Flower-visitor Networks Research Articles

Plant–flower visitor networks in a serpentine metacommunity: assessing traits associated with keystone plant species

Consistent topology of plant–pollinator networks across space may be due to substitutability of the plant species most important for community function (keystone species). It is unclear, however, whether keystone species identity varies within a community type and what traits underlie this variation. Using a network biology approach, we assess whether keystone plant species vary across a metacommunity of five serpentine seeps in California and determine the features that predict their identity. We define keystone species as those with high strength, low node specialization index (NSI), and/or low d′ and determine whether these parameters are predicted by floral traits (flower biomass, number of open flowers per plant, symmetry, or stamen number) and/or ecological features (variation in local floral abundance, endemism) within seeps and across the metacommunity. Keystone species identity varied among seeps and was associated with local flower abundance: mean floral abundance correlated positively with strength but negatively with NSI within most seeps as well as across the metacommunity. For the metacommunity, flower biomass correlated negatively with NSI while variation in flower abundance correlated negatively with strength. Across the metacommunity, the d′ metric was associated with flower biomass, whereby plants with smaller flowers interacted with the most abundant pollinators across the metacommunity. Results suggest that connectance and interaction evenness may not be greatly influenced by community composition turnover due to substitution of keystone plant species across space. Keystone species can be predicted by functional traits but which trait (flower abundance or size) depended on the metric used and the level observed.

Are empidine dance flies major flower visitors in alpine environments? A case study in the Alps, France.

Pollination is one of the most important ecosystem services and bees the most important pollinators. As a population decline of bees has been documented in numerous regions of the world, it is crucial to develop understanding on other possible pollinators. Here, we study the potential pollination impact of Diptera, and among them Empidinae, in an alpine environment, where the abundance of bees is naturally lower. Interactions between 19 entomophilous plants and their flower visitors were recorded in a subalpine meadow in the French Alps during six weeks. Visitation frequencies were used to build the flower-visitor network. Our results show that interactions between flies and plants are dominant; flies represent more than 60% of all visitors, with 54% of them being Empidinae. We especially found that flies, Empidinae and bees are the main visitors of 11, three and one plants, respectively. When considering both bees and Syrphidae together, six plants were more visited by Empidinae; when considering bees and Syrphidae separately, 10 plants were more visited by Empidinae than by bees or Syrphidae. The results support the idea that flies widely replace bees as main flower visitors at altitude, and among them the Empidinae might play a key role in pollination.

Differences in flower visitation networks between an oceanic and a continental island

Two important biological differences between oceanic and continental islands are that the former usually have lower species richness and a higher degree of taxonomic disharmony than the latter. Although there is some evidence of less complex interaction networks on oceanic islands, only a few studies have compared island communities with each other or with mainland communities. Here, we analyse the species composition and structural properties of quantitative flower visitation networks in two communities of each of two different island systems: the Canary Islands (oceanic origin) and the Balearic Islands (continental origin). We compared different network parameters to inform us about their vulnerability in the face of different types of disturbance. The number of species was greater in the Balearic than in the Canarian networks but, contrary to expectations, the total number and diversity of interactions did not differ between them. Moreover, a greater number of opportunistic species and the presence of super-generalist species on the oceanic island led to significantly higher values of quantitative connectance and nestedness relative to those on the continental island. Given that these two parameters are associated with network stability, our findings support the hypothesis that oceanic island communities are less vulnerable to perturbations than are those of continental islands, although further studies with a network approach are needed to determine whether this is a general pattern. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 00, 000–000.

Comparing the Structure and Robustness of Passifloraceae - Floral Visitor and True Pollinator Networks in a Lowland Atlantic Forest

We investigated the plant-pollinator interactions of Passifloraceae occurring in fragments of lowland semi-deciduous Atlantic forest. We described floral biology, pollination syndromes and the pollinators of Passiflora alata, Passiflora kermesina, Passiflora suberosa, Passiflora malacophylla and Mitostemma glaziovii. We examined the robustness of the interaction networks to species loss, a plausible scenario resulting from forest fragmentation. The effects of pollination syndrome (flower size) on network robustness was also examined. Passiflora alata, P. malacophylla and P. suberosa were pollinated by bees of different corporal sizes. P. kermesina and M. glaziovii presented the highest diversity of visitors and were pollinated mainly by hummingbirds and butterflies, respectively. Through the analysis of the networks we differentiate the structures of the flower-visitor network with the ‘true’ plant-pollinator network. The robustness of the flower-visitor network to animal loss was generally high, but it declined when only true pollinators were included in the network. The sequential loss of plants from the flower-visitor network resulted in low robustness: the loss of key plants could have significant cascading effects on the animals feeding on them within the forest fragment. Future studies should consider the interactions between all flowering plants and animals in this habitat in order to guide conservation and management plans for these forest fragments.

