Alfonso M. Sánchez-Lafuente

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.

Factors shaping the seedfall pattern of a bird-dispersed plant.

The spatial distribution of seeds can influence several parameters of the natural regeneration of plant populations. Factors shaping seedfall patterns have been typically explored from the tree perspective (seed shadow) or from the population perspective (seed rain). However, the seed rain is actually composed of multiple seed shadows. In this paper, we use this framework to explore the variables shaping the seedfall pattern of the wild olive tree (Olea europaea var. sylvestris), a fleshy-fruited tree of the Mediterranean scrublands. We monitored the movement patterns of avian seed dispersers and the seedfall around each fruit-bearing O. europaea tree in two contrasting sites, differing in the degree of human management and abundance of scrub cover. None of the seed dispersers moved between microhabitats (different shrub species and open interspaces) as a function of microhabitat relative abundance. All dispersers foraged preferentially at O. europaea; only the smaller species visited open interspaces, and these only sporadically. Avoidance of open sites by frugivores, especially larger species, and their attraction to source trees were the major determinants of the seedfall pattern. Regarding seed size distribution among microhabitats, we found that only small seeds were significantly overrepresented in open interspaces. From the seed shadow perspective, seed density under trees was similar in the two study sites, but it decreased with distance at a higher rate in the disturbed scrubland. From the seed rain perspective, seed density was significantly different among microhabitats, with open interspaces collecting few, if any, seeds, and places under source trees receiving the highest densities. Results from seed shadow and seed rain analyses were integrated to construct a path model to explore the relative contribution of spatial, microhabitat, and individual tree features to the seedfall pattern. Factors related to microhabitat were identified as having a major role in shaping seedfall pattern. Open interspaces collected few seeds, points under shrub species with sparse foliage collected moderate seed densities, and points under shrubs with dense foliage collected the highest seed densities. The comparison between sites suggests that habitat alteration (a reduction of the scrub layer) can lead to contrasting seedfall patterns. The occurrence of an abundant scrub layer in the well-preserved scrubland allowed a complex pattern of seed rain. In contrast, the sparse scrub cover in the disturbed scrubland yielded a seedfall pattern composed of multiple seed shadows constrained to the vicinity of tree crowns. Thus, our sampling design and analytical approach have proved useful in describing the relative importance of the set of variables that shapes the complex seedfall pattern of a bird-dispersed plant. This seedfall pattern, in turn, is central to the understanding of the spatial patterns of plant recruitment and the efficiency of the dispersal mutualism.

Geographical variation in autonomous self-pollination levels unrelated to pollinator service in Helleborus foetidus (Ranunculaceae).

Autonomous self-pollination may be considered as a mechanism enhancing plant reproductive success when plant access to pollen sources may limit seed production. We have studied the relationship between geographical patterns of variation in pollinator service to Helleborus foetidus and self-pollination ability in three widely spaced regions in the Iberian Peninsula. As could be expected from its early flowering period, pollinator visitation rates to both plants and flowers of H. foetidus were very low at all sites. Pollinator composition remained consistent among regions, but there was significant variation among regions in pollinator service. Despite the low visitation rates, fruit set did not appear to be pollen limited in any of the study areas, which may be explained by the long duration of flowers (up to 20 d). When pollinators were excluded experimentally, fruit set decreased significantly, but substantial levels of self-pollination occurred at all regions. Autonomous self-pollination levels were lowest in the two regions with lowest pollinator service and highest in the region with highest pollinator service. This disagreement between our results and the expectations derived from the reproductive assurance hypothesis may reflect a nonequilibrium situation of the northern H. foetidus populations in relation to their current pollinating environment.

