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Generalization in Pollination Systems, and Why it Matters

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Abstract

One view of pollination systems is that they tend toward specialization. This view is implicit in many discussions of angiosperm evolution and plant-pollinator coevolution and in the long-standing concept of "pollination syndromes." But actual pollination systems often are more generalized and dynamic than these traditions might suggest, To illustrate the range of specialization and generalization in pollinators' use of plants and vice versa, we draw on studies of two floras in the United States, and of members of several plant families and solitary bee genera, We also summarize a recent study of one local flora which suggests that, although the colors of flowers are aggregated in "phenotype space," there is no strong association with pollinator types as pollination syndromes would predict. That moderate to substantial generalization often occurs is not surprising on theoretical grounds. Plant generalization is predicted by a simple model as long as temporal and spatial variance in pollinator quality is appreciable, different pollinator species do not fluctuate in unison, and they are similar in their pollination effectiveness. Pollinator generalization is predicted when floral rewards are similar across plant species, travel is costly, constraints of behavior acid morphology are minor, and/or pollinator lifespan is long relative to flowering of individual plant species. Recognizing that pollination systems often are generalized has important implications. In ecological predictions of plant reproductive success and population dynamics it is useful to widen the focus beyond flower visitors within the "correct" pollination syndrome, and to recognize temporal and spatial fluidity of interactions. Behavioral studies of pollinator foraging choices and information-processing abilities will benefit from understanding the selective advantages of generalization. In studies of floral adaptation, microevolution, and plant speciation one should recognize that selection and gene flow vary in time and space and that the contribution of pollinators to reproductive isolation of plant species may be overstated. In conservation biology, generalized pollination systems imply resilience to linked extinctions, but also the possibility for introduced generalists to displace natives with a net loss of diversity.
... Yet, there is still doubt as to the effectiveness of pollinator behavior in inhibiting reproduction and effectively driving speciation (Chittka et al., 1999;Waser, 1998). How can pollinators cause RI when most plants are generalists appealing to a variety of pollinators, and most pollinators are generalists visiting a variety of plants (Jordano, 1987;Ollerton, 2016;Robertson, 1928;Waser et al., 1996)? In order to better address this question, we need a framework for evaluating how quantifiable properties of pollinator behavior can contribute to RI in plants across complex communities. ...
... Most of the flowering plants are visited by multiple pollinators (Robertson, 1928;Waser et al., 1996) ...
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Pollinator behavior is an important contributor to plants speciation, yet how variation in pollinator behavior causes variation in reproductive isolation (RI) is largely uncharacterized. Here I present a model that predicts how two aspects of pollinator behavior, constancy and preference, contribute to a barrier to reproduction in plants. This model is motivated by two observations: most co‐occurring plants vary in frequency over space and time, and most plants have multiple pollinators that differ in behavior. Thus, my goal was to understand how relative frequencies of plants and pollinators in a community influence ethological RI between co‐occurring plants. I find that RI for a focal plant generally increases with increasing relative plant frequency, but the shape of this relationship is highly dependent on the strength of pollinator behavior (constancy and preference). Additionally, when multiple pollinators express different behavior, I find that pollinators with stronger preference disproportionately influence RI. But, I show that RI caused by constancy is the average RI predicted from constancy of each pollinator weighted by pollinator frequency. I apply this model to examples of pollinator‐mediated RI in Phlox and in Ipomopsis to predict the relationships between plant frequency and ethological RI in natural systems. This model provides new insights into how and why pollinator specialization causes RI, and how RI could change with changing biological communities. I create a model that predicts plant ethological reproductive isolation (RI) based on pollinator behavior. This model is motivated by the empirical observation that the relative frequency of hybridizing plants and their pollinators change over space and time. My model predicts how this variation in plant‐pollinator community affects RI between co‐occurring species.
... The other entomophilic syndromes were less expressive, but many plant species presented a generalized pollination system since their flowers can be pollinated by different generalist pollinators. Even when they are not the main food sources for these insects, the resources offered by these plants can be vital for the persistence of populations of these pollinators in the absence of other sources (Waser et al. 1996;Rabeling et al. 2019). Furthermore, this strategy can compensate for the fruiting of several plants in a possible seasonal insect deficiency (Waser et al. 1996). ...
