Limited potential for bird migration to disperse plants to cooler latitudes.

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

Frugivore species maintain their structural role in the trophic and spatial networks of seed dispersal interactions.

Trophic relationships have inherent spatial dimensions associated with the sites where species interactions, or their delayed effects, occur. Trophic networks among interacting species may thus be coupled with spatial networks linking species and habitats whereby animals connect patches across the landscape thanks to their high mobility. This trophic and spatial duality is especially inherent in processes like seed dispersal by animals, where frugivores consume fruit species and deposit seeds across habitats. We analysed the frugivore-plant interactions and seed deposition patterns of a diverse assemblage of frugivores in a heterogeneous landscape in order to determine whether the roles of frugivores in network topology are correlated across trophic and spatial networks of seed dispersal. We recorded fruit consumption and seed deposition by birds and mammals during 2 years in the Cantabrian Range (N Spain). We then constructed two networks of trophic (i.e. frugivore-plant) and spatial (i.e. frugivore-seed deposition habitat) interactions and estimated the contributions of each frugivore species to the network structure in terms of nestedness, modularity and complementary specialization. We tested whether the structural role of frugivore species was correlated across the trophic and spatial networks, and evaluated the influence of each frugivore abundance and body mass in that relationship. Both the trophic and the spatial networks were modular and specialized. Trophic modules matched medium-sized birds with fleshy-fruited trees, and small bird and mammals with small-fruit trees and shrubs. Spatial modules associated birds with woody canopies, and mammals with open habitats. Frugivore species maintained their structural role across the trophic and spatial networks of seed dispersal, even after accounting for frugivore abundance and body mass. The modularity found in our system points to complementarity between birds and mammals in the seed dispersal process, a fact that may trigger landscape-scale secondary succession. Our results open up the possibility of predicting the consumption pattern of a diverse frugivore community, and its ecological consequences, from the uneven distribution of fleshy-fruit resources in the landscape.

RESUMEN Las relaciones tróficas tienen una dimensión espacial asociada a los sitios donde ocurren o tienen lugar sus efectos. Las redes tróficas entre especies pueden, por tanto, emparejarse con las redes espaciales que vinculan a las especies con sus hábitats, y donde los animales conectan parches gracias a su alta movilidad. Esta dualidad trófica y espacial es especialmente inherente a procesos como la dispersión de semillas, donde los animales frugívoros consumen distintas especies de plantas con fruto carnoso y depositan sus semillas en distintos hábitats. Aquí analizamos las interacciones frugívoro-planta y los patrones de deposición de semillas de un conjunto diverso de frugívoros en un paisaje heterogéneo, con el fin de determinar si el papel topológico de los frugívoros en la red trófica de dispersión de semillas se correlaciona con dicho papel en la red espacial de deposición. Para ello, registramos el consumo de frutos y la deposición de semillas por aves y mamíferos durante dos años en la Cordillera Cantábrica (N España). Construimos dos redes de interacciones, una trófica (frugívoro-planta) y otra espacial (frugívoro-hábitat de deposición de semillas), y estimamos la contribución de las especies animales a la estructura de cada red, en términos de anidamiento, modularidad y especialización. Analizamos si el papel estructural de los distintos frugívoros se correlacionaba a través de ambas redes, y evaluamos la influencia de la abundancia relativa y la masa corporal de los frugívoros en dicha relación. Encontramos un patrón general de modularidad y especialización tanto en la red trófica como en la espacial. Los módulos tróficos agruparon principalmente a aves de mediano tamaño con árboles con frutos carnosos, y a aves de pequeño tamaño y mamíferos con arbustos de fruto carnoso. Los módulos espaciales asociaron en general a las aves con hábitats arbolados y a los mamíferos con hábitats abiertos. Las especies de frugívoros mantuvieron su papel estructural tanto en la red trófica como en la espacial, incluso después de tener en cuenta la abundancia relativa y la masa corporal de los frugívoros. El patrón de modularidad detectado en el sistema apunta a una importante complementariedad funcional entre aves y mamíferos en el proceso de dispersión de semillas, de modo que puede favorecer la sucesión secundaria de la vegetación a escala de paisaje. Nuestros resultados abren la posibilidad de predecir el patrón de consumo de una comunidad diversa de frugívoros así como sus consecuencias ecológicas a partir de la distribución desigual de los recursos tróficos en el paisaje.

Interspecific competition for frugivores: population-level seed dispersal in contrasting fruiting communities.

