Seeing through the static: the temporal dimension of plant–animal mutualistic interactions

Most studies of plant–animal mutualistic networks have come from a temporally static perspective. This approach has revealed general patterns in network structure, but limits our ability to understand the ecological and evolutionary processes that shape these networks and to predict the consequences of natural and human‐driven disturbance on species interactions. We review the growing literature on temporal dynamics of plant–animal mutualistic networks including pollination, seed dispersal and ant defence mutualisms. We then discuss potential mechanisms underlying such variation in interactions, ranging from behavioural and physiological processes at the finest temporal scales to ecological and evolutionary processes at the broadest. We find that at the finest temporal scales (days, weeks, months) mutualistic interactions are highly dynamic, with considerable variation in network structure. At intermediate scales (years, decades), networks still exhibit high levels of temporal variation, but such variation appears to influence network properties only weakly. At the broadest temporal scales (many decades, centuries and beyond), continued shifts in interactions appear to reshape network structure, leading to dramatic community changes, including loss of species and function. Our review highlights the importance of considering the temporal dimension for understanding the ecology and evolution of complex webs of mutualistic interactions.     

Motifs in bipartite ecological networks: uncovering indirect interactions

Indirect interactions play an essential role in governing population, community and coevolutionary dynamics across a diverse range of ecological communities. Such communities are widely represented as bipartite networks: graphs depicting interactions between two groups of species, such as plants and pollinators or hosts and parasites. For over thirty years, studies have used indices, such as connectance and species degree, to characterise the structure of these networks and the roles of their constituent species. However, compressing a complex network into a single metric necessarily discards large amounts of information about indirect interactions. Given the large literature demonstrating the importance and ubiquity of indirect effects, many studies of network structure are likely missing a substantial piece of the ecological puzzle. Here we use the emerging concept of bipartite motifs to outline a new framework for bipartite networks that incorporates indirect interactions. While this framework is a significant departure from the current way of thinking about bipartite ecological networks, we show that this shift is supported by analyses of simulated and empirical data. We use simulations to show how consideration of indirect interactions can highlight differences missed by the current index paradigm that may be ecologically important. We extend this finding to empirical plant–pollinator communities, showing how two bee species, with similar direct interactions, differ in how specialised their competitors are. These examples underscore the need to not rely solely on network‐ and species‐level indices for characterising the structure of bipartite ecological networks.     

Plant life history stage and nurse age change the development of ecological networks in an arid ecosystem

Understanding how ecological networks are organised over the course of an organism's lifetime is crucial for predicting the dynamics of interacting populations and communities across temporal scales. However, most studies so far considered only one life history stage at a time, such as adult, when studying networks of interacting species. Therefore, knowledge about how multiple life history stages affect the development and stability of plant–plant association networks is lacking. We measured the understory adult plant community and the soil seed bank across a plant age gradient of the nurse shrub Retama sphaerocarpa in an arid ecosystem in Spain. Using a multilayer network approach, we built adult understory–nurse and seed bank–nurse networks and analysed how network nestedness, species’ role, and species specificity varied between them and with nurse plant age. We found that seed bank and adult understory networks changed depending on nurse plant age in two different ways. With increasing nurse plant age, adult understory networks became significantly more nested than seed bank networks. The nested architecture of seed bank networks was therefore a poor predictor of adult understory network nestedness. The contribution and specificity of species to network nestedness increased with increasing nurse plant age more in the adult understory than in seed bank networks, despite high species turnover. Our data show that life history and ontogeny affect the development of plant–plant association networks. Niche construction and environmental filtering along nurse ontogeny seem pivotal mechanisms structuring adult understory networks while the assembly of seed bank networks seems rather stochastic. We highlight the importance of mature plant communities for maintaining rare species populations and supporting the stability of ecological communities through time.     

