Anthropogenic land-use change decreases pollination and male and female fitness in terrestrial flowering plants.

BACKGROUND AND AIMS: The majority of the earth's land area is currently occupied by humans. Measuring how terrestrial plants reproduce in these pervasive environments is essential for understanding their long-term viability and their ability to adapt to changing environments. METHODS: We conducted hierarchical and phylogenetically-independent meta-analyses to assess the overall effects of anthropogenic land-use changes on pollination, and male and female fitness in terrestrial plants. KEY RESULTS: We found negative global effects of land use change (i.e., mainly habitat loss and fragmentation) on pollination and on female and male fitness of terrestrial flowering plants. Negative effects were stronger in plants with self-incompatibility (SI) systems and pollinated by invertebrates, regardless of life form and sexual expression. Pollination and female fitness of pollination generalist and specialist plants were similarly negatively affected by land-use change, whereas male fitness of specialist plants showed no effects. CONCLUSIONS: Our findings indicate that angiosperm populations remaining in fragmented habitats negatively affect pollination, and female and male fitness, which will likely decrease the recruitment, survival, and long-term viability of plant populations remaining in fragmented landscapes. We underline the main current gaps of knowledge for future research agendas and call out not only for a decrease in the current rates of land-use changes across the world but also to embark on active restoration efforts to increase the area and connectivity of remaining natural habitats.

Elevational and seasonal patterns of plant pollinator networks in two highland tropical ecosystems in Costa Rica.

Many plant species in high montane ecosystems rely on animal pollination for sexual reproduction, however, our understanding of plant-pollinator interactions in tropical montane habitats is still limited. We compared species diversity and composition of blooming plants and floral visitors, and the structure of plant-floral visitor networks between the Montane Forest and Paramo ecosystems in Costa Rica. We also studied the influence of seasonality on species composition and interaction structure. Given the severe climatic conditions experienced by organisms in habitats above treeline, we expected lower plant and insect richness, as well as less specialized and smaller pollination networks in the Paramo than in Montane Forest where climatic conditions are milder and understory plants are better protected. Accordingly, we found that blooming plants and floral visitor species richness was higher in the Montane Forest than in the Paramo, and in both ecosystems species richness of blooming plants and floral visitors was higher in the rainy season than in the dry season. Interaction networks in the Paramo were smaller and more nested, with lower levels of specialization and modularity than those in the Montane Forest, but there were no seasonal differences within either ecosystem. Beta diversity analyses indicate that differences between ecosystems are likely explained by species turnover, whereas within the Montane Forest differences between seasons are more likely explained by the rewiring of interactions. Results indicate that the decrease in species diversity with elevation affects network structure, increasing nestedness and reducing specialization and modularity.

Gone with the wind: Negative genetic and progeny fitness consequences of habitat fragmentation in the wind pollinated dioecious tree Brosimum alicastrum.

PREMISE: Habitat fragmentation negatively affects population size and mating patterns that directly affect progeny fitness and genetic diversity; however, little is known about the effects of habitat fragmentation on dioecious, wind pollinated trees. We assessed the effects of habitat fragmentation on population sex ratios, genetic diversity, gene flow, mating patterns, and early progeny vigor in the tropical dioecious tree, Brosimum alicastrum. METHODS: We conducted our study in three continuous and three fragmented forest sites in a Mexican tropical dry forest. We used eight microsatellite loci to characterize the genetic diversity, gene flow via pollen distances, and mean relatedness of progeny. We compared early progeny vigor parameters of seedlings growing under greenhouse conditions. RESULTS: Sex ratios did not deviate from 1:1 between habitat conditions except for one population in a fragmented habitat, which was female biased. The genetic diversity of adult trees and their offspring was similar in both habitat conditions. Pollen gene flow distances were similar across habitat types; however, paternity correlations were greater in fragmented than in continuous habitats. Germination rates did not differ between habitat conditions; however, progeny from fragmented habitats produced fewer leaves and had a lower foliar area, total height, and total dry biomass than progeny from continuous habitats. CONCLUSIONS: Changes in mating patterns because of habitat fragmentation have negative effects on early progeny vigor. We conclude that negative habitat fragmentation effects on mating patterns and early progeny vigor may be a serious threat to the long-term persistence of tropical dioecious trees.

