Ruben Heleno

Effects of alien plants on insect abundance and biomass: a food-web approach

The replacement of native plants by alien species is likely to affect other trophic levels, particularly phytophagous insects. Nevertheless, the effect of alien plants on insect biomass has not yet been quantified. Given their critical role in transferring energy from plants to higher trophic levels, if alien plants do affect insect biomass, this could have far-reaching consequences for community structure. We used 35 food webs to evaluate the impacts of alien plants on insect productivity in a native forest in the Azores. Our food webs quantified plants, insect herbivores, and their parasitoids, which allowed us to test the effects of alien plants on species richness and evenness, insect abundance, insect biomass, and food-web structure. Species richness of plants and insects, along with plant species evenness, declined as the level of plant invasion increased. Nevertheless, none of the 4 quantitative food-web descriptors (number of links, link density, connectance, and interaction evenness) varied significantly with plant invasion independent of the size of the food web. Overall, insect abundance was not significantly affected by alien plants, but insect biomass was significantly reduced. This effect was due to the replacement of large insects on native plants with small insects on alien plants. Furthermore, the impact of alien plants was sufficiently severe to invert the otherwise expected pattern of species-richness decline with increased elevation. We predict a decrease in insect productivity by over 67% if conservation efforts fail to halt the invasion of alien plants in the Azores.

Invaders of pollination networks in the Galapagos Islands: emergence of novel communities.

The unique biodiversity of most oceanic archipelagos is currently threatened by the introduction of alien species that can displace native biota, disrupt native ecological interactions, and profoundly affect community structure and stability. We investigated the threat of aliens on pollination networks in the species-rich lowlands of five Galápagos Islands. Twenty per cent of all species (60 plants and 220 pollinators) in the pooled network were aliens, being involved in 38 per cent of the interactions. Most aliens were insects, especially dipterans (36%), hymenopterans (30%) and lepidopterans (14%). These alien insects had more links than either endemic pollinators or non-endemic natives, some even acting as island hubs. Aliens linked mostly to generalized species, increasing nestedness and thus network stability. Moreover, they infiltrated all seven connected modules (determined by geographical and phylogenetic constraints) of the overall network, representing around 30 per cent of species in two of them. An astonishingly high proportion (38%) of connectors, which enhance network cohesiveness, was also alien. Results indicate that the structure of these emergent novel communities might become more resistant to certain type of disturbances (e.g. species loss), while being more vulnerable to others (e.g. spread of a disease). Such notable changes in network structure as invasions progress are expected to have important consequences for native biodiversity maintenance.

Seed dispersal networks in the Galápagos and the consequences of alien plant invasions.

Alien plants are a growing threat to the Galápagos unique biota. We evaluated the impact of alien plants on eight seed dispersal networks from two islands of the archipelago. Nearly 10 000 intact seeds from 58 species were recovered from the droppings of 18 bird and reptile dispersers. The most dispersed invaders were Lantana camara, Rubus niveus and Psidium guajava, the latter two likely benefiting from an asynchronous fruit production with most native plants, which facilitate their consumption and spread. Lava lizards dispersed the seeds of 27 species, being the most important dispersers, followed by small ground finch, two mockingbirds, the giant tortoise and two insectivorous birds. Most animals dispersed alien seeds, but these formed a relatively small proportion of the interactions. Nevertheless, the integration of aliens was higher in the island that has been invaded for longest, suggesting a time-lag between alien plant introductions and their impacts on seed dispersal networks. Alien plants become more specialized with advancing invasion, favouring more simplified plant and disperser communities. However, only habitat type significantly affected the overall network structure. Alien plants were dispersed via two pathways: dry-fruited plants were preferentially dispersed by finches, while fleshy fruited species were mostly dispersed by other birds and reptiles.