Phenological phases of the host plant shape plant–treehopper interaction networks

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Structure and dynamics of pollination networks: the role of alien plants

Research on ecological communities, and plant–pollinator mutualistic networks in particular, has increasingly benefited from the theory and tools of complexity science. Nevertheless, up to now there have been few attempts to investigate the interplay between the structure of real pollination networks and their dynamics. This study is one of the first contributions to explore this issue. Biological invasions, of major concern for conservation, are also poorly understood from the perspective of complex ecological networks. In this paper we assess the role that established alien species play within a host community by analyzing the temporal changes in structural network properties driven by the removal of non‐native plants. Three topological measures have been used to represent the most relevant structural properties for the stability of ecological networks: degree distribution, nestedness, and modularity. Therefore, we investigate for a detailed pollination network, 1) how its dynamics, represented as changes in species abundances, affect the evolution of its structure, 2) how topology relates to dynamics focusing on long‐term species persistence; and 3) how both structure and dynamics are affected by the removal of alien plant species. Network dynamics were simulated by means of a stochastic metacommunity model. Our results showed that established alien plants are important for the persistence of the pollination network and for the maintenance of its structure. Removal of alien plants decreased the likelihood of species persistence. On the other hand, both the full network and the subset native network tended to lose their structure through time. Nevertheless, the structure of the full network was better preserved than the structure of the network without alien plants. Temporal topological shifts were evident in terms of degree distribution, nestedness, and modularity. However the effects of removing alien plants were more pronounced for degree distribution and modularity of the network. Therefore, elimination of alien plants affected the evolution of the architecture of the interaction web, which was closely related to the higher species loss found in the network where alien plants were removed.     

Effect of livestock grazing in the partitions of a semiarid plant–plant spatial signed network

In recent times, network theory has become a useful tool to study the structure of the interactions in ecological communities. However, typically, these approaches focus on a particular kind of interaction while neglecting other possible interactions present in the ecosystem. Here, we present an ecological network for plant communities that consider simultaneously positive and negative interactions, which were derived from the spatial association and segregation between plant species. We employed this network to study the structure and the association strategies in a semiarid plant community of Cabo de Gata-Níjar Natural Park, SE Spain, and how they changed in 4 sites that differed in stocking rate. Association strategies were obtained from the partitions of the network, built based on a relaxed structural balance criterion. We found that grazing simplified the structure of the plant community. With increasing stocking rate species with no significant associations became dominant and the number of partitions decreased in the plant community. Independently of stocking rate, many species presented an associative strategy in the plant community because they benefit from the association to certain ‘nurse’ plants. These ‘nurses’ together with species that developed a segregating strategy, intervened in most of the interactions in the community. Ecological networks that combine links with different signs provide a new insight to analyze the structure of natural communities and identify the species which play a central role in them.     

Rewiring of peatland plant–microbe networks outpaces species turnover

Enviro–climatic changes are thought to be causing alterations in ecosystem processes through shifts in plant and microbial communities; however, how links between plant and microbial communities change with enviro–climatic change is likely to be less straightforward but may be fundamental for many ecological processes. To address this, we assessed the composition of the plant community and the prokaryotic community – using amplicon-based sequencing – of three European peatlands that were distinct in enviro–climatic conditions. Bipartite networks were used to construct site-specific plant–prokaryote co-occurrence networks. Our data show that between sites, plant and prokaryotic communities differ and that turnover in interactions between the communities was complex. Essentially, turnover in plant–microbial interactions is much faster than turnover in the respective communities. Our findings suggest that network rewiring does largely result from novel or different interactions between species common to all realised networks. Hence, turnover in network composition is largely driven by the establishment of new interactions between a core community of plants and microorganisms that are shared among all sites. Taken together our results indicate that plant–microbe associations are context dependent, and that changes in enviro–climatic conditions will likely lead to network rewiring. Integrating turnover in plant–microbe interactions into studies that assess the impact of enviro–climatic change on peatland ecosystems is essential to understand ecosystem dynamics and must be combined with studies on the impact of these changes on ecosystem processes.     

