Species functional traits and abundance as drivers of multiplex ecological networks: first empirical quantification of inter-layer edge weights.

Many vertebrate species act as both plant pollinators and seed-dispersers, thus interconnecting these processes, particularly on islands. Ecological multilayer networks are a powerful tool to explore interdependencies between processes; however, quantifying the links between species engaging in different types of interactions (i.e. inter-layer edges) remains a great challenge. Here, we empirically measured inter-layer edge weights by quantifying the role of individually marked birds as both pollinators and seed-dispersers of Galápagos plant species over an entire year. Although most species (80%) engaged in both functions, we show that only a small proportion of individuals actually linked the two processes, highlighting the need to further consider intra-specific variability in individuals' functional roles. Furthermore, we found a high variation among species in linking both processes, i.e. some species contribute more than others to the modular organization of the multilayer network. Small and abundant species are particularly important for the cohesion of pollinator seed-dispersal networks, demonstrating the interplay between species traits and neutral processes structuring natural communities.

Contribution by vertebrates to seed dispersal effectiveness in the Galápagos Islands: a community-wide approach.

Seed dispersal and seedling recruitment are crucial phases in the life cycle of all spermatophyte plants. The net contribution of seed dispersers to plant establishment is known as seed dispersal effectiveness (SDE) and is defined as the product of a quantitative (number of seeds dispersed) and a qualitative (probability of recruitment) component. In Galápagos, we studied the direct contribution to SDE (number of seeds dispersed and effect on seedling emergence) provided by the five island groups of frugivores (giant tortoises, lizards, medium-sized passerine birds, small non-finch passerine birds, and finches) in the two main habitats in this archipelago: the lowland and the highland zones, and found 16 vertebrate species dispersing 58 plant species. Data on frequency of occurrence of seeds in droppings and number of seeds dispersed per unit area produced contrasting patterns of seed dispersal. Based on the former, giant tortoises and medium-sized passerines were the most important seed dispersers. However, based on the latter, small non-finch passerines were the most important dispersers, followed by finches and medium-sized passerines. The effect of disperser gut passage on seedling emergence varied greatly depending on both the disperser and the plant species. Although the contribution to SDE provided by different disperser guilds changed across plant species, medium-sized passerines (e.g., mockingbirds) provided a higher contribution to SDE than lava lizards in 10 out of 16 plant species analysed, whereas lava lizards provided a higher contribution to SDE than birds in five plant species. While both the quantitative and qualitative components addressed are important, our data suggests that the former is a better predictor of SDE in the Galápagos archipelago.

Evaluating the effects of pollinator-mediated interactions using pollen transfer networks: evidence of widespread facilitation in south Andean plant communities.

Information about the relative importance of competitive or facilitative pollinator-mediated interactions in a multi-species context is limited. We studied interspecific pollen transfer (IPT) networks to evaluate quantity and quality effects of pollinator sharing among plant species on three high-Andean communities at 1600, 1800 and 2000 m a.s.l. To estimate the sign of the effects (positive, neutral or negative), the relation between conspecific and heterospecific pollen deposited on stigmas was analysed with GLMMs. Network analyses showed that communities were characterised by the presence of pollen hub-donors and receptors. We inferred that facilitative and neutral pollinator-mediated interactions among plants prevailed over competition. Thus, the benefits from pollinator sharing seem to outweigh the costs (i.e. heterospecific deposition and conspecific pollen loss). The largest proportion of facilitated species was found at the highest elevation community, suggesting that under unfavourable conditions for the pollination service and at lower plant densities facilitation can be more common.

Floral colour variation of Nicotiana glauca in native and non-native ranges: Testing the role of pollinators' perception and abiotic factors.

Invasive plants displaying disparate pollination environments and abiotic conditions in native and non-native ranges provide ideal systems to test the role of different ecological factors driving flower colour variation. We quantified corolla reflectance of the ornithophilous South American Nicotiana glauca in native populations, where plants are pollinated by hummingbirds, and in populations from two invaded regions: South Africa, where plants are pollinated by sunbirds, and the Balearic island of Mallorca, where plants reproduce by selfing. Using visual modelling we examined how corolla reflectance could be perceived by floral visitors present in each region. Through Mantel tests we assessed a possible association between flower colour and different abiotic factors. Corolla reflectance variation (mainly along medium to long wavelengths, i.e. human green-yellow to red colours) was greater among studied regions than within them. Flower colour was more similar between South America and South Africa, which share birds as pollinators. Within invaded regions, corolla reflectance variation was lower in South Africa, where populations could not be distinguished from each other by sunbirds, than in Spain, where populations could be distinguished from each other by their occasional visitors. Differences in corolla colour among populations were partially associated with differences in temperature. Our findings suggest that shifts in flower colour of N. glauca across native and invaded ranges could be shaped by changes in both pollination environment and climatic factors. This is the first study on plant invasions considering visual perception of different pollinators and abiotic drivers of flower colour variation.