... Even when they are not the main food sources for these insects, the resources offered by these plants can be vital for the persistence of populations of these pollinators in the absence of other sources (Waser et al. 1996;Rabeling et al. 2019). Furthermore, this strategy can compensate for the fruiting of several plants in a possible seasonal insect deficiency (Waser et al. 1996). ...
Article
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Studies on pollination and seed dispersal are essential for the conservation of plant diversity. In this study, we aimed to evaluate the pollination and dispersal syndromes of five fragments of the Cerrado Rupestre immersed in an agricultural landscape to answer the following questions: (i) What is the frequency of pollination and dispersal syndromes among species and individuals?; (ii) Which are the predominant pollination and seed dispersal syndromes in this environment?. A total of 66 species, belonging to 44 genera and 29 botanical families, were evaluated. Melittophily was the most common type of pollination syndrome, observed in 54.55% of the species, followed by phalenophily (9.09%), cantharophily, ornithophily, quiropterophilly and sphingophily (all 3.03%), and psychophilly (1.51%). Generalist pollination represented 22.73% of the records. Of the 1246 individuals identified, 59.23% were melitophilous, 25.20% generalists, 5.86% phalenophilous, 3.37% quiropterophilous, 2.49% cantharophilous, 2.25% ornithophilous, 1.44% sphingophilous and 0.16% psychophilous. Regarding dispersion syndromes, zoochory was the most common type of dispersion, observed in 68.18% of the species, followed by anemochory (28.79%) and autochory (3.03%). On the other hand, the frequency among individuals differed from the values found for frequency among species. Of the 1246 individuals identified, 55.38% were anemochoric, 43.10% zoochoric, and 1.52% autochoric. Our results demonstrate the predominance of biotic syndromes in the community, especially melittophily and zoochory, contributing to a better understanding of the functionality and availability of resources in the community, as well as indispensable information for the conservation, management, and restoration of natural environments.
... Instead, selection may favour floral traits that incorporate additional pollinators without excluding the existing ones (Waser et al., 1996;Fenster et al., 2004;Giménez-Benavides et al., 2007). This may be especially relevant as provision of pollination service by nocturnal pollinators can be unpredictable (e.g., moth pollination, Oliveira et al., 2004), and by also attracting diurnal pollinators, nocturnal plants may increase visitation and pollination opportunities (Potascheff et al., 2020). ...
Article
Plants establish pollination interactions with different groups of animals, including nocturnal ones that establish interactions with economically valuable and culturally important crops, as well as wild plants of conservation concern. Despite the considerable number of studies addressing the structure and dynamic of pollination networks, nocturnal interactions have been relatively overlooked. Using a multilayer network approach and considering diurnal and nocturnal interactions, we aimed to understand how interactions at different periods of the day are integrated and contribute to the network structural pattern. We also aimed to highlight how multilayer networks may give a more nuanced assessment of species importance across layers. We assembled a pollination network of an intensively studied Neotropical area by standardizing interaction data from 16 previous studies into a presence/absence (binary) network. Then we used a multilayer network approach to evaluate the network modularity and plant species' roles in these different temporal layers. Plants were classified as nocturnal or diurnal according to the onset of floral opening and pollinators were classified according to their foraging period. The network consisted of 178 pollinator species and 158 plant species, with 870 links. Among plant species, 135 species have diurnal floral opening while 23 species are nocturnal. The multilayer network was significantly modular, and these modules differed in the composition of pollinator groups (e.g., hawk moths, bats, bees, hummingbirds), as well as of diurnal and nocturnal plants. We show that diurnal and nocturnal interactions are organized into interconnected modules in the multilayer network. Nocturnal plants had higher values of versatility and multidegree than diurnal plants, due to their role in connecting the two temporal layers. Synthesis. Our study highlights the importance of integrating different pollination systems to understand the importance of distinct components that structure pollination networks. We also illustrate the value of tapping into existing information, particularly species interaction data, from well studied biodiversity hotspot areas, to gain a better understanding of how communities are structured. Finally, despite the relative scarcity of nocturnal pollination network studies, we showed nocturnal plants, which often make complementary use of diurnal pollinators, to be important in connecting the temporal layers.
... The concept of pollination syndromes, suites of floral traits associated with the attraction and utilization of a specific functional group of animals as pollinators (Fenster et al., 2004), has played a prominent role in the development of pollination ecology. The concept is, however, controversial because many plant species are visited by pollinators from multiple functional groups (Ollerton, 1996(Ollerton, , 1998Waser et al., 1996), and because pollination syndrome classifications have been (incorrectly) used in a typological manner in comparative studies, to replace actual pollinator observations (e.g. Reich et al., 2020). ...
