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Invaders of Pollination Networks in the Galápagos Downloaded from rspb.royalsocietypublishing.org on March 14, 2013 Invaders of pollination networks in the Gala´pagos Islands: emergence of novel communities rspb.royalsocietypublishing.org Anna Traveset1, Ruben Heleno1,2,3, Susana Chamorro1,3, Pablo Vargas4, Conley K. McMullen5, Rocı´o Castro-Urgal1, Manuel Nogales6, Henri W. Herrera3 and Jens M. Olesen7 1Laboratorio Internacional de Cambio Global (LINC-Global), Institut Mediterrani d’Estudis Avanc¸ats (CSIC-UIB), Research Miquel Marque´s 21, 07190 Esporles, Mallorca, Balearic Islands, Spain 2Centre for Functional Ecology, Department of Life Sciences, University of Coimbra, Coimbra, Portugal 3 Cite this article: Traveset A, Heleno R, Charles Darwin Foundation, Puerto Ayora, Santa Cruz, Gala´pagos, Ecuador 4Real Jardı´n Bota´nico (CSIC-RJB), Madrid, Spain Chamorro S, Vargas P, McMullen CK, 5Department of Biology, James Madison University, Harrisonburg, VA, USA Castro-Urgal R, Nogales M, Herrera HW, Olesen 6Instituto de Productos Naturales y Agrobiologı´a (CSIC-IPNA), Tenerife, Canary Islands, Spain JM. 2013 Invaders of pollination networks in 7Department of Bioscience, Aarhus University, Aarhus, Denmark the Gala´pagos Islands: emergence of novel communities. Proc R Soc B 280: 20123040. The unique biodiversity of most oceanic archipelagos is currently threatened by the introduction of alien species that can displace native biota, disrupt http://dx.doi.org/10.1098/rspb.2012.3040 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 Gala´pagos Islands. Twenty per cent of all species (60 plants and 220 pollinators) in the pooled network were aliens, Received: 20 December 2012 being involved in 38 per cent of the interactions. Most aliens were insects, Accepted: 18 February 2013 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. Subject Areas: Moreover, they infiltrated all seven connected modules (determined by geo- graphical and phylogenetic constraints) of the overall network, representing ecology, plant science, environmental science around 30 per cent of species in two of them. An astonishingly high pro- portion (38%) of connectors, which enhance network cohesiveness, was also Keywords: alien. Results indicate that the structure of these emergent novel communities biological invasions, insect and vertebrate might become more resistant to certain type of disturbances (e.g. species loss), pollination, modularity, mutualistic while being more vulnerable to others (e.g. spread of a disease). Such notable interactions, nestedness, oceanic islands changes in network structure as invasions progress are expected to have important consequences for native biodiversity maintenance. Author for correspondence: Anna Traveset 1. Introduction e-mail: [email protected] Islands house a large proportion of global biodiversity. However, much of it is threatened by habitat degradation and loss, exploitation of natural resources and introduction of alien species [1–3]. The impact of alien species is especially severe on islands rich in endemic species [2,4]. As island species are being lost, so are their interactions with other species, initiating cascading effects through entire com- munities [5–7]. Nevertheless, most conservation and restoration projects on islands fail to incorporate interactions as indicators of ecosystem functions, particularly plant–animal mutualisms such as pollination and seed dispersal [8–10]. Animal pollination is essential to the reproductive success of most plant species, and, as such, is crucial to the maintenance of diversity and functioning Electronic supplementary material is available of terrestrial ecosystems [5,11]. There are a few general patterns of pollination net- at http://dx.doi.org/10.1098/rspb.2012.3040 or works on oceanic islands, which include: (i) small network size; (ii) strong via http://rspb.royalsocietypublishing.org. dominance of one or a few taxa and a scarcity or absence of certain groups (e.g. insect pollinators with long proboscises, bees); (iii) low ratio between species richness of pollinators and plants; (iv) dominance of plants with open and easily & 2013 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from rspb.royalsocietypublishing.org on March 14, 2013 accessible flowers, pollinated by either insects or vertebrates, N 2 Pinta especially birds and lizards; and (v) higher generalization rspb.royalsocietypublishing.org Proc R Soc B 280: 20123040 level than mainland networks, with some species even operat- ing as super-generalists or density compensators [12–14]. Small network size together