Similar seed preferences explain trophic ecology of functionally distinct, but co-occurring and closely related harvester ants.

To understand how food resource use and partitioning by closely related species allows local coexistence, it is key to determine whether a species' diet reflects food availability or food preferences. Here, we analysed the diets, seed selection, and seed preferences of three closely related harvester ants: Messor barbarus, M. bouvieri, and M. capitatus. Sympatric within a Mediterranean shrubland, these species differ in foraging behaviour and worker polymorphism. For 2 years, we studied the ants' diets and seed selection patterns as well as the local availability of seeds. Additionally, we performed a seed-choice experiment using a paired comparison design, offering the ants seeds from eight native plant species. The three ant species had the same general diet, which was primarily granivorous. Although they all consumed a wide variety of seeds, they mostly selected seeds from a small subset of plant species. Despite their morphological and behavioural differences, the ants displayed similar seed preferences that were highly consistent with their diets and seed selection patterns. Our results support the idea that the trophic ecology of these three harvester ants is driven by similar seed preferences rather than by their morphological and behavioural differences. Seed diversity and abundance were high near the ants' nests, suggesting that seed availability is not limiting and could in fact favour local species coexistence.

Bees exposed to climate change are more sensitive to pesticides.

Bee populations are exposed to multiple stressors, including land-use change, biological invasions, climate change, and pesticide exposure, that may interact synergistically. We analyze the combined effects of climate warming and sublethal insecticide exposure in the solitary bee Osmia cornuta. Previous Osmia studies show that warm wintering temperatures cause body weight loss, lipid consumption, and fat body depletion. Because the fat body plays a key role in xenobiotic detoxification, we expected that bees exposed to climate warming scenarios would be more sensitive to pesticides. We exposed O. cornuta females to three wintering treatments: current scenario (2007-2012 temperatures), near-future (2021-2050 projected temperatures), and distant-future (2051-2080). Upon emergence in spring, bees were orally exposed to three sublethal doses of an insecticide (Closer, a.i. sulfoxaflor; 0, 4.55 and 11.64 ng a.i./bee). We measured the combined effects of wintering and insecticide exposure on phototactic response, syrup consumption, and longevity. Wintering treatment by itself did not affect winter mortality, but body weight loss increased with increasing wintering temperatures. Similarly, wintering treatment by itself hardly influenced phototactic response or syrup consumption. However, bees wintered at the warmest temperatures had shorter longevity, a strong fecundity predictor in Osmia. Insecticide exposure, especially at the high dose, impaired the ability of bees to respond to light, and resulted in reduced syrup consumption and longevity. The combination of the warmest winter and the high insecticide dose resulted in a 70% longevity decrease. Smaller bees, resulting from smaller pollen-nectar provisions, had shorter longevity suggesting nutritional stress may further compromise fecundity in O. cornuta. Our results show a synergistic interaction between two major drivers of bee declines, and indicate that bees will become more sensitive to pesticides under the current global warming scenario. Our findings have important implications for pesticide regulation and underscore the need to consider multiple stressors to understand bee declines.

Ecological network complexity scales with area.

Larger geographical areas contain more species-an observation raised to a law in ecology. Less explored is whether biodiversity changes are accompanied by a modification of interaction networks. We use data from 32 spatial interaction networks from different ecosystems to analyse how network structure changes with area. We find that basic community structure descriptors (number of species, links and links per species) increase with area following a power law. Yet, the distribution of links per species varies little with area, indicating that the fundamental organization of interactions within networks is conserved. Our null model analyses suggest that the spatial scaling of network structure is determined by factors beyond species richness and the number of links. We demonstrate that biodiversity-area relationships can be extended from species counts to higher levels of network complexity. Therefore, the consequences of anthropogenic habitat destruction may extend from species loss to wider simplification of natural communities.

Spatial variability of hosts, parasitoids and their interactions across a homogeneous landscape.

Species assemblages and their interactions vary through space, generating diversity patterns at different spatial scales. Here, we study the local-scale spatial variation of a cavity-nesting bee and wasp community (hosts), their nest associates (parasitoids), and the resulting antagonistic network over a continuous and homogeneous habitat. To obtain bee/wasp nests, we placed trap-nests at 25 sites over a 32 km2 area. We obtained 1,541 nests (4,954 cells) belonging to 40 host species and containing 27 parasitoid species. The most abundant host species tended to have higher parasitism rate. Community composition dissimilarity was relatively high for both hosts and parasitoids, and the main component of this variability was species turnover, with a very minor contribution of ordered species loss (nestedness). That is, local species richness tended to be similar across the study area and community composition tended to differ between sites. Interestingly, the spatial matching between host and parasitoid composition was low. Host ß-diversity was weakly (positively) but significantly related to geographic distance. On the other hand, parasitoid and host-parasitoid interaction ß-diversities were not significantly related to geographic distance. Interaction ß-diversity was even higher than host and parasitoid ß-diversity, and mostly due to species turnover. Interaction rewiring between plots and between local webs and the regional metaweb was very low. In sum, species composition was rather idiosyncratic to each site causing a relevant mismatch between hosts and parasitoid composition. However, pairs of host and parasitoid species tended to interact similarly wherever they co-occurred. Our results additionally show that interaction ß-diversity is better explained by parasitoid than by host ß-diversity. We discuss the importance of identifying the sources of variation to understand the drivers of the observed heterogeneity.

