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Abstract and Figures

The typical generalist diet of most seed dispersers opens a window of opportunity to the invasion of alien plants. Fleshy-fruits show a diverse combination of traits that allow them to interact with seed dispersers. The outcome of the new relationships established between alien plant species and native fruit-eating animals depends both on attributes of the invader and of the mutualist partners in the native community. Two contrasting hypotheses attempt to explain the integration of exotic species in native communities. Darwin’s naturalization hypothesis (DNH) proposes that alien species that are more different from native species are more likely to integrate in the community. The similarity hypothesis (SH) proposes the opposite idea, that is: alien species that are more similar to native species are more likely to integrate the native community. By comparing chemical and morphological traits of 11 alien and 49 native fleshy-fruited species, we tested DNH and SH as assembly rules of alien species in subtropical Andean forests. We did not find differences in most chemical or morphological traits betweenf alien and native fruit species.. The multidimensional variation of alien fruit traits was nested within that of native species. However, alien fruits tended to score high in the range of variation of native chemical traits, suggesting that fruit-eating birds could promote the dispersal of alien species that display high values ot the traits selected by birds. The striking similarity in fruit traits between alien and native species highlights the potential role of seed dispersers as ecological filters of the invasion of alien plants. In turn, this similarity suggests that alien fruits can be functionally equivalent to native ones in terms of their interaction with fruit-eating birds.
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Being popular or freak: how alien plants integrate
into native plant-frugivore networks
Tobias Nicolas Rojas .Marı
´a Cecilia Fa
´tima Gallo .David Lautaro Vergara-Tabares .
´a Gabriela Nazaro .Iris Catiana Zampini .Marı
´a Ine
´s Isla .
Pedro G. Blendinger
Received: 30 May 2018 / Accepted: 27 April 2019 / Published online: 2 May 2019
Springer Nature Switzerland AG 2019
Abstract The generalist diet of most frugivores
opens a window of opportunity to the invasion of alien
plants whit fleshy-fruits. The outcome of the new
relationships between alien plants and native frugi-
vores depends both on traits of the invaders and of the
mutualist partners in the recipient community. Two
contrasting hypotheses attempt to explain the integra-
tion of alien species in native communities. ‘‘Darwin’s
naturalization hypothesis’’ proposes that alien species
more different from native species are more likely to
integrate in the community. The ‘‘similarity hypoth-
esis’’ proposes the opposite, that alien species more
similar to native species are more likely to integrate
the native community. By comparing chemical and
morphological traits of 12 alien and 48 native fleshy-
fruited species, we tested both hypothesis as assembly
rules of alien species in subtropical Andean forests.
We did not find differences in most chemical or
morphological traits between alien and native fruit
species. The multidimensional variation of alien fruit
traits was nested within that of native species.
However, alien fruits tended to score high in the range
of variation of native chemical traits. Accordingly, we
propose the ‘‘fraction similarity hypothesis’’ as a main
Electronic supplementary material The online version of
this article ( con-
tains supplementary material, which is available to authorized
T. N. Rojas (&)M. G. Nazaro P. G. Blendinger
Instituto de Ecologı
´a Regional, Universidad Nacional de
´n & CONICET, CC 34, 4107 Yerba Buena,
´n, Argentina
M. C. F. Gallo
Instituto de Biotecnologı
´a Farmace
´utica Y Alimentaria,
Universidad Nacional de Tucuma
´n & CONICET, Av.
Kirchner 1900, 4000 San Miguel de Tucuma
´n , Tucuma
D. L. Vergara-Tabares
Instituto de Diversidad Y Ecologı
´a Animal, Universidad
Nacional de Co
´rdoba & CONICET, Ve
´lez Sarsfield 299,
5000 Co
´rdoba, Argentina
I. C. Zampini M. I. Isla
Instituto de Bioprospeccio
´n Y Fisiologı
´a Vegetal,
Universidad Nacional de Tucuma
´n & CONICET, San
Lorenzo 1469, 4000 San Miguel de Tucuma
´n, Tucuma
I. C. Zampini M. I. Isla P. G. Blendinger
Facultad de Ciencias Naturales e Instituto Miguel Lillo,
Universidad Nacional de Tucuma
´n, Miguel Lillo 2005,
4000 San Miguel de Tucuma
´n, Tucuma
´n, Argentina
Biol Invasions (2019) 21:2589–2598,-volV)(0123456789().,-volV)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... In fact, fruit traits and density are important factors that shape structural organization of frugivory networks [31] . Therefore, understanding how invasive plant species are connected within native frugivory networks and how the characteristics of their fruits affect their importance within such networks can be crucial to understanding biological invasions and to predicting how and why species will invade certain regions [32,33] . ...