Indirect interactions among plant species mediated by frugivorous animals can be central to population and community dynamics, since the successful seed dispersal of species may depend on facilitative or competitive interactions with heterospecific plants. Yet, empirical evidence on these interactions is very scarce and mostly available at small spatial scales, within populations. Because lipid-rich fruits are known to be preferred by migratory birds, here we test our prediction of competitive inferiority of a carbohydrate-rich fruited species (the hawthorn Crataegus monogyna) compared to lipid-rich co-fruiting species in a Mediterranean region where the bulk of seed dispersal relies on migratory birds. We assessed avian seed dispersal in both relative (fruit removal rate) and absolute terms (seed dispersal magnitude) in seven hawthorn populations distributed across an altitudinal gradient encompassing three contrasting fruiting contexts: hawthorn is scarce in the lowlands, common in the midlands, and the dominant fruit species in the highlands. We found evidence of seed dispersal reduction due to interspecific competition in the lowland populations, where lipid-rich fruits dominate. Besides, DNA barcoding analysis of bird-dispersed seeds revealed that only a small subset of the local frugivore assemblages consumed hawthorn fruits in the lowland communities. Instead, the consumers of hawthorn fruits resembled the local frugivore assemblages where hawthorn fruits were more dominant and frugivore choices more limited. Our study suggests mechanisms by which the rarity or dominance of plant species might be jointly influenced by environmental constraints (here, precipitation along the altitudinal gradient) and frugivore-mediated indirect interactions among plants hindering or facilitating seed dispersal.

Small size does not restrain frugivory and seed dispersal across the evolutionary radiation of Galápagos lava lizards.

Frugivory in lizards is often assumed to be constrained by body size; only large individuals are considered capable of consuming fruits, with the potential of acting as seed dispersers. However, only one previous study has tested the correlation of frugivory with body and head size at an archipelago scale across closely related species. All nine lava lizards (Microlophus spp.) were studied on the eleven largest Galápagos islands from 2010 to 2016 to investigate whether frugivory is related to body and head size. We also tested whether fruit abundance influences fruit consumption and explored the effect of seed ingestion on seedling emergence time and percentage. Our results showed that across islands, lava lizards varied considerably in size (64-102 mm in mean snout-vent length) and level of frugivory (1-23%, i.e., percentage of droppings with seeds). However, level of frugivory was only weakly affected by size as fruit consumption was also common among small lizards. Lava lizards consumed fruits throughout the year and factors other than fruit abundance may be more important drivers of fruit selection (e.g., fruit size, energy content of pulp). From 2,530 droppings, 1,714 seeds of at least 61 plant species were identified, 76% of the species being native to the Galápagos. Most seeds (91%) showed no external structural damage. Seedling emergence time (44 versus 118 days) and percentage (20% versus 12%) were enhanced for lizard-ingested seeds compared to control (uningested) fruits. De-pulping by lizards (i.e., removal of pulp with potential germination inhibitors) might increase the chances that at least some seeds find suitable recruitment conditions. We concluded that lizards are important seed dispersers throughout the year and across the whole archipelago, regardless of body size.

Zooming into plant-flower visitor networks: an individual trait-based approach.

Understanding how ecological communities are structured is a major goal in ecology. Ecological networks representing interaction patterns among species have become a powerful tool to capture the mechanisms underlying plant-animal assemblages. However, these networks largely do not account for inter-individual variability and thus may be limiting our development of a clear mechanistic understanding of community structure. In this study, we develop a new individual-trait based approach to examine the importance of individual plant and pollinator functional size traits (pollinator thorax width and plant nectar holder depth) in mutualistic networks. We performed hierarchical cluster analyses to group interacting individuals into classes, according to their similarity in functional size. We then compared the structure of bee-flower networks where nodes represented either species identity or trait sets. The individual trait-based network was almost twice as nested as its species-based equivalent and it had a more symmetric linkage pattern resulting from of a high degree of size-matching. In conclusion, we show that by constructing individual trait-based networks we can reveal important patterns otherwise difficult to observe in species-based networks and thus improve our understanding of community structure. We therefore recommend using both trait-based and species-based approaches together to develop a clearer understanding of the properties of ecological networks.

Disclosing the double mutualist role of birds on Galápagos.

