Phenology drives mutualistic network structure and diversity

Several network properties have been identified as determinants of the stability and complexity of mutualistic networks. However, it is unclear which mechanisms give rise to these network properties. Phenology seems important, because it shapes the topology of mutualistic networks, but its effects on the dynamics of mutualistic networks have scarcely been studied. Here, we study these effects with a general dynamical model of mutualistic and competitive interactions where the interaction strength depends on the temporal overlap between species resulting from their phenologies. We find a negative complexity-stability relationship, where phenologies maximising mutualistic interactions and minimising intraguild competitive interactions generate speciose, nested and poorly connected networks with moderate asymmetry and low resilience. Moreover, lengthening the season increases diversity and resilience. This highlights the fragility of real mutualistic communities with short seasons (e.g. Arctic environments) to drastic environmental changes.     

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.     

The network structure of myrmecophilic interactions

1. Ants establish mutualistic interactions involving a wide range of protective relationships (myrmecophily), in which they provide defence against enemies and partners provide food rewards and/or refuge. Although similar in the general outcome, myrmecophilic interactions differ in some characteristics such as quantity and quality of rewards offered by partners which may lead to different specialisation levels and, consequently, to different network properties. 2. The aim of this study was to identify structural patterns in myrmecophilic interaction networks, focusing on aspects related to specialisation: network modularity, nestedness and taxonomic relatedness of interaction ranges. To achieve this, a database of networks was compiled, including the following interactions: ants and domatia‐bearing plants (myrmecophytes); ants and extrafloral nectary‐bearing plants (EFNs); ants and floral nectary‐bearing plants (FNs); ants and Lepidoptera caterpillars; and ants and Hemiptera. 3. Myrmecophilic networks differed in their topology, with ant–myrmecophyte and ant–Lepidoptera networks being similar in their structural properties. A continuum was found, ranging from highly modular networks and phylogenetically structured interaction ranges in ant–myrmecophyte followed by ant–Lepidoptera networks to low modularity and taxonomically unrelated interaction ranges in ant–Hemiptera, EFN and FN networks. 4. These results suggest that different network topologies may be found across communities of species with similar interaction types, but also, that similar network topologies can be achieved through different mechanisms such as those between ants and myrmecophytes or Lepidoptera larvae. This study contributes to a generalisation of myrmecophilic network patterns and a better understanding of the relationship between specialisation and network topology.     

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.     

Low modularity and specialization in a commensalistic epiphyte–phorophyte network in a tropical cloud forest

Species interactions can shape the structure of natural communities. Such sets of interactions have been described as complex ecological networks, an example of which is the commensal network formed by epiphyte–phorophyte interactions. Vascular epiphytes germinate and grow on phorophytes (support trees), assuming a horizontal distribution (among the phorophyte species) and a vertical distribution (from the base of the tree trunk to the crown of phorophytes, i.e., through ecological zones). Here, we investigated the organization of these structural dimensions of the epiphyte–phorophyte network in a Brazilian tropical montane cloud forest. The analyzed network, comprising 66 epiphyte species and 22 phorophyte species, exhibited a nested structure with a low degree of specialization, a typical pattern for epiphyte–phorophyte networks in forests. The network was slightly modular, with 65% of the species common to three modules, and had vertical structure corresponding to the vertical organization of the phorophytes. The size (diameter at breast height) of phorophyte individuals influenced the network structure, possibly due to the increase in habitat area, the time available for colonization by epiphytes, and a greater number of microenvironments. We found that the distribution of the epiphyte species differed between the phorophyte ecological zones, with greater richness in the lower portions and greater abundance in the upper portions of the phorophytes. The results provide relevant guidance for future research on the characteristics and the vertical and horizontal organization of vascular epiphyte and phorophyte networks. Abstract in Portuguese is available with online material.     

Predicting abundances of plants and pollinators using a simple compartmental mutualistic model

Key gaps to be filled in population and community ecology are predicting the strength of species interactions and linking pattern with process to understand species coexistence and their relative abundances. In the case of mutualistic webs, like plant–pollinator networks, advances in understanding species abundances are currently limited, mainly owing to the lack of methodological tools to deal with the intrinsic complexity of mutualisms. Here, we propose an aggregation method leading to a simple compartmental mutualistic population model that captures both qualitatively and quantitatively the size-segregated populations observed in a Mediterranean community of nectar-producing plant species and nectar-searching animal species. We analyse the issue of optimal aggregation level and its connection with the trade-off between realism and overparametrization. We show that aggregation of both plants and pollinators into five size classes or compartments leads to a robust model with only two tunable parameters. Moreover, if, in each compartment, (i) the interaction coefficients fulfil the condition of weak mutualism and (ii) the mutualism is facultative for at least one party of the compartment, then the interactions between different compartments are sufficient to guarantee global stability of the equilibrium population.     