... In this sense, we also found no evidence that frugivore species interact more strongly with plants of a given status since native and invasive plant species establish interactions with similar frugivore species, but native plants interact with a larger group of frugivores than invasive species. These results are in accordance with the ''Fraction Similarity Hypothesis'', which predicts that the success of invasive species in an environment benefit from existing native mutualistic interactions [33] . In other words, fruits of invasive plant species should exhibit the same characteristics as native species and, therefore, would be functionally equivalent to fruit-eating birds. ...
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Although biological invasions are a common and intensively studied phenomenon, most studies often ignore the biotic interactions that invasive species play in the environment. Here, we evaluated how and why invasive plant species are interconnected within the overall frugivory network of the Brazilian Atlantic Forest, an important global biodiversity hotspot. To do this, we used the recently published Atlantic Frugivory Dataset to build a meta-network (i.e., a general network made of several local networks) that included interactions between 703 native and invasive plant species and 331 frugivore species. Using tools derived from complex network theory and a bootstrap simulation approach, we found that the general structure of the Atlantic Forest frugivory network (i.e., nestedness and modularity) is robust against the entry of invasive plant species. However, we observed that invasive plant species are highly integrated within the frugivory networks, since both native and invasive plant species play similar structural roles (i.e., plant status is not strong enough to explain the interactive roles of plant species). Moreover, we found that plants with smaller fruits and with greater lipid content play a greater interactive role, regardless of their native or invasive status. Our findings highlight the biotic homogenization involving plant-frugivore interactions in the Atlantic Forest and that the impacts and consequences of invasive plant species on native fauna can be anticipated based on the characteristics of their fruits.
... The invasion process and success of avian-dispersed invasive alien plants are influenced by plant morphological (Gosper and Vivian-Smith 2009), chemical Blendinger et al. 2016) and phenological traits (Marciniak et al. 2020;Nogueira et al. 2020). Certain traits favour bird-fruit interaction and allow plants to integrate into native seed-dispersal networks (Rojas et al. 2019;Marciniak et al. 2020). For example, plants that produce large fruit crop sizes have a high potential to be consumed by birds (Blendinger and Villegas 2011). ...
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Invasive alien plant species have been identified as a major threat to biodiversity and the relationship with native avian dispersers may increase their invasion potential. The impact of invasive plant species needs to be quantified using comparable assessment tools across different habitats and species to allocate limited resources to high-priority species. Here, we used the Generic Impact Scoring System (GISS) to assess the impacts of 16 fleshy-fruited alien invasive plant species in South Africa generally dispersed by native avian species. The results showed that fleshy-fruited invasive species have both environmental and socio-economic impacts. The cumulated impact scores for lantana ( Lantana camara ) and the tree of heaven ( Ailanthus altissima ) were the highest, with scores of 42 and 32, respectively. Some species, such as white mulberry ( Morus alba ), camphor tree ( Cinnamomum camphora ), American bramble ( Rubus cuneifolius ) and Brazilian pepper tree ( Schinus terebinthifolius ), had low overall impact scores of 8, 18, 14 and 16, respectively, but scored the maximum impact of 5 for certain mechanisms. Environmental impacts of fleshy-fruited invasive plant species had a high impact magnitude through effects on the ecosystem and vegetation. Socio-economic impacts were mainly through effects on forest production, agriculture and human health. Species with large crop sizes, small seeds and fruit sizes had higher environmental and socio-economic impact magnitude. The information generated in this study is important for guiding resource allocation and preventing the uncontrolled introduction of invasive species in South Africa. The impact of the fleshy-fruited invasive species transcended sectors and, therefore, effective management of invasive species will require the collaboration of multiple and inter-sectoral stakeholders in South Africa.
Vascular epiphytes are an important component of the flora of subtropical regions, but they remain understudied compared to tropical regions. Subtropical montane region of Yungas in Argentina has high epiphyte diversity, but information on epiphytes remain in little disseminated sources such as herbariums, theses and publications not available on the web. The objective of this study was to describe the distribution and diversity of epiphytes and to review ecological research on epiphytes in Yungas of northwestern Argentina. Occurrence records of epiphytes were compiled to prepare a floristic list, to describe spatial bias, and latitudinal and altitudinal patterns. There are 168 epiphyte species in Argentinian Yungas, which belong mainly to the families Orchidaceae, Bromeliaceae, and Polypodiaceae. Most species are holoepiphytes and facultative epiphytes (83%), and the rest are trees, herbs, and shrubs that occasionally occur as epiphytes. The species richness of the 14 most abundant epiphyte species in this region peaks at 1500 m, and decreases at higher and lower elevations. Most trees with a diameter at breast height ≥ 10 cm (62.2%) are epiphyte hosts, and epiphytes are most diverse in larger than in smaller native trees of this region. Species richness and cover of epiphytes increased with the diameter at breast height of Ocotea porphyria, the most important host tree for epiphytes in this region. It is expected that this study will serve to acknowledge the high diversity of epiphytes in the region and identify gaps in knowledge for new sampling and studies.
