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.

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.

Genetic diversity, asexual reproduction and conservation of the edible fruit tree Spondias purpurea L. (Anacardiaceae) in the Costa Rican tropical dry forest.

The term circa situm has been used to describe different conservation strategies within agricultural landscapes. Circa situm conserves planted or remnant species in farmlands, where natural vegetation has been modified through anthropogenic intervention. It has been proposed that trees planted or retained under circa situm conditions may contribute to maintaining genetic diversity, however information on the role of this strategy in preserving genetic diversity is scarce. The aim of this study was to determine the levels of genetic diversity and structure, and mating patterns in planted and unmanaged stands of the tropical fruit tree Spondias purpurea L. in north western Costa Rica. In three localities, we used seven polymorphic microsatellite loci and genotyped 201 adults and 648 seeds from planted and wild stands. We found no differences in genetic diversity among planted and wild stands. Genetic structure analysis revealed that gene flow occurs among planted and wild stands within localities. Clones were present and their diversity and evenness were both high and similar between planted and wild stands. The number of pollen donors per progeny array was low (Nep = 1.01) which resulted in high levels of correlated paternity (rp = 0.9). Asexual seeds were found in 4.6% of the progeny arrays, which had multilocus genotypes that were identical to the maternal trees. Our results show that although planted stands under circa situm conditions can maintain similar levels of genetic diversity than wild stands, the low number of sires and asexual seed formation could threaten the long term persistence of populations.

Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment.

Current climate change is disrupting biotic interactions and eroding biodiversity worldwide. However, species sensitive to aridity, high temperatures, and climate variability might find shelter in microclimatic refuges, such as leaf rolls built by arthropods. To explore how the importance of leaf shelters for terrestrial arthropods changes with latitude, elevation, and climate, we conducted a distributed experiment comparing arthropods in leaf rolls versus control leaves across 52 sites along an 11,790 km latitudinal gradient. We then probed the impact of short- versus long-term climatic impacts on roll use, by comparing the relative impact of conditions during the experiment versus average, baseline conditions at the site. Leaf shelters supported larger organisms and higher arthropod biomass and species diversity than non-rolled control leaves. However, the magnitude of the leaf rolls' effect differed between long- and short-term climate conditions, metrics (species richness, biomass, and body size), and trophic groups (predators vs. herbivores). The effect of leaf rolls on predator richness was influenced only by baseline climate, increasing in magnitude in regions experiencing increased long-term aridity, regardless of latitude, elevation, and weather during the experiment. This suggests that shelter use by predators may be innate, and thus, driven by natural selection. In contrast, the effect of leaf rolls on predator biomass and predator body size decreased with increasing temperature, and increased with increasing precipitation, respectively, during the experiment. The magnitude of shelter usage by herbivores increased with the abundance of predators and decreased with increasing temperature during the experiment. Taken together, these results highlight that leaf roll use may have both proximal and ultimate causes. Projected increases in climate variability and aridity are, therefore, likely to increase the importance of biotic refugia in mitigating the effects of climate change on species persistence.

Isolation and characterization of microsatellite loci in Astroniumgraveolens (Anacardiaceae) and cross amplification in related species.

Microsatellite markers are a useful genetic tool to answer ecological and conservation genetics questions. Microsatellite primers were developed and characterized to evaluate forest fragmentation effects on genetic structure, diversity and gene flow patterns in the dioecious tropical tree Astroniumgraveolens (Anacardiaceae). Using genomic library enrichment, sixteen microsatellite loci were developed for A.graveolens. Polymorphism was evaluated in 80 individuals from four localities in Mexico. The overall number of alleles detected was 63, average alleles per locus 3.9 with a range from one to 11 per locus. Cross amplification trails on related species in the Anacardiaceae family: Spondiaspurpurea and Amphipterygiumadstringens, achieved successful amplification for all primers. Microsatellite markers described here are the first to be characterized for A.graveolens. These genetic markers will be a useful tool to assess the genetic consequences of habitat fragmentation and selective logging on A.graveolens populations. Cross amplification success on S.purpureaandA.adstringens suggest that they may be used for population genetic studies in other species within the family.

Janzen-Connell effects shape gene flow patterns and realized fitness in the tropical dioecious tree Spondias purpurea (ANACARDIACEAE).