A test of the reproductive assurance hypothesis in Ipomoea hederacea: does inbreeding depression counteract the benefits of self-pollination?

PREMISE: Darwin proposed that self-pollination in allegedly outcrossing species might act as a reproductive assurance mechanism when pollinators or mates are scarce; however, in natural populations, the benefits of selfing may be opposed by seed discounting and inbreeding depression. While empirical studies show variation among species and populations in the magnitude of reproductive assurance, little is known about the counterbalancing effects of inbreeding depression. METHODS: By comparing the female reproductive success of emasculated and open-pollinated flowers, we assessed the reproductive assurance hypothesis in two Mexican populations of Ipomoea hederacea. In one population, we assessed temporal variation in reproductive assurance for three years. We evaluated inbreeding depression on seed production, seedling germination, and dry plant mass by contrasting self- and cross-hand pollination treatments in one population for two years. RESULT: The contribution of self-pollination to female reproductive success was high and consistent between populations, but there was variation in reproductive assurance across years. Inbreeding depression was absent in the early stages of progeny development, but there was a small negative effect of inbreeding in the probability of germination and the mass of adult progeny. CONCLUSIONS: Self-pollination provided significant reproductive assurance in I. hederacea but this contribution was variable across time. The contribution of reproductive assurance is probably reduced by inbreeding depression in later stages of progeny development, but this counter effect was small in the study populations. This study supports the hypothesis that reproductive assurance with limited inbreeding depression is likely an important selective force in the evolution of self-pollination in the genus Ipomoea.

Reproductive isolation among three sympatric Achimenes species: pre- and post-pollination components.

PREMISE: Closely related species occurring in sympatry may experience the negative consequences of interspecific pollen transfer if reproductive isolation (RI) barriers are not in place. We evaluated the importance of pre- and post-pollination RI barriers in three sympatric species of Achimenes (Gesneriaceae), including ecogeographic, phenological, floral isolation, self-pollination, and hybrid viability (fruit and seed set). METHODS: We recorded geographic distribution throughout species ranges and assessed flowering phenology and pollinator visitation at one site in central Mexico. In the greenhouse, we measured floral traits involved in RI and quantified fruit and seed set for from self, intraspecific, and interspecific crosses. RESULTS: Ecogeographic barriers were important in RI, but under sympatry, phenological and floral barriers contributed more to total RI. Phenological RI varied between species and years, while floral RI was 100% effective at preventing interspecific visitation. Species showed differences in floral morphology, color, and scents associated with specialized pollination systems (A. antirrhina-hummingbirds, A. flava-bees, A. patens-butterflies); heterospecific visitation events were restricted to rare secondary pollinators. Hybrid crosses consistently yielded progeny in lower numbers than intraspecific crosses. CONCLUSIONS: This study indicated that neither autogamy nor early post-pollination barriers prevent interspecific pollen flow between Achimenes species. However, floral isolation, acting through a combination of attraction and reward traits, consistently ensures specificity of the pollination system. These results suggest that selection on floral traits to reduce the costs of hybrid progeny production may have played a role in evolution or maintenance of specialized pollination systems in Achimenes.

The role of pollination effectiveness on the attributes of interaction networks: from floral visitation to plant fitness.