Article
The predictive power of pollination syndromes has been demonstrated for many South African plant species with specialized pollination systems, but has rarely been tested in the florally diverse genus Erica. Here we evaluate the hypothesis that Erica cylindrica is moth-pollinated, based on its tubular, pale, and strongly scented flowers. Pollinator observations revealed exclusive nocturnal flower visitation by several hawkmoth species, and assessment of pollen loads confirmed that two hawkmoth species carried Erica pollen grains on their proboscises. Floral scent showed no clear periodicity in emission, but was dominated by benzenoid scent compounds including benzaldehyde, benzyl alcohol, benzyl acetate, and eugenol that are known to elicit antennal responses in hawkmoths. The pale cream flower colour was characterized by uniform reflectance across the human-visible light spectrum and a small secondary peak in the UV region. The volume of nectar produced was small, but the intermediate sugar concentration and sucrose:hexose ratio of 0.7 are consistent with hawkmoth pollination. More than three-quarters of flowers in an inflorescence are oriented upwards, which is highly unusual among South African ericas but has been shown to be adaptive in other hawkmoth-pollinated flowers. Anther-ring disruption indicated that at least 62% of flowers received visits and was associated with pollen deposition in 68% of visited flowers, suggesting that visitors are effective pollinators. Our study provides evidence for hawkmoth pollination of an Erica species, a system hitherto rarely recorded in Ericaceae. Several floral traits are consistent with the hawkmoth pollination syndrome, but further work is required to confirm the functional significance of these traits and the level of specialization in this hawkmoth pollination system.
... Canola (Brassica napus L.) may serve as an ideal MFC for wild pollinators, as it satisfies all of these conditions. Most plants are pollinated by generalist pollinators (Waser et al., 1996;Bascompte and Jordano, 2007), so generalist foragers should benefit the most from MFC bloom (but see Fijen et al., 2019). However, MFCs have a negative impact on bumble bees (Bombus), as succesful colonies require resources that span longer periods of time than a MFC bloom Riedinger et al., 2015). ...
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Canola (Brassica napus L.) is a valuable crop that occupies a large part of the Canadian prairies, and is visited by wild and managed bees. However, the distribution of foraging bees in mass-flowering crops (MFCs), the value of bee visitation, and how MFCs and semi-natural land (SNL) affect wild bee populations in the context of canola agro-ecosystems is unclear. Using three separate studies, I related pollination and yield to bee visitation, and landscape composition and canola abundance to wild bee abundance. The first study examines honey bee (Apis mellifera L.) visitation in commodity canola fields using a simulation model, and reveals that honey bees most closely followed predictions for solitary efficiency-maximizers, valuing nearby flower sources much more than distant ones. The second study relates visita-tion rates of honey bees and alfalfa leafcutting bees (Megachile rotundata (Fabr.)) to pollen deposition and seed production using a structural equation model. Leafcutter bee visitation strongly increased pollen deposiion, but not honey bee visitation, and extra pollen deposition increased seed production in seed canola, but not in commodity canola. The final study uses solitary bee abundance data from a set of landscapes across southern Alberta, and relates bee abundance to landscape composition from the current and previous year. While the overall response of bee abundance to SNL was positive, individual species' response to SNL ranged from positive to negative, and canola had little effect on any species' abundances. These results reveal that insect visitation in flowering crops decay rapidly with distance, that the plant growth context of canola is equally important as the pollination context, and that while the effect of SNL on wild bee abundance is generally positive, it likely varies depending on the traits of individual bee species. This work provides mechanistic insight into the foraging behaviour and contextual value of pollination by managed bees, and sheds light on how agro-ecological landscapes shape wild bee communities.
... This means that the pollination system and floral signals that work in M. monophyllos should be considered multifaceted. These kinds of complex systems might be preferred in highly variable environments, where the abundance and distribution of pollinators fluctuate temporally and spatially, and where the plants occur in a great dispersion, like it is in the studied M. monophyllos population [11,64]. In any conditions, plants had to find a trade-off between specific pollinators with variable visitation rates and fruit set and more generalist pollinators that may be present in larger abundance. ...
