Julio M. Alcántara

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.

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.

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.

Seedling establishment in Olea europaea: Seed size and microhabitat affect growth and survival

Abstract: We investigated the effects of seed size and microhabitat on the dynamics of seedling establishment in Olea europaea. We tested the hypothesis that the type of microhabitat suitable for O. europaea recruitment is influenced by microhabitat-specific relationships between seed size and seedling growth rate. To test this hypothesis we conducted field experiments evaluating seedling growth and survival as a function of seed size, microhabitat (determined by presence/absence of scrub cover), and competition (established by means of seedling density gradients). Our results show that, first, seed size was related to seedling size and to differential growth rate. Second, seedling growth rate was negatively correlated with initial seedling size, although this correlation varied among microhabitats and temporally. Third, seedling survival differed between microhabitats and was positively affected by initial seedling size until the end of the summer drought. Finally, the effect of seedling size on survival was partly mediated by its negative relationship with growth rate. However, the combined effect of size and growth on seedling survival varied between microhabitats. We conclude that establishment depended on microhabitats through facilitation and inhibition processes, and that seed size-related growth rate strongly affected seedling fate. It is noteworthy that the effectiveness of the size-correlated growth depended on microhabitat.

Geographic variation in the adaptive landscape for seed size at dispersal in the myrmecochorous Helleborus foetidus

Literature on seed dispersal mutualisms suggests that plant populations should hardly adapt to their current dispersers. We address the predictions that selection pressures exerted by ants on dispersal-related diaspore traits of the ant-dispersed Helleborus foetidus are highly variable in space, and that geographic (inter-population) variation in these traits is unrelated to selection by current dispersers. To test these predictions we use the concept of the quantitative adaptive landscape for seed size at dispersal. Such landscape depicts the relationship between the population’s mean trait value (mean seed size in the present study) and the population’s mean fitness (mean dispersal probability in the present study). Adaptive landscapes make it possible to assess whether the mean population’s phenotype agrees with one favored by selection. We first analyse, in 12 populations of H. foetidus from southern Spain, the extent of divergence among populations in seed and elaiosome size, and the abundance, composition, and behavior of the ant communities. Seeds from a fixed set of five of these populations were offered to ants in all the study sites to fit the adaptive landscape for seed size. In addition, seeds from the local population were also offered in each site. Our results show that seed size has undergone a larger divergence among populations than elaiosome size. Despite geographic variation in ant assemblages, the adaptive landscapes for seed size at dispersal were remarkably similar among sites: ants create disruptive selection on seed size in 10 out of 12 study sites. As predicted, the basic features of these adaptive landscapes (curvature and location of the minimum) varied geographically in accordance with variation in the size of seed dispersers. Also as predicted, in most populations, the observed mean seed size does not agree with that expected from the adaptive landscapes at dispersal. However, the relevance of dispersers for seed size evolution should not be neglected since the agreement between observed and optimum seed size was stronger where dispersers were more abundant. Thus, against the general view, our results evidence that, in H. foetidus, the observed geographic variation in dispersal-related plant traits is partly linked to selection exerted by current dispersers. Geographic variation in ant assemblages determines both the existence of a selection mosaic and the degree of adjustment of populations to the patterns of selection in the mosaic.

Intra-population comparison of vegetative and floral trait heritabilities estimated from molecular markers in wild Aquilegia populations.

Measuring heritable genetic variation is important for understanding patterns of trait evolution in wild populations, and yet studies of quantitative genetic parameters estimated directly in the field are limited by logistic constraints, such as the difficulties of inferring relatedness among individuals in the wild. Marker‐based approaches have received attention because they can potentially be applied directly to wild populations. For long‐lived, self‐compatible plant species where pedigrees are inadequate, the regression‐based method proposed by Ritland has the appeal of estimating heritabilities from marker‐based estimates of relatedness. The method has been difficult to implement in some plant populations, however, because it requires significant variance in relatedness across the population. Here, we show that the method can be readily applied to compare the ability of different traits to respond to selection, within populations. For several taxa of the perennial herb genus Aquilegia, we estimated heritabilities of floral and vegetative traits and, combined with estimates of natural selection, compared the ability to respond to selection of both types of traits under current conditions. The intra‐population comparisons showed that vegetative traits have a higher potential for evolution, because although they are as heritable as floral traits, selection on them is stronger. These patterns of potential evolution are consistent with macroevolutionary trends in the European lineage of the genus.