Host functional and phylogenetic composition rather than host diversity structure plant–herbivore networks

Declining plant diversity alters ecological networks, such as plant–herbivore interactions. However, our knowledge of the potential mechanisms underlying effects of plant species loss on plant–herbivore network structure is still limited. We used DNA barcoding to identify herbivore–host plant associations along declining levels of tree diversity in a large‐scale, subtropical biodiversity experiment. We tested for effects of tree species richness, host functional and phylogenetic diversity, and host functional (leaf trait) and phylogenetic composition on species, phylogenetic and network composition of herbivore communities. We found that phylogenetic host composition and related palatability/defence traits but not tree species richness significantly affected herbivore communities and interaction network complexity at both the species and community levels. Our study indicates that evolutionary dependencies and functional traits of host plants determine the composition of higher trophic levels and corresponding interaction networks in species‐rich ecosystems. Our findings highlight that characteristics of the species lost have effects on ecosystem structure and functioning across trophic levels that cannot be predicted from mere reductions in species richness.     

传粉网络的研究进展:网络的结构和动态

植物与传粉者之间相互作用,构成了复杂的传粉网络。近年来,社会网络分析技术的发展使得复杂生态网络的研究成为可能。从群落水平上研究植物与传粉者之间的互惠关系,为理解群落的结构和动态以及花部特征的演化提供了全新的视角。传粉网络的嵌套结构说明自然界的传粉服务存在冗余,而且是相对泛化的物种主导了传粉。在多年或者多季度的传粉网络中,虽然有很高的物种替换率,但是其网络结构仍然保持相对稳定,说明传粉网络对干扰有很强的抗性。尽管有关网络结构和动态的研究逐渐增多,但传粉网络维持的机制仍不清楚。网络结构可以部分由花部特征与传粉者的匹配来解释,也受到系统发生的制约,影响因素还包括群落构建的时间和物种多样性,以及物种在群落中的位置。开展大尺度群落动态的研究,为探索不同时间尺度、不同物种多样性水平上的传粉网络的生态学意义提供了条件。但已有的研究仍存在不足,比如基于访问观察的网络无法准确衡量传粉者的访问效率和植物间的花粉流动,以及结果受到调查精度区域研究不平衡的制约等。目前的研究只深入到传粉者携带花粉构成成分的水平,传粉者访问植物的网络不能代表植物的整个传粉过程。因此,研究应当更多地深入到物种之间关系对有性生殖的切实影响上。     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.     

Ant-Plant Interaction in a Tropical Savanna: May the Network Structure Vary over Time and Influence on the Outcomes of Associations?

Plant-animal interactions occur in a community context of dynamic and complex ecological interactive networks. The understanding of who interacts with whom is a basic information, but the outcomes of interactions among associates are fundamental to draw valid conclusions about the functional structure of the network. Ecological networks studies in general gave little importance to know the true outcomes of interactions and how they may change over time. We evaluate the dynamic of an interaction network between ants and plants with extrafloral nectaries, by verifying the temporal variation in structure and outcomes of mutualism for the plant community (leaf herbivory). To reach this goal, we used two tools: bipartite network analysis and experimental manipulation. The networks exhibited the same general pattern as other mutualistic networks: nestedness, asymmetry and low specialization and this pattern was maintained over time, but with internal changes (species degree, connectance and ant abundance). These changes influenced the protection effectiveness of plants by ants, which varied over time. Our study shows that interaction networks between ants and plants are dynamic over time, and that these alterations affect the outcomes of mutualisms. In addition, our study proposes that the set of single systems that shape ecological networks can be manipulated for a greater understanding of the entire system.     