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Simple Summary: Malaxis monophyllos is an ephemeral orchid with very small, greenish flowers, whose pollination system remains vague. Therefore, the authors aimed to identify the flower's features, including its anatomical micro and ultrastructure as well as scent biochemistry, which are involved in attracting pollinators. In this paper, the authors established the variety of emissions of M. monophyllos volatile compounds, with a high proportion of aldehydes and aliphatic alcohols, listed as chemicals that induce a pronounced reaction in Diptera. Second, the entire M. monophyllos labellum exhibits metabolic and secretory activity, which can be related to both emission of volatiles and visual attractants but also to the nutritional reward for pollinators. All these flower features indicated that its pollination system is dedicated to dipterans, with few signaling modalities corresponding to deceptive species (brood site and food decoy) but also referring to rewarding ones (nutritional secretion, fungus/microbe reward). This research reveals a few new issues in M. monophyllos pollination biology that provides new scientific areas for in-depth insights in the future. Abstract: Many orchid species have evolved complex floral signals to ensure pollination efficiency. Here, the authors combined analyses of anatomical flower structure with analyses of the volatile composition and flower-visiting insects' behaviour, as well as characterised features that can attract pollinators of the inconspicuous orchid Malaxis monophyllos. During field observations, the authors found that only small Diptera (e.g., mosquitos, drosophilids, fungus gnats) visit and are interested in the flowers of M. monophyllos, which was reflected in the characterised flower features that combine well with the pollination system, which engages dipterans. Analyses of the M. monophyllos floral scent revealed substantial concentrations of aliphatic compounds, e.g., 1-octen-3-ol and 1-octanol, which condition the mushroom-like scent and a substantial fraction of alkanes, some of which have been previously described as sex mimicry and aggregation pheromones in orchids' deceptive systems. The labellum anatomical structure exhibits a highly diverse cell cuticle surface and pronounced metabolic and secretory activity of the epidermal and subepidermal cells from all parts of the labellum. Moreover, our study provides evidence for the subsequent decoys of M. monophyllos flowers, including visual signals, such as raphides located on the labellum margin and the rewarding ones connected with lipid secretion limited to the area behind the column. Taking an integrative approach to studying M. monophyllos pollination biology, the authors provide new insight into its previously vague pollination strategies and provide evidence for complex floral signal operation in luring potential pollinators. The synergistic effect of M. monophyllos flowers' Citation: Jermakowicz, E.; Leśniewska, J.; Stocki, M.; Naczk, A.M.; Kostro-Ambroziak, A.; Pliszko, A. The Floral Signals of the Inconspicuous Orchid Malaxis monophyllos: How to Lure Small Pollinators in an Abundant Environment. Biology 2022, 11, 640.
... For instance, when we compare motifs with equal structure for both trophic levels, we found that floral visitors had always over-representation in the positions that implied the highest number of direct links (e.g., positions 16 and 46 from motifs 7 and 17, respectively). Despite this being in good agreement with the current view of the generalist nature of pollinators (Olesen & Jordano, 2002;Ollerton, 2017;Waser et al., 1996), we found that this over-representation of generalist network motifs was driven by the taxonomic group of bees while the rest of the taxonomic groups tended to be under-represented (Supporting Information Figure S6 A). In contrast, non-bee groups were over-represented in motif positions associated with specialised roles. ...
Preprint
Ecological processes leave distinct structural imprints on the species interactions that shape the topology of mutualistic networks. Detecting those relationships is not trivial since they go beyond pairwise interactions, but may get blurred when considering full network descriptors. Recent work has shown that the network meso-scale can capture this important information. The meso-scale describes network subgraphs representing patterns of interactions between a small number of species (i.e., motifs) that constitute the building blocks of the whole network. Despite the possible implications of network motifs to better capture species interactions, they remain overlooked in natural plant-pollinator networks. By exploring 60 empirical plant-pollinator networks from 18 different studies with wide geographical coverage we show that some motifs are consistently under- or over-represented worldwide, suggesting that the building blocks of plant-pollinator networks are not random. Furthermore, we find that distinct motif positions describing species ecological roles (e.g., generalisation and number of indirect interactions) are occupied by different plant and floral visitor groups on both trophic levels. Bees appear less frequently in specialised motif positions with high number of indirect interactions, while the rest of floral visitor groups are infrequent in generalised motif positions with low number of indirect interactions. All plant groups tend to be over-represented on specialised motif positions, except tall plant species with separated sexes (e.g., woody dioecious or monoecious species), which are more frequent on motif positions with low number of indirect interactions. Interestingly, the realized combinations of different species groups within a motif can not be retrieved from their joint probability distributions, indicating that group combinations are not random either. Our result highlights the non-random structure of the meso-scale on plant-pollinators networks and the association of different plant and floral visitor groups with certain motifs that involve different ecological roles at a macro-ecological scale
... Large population sizes could make species of plants and pollinators less susceptible to local extinctions and thus allow greater spatiotemporal persistence allowing for greater generalization. Because spatiotemporal overlap of interacting partners and abundance are primary factors in driving interaction patterns it supports the view that interactions are strongly driven by opportunism (Waser et al. 1996, Memmott 1999. Higher abundances could also increase the detectability of species and their interactions (McCarthy et al. 2013, Chacoff et al. 2018. ...
