Invasion of pollination networks on oceanic islands: importance of invader complexes and endemic super generalists

Abstract. The structure of pollination networks is described for two oceanic islands, the Azorean Flores and the Mauritian Ile aux Aigrettes. At each island site, all interactions between endemic, non-endemic native and introduced plants and pollinators were mapped. Linkage level, i.e. number of species interactions per species, was significantly higher for endemic species than for non-endemic native and introduced species. Linkage levels of the two latter categories were similar. Nine types of interaction may be recognized among endemic, non-endemic native and introduced plants and pollinators. Similar types had similar frequencies in the two networks. Specifically, we looked for the presence of 'invader complexes' of mutualists, defined as groups of introduced species interacting more with each other than expected by chance and thus facilitating each other's establishment. On both islands, observed frequencies of interactions between native (endemic and non-endemic) and introduced pollinators and plants differed from random. Introduced pollinators and plants interacted less than expected by chance. Thus, the data did not support the existence of invader complexes. Instead, our study suggested that endemic super-generalist species, i.e. pollinators or plant species with a very wide pollination niche, include new invaders in their set of food plants or pollinators and thereby improve establishment success of the invaders. Reviewing other studies, super generalists seem to be a widespread island phenomenon, i.e. island pollination networks include one or a few species with a very high generalization level compared to co-occurring species. Low density of island species may lead to low interspecific competition, high abundance and ultimately wide niches and super generalization.     

Shifts in Species Interactions Due to the Evolution of Functional Differences between Endemics and Non-Endemics: An Endemic Syndrome Hypothesis

Species ranges have been shifting since the Pleistocene, whereby fragmentation, isolation, and the subsequent reduction in gene flow have resulted in local adaptation of novel genotypes and the repeated evolution of endemic species. While there is a wide body of literature focused on understanding endemic species, very few studies empirically test whether or not the evolution of endemics results in unique function or ecological differences relative to their widespread congeners; in particular while controlling for environmental variation. Using a common garden composed of 15 Eucalyptus species within the subgenus Symphyomyrtus (9 endemic to Tasmania, 6 non-endemic), here we hypothesize and show that endemic species are functionally and ecologically different from non-endemics. Compared to non-endemics, endemic Eucalyptus species have a unique suite of functional plant traits that have extended effects on herbivores. We found that while endemics occupy many diverse habitats, they share similar functional traits potentially resulting in an endemic syndrome of traits. This study provides one of the first empirical datasets analyzing the functional differences between endemics and non-endemics in a common garden setting, and establishes a foundation for additional studies of endemic/non-endemic dynamics that will be essential for understanding global biodiversity in the midst of rapid species extinctions and range shifts as a consequence of global change.     

Dispersal ability of island endemic plants: What can we learn using multiple dispersal traits?

Island endemic species are expected to have lower dispersal ability than their non-endemic congeners. Several studies have demonstrated differences in diaspore morphology between endemic species and their non-endemic congeners. It is, however, relatively difficult to translate the differences in morphology of the diaspores into differences in dispersal ability. To avoid this problem, we measured directly dispersal values (anemo-, hydro-, exozoo- and endozoo-chory) of 27 pairs of closely related endemic and non-endemic species from Canary Islands. We did not explicitly support the hypothesis about the loss of dispersal ability of island species. The comparison of pairs of endemic and non-endemic species showed the reduction in dispersal potential only for endozoochory. In many cases, endemic species had, in fact, the same or better dispersal ability than their non-endemic congeners. Higher dispersal ability of endemic species could have been evolved as a consequence of species subsequent dispersal to neighboring islands. As a support for this we found that the endemic species dispersing better than their non-endemic congeners also occupy more islands within the archipelago. We conclude that reduction of dispersal ability of species on islands may not be as general as previously expected and we need to take into account multiple species traits to understand the possible evolution of species dispersal potential.     