Interdomain ecological networks between plants and microbes

While macroscopic interkingdom relationships have been intensively investigated in various ecosystems, the above–belowground ecology in natural ecosystems has been poorly understood, especially for the plant–microbe associations at a regional scale. In this study, we proposed a workflow to construct interdomain ecological networks (IDEN) between multiple plants and various microbes (bacteria and archaea in this study). Across 30 latitudinal forests in China, the regional IDEN showed particular topological features, including high connectance, nested structure, asymmetric specialization and modularity. Also, plant species exhibited strong preference to specific microbial groups, and the observed network was significantly different from randomly rewired networks. Network module analysis indicated that a majority of microbes associated with plants within modules rather than across modules, suggesting specialized associations between plants and microorganisms. Consistent plant–microbe associations were captured via IDENs constructed within individual forest locations, which reinforced the validity of IDEN analysis. In addition, the plant–forest link distribution showed the geographical distribution of plants had higher endemicity than that of microorganisms. With cautious experimental design and data processing, this study shows interdomain species associations between plants and microbes in natural forest ecosystems and provides new insights into our understanding of meta‐communities across different domain species.     

Niche partitioning due to adaptive foraging reverses effects of nestedness and connectance on pollination network stability

Much research debates whether properties of ecological networks such as nestedness and connectance stabilise biological communities while ignoring key behavioural aspects of organisms within these networks. Here, we computationally assess how adaptive foraging (AF) behaviour interacts with network architecture to determine the stability of plant–pollinator networks. We find that AF reverses negative effects of nestedness and positive effects of connectance on the stability of the networks by partitioning the niches among species within guilds. This behaviour enables generalist pollinators to preferentially forage on the most specialised of their plant partners which increases the pollination services to specialist plants and cedes the resources of generalist plants to specialist pollinators. We corroborate these behavioural preferences with intensive field observations of bee foraging. Our results show that incorporating key organismal behaviours with well‐known biological mechanisms such as consumer‐resource interactions into the analysis of ecological networks may greatly improve our understanding of complex ecosystems.     

Analysing ecological networks of species interactions

Network approaches to ecological questions have been increasingly used, particularly in recent decades. The abstraction of ecological systems – such as communities – through networks of interactions between their components indeed provides a way to summarize this information with single objects. The methodological framework derived from graph theory also provides numerous approaches and measures to analyze these objects and can offer new perspectives on established ecological theories as well as tools to address new challenges. However, prior to using these methods to test ecological hypotheses, it is necessary that we understand, adapt, and use them in ways that both allow us to deliver their full potential and account for their limitations. Here, we attempt to increase the accessibility of network approaches by providing a review of the tools that have been developed so far, with – what we believe to be – their appropriate uses and potential limitations. This is not an exhaustive review of all methods and metrics, but rather, an overview of tools that are robust, informative, and ecologically sound. After providing a brief presentation of species interaction networks and how to build them in order to summarize ecological information of different types, we then classify methods and metrics by the types of ecological questions that they can be used to answer from global to local scales, including methods for hypothesis testing and future perspectives. Specifically, we show how the organization of species interactions in a community yields different network structures (e.g., more or less dense, modular or nested), how different measures can be used to describe and quantify these emerging structures, and how to compare communities based on these differences in structures. Within networks, we illustrate metrics that can be used to describe and compare the functional and dynamic roles of species based on their position in the network and the organization of their interactions as well as associated new methods to test the significance of these results. Lastly, we describe potential fruitful avenues for new methodological developments to address novel ecological questions.     