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For alien invasive plant species dependent on frugivores for seed dispersal, traits that influence consumption can be important determinants of invasion and spread. However, trait comparisons between native and invasive species have documented mixed results. In Hawai‘i, one of the most invaded systems in the world, nearly all frugivory, and thus seed dispersal, is dependent on non-native birds. Moreover, the majority of dispersal events also involve invasive plants, suggesting the potential for an “invasional meltdown”. Here we compare fruit and seed traits between native and invasive plants and evaluate how those traits influence consumption by non-native avian frugivores. Although we found that most traits examined were similar between native and invasive fruiting species, invasive species tended to have higher fruit protein content, longer fruiting duration, were less likely to have orange fruits, and have less variable seed length. Longer fruiting duration and smaller seed size were important predictors for avian frugivore consumption. In combination, these results suggest that traits that increase probability of encounter (fruiting duration) and ability to be consumed (seed size) are more important for dispersal by frugivores than traits associated with fruit preferences and, thus, are driving the spread of invasive species and limiting dispersal of some native species. Further, we document an apparent seed size threshold for avian consumption (~ 7.0 mm), supporting previous work suggesting that large seeded species, particularly native plant species adapted for extinct large-bodied frugivores, are likely dispersal limited based on gape size limitation of the current non-native frugivore community.
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Biotic interactions and mutualisms in particular have an important role in ecosystem structure and functioning as well as in the maintenance of biodiversity. Understanding how communities respond to the introduction of non-native species and what determines the establishment of novel interactions between native and introduced species will help in determining the potential impacts of biological invasions. The aims of this work were to assess patterns of frugivory and fruit removal in environments with invasion of non-native fleshy-fruited plants and to evaluate whether novel associations between native frugivores and non-native plants are determined by fruit traits. For this we selected eight study sites in areas with different degrees of invasion of non-native fleshy-fruited plants. In each site, we measured fruit availability and fruit traits of native and non-native plants. In addition, we conducted direct frugivory observations. We found that native and non-native fruits differed based on morphological trait variables, such as fruit weight and dimensions. Only two birds, Elaenia albiceps (smaller and migrant) and Turdus falcklandii (bigger and resident), are the main frugivorous present in the area. At the scale of the community of frugivores, neither visit nor fruit removal rates differ between natives and non-natives. However, at the species scale, while E. albiceps preferentially foraged on native plants, T. falcklandii preferred non-natives. Thus, some generalist frugivorous species like T. falcklandii can play a key role in promoting the invasion of non-native plants.
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Ligustrum lucidum is a highly invasive East Asian tree that successfully colonizes several subtropical and temperate areas around the world. Its invasion capacity results from a widespread human use mostly in urban and periurban settings, very abundant fruit and seed production, small bird-dispersed fruits, high germination rates, resprouting capacity, fast growth rates, low herbivory levels and tolerance to a wide range of light, temperature and soil. All these traits contribute to its ability to rapidly increase in abundance, alter biodiversity, landscape ecology and limit its management. This paper reviews the current knowledge on L. lucidum with particular focus on its uses, distribution, invasiveness, ecological and economic impacts and control measures. Most relevant aspect of the review highlight the negative ecological impacts of L. lucidum, its potential to continue expanding its range of distribution and the need of further studies on the eco-physiology of the species, economic impact and social perception of its invasion and early warning systems.
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Aim Alternative hypotheses of Darwin's Naturalization Conundrum (DNC) predict that the non‐native species that successfully establish within a community are those either more closely or more distantly related to the resident native species. Despite the increasing number of studies using phylogenetic data to test DNC and evaluate community assembly, it remains unknown whether phylogenetic relationships alone can be used to predict invasion susceptibility across communities differing environmentally and in disturbance history. In this study, we evaluate whether phylogenetic structure of diverse native communities predicts the occurrence of non‐native species and offers insight into community assembly. Location Eastern United States of America. Methods We examine multiple communities across a north–south transect of the eastern United States to test whether non‐native species richness and abundance are associated with phylogenetic diversity measures of the native community. We also test whether non‐native species are consistently closely or distantly related to native species using two approaches differing in phylogenetic scale and whether this differs with ecologically successful species. Results Our analyses did not unambiguously resolve DNC. Non‐native species richness and abundance decreased with increasing native species phylogenetic diversity. Within some communities, non‐native species were significantly more closely related to native species than expected by chance, and tended to be more often closely related to a native species than that native species was to other native relatives. When considering species abundance, only one community showed that ecologically successful non‐native species were closely related to resident species. Main conclusions Phylogenetic relationships can reveal important details about community assembly in diverse ecological settings. However, given the multifaceted nature of community assembly, phylogenetic metrics alone have limited utility as a general predictive tool for community invasion. Our study highlights a need to incorporate additional types of data to better understand why some communities are more susceptible to non‐native species establishment.
