Selfing in epiphytic bromeliads compensates for the limited pollination services provided by nectarivorous bats in a neotropical montane forest.

Abstract. Plants with specialized pollination systems frequently exhibit adaptations for self-pollination, and this contradictory situation has been explained in terms of the reproductive assurance function of selfing. In the neotropics, several plant lineages rely on specialized vertebrate pollinators for sexual reproduction, including the highly diverse Bromeliaceae family, which also displays a propensity for selfing. Thus far, the scarce evidence on the role of selfing in bromeliads and in other neotropical plant groups is inconclusive. To provide insights into the evolution and persistence of self-fertilization in the breeding systems of Bromeliaceae, we studied four sympatric epiphytic species from the genus Werauhia (Tillandsioideae) in Costa Rica. We documented their floral biology, pollination ecology and breeding systems. We estimated the contribution of selfing by comparing the reproductive success between emasculated flowers requiring pollinator visits and un-manipulated flowers capable of selfing and exposed to open pollination across two flowering seasons. The studied species displayed specialized pollination by nectar-feeding bats as well as a high selfing ability (auto-fertility index values > 0.53), which was attained by a delayed selfing mechanism. Fruit set from natural cross-pollination was low (<26% in both years) and suggested limited pollinator visitation. In line with this, we found a very low bat visitation to flowers using video-camera recording, from 0 to 0.24 visits per plant per night. On the contrary, the contribution of selfing was comparatively significant since 54-80% of the fruit set from un-manipulated flowers can be attributed to autonomous self-pollination. We concluded that inadequate cross-pollination services diminished the reproductive success of the studied Werauhia, which was compensated for by a delayed selfing mechanism. The low negative effects of inbreeding on seed set and germination likely reinforce the persistence of selfing in this bromeliad group. These results suggest that selfing in bat-pollinated bromeliads may have evolved as a response to pollinator limitation.

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.

Genetic diversity and phylogeographic patterns of the dioecious palm Chamaedorea tepejilote (Arecaceae) in Costa Rica: the role of mountain ranges and possible refugia.

Gene flow connects populations and is necessary to sustain effective population sizes, and genetic diversity. In the Lower Central American (LCA) region, the complex topographic and climatic history have produced a wide variety of habitats resulting in high biodiversity. Phylogeographic studies of plants from this area are scarce, and to date none have been conducted on palms. We used SSR and chloroplast DNA (cpDNA) markers to study the genetic diversity and structure of populations of the understory palm Chamaedorea tepejilote in Costa Rica. We found that populations of C. tepejilote have moderate to high nuclear simple sequence repeat (SSR) genetic diversity, likely due to large population sizes and its outcrossing mating system. Habitat loss and fragmentation may have contributed to increased genetic structure within slopes. High-elevation mountain ranges appeared to be a significant barrier for gene flow among populations in the Caribbean and Pacific slopes; however, ranges are permeable through low-elevation passes. In contrast, most populations had a single distinct cpDNA haplotype, supporting the hypothesis of several isolated populations that experienced decline that likely resulted in eroded cytoplasmic genetic diversity within populations. The haplotype network and Bayesian analysis linked populations in the Caribbean and the southern Pacific coast, suggesting that gene flow between Pacific and Caribbean populations may have occurred through the southern extreme of the Talamanca Mountain range in Panama, a colonization pathway not previously suggested for LCA plants. This is one of the first phylogeographic studies conducted on tropical palms in the LCA region and the first in the genus Chamaedorea, which sheds light on possible gene flow and dispersal patterns of C. tepejilote in Costa Rica. Our results also highlight the importance of mountain ranges on shaping gene flow patterns of Neotropical plants.

Blooming plant species diversity patterns in two adjacent Costa Rican highland ecosystems.

