Mutualistic Interaction Networks Research Articles

The Interplay of Binary and Quantitative Structure on the Stability of Mutualistic Networks.

Understanding how the structure of biological systems impacts their resilience (broadly defined) is a recurring question across multiple levels of biological organization. In ecology, considerable effort has been devoted to understanding how the structure of interactions between species in ecological networks is linked to different broad resilience outcomes, especially local stability. Still, nearly all of that work has focused on interaction structure in presence-absence terms and has not investigated quantitative structure, i.e., the arrangement of interaction strengths in ecological networks. We investigated how the interplay between binary and quantitative structure impacts stability in mutualistic interaction networks (those in which species interactions are mutually beneficial), using community matrix approaches. We additionally examined the effects of network complexity and within-guild competition for context. In terms of structure, we focused on understanding the stability impacts of nestedness, a structure in which more-specialized species interact with smaller subsets of the same species that more-generalized species interact with. Most mutualistic networks in nature display binary nestedness, which is puzzling because both binary and quantitative nestedness are known to be destabilizing on their own. We found that quantitative network structure has important consequences for local stability. In more-complex networks, binary-nested structures were the most stable configurations, depending on the quantitative structures, but which quantitative structure was stabilizing depended on network complexity and competitive context. As complexity increases and in the absence of within-guild competition, the most stable configurations have a nested binary structure with a complementary (i.e., anti-nested) quantitative structure. In the presence of within-guild competition, however, the most stable networks are those with a nested binary structure and a nested quantitative structure. In other words, the impact of interaction overlap on community persistence is dependent on the competitive context. These results help to explain the prevalence of binary-nested structures in nature and underscore the need for future empirical work on quantitative structure.

The structure and ecological function of the interactions between plants and arbuscular mycorrhizal fungi through multilayer networks

Abstract Arbuscular mycorrhizas are one of the most frequent mutualisms in terrestrial ecosystems. Although studies on plant mutualistic interaction networks suggest that they may leave their imprint on plant community structure and dynamics, this has not been explicitly assessed. Thus, in the context of plant‐fungi interactions, studies explicitly linking plant‐mycorrhizal fungi interaction networks with key ecological functions of plant communities, such as recruitment, are lacking. In this study, we analyse, in two Mediterranean forest communities of southern Iberian Peninsula, how plant‐arbuscular mycorrhizal fungi (AMF) networks modulate plant‐plant recruitment interaction networks. We use a new approach integrating plant‐AMF and plant recruitment networks into a single multilayer structure. We also develop a new metric (Interlayer Node Neighbourhood Integration, INNI) to explore the impact of a given node on the structure across layers. The similarity of plant species in their AMF communities is positively related to the observed frequency of recruitment interactions in the field. Results reveal that properties of plant‐AMF networks, such as plant degree and centrality, can explain about the properties of plant recruitment network, such as in‐ and out‐degree (i.e. sapling bank and canopy service) and its modular structure. However, these relationships differed between the two forest communities. Finally, we identify particular AMF that contribute to integrate the neighbourhood of recruitment interactions between plants. This multilayer network approach is useful to explore the role of plant‐AMF interactions on recruitment, a key ecosystem function enhanced by fungi. Results provide evidence that the complex structure of plant‐AMF interactions impacts functional and structurally plant‐plant interactions, which in turn may potentially influence plant community dynamics, through their effects on the structure of the recruitment network. Read the free Plain Language Summary for this article on the Journal blog.

Diel niche partitioning of a plant-hummingbird network in the Atlantic forest of Brazil

Niche partitioning is an important mechanism that allows species to coexist. Within mutualistic interaction networks, diel niche partitioning, i.e., partitioning of resources throughout the day, has been neglected. We explored diel niche partitioning of a plant-hummingbird network in the Brazilian Atlantic forest for nine months. To evaluate diel patterns of hummingbird visits and nectar production, we used time-lapse cameras on focal flowers and repeated nectar volume and concentration measures, respectively. Additionally, we measured flower abundance around focal flowers and flower morphological traits. We did not observe diel partitioning for either hummingbirds or plants. Instead, hummingbirds appeared to specialize in different plant species, consistent with trophic niche partitioning, potentially resulting from competition. In contrast, plant species that co-flowered and shared hummingbird visits produced nectar during similar times, consistent with facilitation. Our focus on the fine-scale temporal pattern revealed that plants and hummingbirds appear to have different strategies for promoting co-existence.