Linking divergent selection on vegetative traits to environmental variation and phenotypic diversification in the Iberian columbines (Aquilegia).

Divergent selection is a key in the ecological theory of adaptive radiation. Most evidence on its causes and consequences relies on studies of pairs of populations or closely related taxa. However, adaptive radiation involves multiple taxa adapted to different environmental factors. We propose an operational definition of divergent selection to explore the continuum between divergent and convergent selection in multiple populations and taxa, and its links with environmental variation and phenotypic and taxonomic differentiation. We apply this approach to explore phenotypic differentiation of vegetative traits between 15 populations of four taxa of Iberian columbines (Gen. Aquilegia). Differences in soil rockiness impose divergent selection on inflorescence height and the number of flowers per inflorescence, likely affecting the processes of phenotypic and, in the case of inflorescence height, taxonomic diversification between taxa. Elevational variation imposes divergent selection on the number of leaves; however, the current pattern of divergent selection on this trait seems related to ecotypic differentiation within taxa but not to their taxonomic diversification.

Linking Topological Structure and Dynamics in Ecological Networks

Interaction networks are basic descriptions of ecological communities and are at the core of community dynamics models. Knowledge of their structure should enable us to understand dynamical properties of ecological communities. However, the relationships between dynamical properties of communities and qualitative descriptors of network structure remain unclear. To improve our understanding of such relationships, we develop a framework based on the concept of strongly connected components, which are key structural components of networks necessary to explain stability properties such as persistence and robustness. We illustrate this framework for the analysis of qualitative empirical food webs and plant-plant interaction networks. Both types of networks exhibit high persistence (on average, 99% and 80% of species, respectively, are expected to persist) and robustness (only 0.2% and 2% of species are expected to disappear following the extinction of a species). Each of the networks is structured as a large group of interconnected species accompanied by much smaller groups that most often consist of a single species. This low-modularity configuration can be explained by a negative modularity-stability relationship. Our results suggest that ecological communities are not typically structured in multispecies compartments and that compartmentalization decreases robustness.

Glandular trichomes as an inflorescence defence mechanism against insect herbivores in Iberian columbines.

Glandular trichomes play a defensive role against herbivores in the leaves of many plant species. However, their functional role in inflorescences has not been studied, even though theory suggests that tissues with a higher fitness value, such as inflorescences, should be better defended. Using manipulative experiments, we analysed the defensive role of glandular trichomes against herbivorous insects in the inflorescence of Iberian columbines (genus Aquilegia), and its inter-population and inter-taxa variation in relation to herbivore abundance and potential selective pressure. The experiments were conducted in eight populations belonging to four subspecies of two columbines (Aquilegia vulgaris and Aquilegia pyrenaica). For each population, we estimated the density of glandular trichomes in the inflorescences, the abundance of insects stuck in the inflorescences, the abundance of small herbivorous insects, the incidence of damage on flowers and fruits, and the fruit set. The density of glandular trichomes on the inflorescence of A. vulgaris and A. pyrenaica was higher in regions of higher herbivore abundance. We also found that when the plants lose the protection of glandular trichomes, small insects have better access to flowers and fruits, causing more damage and reducing plant fitness. This study concludes that glandular trichomes are part of an adaptive response against phytophagous insect herbivory. The observed variation in herbivore pressure between taxa, likely caused by habitat differentiation, might have played a role in trait differentiation through divergent selection. This result adds evidence to the differentiation of the Iberian columbines through habitat specialization.