The Costa Rican Paramo is a unique ecosystem with high levels of endemism that is geographically isolated from the Andean Paramos. Paramo ecosystems occur above Montane Forests, below the permanent snow level, and their vegetation differs notably from that of adjacent Montane Forests. We compared the composition and beta diversity of blooming plant species using phenological data from functional plant groups (i.e., insect-visited, bird-visited and insect + bird-visited plants) between a Paramo and a Montane Forest site in Costa Rica and analyzed seasonal changes in blooming plant diversity between the rainy and dry seasons. Species richness was higher in the Montane Forest for all plant categories, except for insect-visited plants, which was higher in the Paramo. Beta diversity and blooming plant composition differed between both ecosystems and seasons. Differences in species richness and beta diversity between Paramo and the adjacent Montane Forest are likely the result of dispersal events that occurred during the last glacial period and subsequent isolation, as climate turned to tropical conditions after the Pleistocene, and to stressful abiotic conditions in the Paramo ecosystem that limit species establishment. Differences in blooming plant composition between both ecosystems and seasons are likely attributed to differential effects of climatic cues triggering the flowering events in each ecosystem, but phylogenetic conservatism cannot be discarded. Analyses of species composition and richness based on flowering phenology data are useful to evaluate potential floral resources for floral visitors (insects and birds) and how these resources change spatially and temporarily in endangered ecosystems such as the Paramo.

Isolation and characterization of microsatellites for the neotropical dioecious palm Chamaedorea tepejilote (Arecaceae) and cross-amplification in other Chamaedorea species.

Palms are important components of tropical and subtropical ecosystems and have even been considered keystone plant resources that can support a large array of pollinators and frugivores. Palms are also economically important. Chamaedorea tepejilote Liebm. is a widely distributed palm with important bioeconomic potential for food, traditional medicine and ornamental purposes. Eighteen microsatellite primers were developed for C. tepejilote. Polymorphism and genetic diversity were evaluated in 71 individuals from four populations in Costa Rica. Thirteen loci were polymorphic and the number of alleles in the pooled sample ranged between 5 and 20, the average number of alleles was 10.61. Average observed heterozygosity was Ho = 0.607 ± 0.04 (SD) and the average expected heterozygosity was He = 0.600 ± 0.03. The exclusion probability of the combined 13 loci, was PE = 0.998. We tested transferability of the markers in the congeneric C. costaricana, C. pinnantifrons and C. macrospadix. Dioecious species are common in tropical forests; however, few studies have analyzed gene flow patterns in these species. The markers developed for C. tepejilote are an important tool to quantify gene flow patterns and the distribution of genetic diversity within populations. This information will be useful for the development of conservation and management practices of this dioecious tropical palm species.

High selfing capability and low pollinator visitation in the hummingbird-pollinated epiphyte Pitcairnia heterophylla (Bromeliaceae) at a Costa Rican mountain forest / Alta capacidad de autofecundación y baja visitación de polinizadores en la epífita polinizada por colibríes Pitcairnia heterophylla (Bromeliaceae) en un bosque montano en Costa Rica

AbstractPitcairnioideae is the second most diverse subfamily of bromeliads (Bromeliaceae), a group exclusive to tropical regions of the New World. Pitcairnioid bromeliads have floral traits assumed to promote outcrossing through biotic pollination systems; however, the reproductive biology of most of the species of this group has not been documented. Pitcairnia heterophylla is an epiphytic (seldom saxicolous) bromeliad occurring from Southern Mexico, into the Northern Andes. We studied the pollination and breeding system of P. heterophylla in an epiphytic population at a mountain forest in Costa Rica from January to April 2013. We performed hand pollination experiments (agamospermy, autonomous self-pollination, hand self-pollination and hand cross-pollination) on 89 flowers from 23 individuals (3-6 flowers per individual) in 2013 flowering season. Nectar production was measured on 18 unvisited flowers of six individuals with a hand-held refractometer. Simultaneously, floral visitors were recorded on eight individuals with trail cameras for a total of 918 hours (115 ± 52 hours per individual, mean ± SE). Under natural conditions, seed set (540.4 ± 55.2) was similar to manually selfed flowers (516.3 ± 41.5) and autonomously selfed flowers (521.1 ± 29.0), but lower to manually outcrossed flowers (670.2 ± 31.3). The flowers of P. heterophylla are self-compatible, capable of autonomous pollination, and non-agamospermous. Intrafloral self-pollination is facilitated by adichogamy and lack of floral herkogamy. The scentless red flowers of P. heterophylla with tubular corollas and nectar production suggested ornithophilic pollination which was confirmed by video recording of 46 hummingbird visits. The most common floral visitor was the short-billed hummingbird Lampornis calolaemus which accounted for 78 % of the visits. However, the visitation rate during the flowering season was low (0.6 visits per day per plant). Selfing in P. heterophylla might be explained as a mechanism of reproductive assurance and to reduce interspecific pollen flow with taxonomically unrelated plants.