A random process may control the number of endemic species

The richness of endemic species is often recognized as an indication of the distinctiveness of certain local faunas and is used for the definition of conservation hotspots as well. Faunas of different animal taxa were considered in sets of contiguous geographical units. Comparing the faunas of different units in one set, we found an exponential increase in the number of endemics when plotted against the number of non-endemics. A model of independent stochastic population dynamics under the control of environmental oscillations produces random fluctuations in the ranges of species. Ranges of endemic species are supposedly narrower than ranges of co-occurring non-endemic species. In such a case, the flow of a random process leads to an exponential relationship between numbers of co-occurring endemic and non-endemic species. This process also produces an apparent positive correlation between total species number and the percentage of endemics.     

Isolation‐driven functional assembly of plant communities on islands

The physical and biotic environment is often considered the primary driver of functional variation in plant communities. Here, we examine the hypothesis that spatial isolation may also be an important driver of functional variation in plant communities where disturbance and dispersal limitation may prevent species from occupying all suitable habitats. To test this hypothesis, we surveyed the vascular plant composition of 30 islands in the Gulf of Maine, USA, and used available functional trait and growth form data to quantify the functional composition of these islands. We categorized species based on dispersal mode and used a landscape metric of isolation to assess the potential role of dispersal limitation as a mechanism of isolation‐driven assembly. We tested for island and species level effects on functional composition using a hierarchical Bayesian framework to better assess the causal link between isolation and functional variation. Growth form composition and the community mean value of functional traits related to growth rate, stress tolerance, and nutrient use varied significantly with island isolation. Functional traits and growth forms were significantly associated with dispersal mode, and spatial isolation was the strongest driver of primary trait variation, while island properties associated with environmental drivers in our system were not strong predictors of trait variation. Despite the species‐level association of dispersal mode and functional traits, dispersal mode only accounted for a small proportion of the overall isolation effect on community‐level trait variation. Our study suggests that spatial isolation can be a key driver of functional assembly in plant communities on islands, though the role of particular dispersal processes remains unclear.     

The ecological causes of functional distinctiveness in communities

Recent work has shown that evaluating functional trait distinctiveness, the average trait distance of a species to other species in a community offers promising insights into biodiversity dynamics and ecosystem functioning. However, the ecological mechanisms underlying the emergence and persistence of functionally distinct species are poorly understood. Here, we address the issue by considering a heterogeneous fitness landscape whereby functional dimensions encompass peaks representing trait combinations yielding positive population growth rates in a community. We identify four ecological cases contributing to the emergence and persistence of functionally distinct species. First, environmental heterogeneity or alternative phenotypic designs can drive positive population growth of functionally distinct species. Second, sink populations with negative population growth can deviate from local fitness peaks and be functionally distinct. Third, species found at the margin of the fitness landscape can persist but be functionally distinct. Fourth, biotic interactions (positive or negative) can dynamically alter the fitness landscape. We offer examples of these four cases and guidelines to distinguish between them. In addition to these deterministic processes, we explore how stochastic dispersal limitation can yield functional distinctiveness. Our framework offers a novel perspective on the relationship between fitness landscape heterogeneity and the functional composition of ecological assemblages.     

Island biogeography extends to small-scale habitats: low competitor density and richness on islands may drive trait variation in nonnative plants

Previous island biogeography studies have quantified species richness on the scale of entire islands rather than smaller scales relevant to plant-to-plant competitive interactions. Further, they have not accounted for density compensation. Using mainland and island sites along the New England coast, we asked two questions. First, are both richness and density lower in small-scale habitats within islands than in similar mainland habitats? Second, do differences in competitor richness and density drive post-establishment trait variation in nonnative plant species? We used field surveys and individual-based rarefaction to estimate richness and density in 100-m² plots and demonstrated that island sites have significantly fewer species and individuals per unit area than mainland sites. We then conducted a field study in which we removed competing neighbors from nonnative plant individuals and found that when competitors were removed, individuals in low-competition environments demonstrated a lesser increase in vegetative growth but a greater increase in reproductive effort and herbivore tolerance relative to mainland individuals whose neighbors were also removed. We found that the central concept of island biogeography, i.e., that islands host fewer species than comparable mainland habitats, can be extended to smaller-scale habitats and that this difference in competitive pressure between mainland and island habitats can act as a driver of trait variation in nonnative plants.     