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Corrigendum

Effects of long-term discharge of acid mine drainage from abandoned coal mines on soil microorganisms: microbial community structure, interaction patterns, and metabolic functions

More than twenty abandoned coal mines in the Yudong River Basin of Guizhou Province have discharged acid mine drainage (AMD) for a long time. The revelation of microbial community composition, interaction patterns, and metabolic functions can contribute to abetter understanding ofsuch ecosystems, which in its turn can be helpfulin the development of strategies aiming atthe ecological remediation of AMD pollution. In this study, reference and contaminated soil samples were collected along the AMD flow path for high-throughput sequencing. Results showed that the long-term AMD pollution promoted the evolution of γ-Proteobacteria, and the acidophilic iron-oxidizing bacteria Ferrovum (relative abundance of 15.50%) and iron-reducing bacteria Metallibacterium (9.87%) belonging to this class became the dominant genera. Co-occurrence analysis revealed that the proportion of positive correlations among bacteria increased from 51.02 (reference soil) to 75.16% (contaminated soil), suggesting that acidic pollution promotes the formation of mutualistic interaction networks of microorganisms. Metabolic function prediction (Tax4Fun) revealed that AMD contamination enhanced microbial functions such as translation, repair, and biosynthesis of peptidoglycan and lipopolysaccharide, etc., which may be an adaptive mechanism for microbial survival in extremely acidic environment. In addition, acidic pollution promoted the high expression of nitrogen-fixing genes in soil, and the discovery of autotrophic nitrogen-fixing bacteria such as Ferrovum highlights the possibility of using this taxon for bioremediation of AMD pollution.

The evolution of ecological networks

Evolutionary Ecology Plants and the animals that eat their fruits and disperse their seeds form complex networks of mutualistic interactions. The structures of many such networks and the ecological forces that shape them are well known, but their deeper evolutionary history has received little attention. Burin et al. address this knowledge gap in a study of frugivorious bird species in documented seed-dispersal networks around the world (see the Perspective by Bello and Barreto). Species occupying central positions in frugivory networks, which thus interact with many plant species, tend to belong to lineages that are more stable over macroevolutionary time scales. These patterns are more evident in regions with warmer and wetter climates and provide evidence that evolutionary processes can leave a signal on the structure of current ecological networks. Science , this issue p. [733][1] see also p. [682][2] [1]: /lookup/doi/10.1126/science.abf0556 [2]: /lookup/doi/10.1126/science.abi8160

From structure to function in mutualistic interaction networks: Topologically important frugivores have greater potential as seed dispersers.

Networks of mutualistic interactions between animals and plants are considered a pivotal part of ecological communities. However, mutualistic networks are rarely studied from the perspective of species-specific roles, and it remains to be established whether those animal species more relevant for network structure also contribute more to the ecological functions derived from interactions. Here, we relate the contribution to seed dispersal of vertebrate species with their topological role in frugivore-plant interaction networks. For one year in two localities with remnant patches of Colombian tropical dry forest, we sampled abundance, morphology, behaviour and fruit consumption from fleshy-fruited plants of various frugivore species. We assessed the network topological role of each frugivore species by integrating their degree of generalization in interactions with plants with their contributions to network nestedness and modularity. We estimated the potential contribution of each frugivore species to community-wide seed dispersal, on the basis of a set of frugivore ecological, morphological and behavioural characteristics important for seed dispersal, together with frugivore abundance and frugivory degree. The various frugivore species showed strong differences in their network structural roles, with generalist species contributing the most to network modularity and nestedness. Frugivores also showed strong variability in terms of potential contribution to seed dispersal, depending on the specific combinations of frugivore abundance, frugivory degree and the different traits and behaviours. For both localities, the seed dispersal potential of a frugivore species responded positively to its contribution to network structure, evidencing that the most important frugivore species in the network topology were also those making the strongest contribution as seed dispersers. Contribution to network structure was correlated with frugivore abundance, diet and behavioural characteristics. This suggests that the species-level link between structure and function is due to the fact that the occurrence of frugivore-plant interactions depends largely on the characteristics of the frugivore involved, which also condition its ultimate role in seed dispersal.