Life on oceanic islands deviate in many ways from that on the mainland. Their biodiversity is relatively poor and some groups are well-represented, others not, especially not insects. A scarcity of insects forces birds to explore alternative food, such as nectar and fruit. In this way, island birds may pollinate and disperse seed to an extent unseen on any mainland; they may even first consume floral resources of a plant species and then later harvest the fruit of the same species. Through this biotic reuse, they may act as double mutualists. The latter have never been studied at the level of the network, because they are traditionally considered rare. We sampled pollination and seed-dispersal interactions on Galápagos and constructed a plant-bird mutualism network of 108 plant (12% being double mutualists) and 21 bird species (48% being double mutualists), and their 479 interactions, being either single (95%) or double mutualisms (5%). Double mutualists constitute the core in the pollination-dispersal network, coupling the two link types together. They may also initiate positive feedbacks (more pollination leading to more dispersal), which theoretically are known to be unstable. Thus, double mutualisms may be a necessary, but risky prerequisite to the survival of island biodiversity.

Galápagos land iguana (Conolophus subcristatus) as a seed disperser.

The role of the most common land iguana (Conolophus subcristatus) in the Galápagos Islands as an effective seed disperser is explored in this study. A total of 5705 seeds of 32 plant species were identified from 160 scats, 4545 of which (80%) appeared visually undamaged. Germination trials of 849 seeds from 29 species revealed that at least 10 species remained viable after passing through the iguana's gut, although only a small proportion of those seeds (4%) germinated. In any case, we argue that C. subcristatus exerts an important role on the 7 Galapagos islands where it occurs because of its abundance and capacity to ingest and disperse seeds at long distances. Our results strongly suggest that the Galápagos C. subcristatus plays an important role as a seed disperser of not only of native species but also some introduced plants in the Galápagos Islands.

Historical isolation of the Galápagos carpenter bee (Xylocopa darwini) despite strong flight capability and ecological amplitude.

Colonization across the Galápagos Islands by the carpenter bee (Xylocopa darwini) was reconstructed based on distribution of mitochondrial haplotypes (cytochrome oxidase II (COII) sequences) and haplotype lineages. A total of 12 haplotypes were found in 118 individuals of X. darwini. Distributional, phylogenetic and phylogeographic analyses suggest early colonization of most islands followed by historical isolation in two main groups: eastern and central-western islands. Evidence of recurrent inter-island colonization of haplotypes is largely lacking, despite strong flight capability and ecological amplitude of the species. Recent palaeogeographic data suggest that several of the current islands were connected in the past and thus the isolation pattern may have been even more pronounced. A contrast analysis was also carried out on 10 animal groups of the Galápagos Islands, and on haplotype colonization of seven animal and plant species from several oceanic archipelagos (the Galápagos, Azores, Canary Islands). New colonization metrics on the number of potential vs. inferred colonization events revealed that the Galápagos carpenter bee shows one of the most significant examples of geographic isolation.

The colonization history of Juniperus brevifolia (Cupressaceae) in the Azores Islands.

BACKGROUND: A central aim of island biogeography is to understand the colonization history of insular species using current distributions, fossil records and genetic diversity. Here, we analyze five plastid DNA regions of the endangered Juniperus brevifolia, which is endemic to the Azores archipelago. METHODOLOGY/PRINCIPAL FINDINGS: The phylogeny of the section Juniperus and the phylogeographic analyses of J. brevifolia based on the coalescence theory of allele (plastid) diversity suggest that: (1) a single introduction event likely occurred from Europe; (2) genetic diversification and inter-island dispersal postdated the emergence of the oldest island (Santa Maria, 8.12 Ma); (3) the genetic differentiation found in populations on the islands with higher age and smaller distance to the continent is significantly higher than that on the younger, more remote ones; (4) the high number of haplotypes observed (16), and the widespread distribution of the most frequent and ancestral ones across the archipelago, are indicating early diversification, demographic expansion, and recurrent dispersal. In contrast, restriction of six of the seven derived haplotypes to single islands is construed as reflecting significant isolation time prior to colonization. CONCLUSIONS/SIGNIFICANCE: Our phylogeographic reconstruction points to the sequence of island emergence as the key factor to explain the distribution of plastid DNA variation. The reproductive traits of this juniper species (anemophily, ornithochory, multi-seeded cones), together with its broad ecological range, appear to be largely responsible for recurrent inter-island colonization of ancestral haplotypes. In contrast, certain delay in colonization of new haplotypes may reflect intraspecific habitat competition on islands where this juniper was already present.