Network analysis is a powerful tool to understand community-level plant-pollinator interactions. We evaluated the role of floral visitors on plant fitness through a series of pollination exclusion experiments to test the effectiveness of pollinators of an Ipomoea community in the Pacific coast of Mexico, including: (1) all flower visitors, (2) visitors that contact the reproductive organs, (3) visitors that deposit pollen on stigmas, and (4) visitors that mediate fruit and seed production. Our results show that networks built from effective pollination interactions are smaller, less connected, more specialized and modular than floral visitor networks. Modules are associated with pollinator functional groups and they provide strong support for pollination syndromes only when non-effective interactions are excluded. In contrast to other studies, the analyzed networks are not nested. Our results also show that only 59% of floral visitors were legitimate pollinators that contribute to seed production. Furthermore, only 27% of the links in visitation network resulted in seed production. Our study shows that plant-pollination networks that consider effectiveness measures of pollination in addition to floral visitation provide insightful information about the different role floral visitors play in a community, encompassing a large number of commensalistic/antagonistic interactions and the more restricted set of mutualistic relationships that underlie the evolution of convergent floral phenotypes in plants.

Habitat fragmentation reduces plant progeny quality: a global synthesis.

Most of the world's land surface is currently under human use and natural habitats remain as fragmented samples of the original landscapes. Measuring the quality of plant progeny sired in these pervasive environments represents a fundamental endeavour for predicting the evolutionary potential of plant populations remaining in fragmented habitats and thus their ability to adapt to changing environments. By means of hierarchical and phylogenetically independent meta-analyses we reviewed habitat fragmentation effects on the genetic and biological characteristics of progenies across 179 plant species. Progeny sired in fragmented habitats showed overall genetic erosion in contrast with progeny sired in continuous habitats, with the exception of plants pollinated by vertebrates. Similarly, plant progeny in fragmented habitats showed reduced germination, survival and growth. Habitat fragmentation had stronger negative effects on the progeny vigour of outcrossing- than mixed-mating plant species, except for vertebrate-pollinated species. Finally, we observed that increased inbreeding coefficients due to fragmentation correlated negatively with progeny vigour. Our findings reveal a gloomy future for angiosperms remaining in fragmented habitats as fewer sired progeny of lower quality may decrease recruitment of plant populations, thereby increasing their probability of extinction.

Consequences of habitat fragmentation on the reproductive success of two Tillandsia species with contrasting life history strategies.

Fragmentation of natural habitats generally has negative effects on the reproductive success of many plant species; however, little is known about epiphytic plants. We assessed the impact of forest fragmentation on plant-pollinator interactions and female reproductive success in two epiphytic Tillandsia species with contrasting life history strategies (polycarpic and monocarpic) in Chamela, Jalisco, Mexico, over three consecutive years. Hummingbirds were the major pollinators of both species and pollinator visitation rates were similar between habitat conditions. In contrast, the composition and frequency of floral visitors significantly varied between habitat conditions in polycarpic and self-incompatible T. intermedia but not in monocarpic self-compatible T. makoyana. There were no differences between continuous and fragmented habitats in fruit set in either species, but T. makoyana had a lower seed set in fragmented than in continuous forests. In contrast, T. intermedia had similar seed set in both forest conditions. These results indicate that pollinators were effective under both fragmented and continuous habitats, possibly because the major pollinators are hummingbird species capable of moving across open spaces and human-modified habitats. However, the lower seed set of T. makoyana under fragmented conditions suggests that the amount and quality of pollen deposited onto stigmas may differ between habitat conditions. Alternatively, changes in resource availability may also cause reductions in seed production in fragmented habitats. This study adds to the limited information on the effects of habitat fragmentation on the reproductive success of epiphytic plants, showing that even related congeneric species may exhibit different responses to human disturbance. Plant reproductive systems, along with changes in pollinator communities associated with habitat fragmentation, may have yet undocumented consequences on gene flow, levels of inbreeding and progeny quality of dry forest tillandsias.

A quantitative review of pollination syndromes: do floral traits predict effective pollinators?

The idea of pollination syndromes has been largely discussed but no formal quantitative evaluation has yet been conducted across angiosperms. We present the first systematic review of pollination syndromes that quantitatively tests whether the most effective pollinators for a species can be inferred from suites of floral traits for 417 plant species. Our results support the syndrome concept, indicating that convergent floral evolution is driven by adaptation to the most effective pollinator group. The predictability of pollination syndromes is greater in pollinator-dependent species and in plants from tropical regions. Many plant species also have secondary pollinators that generally correspond to the ancestral pollinators documented in evolutionary studies. We discuss the utility and limitations of pollination syndromes and the role of secondary pollinators to understand floral ecology and evolution.