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Ecological interactions have been acknowledged to play a key role in shaping biodiversity. Yet a major challenge for evolutionary biology is to understand the role of ecological interactions in shaping trait evolution when progressing from pairs of interacting species to multispecies interaction networks. Here we introduce an approach that integrates coevolutionary dynamics and network structure. Our results show that non-interacting species can be as important as directly interacting species in shaping coevolution within mutualistic assemblages. The contribution of indirect effects differs among types of mutualism. Indirect effects are more likely to predominate in nested, species-rich networks formed by multiple-partner mutualisms, such as pollination or seed dispersal by animals, than in small and modular networks formed by intimate mutualisms, such as those between host plants and their protective ants. Coevolutionary pathways of indirect effects favour ongoing trait evolution by promoting slow but continuous reorganization of the adaptive landscape of mutualistic partners under changing environments. Our results show that coevolution can be a major process shaping species traits throughout ecological networks. These findings expand our understanding of how evolution driven by interactions occurs through the interplay of selection pressures moving along multiple direct and indirect pathways.
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Dispersal abilities of invading species emerge from the interaction between the species and some features of the target community. Ligustrum lucidum is a tree species invading different ecosystems. Major spatial patterns of Ligustrum invasions and their ecological consequences have been analyzed, but no study addressed the dispersal process at a fine scale, assessing the effects of different biological and environmental factors. Ligustrum lucidum is an ornithochoric species. The structure of the environment determines bird movements and thus affects seed dispersal. We used inverse modeling to analyze bird-mediated dispersal of L. lucidum seeds in a secondary Yungas forest and surrounding crop-fields. We assessed the effects of egestion mode (regurgitation and defecation) and tree density (as an environment character) on seed dispersal. Seed dispersal presented different spatial patterns depending on the egestion mode. Tree density was positively associated with the number of regurgitated dispersed seeds and negatively associated with the number of defecated dispersed seeds. In both cases, dispersal distance increased in open areas, but absence of perches inhibited seed arrival. Thus, spread of L. lucidum is facilitated in open areas with some trees; inside the native forest, short distance dispersal facilitates the gradual invasion by this exotic species. Our results suggest that processes like crop abandonment and forest succession, which are active in subtropical montane systems, may facilitate L. lucidum invasion. Our seed dispersal models should be combined with actual distribution maps of L. lucidum to identify areas vulnerable to new invasions.
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A frequent question in invasion ecology is whether the traits of alien plant species differ from natives. This question is increasingly addressed at the plant community scale to assess the role trait differences play in community assembly. Nevertheless, there remains considerable debate as to the value of native vs. alien trait comparisons. Recommendations are made to address seven conceptual and methodological limitations in current approaches used to assess trait differences between native and alien plants: account for spatial scale dependence, make an informed choice of traits, evaluate multiple trait dimensions, incorporate intraspecific trait variation, use appropriate null models, examine environmental gradients, and assess temporal variation in trait spectra. Tackling these limitations will dramatically improve the value of native vs. alien trait comparisons. Traits should be selected based on expectations of abiotic and/or biotic constraints. Phylogenetic distances can provide valuable insights but are no substitute for the measurement of individual traits when contrasting alien and native species. An ideal set of traits would include one or more leaf, stem, seed and root traits as well as flowering phenology and plant height at maturity. Comparisons of intraspecific trait variation among native and alien species within the same plant community are rare but could improve predictions of interspecific competition and the response of communities to plant invasions. The full plant community should be examined rather than selected species subsets and comparisons between native and alien species traits are better undertaken at a neighbourhood scale. The frequency distribution of alien and native species traits may change over time through competitive exclusion as well as contemporary evolution. Repeated surveys of species abundances and traits are required to understand the consequences of trait differences between aliens and natives for plant community assembly. Analyses of the role of species traits in plant invasions need to quantify differences in a priori identified traits within communities along suitable environmental gradients and test hypothetical trait patterns against appropriate null expectations. The infrequent application of such approaches may explain the limited generalisations regarding the role of trait differences between native and alien species in the invasion of plant communities. A plain language summary is available for this article.