Reproductive success of the Canarian Echium simplex (Boraginaceae) mediated by vertebrates and insects.

Oceanic island ecosystems favour the appearance of novel interactions as a consequence of their depauperate and disharmonic flora and fauna. We investigated Echium simplex, endemic to the Anaga Biosphere Reserve in NE Tenerife, Canary Islands, belongs to the Canarian bird-flower element. Along two flowering seasons, we studied the breeding system of E. simplex, identified the floral visitors and compared the pollination effectiveness of different animal guilds (insects versus vertebrates) by means of selective exclosures. E. simplex is self-compatible but selfing significantly reduced fruit set. The flowers were visited by five bird species (mostly Phylloscopus canariensis and Serinus canarius, but also Cyanistes teneriffae, Sylvia atricapilla and Sylvia melanocephala), a lizard species (Gallotia galloti) and over a hundred insect species (mainly hymenopterans and coleopterans). Flying insects increased fruit set whereas small flower dwellers (mostly beetles) decreased both fruit and seed set. Vertebrates had a negligible effect on reproductive success. We conclude that although the floral resources provided by E. simplex may be important to some vertebrate species, these do not appear to contribute to increase fitness of the plant, which was more dependent upon flying insects for fruit and seed set. We additionally found that plant reproductive structures are heavily damaged by feral goats, which threaten the maintenance of this Canarian endemic species.

Plant reproductive ecology and evolution in the Mediterranean islands: state of the art.

The ca. 12,000 islands and islets that encompass the Mediterranean Basin represent a biodiversity hotspot. They have been disconnected from each other and from the continent for hundreds of thousands to millions of years and encompass a high incidence of endemic plant species, with values that can exceed 20% of the local flora. Despite this, relatively few studies have been carried out to unravel ecological and evolutionary aspects of plant reproduction. We synthesise here the available information on the breeding systems, pollination and seed dispersal mode of the Mediterranean island flora. The main objective is to identify general patterns as well as to detect the main gaps in information on reproductive ecology in these particular and vulnerable systems in the face of global change. We also briefly review the information on impacts of invasive species on plant reproduction and dispersal, as these are some of the main threats to island biodiversity in general and Mediterranean island plant diversity in particular. The review has revealed that most available information is very geographically biased towards the western Mediterranean islands, especially the Balearic Islands, although a good fraction of studies have also been carried out on the eastern islands in the Aegean archipelago. Moreover, the majority of data come from species-focused studies, mainly endemic species of restricted range, whereas only a small fraction of studies have been performed at a community level. Relatively little work has involved genetic analyses, mainly focused on assessing the genetic differentiation and variability on narrow endemics. Contrary to our expectations, most island species do not rely on autonomous selfing, which might be related to the relatively high diversity of pollinators. The small, uninhabited, islands might be the last refuges of peculiar interactions that evolved in them in ancient times; they thus should be considered as sanctuaries of extraordinary biodiversity. Finally, we point out the main gaps of information and formulate a set of hypotheses that we believe are worth testing in future studies if we are to advance knowledge on the reproductive biology of Mediterranean island plants.

Critical stages in the recruitment process of Rhamnus alaternus L.

BACKGROUND AND AIMS: Rhamnus alaternus is a Mediterranean shrub commonly used in reforestation programs. Although several aspects of its reproductive biology have been studied, little is known about the importance of the different recruitment stages in the overall regeneration process of this species, which limits its proper use in Mediterranean forests and shrubland management. The aim of the present work was to quantify the importance of the different recruitment stages in the regeneration process of R. alaternus. METHODS: Two populations of Rhamnus alaternus on the island of Mallorca that differ in climatic conditions, type of habitat and sex ratio were studied. The importance of seed production, seed dispersal and predation, seedling emergence and seedling survival for the regeneration of this species were quantified. KEY RESULTS: In both populations, fruit set and fruit removal by animals were not critical stages, since almost half of the flowers became mature fruits and 90% of those were dispersed. Most seeds were deposited under female conspecifics (86 and 47%, at Lloret and Esporles, respectively), and very few were found in open inter-spaces (1 and 5%). Post-dispersal seed predation (mostly by ants and rodents) was very high in both populations. Seedling emergence took place during autumn and early winter and it ranged from 31 to 68% depending upon year and microhabitat. The majority of emerged seedlings died during the first year, mainly due to desiccation; such mortality was influenced by rainfall and differed among microhabitats (varying from 67 to 100%). The general spatial distribution of seed rain was concordant with the seedling emergence and survival pattern in both populations. CONCLUSIONS: The recruitment of Rhamnus alaternus appeared to be mainly limited by seed and seedling survival, regardless of the type of habitat in which the species is found.

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 variability in seed output and pollination and seed dispersal methods suggest the existence of important reproductive correlates that demand further investigation.