FACTORS SHAPING THE SEEDFALL PATTERNOF A BIRD‐DISPERSED PLANT

The spatial distribution of seeds can influence several parameters of the natural regeneration of plant populations. Factors shaping seedfall patterns have been typically explored from the tree perspective (seed shadow) or from the population perspective (seed rain). However, the seed rain is actually composed of multiple seed shadows. In this paper, we use this framework to explore the variables shaping the seedfall pattern of the wild olive tree (Olea europaea var. sylvestris), a fleshy-fruited tree of the Mediterranean scrublands. We monitored the movement patterns of avian seed dispersers and the seedfall around each fruit-bearing O. europaea tree in two contrasting sites, differing in the degree of human management and abundance of scrub cover. None of the seed dispersers moved between microhabitats (different shrub species and open interspaces) as a function of microhabitat relative abundance. All dispersers foraged preferentially at O. europaea; only the smaller species visited open interspaces, and these only sporadically. Avoidance of open sites by frugivores, especially larger species, and their attraction to source trees were the major determinants of the seedfall pattern. Regarding seed size distribution among microhabitats, we found that only small seeds were significantly overrepresented in open interspaces. From the seed shadow perspective, seed density under trees was similar in the two study sites, but it decreased with distance at a higher rate in the disturbed scrubland. From the seed rain perspective, seed density was significantly different among microhabitats, with open interspaces collecting few, if any, seeds, and places under source trees receiving the highest densities. Results from seed shadow and seed rain analyses were integrated to construct a path model to explore the relative contribution of spatial, microhabitat, and individual tree features to the seedfall pattern. Factors related to microhabitat were identified as having a major role in shaping seedfall pattern. Open interspaces collected few seeds, points under shrub species with sparse foliage collected moderate seed densities, and points under shrubs with dense foliage collected the highest seed densities. The comparison between sites suggests that habitat alteration (a reduction of the scrub layer) can lead to contrasting seedfall patterns. The occurrence of an abundant scrub layer in the well-preserved scrubland allowed a complex pattern of seed rain. In contrast, the sparse scrub cover in the disturbed scrubland yielded a seedfall pattern composed of multiple seed shadows constrained to the vicinity of tree crowns. Thus, our sampling design and analytical approach have proved useful in describing the relative importance of the set of variables that shapes the complex seedfall pattern of a bird-dispersed plant. This seedfall pattern, in turn, is central to the understanding of the spatial patterns of plant recruitment and the efficiency of the dispersal mutualism.

Habitat alteration and plant intra-specific competition for seed dispersers: an example with Olea europaea var. sylvestris

This paper examines the hypothesis that intra-specific competition for avian dispersers among wild olive trees (Olea europaea var. sylvestris, Oleaceae) might limit successful dispersal in disturbed habitats. To this aim, we studied the avian fruit removal of wild olive in a disturbed scrubland plot for two consecutive seasons. We found very low overall fruit removal, low abundance of avian seed dispersers, and low levels of fruit damage by biotic or abiotic agents. There was also a high interindividual variation in fruit removal success as well as a high interindividual heterogeneity in plant traits (fruit width, pulp/seed ratio, crop size and ripening phenology) in both seasons. Thus, we conclude that the low abundance of frugivorous birds severely limits the total amount of seeds dispersed from each tree of the population. We analysed the relationship between fruit removal and both plant traits and habitat characteristics. Three different estimates of fruit removal were calculated: number of seeds dispersed, dispersal efficiency (percentage of the crop consumed by avian dispersers) and dispersal success (relative contribution of each individual tree to the amount of seeds dispersed in the population). The number of seeds dispersed was positively affected mainly by crop size, but also by fruit-design traits (fruit width), and negatively by the ripening phenology. Fruit removal efficiency was positively related to fruit-design traits (fruit width and pulp/seed ratio) and ripening phenology (early ripening trees being favoured). Finally, fruit removal success was only related to fecundity (crop size and plant size). The low mean fruit removal levels and the strong interindividual variability in fruit traits produced very asymmetric results (thus enabling some individuals to have many of their seeds dispersed) and, consequently, led to an unbalanced individual contribution to the pool of seeds dispersed by the population. These results support the hypothesis that there is a high interindividual competition among plants for avian dispersers in disturbed habitats. Our results also suggest that a few individuals could probably inundate such habitats with their descendants, thus exerting a long-term influence on the subsequent genetic structure of the population.

The geographic mosaic in predispersal interactions and selection on Helleborus foetidus (Ranunculaceae)

We examine the hierarchical geographic structure of the interaction between a plant, Helleborus foetidus, and its floral herbivores and pollinators (interactors). Six populations from three distant regions of the Iberian Peninsula were used to examine intra‐ and inter‐regional variation in plant traits, interactors and plant fecundity, and to compare, through selection gradient and path analyses, which traits were under selection, and which interactors were responsible for differential selection. Geographic and temporal congruency in interactor‐mediated selection was further tested using a recent analytical approach based on multi‐group comparison in Structural Equation Models. Most plant traits, interactors and fecundity differed among regions but not between populations. Similarly, the identity of the traits under selection, the selection gradients (strength and/or the direction of the selection) and the path coefficients (identifying the ecological basis for selection) varied inter‐ but not intra‐regionally. Results show a selection mosaic at the broad scale and, for some traits, a link of differential selection to trait differentiation.