Inferring coevolution in a plant–pollinator network

Mutualistic interactions are at the core of community dynamics, determining dispersal, colonization and differential survival and reproduction among individuals and species. Mutualistic interactions therefore affect the fitness of interaction partners, hence modifying their respective evolutionary trajectories reciprocally, potentially leading to coevolution. Although mathematical models predict coevolution in mutualistic interaction networks, no empirical data are available. By taking into account the patterns of interactions and reconstructing evolutionary change in plant and pollinator traits, we tested the hypothesis that coevolution occurs between plants and insects that interact more frequently, or more symmetrically. To test this hypothesis, we built an interaction network with data from five flowering seasons, measured plant and insect morphology, mapped morphology on the plant and insect phylogenies, and reconstructed ancestral character changes based on maximum parsimony. We calculated an index, called the coevolutionary ratio, which represents the amount of correlated change in traits that mediate the interaction between plants and pollinators (i.e. proboscis versus corolla length, and body width and corolla aperture). Our results suggest that high frequency of interaction, i.e. the number of times two species interact, does not lead to coevolution. Instead, symmetry of interaction strength, i.e. the reciprocal similarity in the mutual effect of interaction partners, may lead to coevolution, in spite of a pervasive lack of reciprocal specialization and high interaction frequency. Although the statistical signal is quite weak, our results hold for three statistical tests of very different nature. The most specialized species, expected to be under directional selection, do not show more evolutionary change than do generalist species, expected to be under different, perhaps opposing, selective pressures. By dissecting the complexity of an interaction network we show that coevolution may partially shape functional morphology of interaction partners, thus providing the closest evidence to date of mutualistic adaptation of organisms within a community.

Range overlap between the sword-billed hummingbird and its guild of long-flowered species: An approach to the study of a coevolutionary mosaic.

The coevolutionary process among free-living mutualists with extremely long matching traits may favor the formation of mutualistic interaction networks through coevolutionary escalation, complementarity and convergence. These networks may be geographically structured; the links among the species of a local network are shaped by the biotic composition of the community, thus creating selection mosaics at broader geographical scales. Therefore, to fully understand a coevolutionary process, it is crucial to visualize the geographical structure of the interaction network across the landscape. In this study we focused on the poorly known interaction system between Ensifera ensifera and its guild of long-flowered plant species. We combined occurrence data and environmental variables to predict E. ensifera distribution, in addition to range polygons available for plant species in order to evaluate the geographical variation in bill length and plant species richness. A positive relationship between bill length and plant species richness within the E. ensifera range suggests a geographical structuring of the interaction networks. At mid-latitude locations of E. ensifera range, where hummingbirds attained the longest bills, richness of long-flowered plant species was higher than at low latitude locations. These locations likely represent coevolutionary vortices where long-lasting reciprocal selection probably drove the evolution of long traits, consequently drawing new plant species into the coevolutionary network. Conversely, areas where the sword-billed hummingbird was absent or had shorter bills probably represent coevolutionary coldspots. Our results provide a first insight into this phenotypically specialized plant-pollinator network across the landscape and show candidate areas to test the predictions of the coevolutionary hypothesis, such as reciprocal selection.

Connecting Resource Tracking by Frugivores to Temporal Variation in Seed Dispersal Networks

Mutualistic interactions between species are crucial for the maintenance and functioning of the community. Current research has shown the importance of not only understanding the structure of these mutualistic interaction networks but also their temporal dynamics. Temporal changes in species abundance, such as those caused by vertebrate resource tracking, may create temporal variability in a network though neighborhood effects and influence the directedness of dispersal. While much research has been done on resource tracking, neighborhood effects, and directed dispersal individually, little research has been done into their interrelationships and, therefore, theory of how resource tracking can influence frugivory and seed dispersal networks remains poorly developed. We use the available literature to show the prevalence of resource tracking by vertebrate frugivores and hypothesize how, through neighborhood effects, resource tracking may influence short-term variation in network properties. We then discuss how resource tracking can influence long-term network properties by altering the dispersal of plant species. Lastly, we use this information to hypothesize how the introductions of new species into a community may alter the influence of resource tracking on frugivory and seed dispersal. While trait matching and links that are not possible between species in a community (i.e., forbidden links) play a large role in determining the structure of a network, temporal change in the abundance of species due to resource tracking may also affect the properties of networks. By increasing our understanding of the role resource tracking has in the temporal variability of frugivory and seed dispersal networks, we can better determine the full extent of species interactions and provide valuable information for the conservation of ecological communities.