Anthropogenic disturbance and rainfall variation threaten the stability of plant–ant interactions in the Brazilian Caatinga

Climate change is projected to exacerbate the effects of anthropogenic disturbance, with negative impacts on ecosystem stability and functioning. We evaluate the additive and combined effects of chronic anthropogenic disturbance (CAD) and rainfall variation on the temporal stability of mutualistic EFN‐bearing plant–ant networks in a Caatinga dry forest. We evaluated whether changes in the stability of these interactions are driven by changes in the stability of the communities of partners involved and/or in ant behavior. We sampled EFN‐bearing plant–ant networks in sixteen 20 × 20 m plots distributed across CAD and rainfall gradients. The stability of EFN‐bearing plant and attendant–ant communities were measured as the inverse of temporal differences in their community structure and composition. We also computed the stability of EFN‐bearing plant–ant networks by measuring the inverse of temporal differences in network specialization metrics. We found that, in general, the structure and composition of plant and ant interacting communities were similarly stable along both environmental gradients. Only CAD and its interaction with rainfall affected the temporal stability of EFN‐bearing plant diversity, which declined as CAD increased, with a more pronounced relationship in wetter areas. However, variation in levels of CAD and, to a lesser extent, rainfall greatly modulated the stability of EFN‐bearing plant–ant network specialization. CAD reduced the stability of network generality (specialization at the ant level), an effect that was much stronger in wetter areas. Meanwhile, the stability in network vulnerability (specialization at the plant level) decreased with the increase of CAD and the decrease of rainfall levels. Finally, there was a trend of decreasing stability in specialization of the overall network with increasing CAD. Our results suggest that changes in the structure of interaction networks are mainly driven by a switch in ant behavior rather than by changes in the structure and composition of plant and ant communities between years.     

Soil and vegetation features determine the nested pattern of ant–plant networks in a tropical rainforest

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Mutualistic networks: moving closer to a predictive theory

Plant–animal mutualistic networks sustain terrestrial biodiversity and human food security. Global environmental changes threaten these networks, underscoring the urgency for developing a predictive theory on how networks respond to perturbations. Here, I synthesise theoretical advances towards predicting network structure, dynamics, interaction strengths and responses to perturbations. I find that mathematical models incorporating biological mechanisms of mutualistic interactions provide better predictions of network dynamics. Those mechanisms include trait matching, adaptive foraging, and the dynamic consumption and production of both resources and services provided by mutualisms. Models incorporating species traits better predict the potential structure of networks (fundamental niche), while theory based on the dynamics of species abundances, rewards, foraging preferences and reproductive services can predict the extremely dynamic realised structures of networks, and may successfully predict network responses to perturbations. From a theoretician's standpoint, model development must more realistically represent empirical data on interaction strengths, population dynamics and how these vary with perturbations from global change. From an empiricist's standpoint, theory needs to make specific predictions that can be tested by observation or experiments. Developing models using short‐term empirical data allows models to make longer term predictions of community dynamics. As more longer term data become available, rigorous tests of model predictions will improve.     

Do bipartite binary antagonistic and mutualistic networks have different responses to the taxonomic resolution of nodes?

1. Bipartite network analyses are increasingly being used to better understand mutualistic and antagonistic plant–insect interactions at the community level. As a result of taxonomic limitations, it is usually very difficult to identify all nodes of a network down to the species level and many studies leave some specimens identified as lower resolution taxa. Accordingly, we do not know how much a lower resolution taxonomic representation changes the network structure compared with a representation with all nodes at species level. 2. The present study aimed to test whether insect–plant networks built using different combinations of taxonomic levels can still preserve the same basic structure of networks built only with species. 3. In total, 73 bipartite published interaction networks (mutualistic and antagonistic) were selected, which were turned into binary networks and reconstructed using the nodes classified as species, genus, family or order (representing different levels of classification difficulty). The network structures were compared using their binary representations mainly using connectance, NODF (Nestedness metric based on Overlap and Decreasing Fill) and modularity. 4. The mutualistic network structure was strongly linearly related to the original network structures if all nodes were grouped up to genus level. In antagonistic networks, the structure was related to the original network only if nodes were only grouped at the species level. 5. The findings of the present study are especially helpful for comparative network studies, such as those assessing the effects of environmental gradients. For mutualistic networks, Citizen Science programmes can provide useful ecological indicators, even with its taxonomic limitations.