How many animal-pollinated angiosperms are nectar-producing?

The diversity of plant-pollinator interactions is grounded in floral resources, with nectar considered one of the main floral rewards plants produce for pollinators. However, a global evaluation of the number of animal-pollinated nectar-producing angiosperms and their distribution world-wide remains elusive. We compiled a thorough database encompassing 7621 plant species from 322 families to estimate the number and proportion of nectar-producing angiosperms reliant on animal pollination. Through extensive sampling of plant communities, we also explored the interplay between nectar production, floral resource diversity, latitudinal and elevational gradients, contemporary climate, and environmental characteristics. Roughly 223 308 animal-pollinated angiosperms are nectar-producing, accounting for 74.4% of biotic-pollinated species. Global distribution patterns of nectar-producing plants reveal a distinct trend along latitudinal and altitudinal gradients, with increased proportions of plants producing nectar in high latitudes and altitudes. Conversely, tropical communities in warm and moist climates exhibit greater floral resource diversity and a lower proportion of nectar-producing plants. These findings suggest that ecological trends driven by climate have fostered the diversification of floral resources in warmer and less seasonal climates, reducing the proportion of solely nectar-producing plants. Our study provides a baseline for understanding plant-pollinator relationships, plant diversification, and the distribution of plant traits.

Anatomical, histochemical, and developmental approaches reveal the long-term functioning of the floral nectary in Tocoyena formosa (Rubiaceae).

Tocoyena formosa has a persistent floral nectary that continues producing nectar throughout flower and fruit development. This plant also presents an intriguing non-anthetic nectary derived from early-developing floral buds with premature abscised corolla. In this study, we characterize the structure, morphological changes, and functioning of T. formosa floral nectary at different developmental stages. We subdivided the nectary into four categories based on the floral and fruit development stage at which nectar production started: (i) non-anthetic nectary; (ii) anthetic nectary, which follows the regular floral development; (iii) pericarpial nectary, derived from pollinated flowers following fruit development; and (iv) post-anthetic nectary that results from non-pollinated flowers after anthesis. The nectary has a uniseriate epidermis with stomata, nectariferous parenchyma, and vascular bundles, with a predominating phloem at the periphery. The non-anthetic nectary presents immature tissues that release the exudate. The nectary progressively becomes more rigid as the flower and fruit develop. The main nectary changes during flower and fruit development comprised the thickening of the cuticle and epidermal cell walls, formation of cuticular epithelium, and an increase in the abundance of calcium oxalate crystals and phenolic cells near the vascular bundles. Projections of the outer periclinal walls toward the cuticle in the post-anthetic nectary suggest nectar reabsorption. The anatomical changes of the nectary allow it to function for an extended period throughout floral and fruit development. Hence, T. formosa nectary is a bivalent secretory structure that plays a crucial role in the reproductive and defensive interactions of this plant species.

Imprints of indirect interactions on a resource-mediated ant-plant network across different levels of network organization.

Indirect interactions are pivotal in the evolution of interacting species and the assembly of populations and communities. Nevertheless, despite recently being investigated in plant-animal mutualism at the community level, indirect interactions have not been studied in resource-mediated mutualisms involving plant individuals that share different animal species as partners within a population (i.e., individual-based networks). Here, we analyzed an individual-based ant-plant network to evaluate how resource properties affect indirect interaction patterns and how changes in indirect links leave imprints in the network across multiple levels of network organization. Using complementary analytical approaches, we described the patterns of indirect interactions at the micro-, meso-, and macro-scale. We predicted that plants offering intermediate levels of nectar quantity and quality interact with more diverse ant assemblages. The increased number of ant species would cause a higher potential for indirect interactions in all scales evaluated. We found that nectar properties modified patterns of indirect interactions of plant individuals that share mutualistic partners, leaving imprints across different network scales. To our knowledge, this is the first study tracking indirect interactions in multiple scales within an individual-based network. We show that functional traits of interacting species, such as nectar properties, may lead to changes in indirect interactions, which could be tracked across different levels of the network organization evaluated.