Effect of local spatial plant distribution and conspecific density on bumble bee foraging behaviour

1. Size variations in pollinator populations may modify competitive interactions among foragers. Competition among pollinators has been shown to lead to one of two contrasting behaviours: either specialisation to the most profitable plant species or generalisation to several species. When foraging, pollinators are also confronted with heterogeneity in the spatial distribution of plant resources. Because variations in both the forager density and plant spatial distribution can affect pollinator behaviour, focus was on the interactive effect of these two factors. 2. Bumble bee (Bombus terrestris L.) individuals were trained on a focal species (Lotus corniculatus L.) and experimentally tested whether variations in the forager density (two or six bumble bees foraging together), plant community spatial distribution (two plant species: L. corniculatus and Medicago sativa, which were either patchily or randomly distributed), and their interaction modified bumble bee foraging behaviour. 3. It was shown that when confronted with a high forager density, bumble bees focused their visits towards the most familiar species, especially when foraging under a random plant distribution. These modifications affected the fruiting of the focal plant species, with a significantly lower reproductive success under low density/patchy conditions. 4. This study demonstrates that the foraging decisions of bumble bees are influenced by variations in both the conspecific density and plant spatial distribution. Given the increasing impact of human activities on plant‐pollinator communities, this raises the question of the potential implications of these results for plant communities in natural conditions when confronted with variations in the pollinator density and spatial distribution of plants.     

Abundance and generalisation in mutualistic networks: solving the chicken‐and‐egg dilemma

A frequent observation in plant–animal mutualistic networks is that abundant species tend to be more generalised, interacting with a broader range of interaction partners than rare species. Uncovering the causal relationship between abundance and generalisation has been hindered by a chicken‐and‐egg dilemma: is generalisation a by‐product of being abundant, or does high abundance result from generalisation? Here, we analyse a database of plant–pollinator and plant–seed disperser networks, and provide strong evidence that the causal link between abundance and generalisation is uni‐directional. Specifically, species appear to be generalists because they are more abundant, but the converse, that is that species become more abundant because they are generalists, is not supported by our analysis. Furthermore, null model analyses suggest that abundant species interact with many other species simply because they are more likely to encounter potential interaction partners.     

Lifelong foraging and individual specialisation are influenced by temporal changes of resource availability

Resource availability largely determines the distribution and behaviour of organisms. In plant–pollinator communities, availability of floral resources may change so rapidly that pollinator individuals can benefit from switching between multiple resources, i.e. different flowering plant species. Insect pollinator individuals of a given generation often occur in different time windows during the reproductive season. This temporal variation in individual occurrences, together with the rapidly changing resource availability, may lead individuals of the same population to encounter and use different resources, resulting in an apparent individual specialisation. We hypothesized, that 1) individual pollinators change their resource use (flower visitation) during their lifetime according to the changing availability of floral resources, and that 2) temporal variation in individual occurrences of pollinators and in resource availability will partly explain individual specialisation. To test these hypotheses, we observed flower visitations of individually marked clouded Apollo butterflies Parnassius mnemosyne during one reproductive season. We found temporal changes in lifetime individual resource use that followed the changes in resource availability, indicating that butterflies can adjust foraging to varying resource availability. Individuals differed considerably in their resource use. This variation was partly explained by temporal variation in both floral resource availability and temporal occurrence of individual butterflies. We suggest the butterfly as a sequential specialist, i.e. short‐term specialist and long‐term generalist. This foraging plasticity can be essential for short‐living insect pollinators in rapidly changing environments. Although flowering dynamics do not fully explain the variability in foraging, our results highlight the importance of temporal dimension in resource use studies. Ultimately, the relative pace of environmental change compared to individual lifespan may be a key factor in resource use plasticity.     

Ericaceous plant–fungus network in a harsh alpine–subalpine environment

In terrestrial ecosystems, plant species and diverse root‐associated fungi form complex networks of host–symbiont associations. Recent studies have revealed that structures of those below‐ground plant–fungus networks differ between arbuscular mycorrhizal and ectomycorrhizal symbioses. Nonetheless, we still remain ignorant of how ericaceous plant species, which dominate arctic and alpine tundra, constitute networks with their root‐associated fungi. Based on a high‐throughput DNA sequencing data set, we characterized the statistical properties of a network involving 16 ericaceous plant species and more than 500 fungal taxa in the alpine–subalpine region of Mt. Tateyama, central Japan. While all the 16 ericaceous species were associated mainly with fungi in the order Helotiales, they varied remarkably in association with fungi in other orders such as Sebacinales, Atheliales, Agaricales, Russulales and Thelephorales. The ericaceous plant–fungus network was characterized by high symbiont/host preferences. Moreover, the network had a characteristic structure called ‘anti‐nestedness’, which has been previously reported in ectomycorrhizal plant–fungus networks. The results lead to the hypothesis that ericaceous plants in harsh environments can host unexpectedly diverse root‐associated fungal taxa, constituting networks whose structures are similar to those of previously reported ectomycorrhizal networks but not to those of arbuscular mycorrhizal ones.     

