Temporal scale‐dependence of plant–pollinator networks

The study of mutualistic interaction networks has led to valuable insights into ecological and evolutionary processes. However, our understanding of network structure may depend upon the temporal scale at which we sample and analyze network data. To date, we lack a comprehensive assessment of the temporal scale-dependence of network structure across a wide range of temporal scales and geographic locations. If network structure is temporally scale-dependent, networks constructed over different temporal scales may provide very different perspectives on the structure and composition of species interactions. Furthermore, it remains unclear how various factors – including species richness, species turnover, link rewiring and sampling effort – act in concert to shape network structure across different temporal scales. To address these issues, we used a large database of temporally-resolved plant–pollinator networks to investigate how temporal aggregation from the scale of one day to multiple years influences network structure. In addition, we used structural equation modeling to explore the direct and indirect effects of temporal scale, species richness, species turnover, link rewiring and sampling effort on network structural properties. We find that plant–pollinator network structure is strongly temporally-scale dependent. This general pattern arises because the temporal scale determines the degree to which temporal dynamics (i.e. phenological turnover of species and links) are included in the network, in addition to how much sampling effort is put into constructing the network. Ultimately, the temporal scale-dependence of our plant–pollinator networks appears to be mostly driven by species richness, which increases with sampling effort, and species turnover, which increases with temporal extent. In other words, after accounting for variation in species richness, network structure is increasingly shaped by its underlying temporal dynamics. Our results suggest that considering multiple temporal scales may be necessary to fully appreciate the causes and consequences of interaction network structure.Fil: Schwarz, Benjamin. Albert Ludwigs University of Freiburg; AlemaniaFil: Vazquez, Diego P.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Provincia de Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Universidad Nacional de Cuyo. Instituto Argentino de Investigaciones de las Zonas Áridas; ArgentinaFil: Cara Donna, Paul J.. Chicago Botanic Garden; Estados UnidosFil: Knight, Tiffany M.. German Centre for Integrative Biodiversity Research; AlemaniaFil: Benadi, Gita. Albert Ludwigs University of Freiburg; AlemaniaFil: Dormann, Carsten F.. Albert Ludwigs University of Freiburg; AlemaniaFil: Gauzens, Benoit. German Centre for Integrative Biodiversity Research; AlemaniaFil: Motivans, Elena. German Centre for Integrative Biodiversity Research; AlemaniaFil: Resasco, Julian. University of Colorado; Estados UnidosFil: Blüthgen, Nico. Universitat Technische Darmstadt; AlemaniaFil: Burkle, Laura A.. Montana State University; AlemaniaFil: Fang, Qiang. Henan University of Science and Technology; ChinaFil: Kaiser Bunbury, Christopher N.. University of Exeter; Reino UnidoFil: Alarcón, Ruben. California State University; Estados UnidosFil: Bain, Justin A.. Chicago Botanic Garden; Estados UnidosFil: Chacoff, Natacha Paola. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Huang, Shuang Quan. Central China Normal University; ChinaFil: LeBuhn, Gretchen. San Francisco State University; Estados UnidosFil: MacLeod, Molly. Rutgers University; Estados UnidosFil: Petanidou, Theodora. Univversity of the Aegean; Estados UnidosFil: Rasmussen, Claus. University Aarhus; DinamarcaFil: Simanonok, Michael P.. Montana State University; Estados UnidosFil: Thompson, Amibeth H.. German Centre for Integrative Biodiversity Research; AlemaniaFil: Fründ, Jochen. Albert Ludwigs University of Freiburg; Alemani

Untersuchung des Zusammenhangs zwischen Spezialisierungsgrad und Stabilität von Pflanzen-Bestäuber-Netzwerken