Endemics and their common congener plant species on an East Mediterranean island: a comparative functional trait approach

Understanding evolution and ecology of endemic plants is of great importance for conservation of those rare and endangered species. Pairwise comparisons of plant functional traits could be an adequate method to get insights in evolutionary and ecological processes. We examined whether morphological traits representing competitive ability and habitat specificity differ between endemics and common plants. Therefore, we performed pairwise comparison analyses of 9 plant functional traits in 36 congeneric pairs of endemics and their common congeners on the East Mediterranean island of Cyprus, i.e., the first such study conducted on a Mediterranean island. We found that endemic species prefer higher elevations and more extreme habitats. Endemics were smaller and they had smaller flowers than their common congeners. Common species had higher chromosome numbers than endemic ones. Endemic and common species showed no significant differences in canopy height, inflorescence height, leaf length and width, and flowering period. Our study showed that the situation on a large oceanic island does not differ from results in mainland research areas.     

The biogeography and filtering of woody plant functional diversity in North and South America

Aim In recent years evidence has accumulated that plant species are differentially sorted from regional assemblages into local assemblages along local‐scale environmental gradients on the basis of their function and abiotic filtering. The favourability hypothesis in biogeography proposes that in climatically difficult regions abiotic filtering should produce a regional assemblage that is less functionally diverse than that expected given the species richness and the global pool of traits. Thus it seems likely that differential filtering of plant traits along local‐scale gradients may scale up to explain the distribution, diversity and filtering of plant traits in regional‐scale assemblages across continents. The present work aims to address this prediction. Location North and South America. Methods We combine a dataset comprising over 5.5 million georeferenced plant occurrence records with several large plant functional trait databases in order to: (1) quantify how several critical traits associated with plant performance and ecology vary across environmental gradients; and (2) provide the first test of whether the woody plants found within 1° and 5° map grid cells are more or less functionally diverse than expected, given their species richness, across broad gradients. Results The results show that, for many of the traits studied, the overall distribution of functional traits in tropical regions often exceeds the expectations of random sampling given the species richness. Conversely, temperate regions often had narrower functional trait distributions than their smaller species pools would suggest. Main conclusion The results show that the overall distribution of function does increase towards the equator, but the functional diversity within regional‐scale tropical assemblages is higher than that expected given their species richness. These results are consistent with the hypothesis that abiotic filtering constrains the overall distribution of function in temperate assemblages, but tropical assemblages are not as tightly constrained.     

Global analyses underrate part of the story: finding applicable results for the conservation planning of small Sardinian islets’ flora

Although many studies have addressed island biogeography, the biodiversity of very small islets has mostly been ignored due to the lack of high-resolution data. We analysed the vascular plant taxa distribution pattern of 81 satellite islets scattered around Sardinia, the second largest island in the Mediterranean Basin. Power models were used to determine the influence of environmental and anthropogenic factors on both endemic and non-endemic species richness. Analyses of the distribution pattern highlighted the high endemism rate in these islets. In addition, reliable results for conservation, such as correlations with land use diversity, climate and human presence, were found only when categorising the islets by their environmental characteristics instead of their geographical position. This study of a representative set of Mediterranean islets contributes to the knowledge base about the controversial role of very small islets in biological conservation. Large-scale analyses have often underrated their importance and we therefore suggest that local studies about their conservation planning are needed worldwide.     