The mycobiome – a friendly cross-talk between fungal colonizers and their host

The organisms colonizing a living host create together with their host a holobiome. The holobioms are networks of mutualistic interactions between host`s cells and microorganisms communities. The fungi are among these microorganisms and have been also well known to infect human and animals. These organisms are associated with a wide range of diseases as superficial or systemic mycoses. Fungi as colonizers can also modify host physiology and metabolism, energy acquisition, vitamin-cofactor availability, development and function of immune system, and even host behavior. The objective of this review is to familiarize with recent data concerning the role of fungi creating mammalian mycobiome in the maintenance of the host health status

Modularity, pollination systems, and interaction turnover in plant-pollinator networks across space.

Mutualistic interaction networks have been shown to be structurally conserved over space and time while pairwise interactions show high variability. In such networks, modularity is the division of species into compartments, or modules, where species within modules share more interactions with each other than they do with species from other modules. Such a modular structure is common in mutualistic networks and several evolutionary and ecological mechanisms have been proposed as underlying drivers. One prominent explanation is the existence of pollination syndromes where flowers tend to attract certain pollinators as determined by a set of traits. We investigate the modularity of seven community level plant-pollinator networks sampled in rupestrian grasslands, or campos rupestres, in SE Brazil. Defining pollination systems as corresponding groups of flower syndromes and pollinator functional groups, we test the two hypotheses that (1) interacting species from the same pollination system are more often assigned to the same module than interacting species from different pollination systems and; that (2) interactions between species from the same pollination system are more consistent across space than interactions between species from different pollination systems. Specifically we ask (1) whether networks are consistently modular across space; (2) whether interactions among species of the same pollination system occur more often inside modules, compared to interactions among species of different pollination systems, and finally; (3) whether the spatial variation in interaction identity, i.e., spatial interaction rewiring, is affected by trait complementarity among species as indicated by pollination systems. We confirm that networks are consistently modular across space and that interactions within pollination systems principally occur inside modules. Despite a strong tendency, we did not find a significant effect of pollination systems on the spatial consistency of pairwise interactions. These results indicate that the spatial rewiring of interactions could be constrained by pollination systems, resulting in conserved network structures in spite of high variation in pairwise interactions. Our findings suggest a relevant role of pollination systems in structuring plant-pollinator networks and we argue that structural patterns at the sub-network level can help us to fully understand how and why interactions vary across space and time.

Interactive effects of elevation, species richness and extreme climatic events on plant-pollinator networks.

Plant-pollinator interactions are essential for the functioning of terrestrial ecosystems, but are increasingly affected by global change. The risks to such mutualistic interactions from increasing temperature and more frequent extreme climatic events such as drought or advanced snow melt are assumed to depend on network specialization, species richness, local climate and associated parameters such as the amplitude of extreme events. Even though elevational gradients provide valuable model systems for climate change and are accompanied by changes in species richness, responses of plant-pollinator networks to climatic extreme events under different environmental and biotic conditions are currently unknown. Here, we show that elevational climatic gradients, species richness and experimentally simulated extreme events interactively change the structure of mutualistic networks in alpine grasslands. We found that the degree of specialization in plant-pollinator networks (H2') decreased with elevation. Nonetheless, network specialization increased after advanced snow melt at high elevations, whereas changes in network specialization after drought were most pronounced at sites with low species richness. Thus, changes in network specialization after extreme climatic events depended on climatic context and were buffered by high species richness. In our experiment, only generalized plant-pollinator networks changed in their degree of specialization after climatic extreme events. This indicates that contrary to our assumptions, network generalization may not always foster stability of mutualistic interaction networks.