In this dissertation, I examine the relationship between specialisation and stability of plant-pollinator networks, with a focus on two issues: Diversity maintenance in animal-pollinated plant communities and robustness of plant-pollinator systems against disturbances such as those caused by anthropogenic climate change. Chapter 1 of this thesis provides a general introduction to the concepts of ecological stability and specialisation with a focus on plant-pollinator systems, and a brief outline of the following chapters. Chapters 2-5 each consist of a research article addressing a specific question. While chapters 2 and 3 deal with different aspects of diversity maintenance in animal-pollinated plant communities, chapters 4 and 5 are concerned with the consequences of climate change in the form of temporary disturbances caused by extreme climatic events (chapter 4) and shifts in phenology of plants and pollinators (chapter 5). From a methodological perspective, the first three articles (chapter 2-4) can be grouped together as they all employ mathematical models of plant-pollinator systems, whereas chapter 5 describes an empirical study of plant-pollinator interactions along an altitudinal gradient in the Alps. The final chapter (6) provides a review of current knowledge on each of the two main themes of this thesis and places the findings of the four research articles in the context of related studies.In dieser Dissertation untersuche ich den Zusammenhang zwischen Spezialisierung und Stabilität von Pflanzen-Bestäuber-Netzwerken. Dabei konzentriere ich mich speziell auf zwei Themengebiete: Die Erhaltung der Diversität in Pflanzengemeinschaften, die durch Tiere bestäubt werden, und die Widerstandsfähigkeit von Pflanzen-Bestäuber-Systemen gegenüber Störungen, wie sie durch den anthropogenen Klimawandel hervorgerufen werden. Kapitel 1 dieser Arbeit gibt eine allgemeine Einführung zu den Konzepten der ökologischen Stabilität und der Spezialisierung mit einem Schwerpunkt auf Pflanzen-Bestäuber-Systemen, und einen kurzen Überblick über die folgenden Kapitel der Arbeit. Kapitel 2-5 bestehen jeweils aus einem wissenschaftlichen Artikel, der eine spezifische Fragestellung untersucht. Während Kapitel 2 und 3 sich mit verschiedenen Aspekten der Erhaltung der Diversität in tierbestäubten Pflanzengemeinschaften befassen, beschäftigen sich Kapitel 4 und 5 mit den Auswirkungen des Klimawandels in Form von temporären Störungen verursacht durch klimatische Extremereignisse (Kapitel 4) und zeitlichen Verschiebungen der Phänologie von Pflanzen und Bestäubern (Kapitel 5). Aus methodologischer Sicht bilden die ersten drei Artikel eine Einheit, da sie alle mathematische Modelle der Populationsdynamik von Pflanzen und Bestäubern verwenden, während Kapitel 5 eine empirische Studie über Pflanzen-Bestäuber-Interaktionen entlang eines Höhengradienten in den Alpen beschreibt. Das letzte Kapitel (6) gibt einen Überblick über den Wissensstand in den beiden zentralen Themengebieten dieser Arbeit und bettet die Ergebnisse der vier Artikel in den Kontext verwandter wissenschaftlicher Arbeiten ein

Data from: Frequency dependence of pollinator visitation rates suggests that pollination niches can allow plant species coexistence

1. How do many species coexist within a trophic level? Resource niches are the classical answer, but in plants which share a small set of abiotic resources the possibilities for resource partitioning are limited. One possible explanation is that plant species have different pollination niches, with each species specialized to a subset of the available animal species. If this pollinator partitioning results in negative frequency dependence such that each plant species’ reproduction is reduced when it becomes abundant, pollination niches could maintain plant diversity, provided that the strength of negative frequency dependence is sufficient to overcome fitness inequalities between species. 2. We tested this idea by quantifying the effect of species relative abundance on pollinator visitation rate in a 7000 m² plot of South African Fynbos vegetation. In addition, we quantified the effect of intraspecific abundance variation at a smaller spatial scale (9 m² plots), documented species’ pollination niches and tested the importance of pollinators for seed set in a subset of the plant species. 3. We found that visitation rate indeed declined sharply across the 33 plant species with increasing abundance, but visitation rate was also somewhat depressed in very rare species such that the resulting relationship between visitation rate and relative abundance was hump-shaped. Pollinator niche partitioning among plant species was evident, but less pronounced than in many other studies. Visitation rate was slightly higher in more generalized species, suggesting that they have access to a larger pollination resource. At the intraspecific level and smaller spatial scale, results were less clear and varied among species. Pollinators enhanced seed set in most species. 4. Synthesis. The results imply that, above an abundance threshold, intraspecific competition for pollination could limit the reproduction of common species, thus promoting plant species coexistence. However, the rarest plant species could become extinct due to pollen limitation, i.e. an Allee effect. In addition, interactions with pollinators may introduce frequency-independent fitness differences between plant species, thereby increasing the strength of negative frequency dependence required for stable coexistence. These findings shed new light on the role of the pollination niche in plant coexistence

Benadi_Pauw_2018_J_Ecol

Data and code to reproduce the analyses in: Benadi, G. & Pauw, A. (2018) Frequency dependence of pollinator visitation rates suggests that pollination niches can allow plant species coexistence. Journal of Ecology

Specialization and phenological synchrony of plant-pollinator interactions along an altitudinal gradient.