Pollination and seed dispersal patterns determine gene flow within plant populations. In tropical forests, a high proportion of trees are dioecious, insect pollinated and dispersed by vertebrates. Dispersal vectors and density dependent factors may modulate realized gene flow and influence the magnitude of Fine Scale Genetic Structure (FSGS), affecting individual fitness. Spondias purpurea is a vertebrate-dispersed, insect-pollinated dioecious tropical tree. We assessed the influence of sex ratio, effective and realized gene flow on genetic diversity, FSGS and individual fitness within a 30 ha plot in the tropical dry forest reserve of Chamela-Cuixmala, Mexico. All individuals within the plot were tagged, geo-referenced and sampled for genetic analysis. We measured dbh and monitored sex expression during two reproductive seasons for all individuals. We collected seeds directly from maternal trees for effective pollen dispersal analysis, and analyzed established seedlings to assess realized pollen and seed dispersal. Nine microsatellite loci were used to describe genetic diversity parameters, FSGS and gene flow patterns among different size classes. A total of 354 individuals were located and classified into three size classes based on their dbh (<10, 10-20, and >20 cm). Population sex ratios were male biased and diametric size distributions differed among sexes, these differences may be the result of precocious male reproduction at early stages. Autocorrelation analyses indicate low FSGS (Fj <0.07) across all size classes. Long realized pollen and seed dispersal and differences among effective and realized gene flow were detected. In our study site low FSGS is associated with high gene flow levels. Effective and realized gene flow indicate a population recruitment curve indicating Janzen-Connell effects and suggesting fitness advantages for long-distance pollen and seed dispersal events.

Isolation and characterization of microsatellites loci in Spondias purpurea (Anacardiaceae) and cross amplification in congeneric species.

Microsatellite markers provide high polymorphism levels, useful to study genetic diversity and gene flow patterns in plant populations. Here we develop and characterize microsatellite primers to evaluate patterns of genetic structure and diversity, and gene flow levels in the dioecious tropical tree Spondias purpurea (Anacardiaceae). Twenty-four microsatellite primers were developed for Spondias purpurea. Polymorphism was evaluated in 139 individuals from three localities in Mexico. Ten loci were polymorphic. The number of alleles ranged between two and 21, the average number of alleles was 5.88. Cross-amplification trials on S. mombin, S. radlkoferi, Astronium graveolens and Amphipterygium adstringens achieved successful amplification for only six microsatellites in S. mombin and S. radlkoferi. Microsatellites developed for S. purpurea will be a useful tool to estimate genetic diversity within and among populations, as well as to assess the consequences of habitat fragmentation on gene flow patterns of this species.

Positive effects of the catastrophic Hurricane Patricia on insect communities.

Highly seasonal conditions of tropical dry forests determine the temporal patterns of insect abundance. However, density-independent factors such as natural disturbances can abruptly change environmental conditions, affecting insect populations. We address the effects of the Hurricane Patricia (category 5) on species density and abundance of three feeding guilds of herbivorous insects (sap-sucking, folivorous beetles and xylophagous) and predatory beetles associated to the canopy of a tropical dry forest. Hurricane Patricia has been the strongest tropical hurricane ever reported in the Western Hemisphere. Herbivorous insects (sap-sucking and xylophagous) and predatory beetles increased in species density and abundance in the following months after the hurricane, compared to samples before it. The positive response of sap-sucking insects to Hurricane Patricia was probably related to an increase in the availability of new shoots and leaf meristems after the natural coppicing by the hurricane, while xylophagous guild seems to have been positively affected by the increase in the amount and diversity of deadwood resources. The positive response of predatory beetles may be the result of a bottom-up effect due to a greater availability of arthropod preys after the hurricane. We demonstrated that catastrophic hurricane disturbances could be important events that temporarily increase the species density and abundance of insects in tropical dry forests.

Ecosystem engineering and manipulation of host plant tissues by the insect borer Oncideres albomarginata chamela.

Ecosystem engineering by insect herbivores occurs as the result of structural modification of plants manipulated by insects. However, only few studies have evaluated the effect of these modifications on the plant responses induced by stem-borers that act as ecosystem engineers. In this study, we evaluated the responses induced by the herbivory of the twig-girdler beetle Oncideres albomarginata chamela (Cerambycidae: Lamiinae) on its host plant Spondias purpurea (Anacardiaceae), and its relationship with the ecosystem engineering process carried out by this stem-borer. Our results demonstrated that O. albomarginata chamela branch removal induced the development of lateral branches increasing the resources needed for the development of future insect generations, of its own offspring and of many other insect species. Detached branches represent habitats with high content of nitrogen and phosphorous, which eventually can be incorporated into the ecosystem, increasing nutrient cycling efficiency. Consequently, branch removal and the subsequent plant tissue regeneration induced by O. albomarginata chamela represent key mechanisms underlying the ecosystem engineering process carried out by this stem-borer, which enhances arthropod diversity in the ecosystem.