Measuring effective dispersal

Community Ecology![Figure][1] Gallotia galloti is an important seed disperser on Tenerife IMAGE: © CULTURA RM/ALAMY Dispersal fundamentally shapes ecological communities and maintains biodiversity, yet it is extremely difficult to quantify. Estimating seed dispersal effectiveness (SDE) requires measurement of both the number of seeds dispersed and the probability of successful germination. Gonzalez-Castro et al. laboriously measured the SDE of frugivorous lizards and birds as dispersers of seeds over 6 years in plant communities on the oceanic island of Tenerife. Their results allowed for comparisons between the SDE of the two main frugivore groups for different plant species and different communities (such as woodland and shrubland), revealing the networks of mutualistic interactions that underpin community persistence. Ecology 96 , 808 (2015). [1]: pending:yes

Richness and diversity of mammalian fungal communities shape innate and adaptive immunity in health and disease.

Human holobiomes are networks of mutualistic interactions between human cells and complex communities of bacteria and fungi that colonize the human body. The immune system must tolerate colonization with commensal bacteria and fungi but defend against invasion by either organism. Molecular ecological surveys of the human prokaryotic microbiota performed to date have revealed a remarkable degree of bacterial diversity and functionality. However, there is a dearth of information regarding the eukaryotic composition of the microbiota. In this review, we describe the ecology and the human niches of our fungal "fellow travelers" in both health and disease, discriminating between passengers, colonizers, and pathogens based on the interaction of these fungi with the human immune system. We conclude by highlighting the need to reconsider the etiology of many fungal and immune-related diseases in the context of the crosstalk between the human system and its resident microbial communities.

Detecting phylogenetic signal in mutualistic interaction networks using a Markov process model.

Ecological interaction networks, such as those describing the mutualistic interactions between plants and their pollinators or between plants and their frugivores, exhibit non-random structural properties that cannot be explained by simple models of network formation. One factor affecting the formation and eventual structure of such a network is its evolutionary history. We argue that this, in many cases, is closely linked to the evolutionary histories of the species involved in the interactions. Indeed, empirical studies of interaction networks along with the phylogenies of the interacting species have demonstrated significant associations between phylogeny and network structure. To date, however, no generative model explaining the way in which the evolution of individual species affects the evolution of interaction networks has been proposed. We present a model describing the evolution of pairwise interactions as a branching Markov process, drawing on phylogenetic models of molecular evolution. Using knowledge of the phylogenies of the interacting species, our model yielded a significantly better fit to 21% of a set of plant - pollinator and plant - frugivore mutualistic networks. This highlights the importance, in a substantial minority of cases, of inheritance of interaction patterns without excluding the potential role of ecological novelties in forming the current network architecture. We suggest that our model can be used as a null model for controlling evolutionary signals when evaluating the role of other factors in shaping the emergence of ecological networks.

Island biogeography of mutualistic interaction networks

AbstractAimThe seminal theory of island biogeography, based on changing rates of immigration and extinction, should be seen in a geological context, as an island's maturity influences the richness of its biota. Here, we develop an island biogeography of biotic interactions, recognizing that, besides species richness, biodiversity also encompasses the multitude of interactions among species. By sampling interactions between plants and pollinators across the Canarian archipelago, we illustrate how the local richness, specialization and endemism of biotic interactions vary with island age and area.LocationCanary Islands (27.62° N–29.42° N and 13.33° W–18.17° W).MethodsOn five islands, covering the full age range of the archipelago, plant–pollinator interactions were catalogued and their strength estimated. Network parameters (e.g. interaction richness and specialization) and the number of single‐island interactions (equivalent to single‐island endemics) were estimated from interaction matrices and related to island area and age.ResultsPlant species richness, interaction richness and average degree of specialization of pollinator species showed hump‐shaped relationships with island age. Pollinator richness varied with island area and plant richness. Plant specialization increased with island age, and the proportion of single‐island interactions (pSII) exhibited a U‐shaped relationship with age.Main conclusionsThe previously reported hump‐shaped relationship between species richness and island age, both on the scale of islands and of habitats, was confirmed for plant species in local networks. Both plants and pollinators were more generalized on the youngest island, which may be due to a predominance of generalist colonists. Pollinator specialization peaked on mid‐aged islands, whereas plants showed the highest specialization on old islands, potentially reflecting their different life histories. The U‐shaped relationship between the proportion of single‐island interactions and island age might be explained by (1) young islands having a high proportion of unique interactions, due to interactions between generalists, and (2) old islands having unique interactions due to an accumulation of unique pairwise interactions that have evolved through time. Thus, island age – which not only captures time per se, but also the geomorphological changes of islands – may act as a regional driver of local network structure, and so the contemporary networks we observed across the Canarian archipelago illustrate the development of a network through geological time.