Plant-pollinator interactions and floral convergence in two species of Heliconia from the Caribbean Islands.

Variation in interspecific interactions across geographic space is a potential driver of diversification and local adaptation. This study quantitatively examined variation in floral phenotypes and pollinator service of Heliconia bihai and H. caribaea across three Antillean islands. The prediction was that floral characters would correspond to the major pollinators of these species on each island. Analysis of floral phenotypes revealed convergence among species and populations of Heliconia from the Greater Antilles. All populations of H. caribaea were similar, characterized by long nectar chambers and short corolla tubes. In contrast, H. bihai populations were strongly divergent: on Dominica, H. bihai had flowers with short nectar chambers and long corollas, whereas on Hispaniola, H. bihai flowers resembled those of H. caribaea with longer nectar chambers and shorter corolla tubes. Morphological variation in floral traits corresponded with geographic differences or similarities in the major pollinators on each island. The Hispaniolan mango, Anthracothorax dominicus, is the principal pollinator of both H. bihai and H. caribaea on Hispaniola; thus, the similarity of floral phenotypes between Heliconia species suggests parallel selective regimes imposed by the principal pollinator. Likewise, divergence between H. bihai populations from Dominica and Hispaniola corresponded with differences in the pollinators visiting this species on the two islands. The study highlights the putative importance of pollinator-mediated selection as driving floral convergence and the evolution of locally-adapted plant variants across a geographic mosaic of pollinator species.

Evolutionary breakdown of pollination specialization in a Caribbean plant radiation.

• Ecological generalization is postulated to be the rule in plant-pollinator interactions; however, the evolution of generalized flowers from specialized ancestors has rarely been demonstrated. This study examines the evolution of pollination and breeding systems in the tribe Gesnerieae (Gesneriaceae), an Antillean plant radiation that includes specialized and generalized species. • Phylogenetic reconstruction was based on two nDNA markers (internal transcribed spacer (ITS) and G-CYCLOIDEA (GCYC) and morphology. The total evidence Bayesian phylogeny was used for assessment of floral character evolution using Bayesian stochastic character mapping. • Mapping of the pollination system resulted in at least two origins of bat pollination and two origins of generalized pollination (bats, moths and hummingbirds). The evolution of bat pollination was associated with floral transitions reflecting the chiropterophilous floral syndrome. The evolution of generalization was associated with subcampanulate corollas. Autonomous breeding systems evolved only in hummingbird-pollinated lineages. • The correlated evolution of floral traits and pollination systems provides support for the pollination syndrome concept. Floral transitions may have been favored by the low frequency of hummingbird visitation in the Antilles, while the presence of autonomous pollination may have allowed the diversification of ornithophilous lineages. Results suggest that pollinator depauperate faunas on islands select for the evolution of reproductive assurance mechanisms, including generalization and autogamy.

Pollen limitation and reproductive assurance in Antillean Gesnerieae: a specialists vs. generalist comparison.

Pollen limitation of female fecundity is widespread among angiosperms, a signal that pollinators frequently fail to transfer pollen to fertilize all ovules. Recent surveys have suggested that pollen limitation is associated with floral specialization. This study uses a group of Antillean Gesneriaceae with contrasting pollination systems (bat, hummingbird, and generalist) to assess the premise that plants with specialized pollination systems and infrequent pollinator visitation experience greater pollen limitation of fruit and seed set than their generalist congeners. Alternatively, specialists may possess mechanisms that reduce pollen limitation, such as autonomous self-pollination. A survey of autonomous self-pollination conducted on 13 Gesneria and Rhytidophyllum species during 2006-2008 revealed no significant association between reproductive assurance mechanisms and pollination system specialization. However, high levels of potential autonomous self-pollination were only found among specialized hummingbird-pollinated species. A comparison of fruit and seed set between emasculated and unmanipulated flowers provided evidence for autonomous selfing acting as a reproductive assurance mechanism in three out of four ornithophilous species. Furthermore, the Puerto Rican population of G. reticulata relies almost exclusively on self-pollination for reproduction. Two-year pollen supplementation experiments conducted on nine Gesnerieae species from the Dominican Republic and Puerto Rico provided evidence for significant pollen limitation associated with pollination specialization including both bat- and hummingbird-pollinated Gesnerieae; no pollen limitation was detected in any of the four generalist species. No pollen limitation was detected either in two ornithophilous Gesneria species with low hummingbird visitation and high levels of autonomous self-pollination. This study provides support for the idea that generalized pollination systems may, in some cases, buffer against fluctuations in the pollinator environment. However, the use of reproductive assurance mechanisms allows the maintenance of highly specialized pollination systems in pollinator depauperate environments.

