Pedro J. Rey

Beyond species loss: the extinction of ecological interactions in a changing world

Summary 1. The effects of the present biodiversity crisis have been largely focused on the loss of species. However, a missed component of biodiversity loss that often accompanies or even precedes species disappearance is the extinction of ecological interactions. 2. Here, we propose a novel model that (i) relates the diversity of both species and interactions along a gradient of environmental deterioration and (ii) explores how the rate of loss of ecological functions, and consequently of ecosystem services, can be accelerated or restrained depending on how the rate of species loss covaries with the rate of interactions loss. 3. We find that the loss of species and interactions are decoupled, such that ecological interactions are often lost at a higher rate. This implies that the loss of ecological interactions may occur well before species disappearance, affecting species functionality and ecosystems services at a faster rate than species extinctions. We provide a number of empirical case studies illustrating these points. 4. Our approach emphasizes the importance of focusing on species interactions as the major biodiversity component from which the ‘health’ of ecosystems depends.

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.

Spatio‐Temporal Variation in Fruit and Frugivorous Bird Abundance in Olive Orchards

Fruit availability and its relation to bird abundance at different spatio-tem- poral scales were examined in olive orchards in southern Spain. Because olive abundance in orchards can be manipulated, this system provides an opportunity to examine the link between populations of fruit-eating birds and fruiting plants in much more detail than possible in natural systems. Olive availability varied in space and time as a result of differences in olive yield and in ripening and harvesting rates. The most abundant frugiv- orous birds in the orchards (Sylvia atricapilla and Turdus philomelos) were frequently able to track olive availability on both local and regional scales. S. atricapilla showed a response to even small-scale harvesting of olives by humans, distributing itself preferentially in unharvested patches. The ability of both species to track fruit availability may explain their high abundance. Other less abundant frugivores (Erithacus rubecula and S. melanocephala) showed less capacity to track olive availability. I suggest that their inability to respond to rapidly changing patterns of olive abundance may partially account for their scarcity in olive orchards. Olive orchards play an important role in maintaining frugivorous bird populations in the Mediterranean area. My data suggest that a key reason for this is great spatial and temporal variability in the availability of olives in orchards, which results in a widely scattered but temporally continuous availability of olives. The capacity of some frugivorous species to track complex spatio-temporal patterns of fruit availability was, I hypothesize, a pre-adaptive feature that allowed them to flourish in the highly modified habitat of southern Spain.

Floral integration, phenotypic covariance structure and pollinator variation in bumblebee-pollinated Helleborus foetidus

By analysing patterns of phenotypic integration and multivariate covariance structure of five metric floral traits in nine Iberian populations of bumblebee‐pollinated Helleborus foetidus (Ranunculaceae), this paper attempts to test the general hypothesis that pollinators enhance floral integration and selectively modify phenotypic correlations between functionally linked floral traits. The five floral traits examined exhibited significant phenotypic integration at all populations, and both the magnitude and the pattern of integration differed widely among populations. Variation in extent and pattern of integration was neither distance‐dependent nor significantly related to between‐population variation in taxonomical composition and morphological diversity of the pollinator assemblage. Patterns of floral integration were closer to expectations derived from consideration of developmental affinities between floral whorls than to expectations based on a pollinator‐mediated adaptive hypothesis. Taken together, results of this study suggest that between‐population differences in magnitude and pattern of floral integration in H. foetidus are probably best explained as a consequence of random genetic sampling in the characteristically small and ephemeral populations of this species, rather than reflecting the selective action of current pollinators.

Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea

Recent evidence indicates that fruit size has evolved according to dispersers’ size. This is hypothesized to result from a balance between factors favouring large seeds and dispersers setting the maximum fruit size. This hypothesis assumes that (1) the size of fruits that can be consumed by dispersers is limited, (2) fruit and seed size are positively correlated, and (3) the result of multiple selection pressures on seed size is positive. Our studies on the seed dispersal mutualism of Olea europaea have supported the first and second assumptions, but valid tests of the third assumption are still lacking. Here we confirm the third assumption. Using multiplicative fitness components, we show that conflicting selection pressures on seed size during and after dispersal reverse the negative pattern of selection exerted by dispersers.

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.

Environmental aridity is associated with cytotype segregation and polyploidy occurrence in Brachypodium distachyon (Poaceae)

• The ecological and adaptive significance of plant polyploidization is not well understood and no clear pattern of association between polyploid frequency and environment has emerged. Climatic factors are expected to predict cytotype distribution. However, the relationship among climate, cytotype distribution and variation of abiotic stress tolerance traits has rarely been examined. • Here, we use flow cytometry and root-tip squashes to examine the cytotype distribution in the temperate annual grass Brachypodium distachyon in 57 natural populations distributed across an aridity gradient in the Iberian Peninsula. We further investigate the link between environmental aridity, ploidy, and variation of drought tolerance and drought avoidance (flowering time) traits. • Distribution of diploids (2n = 10) and allotetraploids (2n = 30) in this species is geographically structured throughout its range in the Iberian Peninsula, and is associated with aridity gradients. Importantly, after controlling for geographic and altitudinal effects, the link between aridity and polyploidization occurrence persisted. Water-use efficiency varied between ploidy levels, with tetraploids being more efficient in the use of water than diploids under water-restricted growing conditions. • Our results indicate that aridity is an important predictor of polyploid occurrence in B. distachyon, suggesting a possible adaptive origin of the cytotype segregation.

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.