A new seed-feeding species of Hemicolpus Heller, 1895 from south Brazil and redescription of Hemicolpus abdominalis Hustache, 1938 (Coleoptera: Curculionidae: Conoderinae).

The genus Hemicolpus Heller, 1895 (Curculionidae: Conoderinae) currently includes six species: H. cubicus (Lacordaire) (Brazil); H. heteromorphus Hustache (Brazil); H. abdominalis Hustache (Bolivia, Brazil, and Paraguay); H. costaricensis Hespenheide (Costa Rica); H. randiae Hespenheide (El Salvador and Mexico) and H. prenai Hespenheide (El Salvador and Mexico). The known species are predispersal seed predators whose larvae feed and develop within fruits of Rubiaceae. Species from Central America have been reared from the fruits of Randia L. (Rubiaceae). In contrast, the only host plant known for the South American species, H. abdominalis, is Tocoyena formosa (Cham. & Schltdl.) K. Schum. (Rubiaceae), a plant species widely distributed in the Cerrado biome, occurring from southeast to north and northeast of Brazil. Here, we describe a seventh species of Hemicolpus, H. maragatensis Sanz-Veiga, Savaris & Leivas, sp. nov., morphologically close to H. abdominalis, associated with fruits of Randia ferox (Cham. & Schltdl.) DC. in the south of Brazil. Furthermore, we designate a lectotype and provide a redescription of H. abdominalis, including additional characters to differentiate it from H. maragatensis. For both species, we provide morphological descriptions of external and internal characters, including male and female genitalia illustrations, distribution data, and notes on the biology and host plant. A barcode region of the mitochondrial DNA is also included for both species adding genetic information to the species characterization and differentiation. We also provide an identification key for the species of the genus.

Data standardization of plant-pollinator interactions.

BACKGROUND: Animal pollination is an important ecosystem function and service, ensuring both the integrity of natural systems and human well-being. Although many knowledge shortfalls remain, some high-quality data sets on biological interactions are now available. The development and adoption of standards for biodiversity data and metadata has promoted great advances in biological data sharing and aggregation, supporting large-scale studies and science-based public policies. However, these standards are currently not suitable to fully support interaction data sharing. RESULTS: Here we present a vocabulary of terms and a data model for sharing plant-pollinator interactions data based on the Darwin Core standard. The vocabulary introduces 48 new terms targeting several aspects of plant-pollinator interactions and can be used to capture information from different approaches and scales. Additionally, we provide solutions for data serialization using RDF, XML, and DwC-Archives and recommendations of existing controlled vocabularies for some of the terms. Our contribution supports open access to standardized data on plant-pollinator interactions. CONCLUSIONS: The adoption of the vocabulary would facilitate data sharing to support studies ranging from the spatial and temporal distribution of interactions to the taxonomic, phenological, functional, and phylogenetic aspects of plant-pollinator interactions. We expect to fill data and knowledge gaps, thus further enabling scientific research on the ecology and evolution of plant-pollinator communities, biodiversity conservation, ecosystem services, and the development of public policies. The proposed data model is flexible and can be adapted for sharing other types of interactions data by developing discipline-specific vocabularies of terms.

The diversity and evolution of pollination systems in large plant clades: Apocynaceae as a case study.

Background and Aims: Large clades of angiosperms are often characterized by diverse interactions with pollinators, but how these pollination systems are structured phylogenetically and biogeographically is still uncertain for most families. Apocynaceae is a clade of >5300 species with a worldwide distribution. A database representing >10 % of species in the family was used to explore the diversity of pollinators and evolutionary shifts in pollination systems across major clades and regions. Methods: The database was compiled from published and unpublished reports. Plants were categorized into broad pollination systems and then subdivided to include bimodal systems. These were mapped against the five major divisions of the family, and against the smaller clades. Finally, pollination systems were mapped onto a phylogenetic reconstruction that included those species for which sequence data are available, and transition rates between pollination systems were calculated. Key Results: Most Apocynaceae are insect pollinated with few records of bird pollination. Almost three-quarters of species are pollinated by a single higher taxon (e.g. flies or moths); 7 % have bimodal pollination systems, whilst the remaining approx. 20 % are insect generalists. The less phenotypically specialized flowers of the Rauvolfioids are pollinated by a more restricted set of pollinators than are more complex flowers within the Apocynoids + Periplocoideae + Secamonoideae + Asclepiadoideae (APSA) clade. Certain combinations of bimodal pollination systems are more common than others. Some pollination systems are missing from particular regions, whilst others are over-represented. Conclusions: Within Apocynaceae, interactions with pollinators are highly structured both phylogenetically and biogeographically. Variation in transition rates between pollination systems suggest constraints on their evolution, whereas regional differences point to environmental effects such as filtering of certain pollinators from habitats. This is the most extensive analysis of its type so far attempted and gives important insights into the diversity and evolution of pollination systems in large clades.