A conceptual framework for studying the strength of plant–animal mutualistic interactions

The strength of species interactions influences strongly the structure and dynamics of ecological systems. Thus, quantifying such strength is crucial to understand how species interactions shape communities and ecosystems. Although the concepts and measurement of interaction strength in food webs have received much attention, there has been comparatively little progress in the context of mutualism. We propose a conceptual scheme for studying the strength of plant–animal mutualistic interactions. We first review the interaction strength concepts developed for food webs, and explore how these concepts have been applied to mutualistic interactions. We then outline and explain a conceptual framework for defining ecological effects in plant–animal mutualisms. We give recommendations for measuring interaction strength from data collected in field studies based on a proposed approach for the assessment of interaction strength in plant–animal mutualisms. This approach is conceptually integrative and methodologically feasible, as it focuses on two key variables usually measured in field studies: the frequency of interactions and the fitness components influenced by the interactions.     

Influence of extrafloral nectary phenology on ant–plant mutualistic networks in a neotropical savanna

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Pollinators visit related plant species across 29 plant–pollinator networks

Understanding the evolution of specialization in host plant use by pollinators is often complicated by variability in the ecological context of specialization. Flowering communities offer their pollinators varying numbers and proportions of floral resources, and the uniformity observed in these floral resources is, to some degree, due to shared ancestry. Here, we find that pollinators visit related plant species more so than expected by chance throughout 29 plant–pollinator networks of varying sizes, with “clade specialization” increasing with community size. As predicted, less versatile pollinators showed more clade specialization overall. We then asked whether this clade specialization varied with the ratio of pollinator species to plant species such that pollinators were changing their behavior when there was increased competition (and presumably a forced narrowing of the realized niche) by examining pollinators that were present in at least three of the networks. Surprisingly, we found little evidence that variation in clade specialization is caused by pollinator species changing their behavior in different community contexts, suggesting that clade specialization is observed when pollinators are either restricted in their floral choices due to morphological constraints or innate preferences. The resulting pollinator sharing between closely related plant species could result in selection for greater pollinator specialization.     

Effects of emergence phenology, taxa tolerances and taxonomic resolution on the use of the Chironomid Pupal Exuvial Technique in river biomonitoring

1. We studied chironomid communities of four rivers in south‐eastern Finland, differing in their water quality, during summer 2004 using the Chironomid Pupal Exuvial Technique, CPET. The aims of the study were to (i) test the adequacy of the generic‐level identification in the CPET method, (ii) define the emergence patterns of chironomid taxa classified as intolerant to organic pollution, (iii) assess the tolerance levels of intolerant chironomids and (iv) identify taxa most indicative of good water quality. 2. Procrustean rotation analysis indicated very strong concordance between the ordinations using either species or genus‐level data, suggesting that generic‐level identification of chironomids is adequate for biomonitoring based on CPET. However, when only a few taxa occur in great numbers, it may be advisable to identify these to the species level, especially if these taxa are important indicators of the impact in question. 3. The detection of a particular species may require accurate timing of sampling, whereas a species‐rich genus might be detected throughout a season. Given that the emergence of chironomid species may vary from year‐to‐year and between sampling sites, community differences detected at the species level may be related to between‐site variation in species’ emergence patterns rather than true differences in species composition. 4. Indicator species analysis (IndVal) showed that the distribution and abundance of intolerant chironomid taxa differed strongly among the studied rivers. Some of the intolerant taxa were restricted to unimpacted conditions, whereas others occurred mainly in impacted rivers. Thus, the indicator status of some genera (e.g. Eukiefferiella, Parametriocnemus, Stempellinella and Tvetenia) needs reassessment.     