Natural and human-mediated factors in the recovery and subsequent expansion of the Purple swamphen Porphyrio porphyrio L. (Rallidae) in the Iberian Peninsula

Instances of range contraction and population decline in bird species in Europe are more common than cases of recovery following decline. Here we report on the recovery and expansion processes of an endangered bird species in Europe, the purple swamphen (Porphyrio porphyrio L., Rallidae), with special reference to the Iberian Peninsula, its main distribution area in Western Europe. After a drastic decline during the first half of the 20th century, which restricted its range to a few areas in southern Spain, the Iberian population has recovered. Currently, the species occurs in a range similar to the one it had at the beginning of the 20th century, and has even colonized new areas. These processes seem to be the result of both human-mediated (effective protection of the species and suitable habitats; success of reintroduction programs as expansion focuses of birds colonizing nearby and distant regions [>300 km] wetlands) and natural factors (inter- and intra-seasonal cycles of wet and dry years). Thus, we found a significant relationship between rainfall and bird abundance and productivity, suggesting that such inter- and intra-seasonal cycles may have significant effects on demographic parameters that could be related to the expansion process. Finally the species shows remarkable adaptability, as proven by data on breeding success in recently colonized areas and the ability to breed shortly after reintroduction. We hypothesize that saturation of breeding habitats in established areas, a reasonable habitat continuity and favorable environmental conditions, and protection have facilitated the dispersion of birds.

Interaction frequency and per-interaction effects as predictors of total effects in plant–pollinator mutualisms: a case study with the self-incompatible herb Linaria lilacina

It is widely recognized that pollinators vary in their effectiveness in pollination mutualisms, due both to differences in flower–pollinator morphological fit as well as pollinator behaviour. However, pollination webs typically treat all interactions as equal, and we contend that this method may provide misleading results. Using empirical and theoretical data, we present the case study of a self-incompatible herb in which the number of flowers visited by a pollinator cannot be used as a surrogate for the total effect of a pollinator on a plant due to differences in per-visit effectiveness at producing seeds. In self-incompatible species, the relationship between interaction frequency and per-interaction effect may become increasingly negative as more flowers per plant are visited due to geitonogamous pollen transfer. We found that pollinators making longer bouts (i.e. visiting more flowers per plant visit) had an overall higher pollination success per bout. However, per-interaction effects tended to decrease as the bout progressed, particularly for pollinators that cause higher pollen deposition. Since the same interaction frequency may result from different combinations of number of bouts (plant visits) and bout length (flowers visited/bout), pollinators making repeatedly shorter bouts may contribute more to plant reproduction for the same number of flowers visited. Consequently, the magnitude of the differences in number of interactions of different insect types may be overridden by the magnitude of the differences in effectiveness as pollinators, even if the same pollinators consistently interact more frequently. We discuss two predictions regarding the validity of using interaction frequency as a surrogate for plant seed production (as a measure of total effect), depending on the degree of self-compatibility, plant size and floral display. We suggest that the role of interaction frequency must be tested for different species, environments, and across wider scales to validate its use as a surrogate for total effect in plant–pollinator networks.

Seed- vs. microsite-limited recruitment in a myrmecochorous herb

Dispersal in myrmecochorous herbs is frequently short-distance and this might limit patch occupancy. Here we ask whether recruitment and patch occupancy in the myrmecochere Helleborus foetidus are seed- or microsite-limited and what role dispersal plays in recruitment limitation. In pine forests from two widely separated mountain systems in the Iberian Peninsula, we performed two seed addition experiments to explore the nature of recruitment limitation in this perennial herb. In an introduction experiment, we added seeds in patches far from reproductive individuals, which rarely receive any seed. In an augmentation experiment, we added seeds in patches beneath reproductive plants. Each experiment considered three main factors: seed addition (added or not added), rodent exclusion (excluded or not excluded), and microhabitat (scrub-covered or not scrub-covered). The augmentation experiment tests whether recruitment is limited by seed availability (exploring also the possible role of rodent granivory in such limitation) while the introduction experiment tests whether the empty patches occur either because they are unsuitable for the species (microsite limitation) or due to a low probability of seed arrival (dispersal limitation). Adding seeds almost always increased seedling emergence and recruitment, demonstrating that recruitment in this species is seed-limited and refuting the possibility of microsite limitation. The comparison of the introduction and augmentation experiments indicated that Helleborus recruitment dynamics and patch occupancy are constrained by additive effects of fecundity and dispersal limitation.

Breeding system and the role of floral visitors in seed production of a ‘few-flowered’ perennial herb, Paeonia broteroi Boiss. & Reut. (Paeoniaceae)

AbstractThe breeding system and pollination ecology of Paeonia broteroi (Paeoniaceae), a self-compatible, perennial herb, which produces few flowers (one to eight) per season, are described in two populations in mountains of southern Spain. Experimentally self-pollinated flowers yielded a significantly lower seed set (6-18%) than cross-pollinated flowers (23-29%), but the latter did not differ in seed set from open-pollinated flowers (30-31%). Seeds obtained from self-pollinated flowers were significantly lighter then seeds obtained from open- and cross-pollinated flowers. Pollen and resource limitation, inbreeding depression, and allocation to sexual functions are discussed to explain seed set. The role of different floral visitors (including bees, beetles, and ants) on reproductive success was examined through exclusion experiments and efficiency tests. Only one species of bee (Andrena assimilis, Andrenidae) from the 25 insect species that were recorded during two study seasons seemed to be responsible ...