Carlos M. Herrera

Recruitment of a Mast-Fruiting, Bird-Dispersed Tree: Bridging Frugivore Activity and Seedling Establishment

The recruitment of Phillyrea latifolia L. (Oleaceae), a bird-dispersed tree of Mediterranean forest, is described. Fruit removal by birds, seed rain, post-dispersal seed predation, seed germination, and seedling emergence, survival, and establishment were studied. The main objective was testing whether seed dispersal by birds produced a pre- dictable seedling shadow as a result of coupled patterns of seed rain, seedling emergence, and seedling establishment. P. latifolia is a mast-fruiting species and large fruit crops were produced in only 2 (1981 and 1989) out of 15 yr (1978-1992). We report here on the 1989 fruiting event at one scrubland and one forest site. Ripe fruits were available from mid-September to early June. Extensive removal by birds started after fruit crops of other species were depleted. Seed dispersers were more abundant, and fruit predators more scarce, in scrubland than in forest. P. latifolia fruits were a major component in the diet of principal seed dispersers (Sylvia atricapilla and Erithacus rubecula) that depended almost exclusively on them for food late in the season. Fruit removal levels were higher, crops were depleted earlier, and individual plants dis- persed more seeds in scrubland than in forest. Crop size was the best predictor of number of seeds dispersed by individual plants in scrubland, while fruit characteristics were more influential in forest. Seed dispersal was largely a within-population phenomenon, as no seed fall occurred in traps set beyond the distributional limits of P. latifolia in the study region. Frugivores produced a spatially predictable seed rain at the two sites. Seed rain was greatest beneath fleshy fruit-producing species (under female individuals in dioecious species) in scrubland and at forest-gap interfaces in forest. Post-dispersal seed predation was low at the two sites (39 and 54% after 1-yr exposure). In forest, seed survival was lower in gaps than in forest interior or forest edges. In scrubland, seed survival differed widely among microhabitats (defined by overlying plant species), ranging from 19% (open ground) to 61% (beneath Rosmarinus officinalis). In forest, density of emerging seedlings was unrelated to location in the habitat mosaic (gap, forest edge, interior). Seedling density did differ among microhabitats in scrubland, where emergence was greatest under fleshy fruit-producing species. Seedling survival was higher in forest than in scrubland, where seedlings incurred greater mortality due to desiccation. In both sites, seedling survival depended significantly on microhabitat and was depressed under adult conspecifics. The activity of frugivores directly impacted seedling distribution in scrubland, as spatial patterns of seed deposition were not overshadowed by later-acting factors, such as rodent seed predation or variation in germination. In forest, there was spatial discordance between seed rain and seedling distribution, as a consequence of uncoupled seed rain and seedling emergence. Spatial patterns of seed deposition by birds may thus have a lasting impact on the population dynamics of P. latifolia, but this will vary among populations depending on the extent of coupling of the different stages in the recruitment process (dispersal-seed rain-germination and seedling establishment).

Annual Variability in Seed Production by Woody Plants and the Masting Concept: Reassessment of Principles and Relationship to Pollination and Seed Dispersal

By analyzing 296 published and unpublished data sets describing annual variation in seed output by 144 species of woody plants, this article addresses the following questions. Do plant species naturally fall into distinct groups corresponding to masting and nonmasting habits? Do plant populations generally exhibit significant bimodality in annual seed output? Are there significant relationships between annual variability in seed production and pollination and seed dispersal modes, as predicted from economy of scale considerations? We failed to identify distinct groups of species with contrasting levels of annual variability in seed output but did find evidence that most polycarpic woody plants seem to adhere to alternating supra‐annual schedules consisting of either high or low reproduction years. Seed production was weakly more variable among wind‐pollinated taxa than animal‐pollinated ones. Plants dispersed by mutualistic frugivores were less variable than those dispersed by either inanimate means or animals that predominantly behave as seed predators. We conclude that there are no objective reasons to perpetuate the concept of mast fruiting in the ecological literature as a shorthand to designate a distinct biological phenomenon. Associations between supra‐annual variabiity in seed output and pollination and seed dispersal methods suggest the existence of important reproductive correlates that demand further investigation.

Floral Traits and Plant Adaptation to Insect Pollinators: A Devil’s Advocate Approach

Certain natural history phenomena may provide a vivid illustration of selection in action and its adaptive products, and nearly every evolutionary biologist would agree that the pollination of flowers by animals provides a most illustrative example. It was surely not by chance that the first of Darwin’s books to be published after The Origin of Species was precisely his treatise on the “contrivances by which orchids are fertilised by insects” (Darwin, 1862), the first in a series of monographs aimed at providing detailed supporting evidence for the theory of natural selection. Darwin’s book on orchids evoked a major revolution in botany and gave rise to an enormous literature on pollination ecology (Ghiselin, 1984). It also marked the starting point for a tradition in the practice of pollination biology.

