas comparaciones entre UM, también los murciélagos fueron clasificados a nivel de especie, por gremio trófico y por su respuesta a la condición de perturbación en cada UM. Se registraron 561 individuos de 26 especies de murciélagos, que no mostraron diferencias en el número efectivo de especies por UM. El gremio frugívoro estuvo representado por el 38% de las especies de murciélagos y el 50% de las especies registradas tuvieron una respuesta vulnerable ante la condición de perturbación. La diversidad de murciélagos observada es un bioindicador de que a pesar de la fragmentación y perturbación del BMM, las especies se han adaptado a las condiciones actuales del paisaje.
... Agaves such as A. havardiana are thought to progressively adopt generalist pollination strategies in the northern edge of their range where the number of nectarivorous bat species is low (Munguía-Rosas et al. 2009), often involving characteristics that facilitate diurnal pollination by insects and birds (Kuban 1989;Slauson 2000). Despite the unpredictability of the arrival of phyllostomid bat pollinators, both A. havardiana and A. palmeri produce nocturnal nectar and pollen (Kuban 1989;Slauson 2000). ...
Pallid bats, Antrozous pallidus, despite being primarily insectivorous gleaning predators, consume nectar of the cardón cactus, Pachycereus pringlei, in the Sonoran Desert. It is unknown whether nectar feeding occurs in the Chihuahuan Desert of Texas, where pallid bats covered in pollen have been captured. We collected pollen samples from 67 pallid bats in Brewster County, Texas, United States, between April and August 2018. Pollen-covered pallid bats were captured in every month sampled. Pollen densities were three times higher on wings than on the head or ventral body. In all samples collected, the pollen was homogeneous and identified as Agave pollen. Although two species of Agave, A. havardiana and A. lechuguilla, occur in this region of Texas, linear discriminant analysis classified 701 of 723 (97%) of pollen grains analyzed as A. lechuguilla. Additional evidence from infrared video footage collected in August 2018 indicated that pallid bats became covered in A. lechuguilla pollen while consuming nectar. Pallid bats might be engaging in facultative nectarivory across their range and could be important nocturnal pollinators.
... Some of those biological interactions shaped the evolution of certain lineages. For example, it has been shown that the evolution of columnar cacti both in North and South America was possibly driven by the interaction with bird, bat or moth pollinators (Valiente-Banuet et al. 1996Munguía-Rosas et al. 2009;Hernández-Hernández et al. 2014). In addition, the dispersion of seeds mainly by bats and birds (Bregman 1988;Godínez-Alvarez et al. 2002;Pérez-Villafaña and Valiente-Banuet 2009), plays an important role in shaping the genetic structure of populations Figueredo et al. 2010;Bustamante et al. 2016). ...
Members of the cactus family are keystone species of arid and semiarid biomes in the Americas, as they provide shelter and resources to support other members of ecosystems. Extraordinary examples are the several species of flies of the genus Drosophila that lay eggs and feed in their rotting stems, which provide a model system for studying evolutionary processes. Although there is significant progress in understanding the evolution of Drosophila species, there are gaps in our knowledge about the cactus lineages hosting them. Here we review the current knowledge about the evolution of Cactaceae, focusing on phylogenetic relationships and trends revealed by the study of DNA sequence data. During the last several decades, the availability of molecular phylogenies has considerably increased our understanding of the relationships, biogeography, and evolution of traits in the family. Remarkably, although succulent cacti have very low growth rates and long generation times, they underwent some of the fastest diversifications observed in the plant kingdom, possibly fostered by strong ecological interactions. We have a better understanding of the reproductive biology, population structure and speciation mechanisms in different clades. The recent publication of complete genomes for some species has revealed the importance of phenomena such as incomplete lineage sorting. Hybridization and polyploidization are common in the family, and have been studied using a variety of phylogenetic methods. We discuss potential future avenues for research in Cactaceae, emphasizing the need of a concerted effort among scientists in the Americas, together with the analyses of data from novel sequencing techniques.
... Vertebrate-pollinated plants inside the tropics are more dependent on pollinators than vertebrate-pollinated plants outside the tropics, conceivably due to a higher degree of plant specialization near the Equator (Olesen and Jordano 2002;Dalsgaard et al. 2011;Trøjelsgaard and Olesen 2013). For example, columnar cacti pollination systems range from exclusively batpollinated species in the tropics to species with more generalized pollinator interactions involving both diurnal and nocturnal pollinators outside the tropics (Munguia-Rosas et al. 2009). When plants are more specialized (that is, visited by a narrower range of pollinators), then the removal of one pollinator species or group might be expected to have a larger impact on those plants. ...
Vertebrate pollinators are increasingly threatened worldwide, but little is known about the potential consequences of their declines for plants and wider ecosystems. We present the first global assessment of the importance of vertebrate pollinators for zoophilous plant reproduction. Our meta-analysis of 126 experiments on plants revealed that excluding vertebrate pollinators reduced fruit and/or seed production by 63% on average. We found bat-pollinated plants to be more dependent on pollinators than bird-pollinated plants (an average 84% reduction in fruit/seed production when bats were being excluded, compared to 46% when birds were excluded). Dependence on vertebrate pollinators for fruit/seed production was greater in the tropics than at higher latitudes. With such a large potential impact of vertebrate pollinator loss, there is a clear need for prompt, effective conservation action for threatened flower-visiting vertebrate species. More research is needed on how such changes might affect wider ecosystems.
... Vertebrate-pollinated plants inside the tropics are more dependent on pollinators than vertebrate-pollinated plants outside the tropics, conceivably due to a higher degree of plant specialization near the Equator (Olesen and Jordano 2002;Dalsgaard et al. 2011;Trøjelsgaard and Olesen 2013). For example, columnar cacti pollination systems range from exclusively batpollinated species in the tropics to species with more generalized pollinator interactions involving both diurnal and nocturnal pollinators outside the tropics (Munguia-Rosas et al. 2009). When plants are more specialized (that is, visited by a narrower range of pollinators), then the removal of one pollinator species or group might be expected to have a larger impact on those plants. ...
Vertebrate pollinators are increasingly threatened worldwide, but little is known about the potential consequences of declining pollinator populations on plants and ecosystems. Here, we present the first global assessment of the importance of vertebrate pollinators in the reproductive success of selected flowering plants. Our meta-analysis of 126 experiments on animal-pollinated plants revealed that excluding vertebrate pollinators – but not insect pollinators – reduced fruit and/or seed production by 63% on average. We found bat-pollinated plants to be more dependent on their respective vertebrate pollinators than bird-pollinated plants (an average 83% reduction in fruit/seed production when bats were excluded, as compared to a 46% reduction when birds were excluded). Plant dependence on vertebrate pollinators for fruit/seed production was greater in the tropics than at higher latitudes. Given the potential for substantial negative impacts associated with the loss of vertebrate pollinators, there is a clear need for prompt, effective conservation action for threatened flower-visiting vertebrate species. Additional research on how such changes might affect wider ecosystems is also required.