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In visually-driven seed dispersal mutualisms, natural selection should promote plant strategies that maximize fruit visibility to dispersers. Plants might increase seed dispersal profitability by increasing conspicuousness of fruit display, understood as a plant strategy to maximize fruit detectability by seed dispersers. The role of different plant traits in fruit choice and consumption by seed dispersers has been broadly studied. However, there is no clear evidence about the importance of the traits that increase conspicuousness of fruit display. Because strategies to maximize conspicuousness of fruit display are diverse, and usually are expected to be costly, we would expect that individual plant species will produce an efficient combination of traits. We explored this prediction with 62 fleshy-fruited plant species of a subtropical Andean forest (Southern Yungas), and using a large dataset of fruit consumption by birds (4,476 records). Conspicuousness of fruit display was characterized by both fruit and plant traits including chromatic contrast, size, exposure, aggregation, and crop size of fruits. We also considered phylogenetic effects on phenotypic variation. Fruit consumption was explained by fruit chromatic contrast depending on fruit crop size. These traits revealed low phylogenetic effects, with the exception of four plant clades at different levels in the phylogenetic tree. Negative correlations between pairs of traits support our assumption that fruit display traits are costly, suggesting natural selection favours parsimonious evolutionary pathways. Plant species seem to rely on conspicuousness of fruit display by a combination of traits that might minimize costs of fruit display. This appears adaptively relevant to improve communication with mutualistic animals, to increase fruit consumption in a community context and, ultimately, to enhance the profitability of seed dispersal.
Biological invasion remains a major threat to biodiversity in general and a dis-ruptor to mutualistic interactions in particular. While a number of empirical studies have directly explored the role of invasion in mutualistic pollination networks, a clear picture is yet to emerge and a theoretical model for comprehension still lacking. Here, using an eco-evolutionary model of bipartite mutu-alistic networks with trait-mediated interactions, we explore invader trait, propagule pressure, and network features of recipient community that contribute importantly to the success and impact of an invasion. High level of invasiveness is observed when invader trait differs from those of the community average, and level of interaction generalization equals to that of the community average. Moreover, multiple introductions of invaders with declining propagules enhance invasiveness. Surprisingly, the most successful invader is not always the one having the biggest impact on the recipient community. The network structure of recipient community, such as nestedness and modularity, is not a primary indicator of its invasibility; rather, the invasibility is best correlated with measurements of network stability such as robustness, resilience, and disrup-tiveness (a measure of evolutionary instability). Our model encompasses more general scenarios than previously studied in predicting invasion success and impact in mutualistic networks, and our results highlight the need for coupling eco-evolutionary processes to resolve the invasion dilemma.
1. Interactions between resource and consumer species result in complex ecological networks. The overall structure of these networks is often stable in space and time, but little is known about the temporal stability of the functional roles of consumer species in these networks. 2. We used a trait-based approach to investigate whether consumers (frugivorous birds) show similar degrees of functional specialisation on resources (plants) in ecological networks across seasons. We additionally tested whether closely related bird species have similar degrees of functional specialisation and whether birds that are functionally specialised on specific resource types within a season are flexible in switching to other resource types in other seasons. 3. We analysed four seasonal replicates of two species-rich plant–frugivore networks from the tropical Andes. To quantify fruit preferences of frugivorous birds, we projected their interactions with plants into a multidimensional plant trait space. To measure functional specialisation of birds, we calculated a species’ functional niche breadth (the extent of seasonal plant trait space utilised by a particular bird) and functional originality (the extent to which a bird species’ fruit preference functionally differs from those of other species in a seasonal network). We additionally calculated functional flexibility, i.e. the ability of bird species to change their fruit preference across seasons in response to variation in plant resources. 4. Functional specialisation of bird species varied more among species than across seasons, and phylogenetically similar bird species showed similar degrees of functional niche breadth (phylogenetic signal λ = 0·81) and functional originality (λ = 0·89). Additionally, we found that birds with high functional flexibility across seasons had narrow functional niche breadth and high functional originality per season, suggesting that birds that are seasonally specialised on particular resources are most flexible in switching to other fruit resources across seasons. 5. The high flexibility of functionally specialised bird species to switch seasonally to other resources challenges the view that consumer species rely on functionally similar resources throughout the year. This flexibility of consumer species may be an important, but widely neglected mechanism that could potentially stabilise consumer–resource networks in response to human disturbance and environmental change.