Pericarpial nectary-visiting ants do not provide fruit protection against pre-dispersal seed predators regardless of ant species composition and resource availability.

Extrafloral nectaries can occur in both vegetative and reproductive plant structures. In many Rubiaceae species in the Brazilian Cerrado, after corolla abscission, the floral nectary continues to secret nectar throughout fruit development originating post-floral pericarpial nectaries which commonly attract many ant species. The occurrence of such nectar secreting structures might be strategic for fruit protection against seed predators, as plants are expected to invest higher on more valuable and vulnerable parts. Here, we performed ant exclusion experiments to investigate whether the interaction with ants mediated by the pericarpial nectaries of Tocoyena formosa affects plant reproductive success by reducing the number of pre-dispersal seed predators. We also assessed whether ant protection was dependent on ant species composition and resource availability. Although most of the plants were visited by large and aggressive ant species, such as Ectatomma tuberculatum and species of the genus Camponotus, ants did not protect fruits against seed predators. Furthermore, the result of the interaction was neither related to ant species composition nor to the availability of resources. We suggest that these results may be related to the nature and behavior of the most important seed predators, like Hemicolpus abdominalis weevil which the exoskeleton toughness prevent it from being predated by most ant species. On the other hand, not explored factors, such as reward quality, local ant abundance, ant colony characteristics and/or the presence of alternative energetic sources could also account for variations in ant frequency, composition, and finally ant protective effects, highlighting the conditionality of facultative plant-ant mutualisms.

The long and the short of it: a global analysis of hawkmoth pollination niches and interaction networks.

1. Proboscis length has been proposed as a key dimension of plant pollination niches, but this niche space has not previously been explored at regional and global scales for any pollination system. Hawkmoths are ideal organisms for exploring pollinator niches as they are important pollinators in most of the biodiverse regions of the earth and vary greatly in proboscis length, with some species having the longest proboscides of all insects. 2. Using datasets for nine biogeographical regions spanning the Old and New World, we ask whether it is possible to identify distinct hawkmoth pollination niches based on the frequency distribution of proboscis length, and whether these niches are reflected in the depths of flowers that are pollinated by hawkmoths. We also investigate the levels of specialization in hawkmoth pollination systems at the regional and community level using data from interaction network studies. 3. We found that most regional hawkmoth assemblages have bimodal or multimodal distributions of proboscis length, and that these are matched by similar distributions of floral tube lengths. Hawkmoths, particularly those with longer proboscides, are polyphagous and at the network level show foraging specialization equivalent to or less than that of bees and hummingbirds. In the case of plants, shorter-tubed flowers are usually visited by numerous hawkmoth species, while those that are longer-tubed tend to exclude shorter-proboscid hawkmoths and thus become ecologically specialized on longer-proboscid hawkmoth species. Longer-tubed flowers tend to have greater nectar rewards and this promotes short-term constancy by long-proboscid hawkmoths. 4. Our results show that pollinator proboscis length is a key niche axis for plants and can account for patterns of evolution in functional traits such as floral tube length and nectar volume. We also highlight a paradoxical trend for nectar resource niche breadth to increase according to proboscis length of pollinators, while pollinator niche breadth decreases according to the tube length of flowers.

Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks.