One of the most noticeable effects of anthropogenic climate change is the shift in timing of seasonal events towards earlier occurrence. The high degree of variation in species' phenological shifts has raised concerns about the temporal decoupling of interspecific interactions, but the extent and implications of this effect are largely unknown. In the case of plant-pollinator systems, more specialized species are predicted to be particularly threatened by phenological decoupling, since they are assumed to be less flexible in the choice of interaction partners, but until now this hypothesis has not been tested. In this paper, we studied phenology and interactions of plant and pollinator communities along an altitudinal gradient in the Alps as a model for the possible effects of climate change in time. Our results show that even relatively specialized pollinators were much more flexible in their use of plant species as floral resources than their local flower visitation suggested. We found no relationship between local specialization of pollinators and the consistency of their visitation patterns across sites, and also no relationship between specialization and phenological synchrony of pollinators with particular plants. Thus, in contrast to the conclusions of a recent simulation study, our results suggest that most pollinator species included in this study are not threatened by phenological decoupling from specific flowering plants. However, the flexibility of many rarely observed pollinator species remains unknown. Moreover, our results suggest that specialized flower visitors select plant species based on certain floral traits such as the length of the nectar holder tube. If that is the case, the observed flexibility of plant-pollinator interactions likely depends on a high degree of functional redundancy in the plant community, which may not exist in less diverse systems

Contrasting specialization-stability relationships in plant-animal mutualistic systems

Abstract Specialization has often been suggested as one of the main factors influencing the stability of ecological systems at the population and community level. Generally, highly specialized systems are believed to be the most sensitive toward disturbances, as the dependence of specialized species on the availability of particular resources or partner species is greatest. The flip side of specialization is, however, that it reduces the intensity of interspecific competition and thus the risk of extinction through competitive exclusion. Moreover, since ecological stability is a highly ambiguous concept, general statements about the relationship between specialization and stability cannot be made based on a single stability criterion. In this study, we examine the relationship between specialization and stability in plant–animal mutualistic systems using a population dynamic model with two species in each group. We compare results for four different stability criteria, both for a general type of plant–animal mutualism and specifically for a plant–pollinator system. Contrary to previous studies which concluded that specialization increases system vulnerability to disturbances, we find that positive, negative and unimodal relationships are possible depending on the stability criterion applied and the characteristics of species interactions. Our results call for further investigations of the consequences of ecological specialization, and emphasize the special properties of pollination mutualisms

When can plant-pollinator interactions promote plant diversity?

Abstract In the light of rapid losses of biodiversity worldwide, it has become more important than ever to study the factors that ensure the continued existence of diverse ecological communities. Whereas the diversity-enhancing effects of antagonistic interactions are relatively well understood, much less is known about the contribution of mutualistic interactions to biodiversity maintenance. This study assesses the influence of mutualistic interactions with pollinators on the diversity of plant communities with alternative means of reproduction besides animal pollination. In contrast to a recent more general model of plant-animal mutualisms, the results of our simulations suggest that interactions with pollinators do not generally promote plant diversity, irrespective of the structure of the interaction network. Despite a potential for increased plant species richness through the positive effect of pollinators on plant birth rates, species richness was mostly negatively affected by the presence of pollinators because existing abundance asymmetries were amplified by animal pollination. Our results imply that for plant communities with alternative means of reproduction, the loss of pollinators will usually not lead to decreased diversity. However, whereas the immediate effects of pollinator loss on plant community composition may be negligible, the long-term population genetic consequences are likely to be severe

Population dynamics of plant and pollinator communities: stability reconsidered.