Shuffling the offspring: Uncoupling and spatial discordance of multiple stages in vertebrate seed dispersal

Abstract:Recruitment of vertebrate-dispersed plants may be divided into a series of sequential stages including fruit removal by frugivores, seed delivery to the ground, post-dispersal seed surviva...

Pollinator abundance, morphology, and flower visitation rate analysis of the quantity component in a plant pollinator system

SummaryAbundance and flower visitation rate of the pollinators of Lavandula latifolia (Labiatae), an insect-pollinated shrub, were studied over a 6-year period. The objective was to elucidate interspecific patterns in the “quantity” component of the plant-pollinator interaction. A total of 54 insect taxa are considered in the analyses, including hynenopterans, dipterans and lepidopterans. Most pollinators were comparatively scarce, with a few taxa acounting collectively for the majority of individuals. Pollinators differed broadly in flower visitation rate (0.2–30 flowers/min). Most of this variation was explained by differences in flower handling time (HT). Regardless of proboscis length, hymenopterans had intrinsically shorter handling times than lepidopterans. Within each group, HT decreased exponentially with increasing proboscis length. Abundance and visitation rate were uncorrelated across pollinator taxa. The total number of visits that each pollinator contributed to the plant (NFV) was estimated as the product of abundance x visitation rate. NFV values spanned four orders of magnirade. A small, taxonomically diverse group of species (1 moth, 1 butterfly, 4 bees) accounted for most visits and thus could effectively exert some selection on floral features. Nevertheless, the morphological diversity represented in this group of dominant pollinators probably constrains plant specialization, as they will most likely select for different floral features or in opposing directions on the same traits.

Microclimate and individual variation in pollinators: flowering plants are more than their flowers

Variation in pollinator composition at the individual plant level is an im- portant prerequisite for plant specialization on pollinators that does not seem to have been investigated previously. I studied variation in pollinator composition in a southeastern Spanish population of the insect-pollinated shrub Lavandula latifolia (Labiatae) and ex- amined its correlates, with particular reference to the distinction between factors intrinsic (flower morphology, nectar standing crop, size of floral display) and extrinsic (sunlight regime, ambient temperature, humidity) to the plants. L. latifolia shrubs differed signifi- cantly in all intrinsic variables measured, in average irradiance levels (due to site-dependent variation in timing and duration of insolation periods), and in pollinator composition at both the species and order levels. Individual variation in pollinator composition was largely due to differences among insect taxa in their foraging responses to the sunlight mosaic. While some pollinators foraged indiscriminately over that mosaic, others preferred sites characterized by high irradiance. Variation among plants in intrinsic variables was unrelated to differences in pollinator composition, which depended significantly only on the sunlight regime associated with each plants location in the habitat. Site-specific effects in pollination will generally act to reduce the likelihood of selective pressures by animals on plant traits. Their importance should be greatest in habitats characterized by patchiness in environmental variables that affect pollinator behavior and in plants with pollinator assemblages dominated by ectothermic species.

Interaction of pollinators and herbivores on plant fitness suggests a pathway for correlated evolution of mutualism- and antagonism-related traits

Different kinds of plant–animal interactions are ordinarily studied in isolation, yet considering the combined fitness effects of mutualistic and antagonistic interactions is essential to understanding plant character evolution. Functional, structural, or phylogenetic associations between attractive and defensive traits may be nonadaptive or result from correlational selection on sets of herbivory- and pollination-linked traits. Nonadditivity of fitness effects of mutualists and antagonists, a requisite for correlational selection, was experimentally tested in the field. We created experimental populations of the insect-pollinated perennial herb, Helleborus foetidus, at 16 different locations distributed among three regions in the Iberian Peninsula. Plants experienced one of four possible selective regimes generated by independently weakening the effects of pollinators and herbivores (flower and fruit predators) according to a two-way fully factorial design. Effects were assessed in terms of number of next-generation offspring recruited per mother plant under natural field conditions. Differences among H. foetidus plants in the strength of their interactions with pollinators and herbivores translated into differential fitness, as measured in terms of recruited offspring, and subsequent changes in plant population densities. A strong, geographically consistent nonadditivity in the fitness consequences of pollinators and herbivores was found also. Plants possessing the particular combination of “traits” simultaneously enhancing pollination and escape from herbivores enjoyed a disproportionate fitness advantage over plants possessing any of the other three possible “trait” combinations. Results suggest a simple, possibly widespread ecological pathway favoring the adaptive correlated evolution of mutualism- and antagonism-related plant traits in pollinator-dependent plants suffering intense flower and fruit herbivory.