A major challenge in evolutionary ecology is to understand how co-evolutionary processes shape patterns of interactions between species at community level. Pollination of flowers with long corolla tubes by long-tongued hawkmoths has been invoked as a showcase model of co-evolution. Recently, optimal foraging models have predicted that there might be a close association between mouthparts' length and the corolla depth of the visited flowers, thus favouring trait convergence and specialization at community level. Here, we assessed whether hawkmoths more frequently pollinate plants with floral tube lengths similar to their proboscis lengths (morphological match hypothesis) against abundance-based processes (neutral hypothesis) and ecological trait mismatches constraints (forbidden links hypothesis), and how these processes structure hawkmoth-plant mutualistic networks from five communities in four biogeographical regions of South America. We found convergence in morphological traits across the five communities and that the distribution of morphological differences between hawkmoths and plants is consistent with expectations under the morphological match hypothesis in three of the five communities. In the two remaining communities, which are ecotones between two distinct biogeographical areas, interactions are better predicted by the neutral hypothesis. Our findings are consistent with the idea that diffuse co-evolution drives the evolution of extremely long proboscises and flower tubes, and highlight the importance of morphological traits, beyond the forbidden links hypothesis, in structuring interactions between mutualistic partners, revealing that the role of niche-based processes can be much more complex than previously known.

Low abundance of long-tongued pollinators leads to pollen limitation in four specialized hawkmoth-pollinated plants in the Atlantic Rain forest, Brazil.

Long-tubed hawkmoth-pollinated species present some of the most remarkable examples of floral specialization depending exclusively on long-tongued hawkmoths for sexual reproduction. Nonetheless, long-tongued hawkmoths do not rely exclusively on specialized plants as nectar sources, which may limit sexual reproduction through pollen limitation. However, very few studies have quantified the level of pollen limitation in plants with highly specialized floral traits in tropical regions. In this context, we studied four sympatric hawkmoth-pollinated species in a highland Atlantic Rain forest and assessed pollen limitation and their dependence on pollinators by analyzing the floral biology, breeding system, pollination mechanisms, and abundance of long-tongued pollinators. We showed that the four species are self-compatible, but are completely dependent on long-tongued hawkmoths to set fruits, and that flower visitation was infrequent in all plant species. Pollen limitation indices ranged from 0.53 to 0.96 showing that fruit set is highly limited by pollen receipt. Long-tongued moths are much less abundant and comprise only one sixth of the hawkmoth fauna. Pollen analyses of 578 sampled moths revealed that hawkmoths visited ca. 80 plant species in the community, but only two of the four species studied. Visited plants included a long-tubed hawkmoth-pollinated species endemic to the lowland forest ca. 15-20 km away from the study site. Specialization index (H 2 ' = 0.20) showed that community-level interactions between hawkmoths and plants are generalized. We suggest that sexual reproduction of these highly specialized hawkmoth-pollinated species is impaired by competition among plants for pollinators, in conjunction with the low abundance and diversity of long-tongued pollinators.

Armament imbalances: match and mismatch in plant-pollinator traits of highly specialized long-spurred orchids.

BACKGROUND: Some species of long-spurred orchids achieve pollination by a close association with long-tongued hawkmoths. Among them, several Habenaria species present specialized mechanisms, where pollination success depends on the attachment of pollinaria onto the heads of hawkmoths with very long proboscises. However, in the Neotropical region such moths are less abundant than their shorter-tongued relatives and are also prone to population fluctuations. Both factors may give rise to differences in pollinator-mediated selection on floral traits through time and space. METHODOLOGY/PRINCIPAL FINDINGS: We characterized hawkmoth assemblages and estimated phenotypic selection gradients on orchid spur lengths in populations of three South American Habenaria species. We examined the match between hawkmoth proboscis and flower spur lengths to determine whether pollinators may act as selective agents on flower morphology. We found significant directional selection on spur length only in Habenaria gourlieana, where most pollinators had proboscises longer than the mean of orchid spur length. CONCLUSIONS/SIGNIFICANCE: Phenotypic selection is dependent on the mutual match between pollinator and flower morphologies. However, our findings indicate that pollinator-mediated selection may vary through time and space according to local variations in pollinator assemblages.