Evaluation of restoration effectiveness: community response to the removal of alien plants

Plant invasions are a key cause of biodiversity loss and motivate many restoration programs worldwide. We assessed restoration success of an invaded forest in the Azores using two complementary experimental designs: a before-after control-impact (BACI) design compared a restored and a control (unmanipulated) site over three years, while a control-impact (CI) design evaluated the short-term effects of restoration on restored-control replicated pairs. In both designs, a food web approach was used to evaluate both structural and functional aspects of the restoration. Two years after removing alien plants from the BACI design, there were increases in the abundance of native seeds (110%), herbivorous insects (85%), insect parasitoids (5%), and birds (7%) in the experimental plot compared to the unmanipulated plot. In the CI design, five experimental plots were weeded and paired with five adjacent unmanipulated plots. Immediately following the removal of alien plants within the experimental plots, there was a significant decrease in native plant species, likely attributed to the effect of disturbance. Nevertheless, the production of native seeds increased by 35% in year 1, and seed production of the focal endemic plant, Ilex perado (holly), increased 159% in year 2. Weeding increased the survivorship and growth of seedlings transplanted into the plots, particularly those of alien species. Both experiments provide evidence of the positive effects of weeding cascading through the food web from native plants to herbivorous insects, insect parasitoids, and birds. Two aspects that could prove critical to the outcome of restoration programs deserve further attention: most bird-dispersed seeds were alien, and weeding favored alien over native seedling growth.

Evidence for overlooked mechanisms of long‐distance seed dispersal to and between oceanic islands

This study is framed within a biodiversity project in the Galapagos Islands, financed by BBVA Foundation (Spain). We also thank the Charles Darwin Foundation and the Parque Nacional de Galapagos for giving us logistic support while working there.

Ecological networks: delving into the architecture of biodiversity

In recent years, the analysis of interaction networks has grown popular as a framework to explore ecological processes and the relationships between community structure and its functioning. The field has rapidly grown from its infancy to a vibrant youth, as reflected in the variety and quality of the discussions held at the first international symposium on Ecological Networks in Coimbra—Portugal (23–25 October 2013). The meeting gathered 170 scientists from 22 countries, who presented data from a broad geographical range, and covering all stages of network analyses, from sampling strategies to effective ways of communicating results, presenting new analytical tools, incorporation of temporal and spatial dynamics, new applications and visualization tools.1 During the meeting it became evident that while many of the caveats diagnosed in early network studies are successfully being tackled, new challenges arise, attesting to the health of the discipline.

Frugivory and seed dispersal in the Galapagos: what is the state of the art?

The Galápagos are considered a model oceanic archipelago, with unique flora and fauna currently threatened by alien invasive species. Seed dispersal is an important ecosystem function with consequences for plant population dynamics and vegetation structure. Hence, understanding the seed dispersal abilities of the assemblages of frugivores will inform scientists and managers of the dynamics of plant invasions and improve management planning. Here we provide the first comprehensive review of published information on frugivory and animal seed dispersal in the Galápagos. We collected data from a variety of sources, including notes of the first naturalist expeditions, gray literature available only in Galápagos collections, and peer-reviewed journal articles. Plant-animal frugivorous interactions were retrieved from 43 studies and compiled into an interaction matrix describing 366 unique interactions. Most studies focused on fruit consumption as a driving force for natural selection, but seed fate was seldom considered. Although most (71%) of the interactions involved native plants, more than one-quarter (28%) involved introduced species. Interactions involving birds are considerably more common than those of reptiles and mammals, probably reflecting a research bias towards birds. Despite the historical importance of the archipelago as the laboratory for evolutionary and ecological research, understanding of its seed dispersal systems is limited. We end the review by suggesting 3 priority areas of research on frugivory and seed dispersal in the Galápagos: (i) target research to close knowledge gaps; (ii) the use of a network approach to frame seed dispersal at the community level; and (iii) evaluation of the effect of seed dispersal as a selective pressure acting upon plants and frugivores. Finally, the output of this research has to be properly delivered to the Galápagos National Park Services to help increase management effectiveness.