Adaptation to Frugivory of Mediterranean Avian Seed Dispersers

I/~.\tr.ac.t. Morphological and digestive correlates of seed dispersal were investigated in 41 bird species of mediterranean scrublands of southern Spain. Seed dispersers (feeding on whole fruits and voiding seeds unharmed) are indistinguishable from nonfrugivores and frult predators (feedlng on pulp or seeds and not performing dispersal) in the ratlo of glzzard mass. liver mass. and intestine length to body mass. but direr significantly in bill morphology and average gut passage time (GPT). Seed dispersers tend to be flatter and broader billed than other groups. and have a wider mouth relative to bill wldth. GPT of seed dispersers is significantly shorter than that of other groups. Morphological correlates of seed dispersers suggest that adaptatlons for insectivory serve as preadaptations for feeding on whole fru~ts. Shorter GPTs, in contrast. appear to be an adaptation indispensable to sustained. intense frugibory. Seasonal frugivon imposes limlts on commitments to permanent structural modifications. and more subtle functional adaptatlons are to be expected. In the context of plant-disperser coevolution. unapparent adaptations ofseed dispersers to plants are as relevant as the more conspicuous structural adaptations reported for year-round fruglvores. In mediterranean scrublands they suffice to maintain a hlgh-efficiency seed dispersal system.

Epigenetic differentiation and relationship to adaptive genetic divergence in discrete populations of the violet Viola cazorlensis

*In plants, epigenetic variations based on DNA methylation are often heritable and could influence the course of evolution. Before this hypothesis can be assessed, fundamental questions about epigenetic variation remain to be addressed in a real-world context, including its magnitude, structuring within and among natural populations, and autonomy in relation to the genetic context. *Extent and patterns of cytosine methylation, and the relationship to adaptive genetic divergence between populations, were investigated for wild populations of the southern Spanish violet Viola cazorlensis (Violaceae) using the methylation-sensitive amplified polymorphism (MSAP) technique, a modification of the amplified fragment length polymorphism method (AFLP) based on the differential sensitivity of isoschizomeric restriction enzymes to site-specific cytosine methylation. *The genome of V. cazorlensis plants exhibited extensive levels of methylation, and methylation-based epigenetic variation was structured into distinct between- and within- population components. Epigenetic differentiation of populations was correlated with adaptive genetic divergence revealed by a Bayesian population-genomic analysis of AFLP data. Significant associations existed at the individual genome level between adaptive AFLP loci and the methylation state of methylation-susceptible MSAP loci. *Population-specific, divergent patterns of correlated selection on epigenetic and genetic individual variation could account for the coordinated epigenetic-genetic adaptive population differentiation revealed by this study.

INVISIBLE FLORAL LARCENIES: MICROBIAL COMMUNITIES DEGRADE FLORAL NECTAR OF BUMBLE BEE-POLLINATED PLANTS

The ecology of nectarivorous microbial communities remains virtually unknown, which precludes elucidating whether these organisms play some role in plant-pollinator mutualisms beyond minor commensalism. We simultaneously assessed microbial abundance and nectar composition at the individual nectary level in flowers of three southern Spanish bumble bee-pollinated plants (Helleborus foetidus, Aquilegia vulgaris, and Aquilegia pyrenaica cazorlensis). Yeasts were frequent and abundant in nectar of all species, and variation in yeast density was correlated with drastic changes in nectar sugar concentration and composition. Yeast communities built up in nectar from early to late floral stages, at which time all nectaries contained yeasts, often at densities between 10(4) and 10(5) cells/mm3. Total sugar concentration and percentage sucrose declined, and percentage fructose increased, with increasing density of yeast cells in nectar. Among-nectary variation in microbial density accounted for 65% (H. foetidus and A. vulgaris) and 35% (A. p. cazorlensis) of intraspecific variance in nectar sugar composition, and 60% (H. foetidus) and 38% (A. vulgaris) of variance in nectar concentration. Our results provide compelling evidence that nectar microbial communities can have detrimental effects on plants and/or pollinators via extensive nectar degradation and also call for a more careful interpretation of nectar traits in the future, if uncontrolled for yeasts.