Extensions of Island Biogeography Theory predict the scaling of functional trait composition with habitat area and isolation

The Theory of Island Biogeography (TIB) predicts how area and isolation influence species richness equilibrium on insular habitats. However, the TIB remains silent about functional trait composition and provides no information on the scaling of functional diversity with area, an observation that is now documented in many systems. To fill this gap, we develop a probabilistic approach to predict the distribution of a trait as a function of habitat area and isolation, extending the TIB beyond the traditional species–area relationship. We compare model predictions to the body‐size distribution of piscivorous and herbivorous fishes found on tropical reefs worldwide. We find that small and isolated reefs have a higher proportion of large‐sized species than large and connected reefs. We also find that knowledge of species body‐size and trophic position improves the predictions of fish occupancy on tropical reefs, supporting both the allometric and trophic theory of island biogeography. The integration of functional ecology to island biogeography is broadly applicable to any functional traits and provides a general probabilistic approach to study the scaling of trait distribution with habitat area and isolation.     

Patterns and traits of the endemic plants of Greece

Greece is characterized by high plant diversity (5800 species) and endemism (15.6%). This study attempts a first overall assessment of the taxonomy, distribution, traits and conservation status of the Greek endemic plants. The endemic species belong to 56 families and 242 genera. Most of the endemic plants have a narrow geographical and altitudinal distribution range. The southern floristic regions are richer in endemic species. The species area relationships for endemics (EARs) for island and continental floristic regions explain over 50% of the variation in number of species and are characterized by steep curves. Analysis of the distributional pattern of the endemics by similarity coefficients offers useful insights into the palaeogeography and biogeography of Greece. The endemic species occur at all altitudes, but the altitudinal distribution shows a predominance of local endemics at 0–600 m in the island regions and in higher zones in the continental regions. The life form spectra show a predominance of hemicryptophytes and chamaephytes. This trait seems indicative of their habitat and adaptive strategy and may be related to speciation processes. The overview of the conservation status of the Greek endemics indicates that over 40% of the taxa are threatened or near threatened. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 162 , 130–422.     

A comparative analysis of island floras challenges taxonomy‐based biogeographical models of speciation

Speciation on islands, and particularly the divergence of species in situ, has long been debated. Here, we present one of the first, complete assessments of the geographic modes of speciation for the flora of a small oceanic island. Cocos Island (Costa Rica) is pristine; it is located 550 km off the Pacific coast of Central America. It harbors 189 native plant species, 33 of which are endemic. Using phylogenetic data from insular and mainland congeneric species, we show that all of the endemic species are derived from independent colonization events rather than in situ speciation. This is in sharp contrast to the results of a study carried out in a comparable system, Lord Howe Island (Australia), where as much as 8.2% of the plant species were the product of sympatric speciation. Differences in physiography and age between the islands may be responsible for the contrasting patterns of speciation observed. Importantly, comparing phylogenetic assessments of the modes of speciation with taxonomy‐based measures shows that widely used island biogeography approaches overestimate rates of in situ speciation.     

High evolutionary and functional distinctiveness of endemic monocots in world islands

Functionally and evolutionarily distinct species have traits or an evolutionary history that are shared by few others in a given set, which make them priority species for biodiversity conservation. On islands, life in isolation has led to the evolution of many distinct forms and functions as well as to a high level of endemism. The aim of this study is to assess the evolutionary and functional distinctiveness of insular monocotyledons and their distribution across 126 islands worldwide. We show that evolutionary and functional distinctiveness are decoupled but that both are higher on islands than on continental areas. Anagenesis on islands followed by extinctions and/or diversification on the mainland may have led to highly evolutionarily distinct species while functionally distinct species may have arisen from ecological niche shift or niche expansion. Insular endemic species with high evolutionary distinctiveness but not with high functional distinctiveness are significantly range-restricted compared to less distinct species, possibly indicating differences in dispersal potential. By showing that distinctiveness is high on islands and that the most distinct species are range-restricted, our study has important conservation implications. Indeed, islands are among the most threatened systems of the world, and extinctions of the most distinct species could lead to significant loss of phylogenetic and functional diversity.