How different link weights affect the structure of quantitative flower–visitation networks

Despite the considerable work carried out to assess the structure of weighted and unweighted mutualistic networks, little is known about how different ways to measure the weight of interactions can influence network parameters used to describe such structures. The use of an appropriate ‘link weight’ is especially important if we want to move toward a more functional perspective in ecological network studies. Here, we evaluated how the use of five different link weights, starting with the simplest one – the number of visits – and including progressively information on total census time, number of flowers observed, number of flowers visited and total flower abundance of each species in a plant community, influences widely used descriptors of network structure. We analyzed different network-level properties: weighted nestedness, flower–visitor generality, plant generality, complementary specialization H2′, interaction evenness and interaction diversity, as well as species-level parameters: specialization index d′ and strength. We built two quantitative flower–visitation networks from two different communities sampled during two consecutive years, in which we also measured independently flower abundance of each plant species. Results showed that the type of link weight used can significantly alter network structure. A clear trend toward more specialized interactions (decreased flower–visitor generality, increased H2′ and d′), higher heterogeneity in the frequency of interactions (lower evenness and diversity of interactions) and higher weighted nestedness was found as interaction weight gained in complexity. However, standardizing only for total censusing time had only weak effects on network parameters. Our findings highlight the importance of carefully considering the most appropriate link weight for each ecological network study, emphasizing that comparisons across networks that use different weights might lead to flawed results and thus to ecological misinterpretations of network structures.

Strong, Long-Term Temporal Dynamics of an Ecological Network

Nature is organized into complex, dynamical networks of species and their interactions, which may influence diversity and stability. However, network research is, generally, short-term and depict ecological networks as static structures only, devoid of any dynamics. This hampers our understanding of how nature responds to larger disturbances such as changes in climate. In order to remedy this we studied the long-term (12-yrs) dynamics of a flower-visitation network, consisting of flower-visiting butterflies and their nectar plants. Global network properties, i.e. numbers of species and links, as well as connectance, were temporally stable, whereas most species and links showed a strong temporal dynamics. However, species of butterflies and plants varied bimodally in their temporal persistance: Sporadic species, being present only 1–2(-5) years, and stable species, being present (9-)11–12 years, dominated the networks. Temporal persistence and linkage level of species, i.e. number of links to other species, made up two groups of species: Specialists with a highly variable temporal persistence, and temporally stable species with a highly variable linkage level. Turnover of links of specialists was driven by species turnover, whereas turnover of links among generalists took place through rewiring, i.e. by reshuffling existing interactions. However, in spite of this strong internal dynamics of species and links the network appeared overall stable. If this global stability-local instability phenomenon is general, it is a most astonishing feature of ecological networks.

Daily temporal structure in African savanna flower visitation networks and consequences for network sampling

Ecological interaction networks are a valuable approach to understanding plant-pollinator interactions at the community level. Highly structured daily activity patterns are a feature of the biology of many flower visitors, particularly provisioning female bees, which often visit different floral sources at different times. Such temporal structure implies that presence/absence and relative abundance of specific flower-visitor interactions (links) in interaction networks may be highly sensitive to the daily timing of data collection. Further, relative timing of interactions is central to their possible role in competition or facilitation of seed set among coflowering plants sharing pollinators. To date, however, no study has examined the network impacts of daily temporal variation in visitor activity at a community scale. Here we use temporally structured sampling to examine the consequences of daily activity patterns upon network properties using fully quantified flower-visitor interaction data for a Kenyan savanna habitat. Interactions were sampled at four sequential three-hour time intervals between 06:00 and 18:00, across multiple seasonal time points for two sampling sites. In all data sets the richness and relative abundance of links depended critically on when during the day visitation was observed. Permutation-based null modeling revealed significant temporal structure across daily time intervals at three of the four seasonal time points, driven primarily by patterns in bee activity. This sensitivity of network structure shows the need to consider daily time in network sampling design, both to maximize the probability of sampling links relevant to plant reproductive success and to facilitate appropriate interpretation of interspecific relationships. Our data also suggest that daily structuring at a community level could reduce indirect competitive interactions when coflowering plants share pollinators, as is commonly observed during flowering in highly seasonal habitats.