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Generalist species are important for maintaining network structure and function. Previous studies showed that interactions between generalists persist across sites and years. However, the mechanisms for persistence across spatiotemporal scales are not clear. To address this gap, we collected data on plant–pollinator interactions throughout the flowering period for five years across six plots in a subalpine meadow. We hypothesized that tolerance of environmental variation across time and space plays a key role in species’ generalization by regulating spatiotemporal overlap with partners. We found that interactions between species with broader temporal and spatial distributions tended to be more generalized such that interactions near the network core were more persistent across years and plots and within seasons. These results further understanding of networks by linking the role of environmental variation in time and space in organizing interactions, marrying niche concepts that emphasize species environmental constraints and their role in the community.
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Ornithophily has been long speculated to occur in the subtribe Maxillariinae (Orchidaceae), relying either solely on micromorphological analyses or scarce field observations of undefined species. In Guatemala we were able to observe regular visits of the azure-crowned hummingbirds feeding on flowers of Ornithidium fulgens. These observations have led us to investigation of floral attractants by means of scanning and transmission microscopy, histochemical and chemical analyses (GC–MS). Conducted investigation revealed that the epidermis of basal protuberance of column-foot has features proving the secretory activity and that secreted nectar is sucrose-dominant. Slight secretion on the middle part of the lip is puzzling. The presence of other potential pollinators has not been reported. Based on the results of this study, we confirmed that the flowers of O. fulgens meet all criteria of ornithophily and thus that the hypothesis about bird pollination in the subtribe Maxillariinae is proven. The presented results confirm that the previously described floral features predicting the bird pollination in this group are justified. This strengthens the theory about floral adaptations to different pollinators and gives valid reasons to consider species with flowers with a certain set of traits as ornithophilous, even in the absence of the pollination observation.
Chapter
This chapter provides an overview on flowering and fruiting phenology, pollination and seed dispersal syndromes of species occurring in the capões (natural forest patches) of the southern Pantanal wetland, Brazil. We monthly sampled three to five different capões from May 1999 to May 2000 for all reproductive plant individuals and recorded their habits, numbers of open flowers, unripe and ripe fruits. The dataset comprised 52 capões in total. We classified the species into pollination and seed dispersal syndromes based on flower and fruit traits, respectively. In total, we recorded 248 flowering species and 111 fruiting species. According to floral traits, melittophily (47%) was the most frequent pollination syndrome, whereas anemophily was recorded for only 3% of the species. Zoochory was the most frequent seed dispersal syndrome (64%), followed by anemochory (19%) and autochory (17%). Epizoochory represented 5% of the zoochoric species. The present study highlights the high resource availability for pollinators and seed dispersers in the capões throughout the year, with a peak during the rainy season. In addition, we show that most plant species in these forest patches depend on biotic vectors for reproduction, thereby ensuring the maintenance of biological diversity in the Pantanal.
Article
In the hummingbird-pollinated herb Ipomopsis aggregata, selection through male function during pollination favors wide corolla tubes. We explored the mechanisms behind this selection, using phenotypic selection analysis to compare effects of corolla width on two components of male pollination success, pollinator visit rate and pollen exported per visit. During single visits by captive hummingbirds, flowers with wider corollas exported more pollen, and more dye used as a pollen analogue, to stigmas of recipient flowers. Corolla width was less strongly related to visit rate in the field, and had no direct effect on visit rate after nectar production and corolla length were controlled for. Moreover, the phenotypic selection differential was 80% higher for the effect on pollen exported per visit, suggesting that this is the more important mechanism of selection.