     

Relationship between maximum leaf photosynthesis,nitrogen content and specific leaf area in balearic endemic and non-endemic mediterranean species

Gas exchange parameters, leaf nitrogen content and specific leaf area (SLA) were measured in situ on 73 C3 and five C4 plant species in Mallorca, west Mediterranean, to test whether species endemic to the Balearic Islands differed from widespread, non-endemic Mediterranean species and crops in their leaf traits and trait inter-relationships. Endemic species differed significantly from widespread species and crops in several parameters; in particular, photosynthetic capacity, on an area basis (A), was 20 % less in endemics than in non-endemics. Similar differences between endemics and non-endemics were found in parameters such as SLA and leaf nitrogen content per area (Na). Nevertheless, most of the observed differences were found only within the herbaceous deciduous species. These could be due to the fact that most of the non-endemic species within this group have adapted to ruderal areas, while none of the endemics occupies this kind of habitat. All the species-including the crops-showed a positive, highly significant correlation between photosynthetic capacity on a mass basis (Am), leaf nitrogen content on a mass basis (Nm) and SLA. However, endemic species had a lower Am for any given SLA and Nm. Hypotheses are presented to explain these differences, and their possible role in reducing the distribution of many endemic Balearic species is discussed.     

Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities

Aim

Rare species typically contribute more to functional diversity than common species. However, humans have altered the occupancy and abundance patterns of many species—the basis upon which we define “rarity.” Here, we use a globally unique dataset from hydrothermal vents—an untouched ecosystem—to test whether rare species over‐contribute to functional diversity.

Location

Juan de Fuca Ridge hydrothermal vent fields, Northeast Pacific Ocean.

Methods

We first conduct a comprehensive review to set up expectations for the relative contributions of rare and common species to functional diversity. We then quantify the rarity and commonness of 37 vent species with relevant trait information to assess the relationship between rarity and functional distinctiveness—a measure of the uniqueness of the traits of a species relative to traits of coexisting species. Next, we randomly assemble communities to test whether rare species over‐contribute to functional diversity in artificial assemblages ranging in species richness. Then, we test whether biotic interactions influence functional diversity contributions by comparing the observed contribution of each species to a null expectation. Finally, we identify traits driving functional distinctiveness using a distance‐based redundancy analysis.

Results

Across functional diversity metrics and species richness levels, we find that both rare and common species can contribute functional uniqueness. Some species always offer unique trait combinations, and these species host bacterial symbionts and provide habitat complexity. Moreover, we find that contributions of species to functional diversity may be influenced by biotic interactions.

Main conclusions

Our findings show that many common species make persistent, unique contributions to functional diversity. Thus, it is key to consider whether the abundance and occupancy of species have been reduced, relative to historical baselines, when interpreting the contributions of rare species to functional diversity. Our work highlights the importance of testing ecological theory in ecosystems unaffected by human activities for the conservation of biodiversity.     

Woody species in resource‐rich microrefugia of granite outcrops display unique functional signatures

Refugia are key environments in biogeography and conservation. Because of their unique eco‐evolutionary formation and functioning, they should display distinct functional trait signatures. However, comparative trait‐based studies of plants in refugia and non‐refugia are lacking. Here, we provide a comparison between resource‐rich (putative microrefugia for species preferring mesic habitats under increasing aridity) and resource‐impoverished woodlands (non‐refugia) around two granite outcrops in south‐western Australia. We measured and compared six functional traits (bark thickness, foliar δ¹³C, foliar C:N, leaf dry matter content, plant height, specific leaf area) in four woody species. We performed multiple‐trait, multiple‐species and single‐trait, within‐species analyses to test whether plants in resource‐rich habitats were functionally distinct and more diverse than those in the surrounding resource‐impoverished woodlands. We found that species in resource‐rich woodlands occupied larger and distinct multiple‐trait functional spaces and showed distinct single‐trait values (for specific leaf area and bark thickness). This suggests that plants in resource‐rich woodlands can deploy unique and more diverse ecological strategies, potentially making these putative microrefugia more resilient to environmental changes. These findings suggest that species in microrefugia may be characterised by unique functional signatures, illustrating the utility of comparative trait‐based approaches to improve understanding of the functioning of refugia.     