Scaling down from species to individuals: a flower–visitation network between individual honeybees and thistle plants

Studies of ecological networks usually focus upon interaction patterns among species. However, linkage among species is mediated by their constituting individuals. Thus, every linked species pair in a network encapsulates a new network of interacting individuals. Very few studies outside the sociology of larger animals have investigated networks at the level of the individual. Here, we analyse the structure of a flower–visitation network of individual thistles Cirsium arvense and honeybees Apis mellifera in a small meadow patch in Denmark. We marked and numbered 62 honeybees and 32 thistle stems and monitored all floral visits. The constructed bipartite network of individual plants and bees had a high connectance and low nestedness, but it was not significantly modular. Frequency distributions of number of links per species (i.e. linkage level) had their best fit to a truncated power law, and interactions were asymmetrical. Unipartite networks of either plants or bees had exceedingly short average path length and high clustering. Linkage level of plants increased with their number of flower heads and height of inflorescence (floral display parameters). Overall, the individual network of honeybees and thistles was denser linked than what is known from species pollination networks. Characteristics of both plants (e.g. floral display) and animals (e.g. foraging behaviour) are likely to generate this intra–specific, inter–individual link pattern. Such features of individual–individual networks may scale up and become important drivers of the structure and dynamics of species–species networks.

Land use intensity in grasslands: Changes in biodiversity, species composition and specialisation in flower visitor networks

The relationship between resource availability and biodiversity of consumers has gained particular attention with the increasing loss of biodiversity. We evaluated resource availability on meadows of low intensity (low/unfertilised, mown once or twice per year) and meadows of high-intensity land use (high fertilisation, mown twice or thrice) before and after the first mowing in relation to network specialisation, species richness and composition of flower visitors. We studied 40 meadows, simultaneously sampling one meadow of low intensity and one meadow of high-intensity land use. Each survey yielded a separate interaction network, comprising all flower visitors found during 6 h in an area of 1000 m 2. In total we recorded 105 plant species and 586 flower visitor species. Species composition of plants and flower visitors differed considerably between the two management regimes, with species overlaps of 43% in plants and 42% in flower visitors. Complementary specialisation of flower visitors differed between taxa: dipterans were significantly less specialised than beetles and butterflies, and bees had the highest degree of specialisation. Earlier in the season (before mowing), meadows of low-intensity land use were significantly richer in flowering plant, bee and butterfly species. They also showed more plant–flower visitor interactions, greater flowering areas and higher individual numbers of butterflies than meadows of high-intensity land use. However, later in the season (after mowing) management types differed only in plant species richness, being higher on meadows of low-intensity land use. We conclude that variations in plant species composition resulting from differences in grassland management may alter plant–flower visitor interactions. Moreover, an impoverishment of flower diversity has stronger effects on the diversity and species composition of specialised flower visitor groups than on little or unspecialised flower visitors.

Agricultural surroundings support flower–visitor networks in an Afrotropical rain forest

Local habitat structure and resource availability appear to be of great importance for the diversity, abundance, and community structure of bees. We examined the contribution of three different habitat types (farmland, forest edge, forest understory) to bee diversity in a tropical forest-agriculture mosaic in Western Kenya and analysed differences and overlap in plant-bee community interactions between nearby habitats. We used network properties (network size and specialization indices) and bee species turnover to examine temporal and spatial variation of flower–visitation interaction networks in general and in bee species composition in detail across habitats. In total we found 121 bee and 89 plant species involved in the interactions. Results suggest that bees were limited by floral resources because the largest networks, highest diversity, and largest abundances were found at the forest edge and in the farmland which hosted higher amounts of flowers and a more homogeneous distribution of resources in space and time. Forest in the study area is characterized by (1) lower flower density and (2) more humid conditions relative to the farmland. We therefore suggest that the species-rich and structurally diverse farmland acts as a “pollinator rescue” which supports bee communities in the natural forest. We advise conservation managers and politicians to conserve the structural richness of the farmland to (1) preserve bee diversity within the farmland and (2) conserve positive effects of the farmland on bee activity in the forest remnant.