with the presence of super-generalists result in highly connected networks (i.e. many potential inter- Santiago actions are also realized). Some of these network properties Fernandina actually facilitate the integration of alien species [15,16]. (a) Vulnerability of network structure to alien species The arrival of new species to islands may notably alter the struc- Santa Cruz ture and dynamics of their networks [9,16–19]. However, the San Cristóbal generality of this is still under debate, and our knowledge of km the mechanisms underlying the integration of alien species into 02550 native networks and their subsequent impact is still limited. Net- work analysis is a highly valuable tool in our effort to understand Figure 1. Map of the Gala´pagos Islands showing the study sites. Inset: location this process of integration, and to plan robust conservation and of Gala´pagos archipelago. restoration strategies [10,18,20]. A number of network metrics can inform us about the ability of communities to respond to var- ious kinds of environmental perturbations, and may easily be 2. Methods incorporated into conservation monitoring [20]. For example, (a) Study sites higher interaction diversity may increase the rates of ecosystem The Gala´pagos Islands lie on the Equator in the eastern Pacific, processes; in pollination networks, it may lead to larger seed 960 km to the west of the South American continent. This set because of increased functional complementarity [21]. Gener- young volcanic archipelago (0.035–4 Ma [32]) comprises 18 ally, integration of aliens into pollinator networks does not seem islands larger than 1 km2 and numerous islets. Arid zones dom- to affect overall connectance (but see [22]), although the number inate the lowland on all islands (around 60% of total land area); of interactions among natives may decline [16,23]. Likewise, they show the highest plant diversity and endemicity, and a rela- interaction evenness, which measures the uniformity in the dis- tively low fraction of alien plant species compared with the tribution of interaction frequencies and is inversely related to transition and humid zones [29]. The Gala´pagos flora consists network stability [24], may decrease with higher invasion inten- of 557 native vascular species, of which 32 per cent are endemic, and an additional 825 (approx. 60%) aliens [30]. sity [18]. Level of invasion may also reduce species specialization A recent study has reviewed all known plant–pollinator (d0)ofnativespecies[19],implyingthattheybecomelessselec- interactions in the archipelago [33]. Only one of them, performed tive in their choice of mutualists by being compelled to interact at Isabela Island, involved a network analysis of pollination with the most abundant aliens as invasion progresses. Invaders interactions [34]. These authors found high connectance, nested- can also induce changes in levels of network nestedness [16,25] ness (‘asymmetrical pattern of number of interactions per and modularity [25]; both link patterns are also diagnostic species’), higher pollinator than plant linkage level and high signs of network stability [26,27]. Hence, invaded networks dependence of seed production on insect visits. However, the couldbemorestable,becauseofalowerinteractionevenness ratio between pollinator and plant species was only 0.5, which and specific changes in nestedness and modularity, making is very low, indicating that the study site was very poor in restoration more difficult [22,28]. insects, even for an insular environment [14]. We built a lowland pollination network for each of five islands (figure 1), differing in age and degree of disturbance, from young- (b) The threatened Gala´pagos ecosystems est/pristine to oldest/disturbed: Fernandina (0.035–0.07 Ma), Pinta Over the last century, the unique Gala´pagos ecosystems have (earlier than 0.7 Ma, undetermined maximum), Santiago (0.8– become jeopardized by the effects of globalization. Humans 1.4 Ma), Santa Cruz (1.1–2.3 Ma) and San Cristo´bal (2.4–4 Ma) [32]. have increasingly settled on the islands, mediating the establish- ment of many aliens [29]. The number of alien plants has (b) Observation of pollinators increased exponentially, currently forming 60 per cent of the vas- In February 2010 and 2011, during the peak of the flowering cular flora [30]. Likewise, around 500 insect species (representing season, we collected data on visitation interactions to flower- 25% of all Gala´pagos insect species) have been introduced, a ing plants in the arid zone of each island. Upon arrival to each number continuously growing [31].
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