Effects of different types of low‐intensity management on plant‐pollinator interactions in Estonian grasslands

In the face of global pollinator decline, extensively managed grasslands play an important role in supporting stable pollinator communities. However, different types of extensive management may promote particular plant species and thus particular functional traits. As the functional traits of flowering plant species (e.g., flower size and shape) in a habitat help determine the identity and frequency of pollinator visitors, they can also influence the structures of plant−pollinator interaction networks (i.e., pollination networks). The aim of this study was to examine how the type of low‐intensity traditional management influences plant and pollinator composition, the structure of plant−pollinator interactions, and their mediation by floral and insect functional traits. Specifically, we compared mown wooded meadows to grazed alvar pastures in western Estonia. We found that both management types fostered equal diversity of plants and pollinators, and overlapping, though still distinct, plant and pollinator compositions. Wooded meadow pollination networks had significantly higher connectance and specialization, while alvar pasture networks achieved higher interaction diversity at a standardized sampling of interactions. Pollinators with small body sizes and short proboscis lengths were more specialized in their preference for particular plant species and the specialization of individual pollinators was higher in alvar pastures than in wooded meadows. All in all, the two management types promoted diverse plant and pollinator communities, which enabled the development of equally even and nested pollination networks. The same generalist plant and pollinator species were important for the pollination networks of both wooded meadows and alvar pastures; however, they were complemented by management‐specific species, which accounted for differences in network structure. Therefore, the implementation of both management types in the same landscape helps to maintain high species and interaction diversity.     

Relative effectiveness of insects versus hummingbirds as pollinators of Rubiaceae plants across elevation in Dominica,Caribbean

• Most angiosperms rely on animal pollination for reproduction, but the dependence on specific pollinator groups varies greatly between species and localities. Notably, such dependence may be influenced by both floral traits and environmental conditions. Despite its importance, their joint contribution has rarely been studied at the assemblage level.
• At two elevations on the Caribbean island of Dominica, we measured the floral traits and the relative contributions of insects versus hummingbirds as pollinators of plants in the Rubiaceae family. Pollinator importance was measured as visitation rate (VR) and single visit pollen deposition (SVD), which were combined to assess overall pollinator effectiveness (PE).
• In the wet and cool Dominican highland, we found that hummingbirds were relatively more frequent and effective pollinators than insects, whereas insects and hummingbirds were equally frequent and effective pollinators at the warmer and less rainy midelevation. Furthermore, floral traits correlated independently of environment with the relative importance of pollinators, hummingbirds being more important in plant species having flowers with long and wide corollas producing higher volumes of dilute nectar.
• Our findings show that both environmental conditions and floral traits influence whether insects or hummingbirds are the most important pollinators of plants in the Rubiaceae family, highlighting the complexity of plant–pollinator systems.

     

The effects of macroinvertebrate taxonomic resolution in large landscape bioassessments: an example from the Mid-Atlantic Highlands, U.S.A.

1. During late spring 1993–1995, the U.S. Environmental Protection Agency's Environmental Monitoring and Assessment Program (EMAP) sampled 490 wadeable streams in the mid‐Atlantic Highlands (MAH) of the U.S. for a variety of physical, chemical and biological indicators of environmental condition. We used the resulting data set to evaluate the importance of differing levels of macroinvertebrate taxonomic resolution in bioassessments by comparing the ability of family versus genus to detect differences among sites classified by type and magnitude of human impact and by stream size. We divided the MAH into two physiographic regions: the Appalachian Plateau where mine drainage (MD) and acidic deposition are major stressors, and the Ridge and Valley where nutrient enrichment is a major stressor. Stream sites were classified into three or four impact classes based on water chemistry and habitat. We used stream order (first to third Strahler order) in each region as a measure of stream size. Ordination, 2 × 2 chi‐square and biotic metrics were used to compare the ability of family and genus to detect differences among both stressor and size classes. 2. With one notable exception, there were only a small number of different genera per family (interquartile range = 1–4). Family Chironomidae, however, contained 123 different genera. As a result, significant information loss occurred when this group was only classified to family. The family Chironomidae did not discriminate among the predefined classes but many chironomid genera did: by chi‐square analysis, 10 and 28 chironomid genera were significant in discriminating MD and nutrient impacts, respectively. 3. Family and genus data were similar in their ability to distinguish among the coarse impacts (e.g. most severe versus least severe impact classes) for all cases. Though genus data in many cases distinguished the subtler differences (e.g. mixed/moderate impacts versus high or low impacts) better than family, differences in significance levels between family and genus analyses were relatively minor. However, genus data detected differences among stream orders in ordination analyses that were not revealed at the family level. In the ordinations, both family and genus levels of analysis responded to similar suites of environmental variables. 4. Our results suggest that identification to the family level is sufficient for many bioassessment purposes. However, identifications to genus do provide more information in genera‐rich families like Chironomidae. Genus or finer levels of identification are important for investigating natural history, stream ecology, biodiversity and indicator species. Decisions about the taxonomic level of identification need to be study specific and depend on available resources (cost) and study objectives.