ResumenLa subfamilia Pitcairnioideae es la segunda más diversa de las bromelias (Bromeliaceae), un grupo exclusivo de la región Neotropical. Las bromelias pitcairnioideas poseen rasgos florales que se asume promueven el exo-cruzamiento a través de sistemas de polinización biótica; sin embargo, la biología reproductiva de la mayoría de especies de este grupo no se ha documentado. Pitcairnia heterophylla es una bromelia epífita (raramente saxícola) que se encuentra en el sur de México, América Central y el norte de los Andes. Se estudió la polinización y el sistema de apareamiento de una población P. heterophylla en un bosque montano en Costa Rica entre enero y abril 2013. Se realizaron cuatro experimentos de polinización (agamospermia, auto-polinización espontánea, auto-polinización manual, exo-polinización manual) en 89 flores de 23 individuos (3-6 flores por individuo). Se cuantificó la producción de néctar de 18 flores en seis individuos con un refractómetro. Simultáneamente, se registraron los visitantes florales de ocho individuos en el campo con ayuda de cámaras trampa por un total de 918 horas (115 ± 52 horas por individuo, promedio ± ES). Bajo condiciones naturales la producción de semillas fue similar (540.4 ± 55.2) a la producción de las flores auto-polinizadas manualmente (516.3 ± 41.5) y las flores auto-polinizadas espontáneamente (521.1 ± 29.0), pero fue menor a las flores exo-cruzadas (670.2 ± 31.3). Las flores de P. heterophylla son auto-compatibles, con alta capacidad de polinización espontánea y sin capacidad de agamospermia. La auto-polinización intra-floral es facilitada por la ausencia de dicogamia y hercogamia floral. Las flores rojas, sin aroma, con corola tubular y con producción de néctar sugirieron polinización por ornitofilia, lo que se confirmó con el registro de 46 visitas por colibríes (Apodiformes: Trochilidae). El visitante floral más común fue Lampornis calolaemus (78 % de las visitas). A pesar de esto, la tasa de visitas durante el periodo de estudio fue baja (0.6 visitas por día por planta). La capacidad de autofecundación de P. heterophylla puede ser explicada como un mecanismo de aseguramiento reproductivo, así como para reducir el flujo de polen inter-específico de plantas taxonómicamente no relacionadas.

Evaluating factors that predict the structure of a commensalistic epiphyte-phorophyte network.

A central issue in ecology is the understanding of the establishment of biotic interactions. We studied the factors that affect the assembly of the commensalistic interactions between vascular epiphytes and their host plants. We used an analytical approach that considers all individuals and species of epiphytic bromeliads and woody hosts and non-hosts at study plots. We built models of interaction probabilities among species to assess if host traits and abundance and spatial overlap of species predict the quantitative epiphyte-host network. Species abundance, species spatial overlap and host size largely predicted pairwise interactions and several network metrics. Wood density and bark texture of hosts also contributed to explain network structure. Epiphytes were more common on large hosts, on abundant woody species, with denser wood and/or rougher bark. The network had a low level of specialization, although several interactions were more frequent than expected by the models. We did not detect a phylogenetic signal on the network structure. The effect of host size on the establishment of epiphytes indicates that mature forests are necessary to preserve diverse bromeliad communities.