A roadmap to plant functional island biogeography

Island biogeography is the study of the spatio-temporal distribution of species, communities, assemblages or ecosystems on islands and other isolated habitats. Island diversity is structured by five classes of process: dispersal, establishment, biotic interactions, extinction and evolution. Classical approaches in island biogeography focused on species richness as the deterministic outcome of these processes. This has proved fruitful, but species traits can potentially offer new biological insights into the processes by which island life assembles and why some species perform better at colonising and persisting on islands. Functional traits refer to morphological and phenological characteristics of an organism or species that can be linked to its ecological strategy and that scale up from individual plants to properties of communities and ecosystems. A baseline hypothesis is for traits and ecological strategies of island species to show similar patterns as a matched mainland environment. However, strong dispersal, environmental and biotic-interaction filters as well as stochasticity associated with insularity modify this baseline. Clades that do colonise often embark on distinct ecological and evolutionary pathways, some because of distinctive evolutionary forces on islands, and some because of the opportunities offered by freedom from competitors or herbivores or the absence of mutualists. Functional traits are expected to be shaped by these processes. Here, we review and discuss the potential for integrating functional traits into island biogeography. While we focus on plants, the general considerations and concepts may be extended to other groups of organisms. We evaluate how functional traits on islands relate to core principles of species dispersal, establishment, extinction, reproduction, biotic interactions, evolution and conservation. We formulate existing knowledge as 33 working hypotheses. Some of these are grounded on firm empirical evidence, others provide opportunities for future research. We organise our hypotheses under five overarching sections. Section A focuses on plant functional traits enabling species dispersal to islands. Section B discusses how traits help to predict species establishment, successional trajectories and natural extinctions on islands. Section C reviews how traits indicate species biotic interactions and reproduction strategies and which traits promote intra-island dispersal. Section D discusses how evolution on islands leads to predictable changes in trait values and which traits are most susceptible to change. Section E debates how functional ecology can be used to study multiple drivers of global change on islands and to formulate effective conservation measures. Islands have a justified reputation as research models. They illuminate the forces operating within mainland communities by showing what happens when those forces are released or changed. We believe that the lens of functional ecology can shed more light on these forces than research approaches that do not consider functional differences among species.     

Biogeographical determinants for total and endemic species richness in a continental archipelago

We examined the relationship between plant species richness and biogeographical variables (island area, island maximum elevation, distance from nearest inhabited island, distance from nearest mainland) using a data set comprising 201 islands of the Aegean archipelago. We found that endemic species richness was strongly correlated to total species richness. Single-island endemic species richness was most strongly correlated to island maximum elevation, and then to island area, with an apparent small island effect for islands smaller than 47 km². Total species richness was most strongly correlated to island area (with no apparent small island effect), and less strongly correlated to island maximum elevation. Distance from the mainland or other inhabited islands displayed limited predictive value in our data set. The slope of the relationship between species richness and geographical factors (island area, elevation, distance from island/mainland) was steeper for endemic species richness than for total richness. Finally, the different scales of endemicity (single-island endemics, island group endemics and Aegean regional endemics) displayed similar qualitative trends and only differed quantitatively. Thus, we conclude that different biogeographical factors act as drivers for total species richness than for endemic species richness.     

A unified model of island biogeography sheds light on the zone of radiation

Islands acquire species through immigration and speciation. Models of island biogeography should capture both processes; however quantitative island biogeography theory has either neglected speciation or treated it unrealistically. We introduce a model where the dominance of immigration on small and near islands gives way to an increasing role for speciation as island area and isolation increase. We examine the contribution of immigration and speciation to the avifauna of 35 archipelagoes and find, consistent with our model, that the zone of radiation comprises two regions: endemic species diverged from mainland sister-species at intermediate isolation and from insular sister-species at higher levels of isolation. Our model also predicts species-area curves in accord with existing research and makes new predictions about species ages and abundances. We argue that a paucity of data and theory on species abundances on isolated islands highlights the need for island biogeography to be reconnected with mainstream ecology.