Plant-pollinator networks are systems of outstanding ecological and economic importance. A particularly intriguing aspect of these systems is their high diversity. However, earlier studies have concluded that the specific mechanisms of plant-pollinator interactions are destabilizing and should lead to a loss of diversity. Here we present a mechanistic model of plant and pollinator population dynamics with the ability to represent a broad spectrum of interaction structures. Using this model, we examined the influence of pollinators on the stability of a plant community and the relationship between pollinator specialization and stability. In accordance with earlier work, our results show that plant-pollinator interactions may severely destabilize plant coexistence, regardless of the degree of pollinator specialization. However, if plant niche differentiation, a classical stabilizing mechanism, is sufficiently strong to overcome the minority disadvantage with respect to pollination, interactions with pollinators may even increase the stability of a plant community. In addition to plant niche differentiation, the relationship between specialization and stability depends on a number of parameters that affect pollinator growth rates. Our results highlight the complex effects of this particular type of mutualism on community stability and call for further investigations of the mechanisms of diversity maintenance in plant-pollinator systems

Data from: Specialization and phenological synchrony of plant–pollinator interactions along an altitudinal gradient

1. One of the most noticeable effects of anthropogenic climate change is the shift in timing of seasonal events towards earlier occurrence. The high degree of variation in species' phenological shifts has raised concerns about the temporal decoupling of interspecific interactions, but the extent and implications of this effect are largely unknown. In the case of plant–pollinator systems, more specialized species are predicted to be particularly threatened by phenological decoupling, since they are assumed to be less flexible in the choice of interaction partners, but until now this hypothesis has not been tested. 2. In this paper, we studied phenology and interactions of plant and pollinator communities along an altitudinal gradient in the Alps as a model for the possible effects of climate change in time. 3. Our results show that even relatively specialized pollinators were much more flexible in their use of plant species as floral resources than their local flower visitation suggested. We found no relationship between local specialization of pollinators and the consistency of their visitation patterns across sites, and also no relationship between specialization and phenological synchrony of pollinators with particular plants. 4. Thus, in contrast to the conclusions of a recent simulation study, our results suggest that most pollinator species included in this study are not threatened by phenological decoupling from specific flowering plants. However, the flexibility of many rarely observed pollinator species remains unknown. Moreover, our results suggest that specialized flower visitors select plant species based on certain floral traits such as the length of the nectar holder tube. If that is the case, the observed flexibility of plant–pollinator interactions likely depends on a high degree of functional redundancy in the plant community, which may not exist in less diverse systems

Quantitative prediction of interactions in bipartite networks based on traits, abundances, and phylogeny

Ecological interactions link species in networks. Loss of species from or introduction of new species into an existing network may have substantial effects for interaction patterns. Predicting changes in interaction frequency while allowing for rewiring of existing interactions—and hence estimating the consequences of community compositional changes—is thus a central challenge for network ecology. Interactions between species groups, such as pollinators and flowers or parasitoids and hosts, are moderated by matching morphological traits or sensory clues, most of which are unknown to us. If these traits are phylogenetically conserved, however, we can use phylogenetic distances to construct latent, surrogate traits and try to match those across groups, in addition to observed traits. Understanding how important traits and trait matching are, relative to abundances and chance, is crucial to estimating the fundamental predictability of network interactions. Here, we present a statistically sound approach (“tapnet”) to fitting abundances, traits, and phylogeny to observed network data to predict interaction frequencies. We thereby expand existing approaches to quantitative bipartite networks, which so far have failed to correctly represent the nonindepen-dence of network interactions. Furthermore, we use simulations and cross validation on independent data to evaluate the predictive power of the fit. Our results show that tapnet is on a par with abundance-only, matching centrality, and machine learning approaches. This approach also allows us to evaluate how well current concepts of trait matching work. On the basis of our results, we expect that interactions in well-sampled networks can be well predicted if traits and abundances are the main driver of interaction frequency.Fil: Benadi, Gita. Albert Ludwigs University of Freiburg; AlemaniaFil: Dormann, Carsten. Albert Ludwigs University of Freiburg; AlemaniaFil: Fründ, Jochen. Albert Ludwigs University of Freiburg; AlemaniaFil: Stephan, Ruth. Albert Ludwigs University of Freiburg; AlemaniaFil: Vazquez, Diego P.. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Provincia de Mendoza. Instituto Argentino de Investigaciones de las Zonas Áridas. Universidad Nacional de Cuyo. Instituto Argentino de Investigaciones de las Zonas Áridas; Argentina. Albert Ludwigs University of Freiburg; Alemani