Potential autonomous selfing in Gesneria citrina (Gesneriaceae), a specialized hummingbird pollinated species with variable expression of herkogamy.

Species with mixed mating systems often demonstrate variable expression of breeding system characteristics and thus represent the opportunity to understand the factors and mechanisms that promote both outcrossed and selfed seed production. Here, we investigate variation in levels of herkogamy (variation in stigma-anther separation distance) in a Puerto Rican population of hummingbird pollinated Gesneria citrina Urban. There is significant variation in herkogamy levels among individuals of this species and stigma-anther separation is negatively associated with the ability to set fruits and seeds in the absence of pollinators. The variation in levels of herkogamy may represent a mechanism to ensure the production of some self-fertilized progeny in the absence of hummingbird pollinators. We also describe a novel breeding system in G. citrina, where stamens elongate over time to reach stigma height, but stamen elongation is accelerated by pollination. These results suggest that once the flowers are pollinated, stamen elongation may favor increased pollen removal and siring success, while the reduction in stigma-anther distance no longer imposes the risk of interference between male and female functions. We discuss our findings of breeding system variation in the context of pollination system evolution in an island setting (Antillean islands).

Pollination ecology and breeding systems of five Gesneria species from Puerto Rico.

BACKGROUND AND AIMS: The genus Gesneria diversified in the Greater Antilles giving rise to various floral designs corresponding to different pollination syndromes. The goal of this study was to characterize the pollination and breeding systems of five Puerto Rican Gesneria species. METHODS: The study was conducted in Arecibo and El Yunke National Forest, Puerto Rico, between 2003 and 2007. Floral visitors were documented by human observers and video cameras. Floral longevity and nectar production were recorded for the five study species. Tests for self-compatibility and autonomous selfing were conducted through hand-pollination and bagging experiments. KEY RESULTS: Floral phenology and nectar production schedules agree with nocturnal (in bell-shaped flowered G. pedunculosa and G. viridiflora subsp. sintenisii) or diurnal pollination syndromes (in tubular-flowered G. citrina, G. cuneifolia and G. reticulata). Nectar concentration is consistently low (8-13 %) across species. Gesneria citrina and G. cuneifolia are exclusively pollinated by hummingbirds, while Gesneria reticulata relies mostly on autonomous self-pollination, despite having classic ornithophilous flowers. A variety of floral visitors was recorded for the two species with bell-shaped flowers; however, not all visitors have the ability to transfer pollen. Bats are the primary pollinators of G. pedunculosa, with bananaquits probably acting as secondary pollinators. For G. viridiflora subsp. sintenisii, both bats and hummingbirds contact the flower's reproductive organs, thus, this species is considered to be a generalist despite its nocturnal floral syndrome. All species are self-compatible but only tubular-flowered Gesneria are capable of autonomous self-pollination. CONCLUSIONS: The visitation patterns described in this study fit the predicted hummingbird and bat pollination syndromes and support both specialization and generalization of pollination systems in Puerto Rican Gesneria. Specialization is associated with low pollinator visitation, particularly by hummingbirds, which may explain the occurrence of autonomous selfing mechanisms in tubular-flowered species.