Cheaters in mutualism networks

Mutualism-network studies assume that all interacting species are mutualistic partners and consider that all links are of one kind. However, the influence of different types of links, such as cheating links, on network organization remains unexplored. We studied two flower-visitation networks (Malpighiaceae and Bignoniaceae and their flower visitors), and divide the types of link into cheaters (i.e. robbers and thieves of flower rewards) and effective pollinators. We investigated if there were topological differences among networks with and without cheaters, especially with respect to nestedness and modularity. The Malpighiaceae network was nested, but not modular, and it was dominated by pollinators and had much fewer cheater species than Bignoniaceae network (28% versus 75%). The Bignoniaceae network was mainly a plant-cheater network, being modular because of the presence of pollen robbers and showing no nestedness. In the Malpighiaceae network, removal of cheaters had no major consequences for topology. In contrast, removal of cheaters broke down the modularity of the Bignoniaceae network. As cheaters are ubiquitous in all mutualisms, the results presented here show that they have a strong impact upon network topology.

Ecological modules and roles of species in heathland plant–insect flower visitor networks

1. Co-existing plants and flower-visiting animals often form complex interaction networks. A long-standing question in ecology and evolutionary biology is how to detect nonrandom subsets (compartments, blocks, modules) of strongly interacting species within such networks. Here we use a network analytical approach to (i) detect modularity in pollination networks, (ii) investigate species composition of modules, and (iii) assess the stability of modules across sites. 2. Interactions between entomophilous plants and their flower-visitors were recorded throughout the flowering season at three heathland sites in Denmark, separated by >or= 10 km. Among sites, plant communities were similar, but composition of flower-visiting insect faunas differed. Visitation frequencies of visitor species were recorded as a measure of insect abundance. 3. Qualitative (presence-absence) interaction networks were tested for modularity. Modules were identified, and species classified into topological roles (peripherals, connectors, or hubs) using 'functional cartography by simulated annealing', a method recently developed by Guimerà & Amaral (2005a). 4. All networks were significantly modular. Each module consisted of 1-6 plant species and 18-54 insect species. Interactions aggregated around one or two hub plant species, which were largely identical at the three study sites. 5. Insect species were categorized in taxonomic groups, mostly at the level of orders. When weighted by visitation frequency, each module was dominated by one or few insect groups. This pattern was consistent across sites. 6. Our study adds support to the conclusion that certain plant species and flower-visitor groups are nonrandomly and repeatedly associated. Within a network, these strongly interacting subgroups of species may exert reciprocal selection pressures on each other. Thus, modules may be candidates for the long-sought key units of co-evolution.

Size constraints and flower abundance determine the number of interactions in a plant–flower visitor web

The number of interactions with flower visitor species differs considerably among insect pollinated plants. Knowing the causes for this variation is central to the conservation of single species as well as whole plant–flower visitor communities. Species specific constraints on flower visitor numbers are seldom investigated at the community level. In this study we tested whether flower size parameters set constraints on the morphology of the potential nectar feeding visitors and thus determine the number of visitor species. We studied three possible constraints: the depth and width of tubular structures hiding the nectar (nectar holder depth and width) and the size of flower parts that visitors can land on (size of the alighting place). In addition we assess the role of flower abundance on this relationship. We hypothesized that the stronger size constraints and the smaller flower abundance, the smaller the number of visitor species will be. Our study of a Mediterranean plant–flower visitor community revealed that nectar holder depth, nectar holder width and number of flowers explained 71% of the variation in the number of visitor species. The size of the alighting place did not restrict the body length of the visitors and was not related to visitor species number. In a second step of the analyses we calculated for each plant species the potential number of visitors by determining for each insect species of the local visitor pool whether it passed the morphological limits set by the plant. These potential numbers were highly correlated with the observed numbers (r2=0.5, p<0.001). For each plant species we tested whether the observed visitors were a random selection out of these potential visitors by comparing the mean of the observed and expected proboscis length distributions. For most plant species the observed mean was not significantly different from the random means. Our findings shed light on the way plant–flower visitor networks are structured. Knowing the constraints on interaction patterns will be an important prerequisite to formulate realistic null models and understand patterns of resource partitioning as well as coevolutionary processes.

Foliar Herbivory Affects Floral Characters and Plant Attractiveness to Pollinators: Implications for Male and Female Plant Fitness

Foliar Herbivory Affects Floral Characters and Plant Attractiveness to Pollinators: Implications for Male and Female Plant Fitness