Pollination patterns and plant breeding systems in the Galápagos: a review

BACKGROUND Despite the importance of the Galápagos Islands for the development of central concepts in ecology and evolution, the understanding of many ecological processes in this archipelago is still very basic. One such process is pollination, which provides an important service to both plants and their pollinators. The rather modest level of knowledge on this subject has so far limited our predictive power on the consequences of the increasing threat of introduced plants and pollinators to this unique archipelago. SCOPE As a first step toward building a unified view of the state of pollination in the Galápagos, a thorough literature search was conducted on the breeding systems of the archipelagos flora and compiled all documented flower-visitor interactions. Based on 38 studies from the last 100 years, we retrieved 329 unique interactions between 123 flowering plant species (50 endemics, 39 non-endemic natives, 26 introduced and eight of unknown origin) from 41 families and 120 animal species from 13 orders. We discuss the emergent patterns and identify promising research avenues in the field. CONCLUSIONS Although breeding systems are known for <20 % of the flora, most species in our database were self-compatible. Moreover, the incidence of autogamy among endemics, non-endemic natives and alien species did not differ significantly, being high in all groups, which suggests that a poor pollinator fauna does not represent a constraint to the integration of new plant species into the native communities. Most interactions detected (approx. 90 %) come from a single island (most of them from Santa Cruz). Hymenopterans (mainly the endemic carpenter bee Xylocopa darwinii and ants), followed by lepidopterans, were the most important flower visitors. Dipterans were much more important flower visitors in the humid zone than in the dry zone. Bird and lizard pollination has been occasionally reported in the dry zone. Strong biases were detected in the sampling effort dedicated to different islands, time of day, focal plants and functional groups of visitors. Thus, the existing patterns need to be confronted with new and less biased data. The implementation of a community-level approach could greatly increase our understanding of pollination on the islands and our ability to predict the consequences of plant invasions for the natural ecosystems of the Galápagos.

Throwing the baby out with the bathwater: does laurel forest restoration remove a critical winter food supply for the critically endangered Azores bullfinch?

The invasive Clethra arborea has a dual-role in the diet of the Azores bullfinch, a critically endangered bird species endemic to the island of São Miguel (Azores, Portugal). This is a crucial winter food resource but it lowers the availability of native laurel forest species that compose most of the bird’s diet throughout the year. The removal of this and other invasive alien species is part of current laurel forest habitat restoration programmes, disregarding the impact on the Azores bullfinch population. In order to evaluate the first responses of the Azores bullfinch to habitat restoration, we studied bird diet, foraging behaviour, food availability and habitat occupancy in managed (without C. arborea) and control areas. Significant increases in the availability of native food resources in managed areas were noticeable in the diet, particularly the intake of Ilex perado ssp. azorica and Prunus lusitanica ssp. azorica flower buds. In most of the studied months birds heavily used and foraged in managed over control areas. The one exception was in December, when a resource-gap occurred in managed areas, which may be overcome in the short-term due to re-establishment of native plants following removal of invasive aliens.

A Pragmatic Approach to the Management of Plant Invasions in Galapagos

This chapter presents an overview of the process undertaken to understand alien plant invasions and work towards their effective management in the Galapagos Islands. Galapagos is a unique case study for the management of alien plants in protected areas because much the archipelago has few alien plants and the original ecosystems are relatively intact. We discuss a pragmatic approach developed over 15 years to help prioritise management of 871 plant species introduced to the islands. This approach includes understanding invasion pathways; identifying which species are present and their distribution; determining invasive species impact on biodiversity, ecosystem function and mutualisms; prioritising management using weed risk assessment; guidelines to prevent further introduction through quarantine and early intervention; and developing methods to control or eradicate priority species. Principal barriers to application of the approach are limited capacity and coordination among managers and inherent difficulties arising from invasive species traits such as seed banks and dispersal and their interactions with ecosystems. We also discuss the approach of managing invasive species individually and suggest it may be more appropriate, when feasible, for the relatively intact uninhabited islands and dry regions of Galapagos. The more degraded highlands of the inhabited islands need a more complex approach that balances costs with prioritised outcomes for biodiversity and ecosystem functionality.