Specialization of Mutualistic Interaction Networks Decreases toward Tropical Latitudes

Species-rich tropical communities are expected to be more specialized than their temperate counterparts. Several studies have reported increasing biotic specialization toward the tropics, whereas others have not found latitudinal trends once accounting for sampling bias or differences in plant diversity. Thus, the direction of the latitudinal specialization gradient remains contentious. With an unprecedented global data set, we investigated how biotic specialization between plants and animal pollinators or seed dispersers is associated with latitude, past and contemporary climate, and plant diversity. We show that in contrast to expectation, biotic specialization of mutualistic networks is significantly lower at tropical than at temperate latitudes. Specialization was more closely related to contemporary climate than to past climate stability, suggesting that current conditions have a stronger effect on biotic specialization than historical community stability. Biotic specialization decreased with increasing local and regional plant diversity. This suggests that high specialization of mutualistic interactions is a response of pollinators and seed dispersers to low plant diversity. This could explain why the latitudinal specialization gradient is reversed relative to the latitudinal diversity gradient. Low mutualistic network specialization in the tropics suggests higher tolerance against extinctions in tropical than in temperate communities.

The disentangled bank: How loss of habitat fragments and disassembles ecological networks

Habitat transformation is one of the leading causes of changes in biodiversity and the breakdown of ecosystem function and services. The impacts of habitat transformation on biodiversity are complex and can be difficult to test and demonstrate. Network approaches to biodiversity science have provided a powerful set of tools and models that are beginning to present new insight into the structural and functional effects of habitat transformation on complex ecological systems. We propose a framework for studying the ways in which habitat loss and fragmentation jointly affect biodiversity by altering both habitat and ecological interaction networks. That is, the explicit study of "networks of networks" is required to understand the impacts of habitat change on biodiversity. We conduct a broad review of network methods and results, with the aim of revealing the common approaches used by landscape ecology and community ecology. We find that while a lot is known about the consequences of habitat transformation for habitat network topology and for the structure and function of simple antagonistic and mutualistic interaction networks, few studies have evaluated the consequences for large interaction networks with complex and spatially explicit architectures. Moreover, almost no studies have been focused on the continuous feedback between the spatial structure and dynamics of the habitat network and the structure and dynamics of the interaction networks inhabiting the habitat network. We conclude that theory and experiments that tackle the ecology of networks of networks are needed to provide a deeper understanding of biodiversity change in fragmented landscapes.

Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction

The 5th Symposium on Frugivores and Seed Dispersal, held in Montpellier (France), 13-18 June 2010, brought together more than 220 researchers exemplifying a wide diversity of approaches to the study of frugivory and dispersal of seeds. Following Ted Fleming and Alejandro Estrada's initiative in 1985, this event was a celebration of the 25th anniversary of the first meeting in Veracruz, Mexico. Frugivory and seed dispersal are active research areas that have diversified in multiple directions since 1985 to include evolution (e.g. phylogenetic diversity and dispersal adaptations), physiology (e.g. sensory cues and digestion), landscape ecology (movement patterns), molecular ecology (e.g. gene flow, genetic diversity and structure), community ecology (e.g. mutualistic interaction networks) and conservation biology (effects of hunting, fragmentation, invasion and extinction), among others. This meeting provided an opportunity to assess conceptual and methodological progress, to present ever more sophisticated insights into frugivory in animals and dispersal patterns in plants, and to report the advances made in examining the mechanisms and consequences of seed dispersal for plants and frugivores.