A new native plant in the neighborhood: effects on plant-pollinator networks, pollination, and plant reproductive success.

Ecological communities are dynamic entities subjected to extinction/colonization events. Because species are connected through complex interaction networks, the arrival of a new species is likely to affect various species across the community, as observed in plant biological invasions. However, plant invasions usually represent extreme scenarios in which the community is strongly dominated by the alien species, confounding the effects of a change in species composition with a massive increase in floral resource availability. Our study addresses changes in plant community composition involving native species, a common phenomenon under the current climate change scenario in which plants are modifying their distribution ranges. We experimentally manipulated patches of a natural scrubland community by introducing a native plant (henceforth colonizing plant). To avoid introducing a disproportionate amount of floral resources we adjusted the number of flowers of the colonizing plant to the amount of floral resources locally available in each patch. We had two objectives: (1) to analyse the effects of the arrival of a new plant on the pollinator community, the rearrangement of plant-pollinator interactions and the structure of the plant-pollinator network; (2) to evaluate potential consequences for pollination and the reproductive success of resident plant species. The colonizing plant acted as a magnet species, attracting bumble bees and facilitating interactions to other plants through spill-over. The introduction of the colonizing plant also affected the structure of plant-pollinator networks (colonized networks were more generalized and more nested than control networks) and modified the arrangement of plant and pollinator species into modules. Ultimately, these changes resulted in higher heterospecific (but not conspecific) pollen deposition and had contrasting effects on the reproductive success of two resident plant species (higher fruit set and lower seed set, respectively). Our study shows that relationships between plants and pollinators are rapidly rearranged in response to novel situations (even when the new plant is not overly dominant), with important functional consequences on pollination and plant reproductive success. Our study establishes a link between network structure and pollination and plant reproductive success, which may be mediated by differences among pollinator species in foraging behavior.

A novel method to measure hairiness in bees and other insect pollinators.

Hairiness is a salient trait of insect pollinators that has been linked to thermoregulation, pollen uptake and transportation, and pollination success. Despite its potential importance in pollination ecology, hairiness is rarely included in pollinator trait analyses. This is likely due to the lack of standardized and efficient methods to measure hairiness. We describe a novel methodology that uses a stereomicroscope equipped with a live measurement module software to quantitatively measure two components of hairiness: hair density and hair length. We took measures of the two hairiness components in 109 insect pollinator species (including 52 bee species). We analyzed the relationship between hair density and length and between these two components and body size. We combined hair density and length measures to calculate a hairiness index and tested whether hairiness differed between major pollinator groups and bee genera. Body size was strongly and positively correlated to hair length and weakly and negatively correlated to hair density. The correlation between the two hairiness components was weak and negative. According to our hairiness index, butterflies and moths were the hairiest pollinator group, followed by bees, hoverflies, beetles, and other flies. Among bees, bumblebees (Bombus) and mason bees (Osmia) were the hairiest taxa, followed by digger bees (Anthophorinae), sand bees (Andrena), and sweat bees (Halictini). Our methodology provides an effective and standardized measure of the two components of hairiness (hair density and length), thus allowing for a meaningful interpretation of hairiness. We provide a detailed protocol of our methodology, which we hope will contribute to improve our understanding of pollination effectiveness, thermal biology, and responses to climate change in insects.

Interaction strength in plant-pollinator networks: Are we using the right measure?

Understanding how ecological networks are assembled is important because network structure reflects ecosystem functioning and stability. Quantitative network analysis incorporates measures of interaction strength as an estimate of the magnitude of the effect of interaction partners on one another. Most plant-pollinator network studies use frequency of interaction between individual pollinators and individual plants (encounter) as a surrogate of interaction strength. However, the number of flowers visited per encounter may strongly vary among pollinator and plant species, and therefore not all encounters are quantitatively equivalent. We sampled plant-pollinator interactions in a Mediterranean scrubland and tested whether using a measure of interaction strength based on the number of flowers visited resulted in changes in species (species strength, interaction species asymmetry, specialization) and network descriptors (nestedness, H2', interaction evenness, plant generality, pollinator generality) compared to the encounter-based measure. Several species (including some of the most abundant ones) showed important changes in species descriptors, notably in specialization. These changes were especially important in plant species with large floral displays, which became less specialized with the visit-based measure of interaction strength. At the network level we found significant changes in all properties analysed. With the encounter-based approach plant generality was much higher than pollinator generality (high specialization asymmetry between trophic levels). However, with the visit-based approach plant generality was greatly reduced so that plants and pollinators had similar levels of generalization. Interaction evenness also decreased strongly with the visit-based approach. We conclude that accounting for the number of flowers visited per encounter provides a more ecologically relevant measure of interaction strength. Our results have important implications for the stability of pollination networks and the evolution of plant-pollinator interactions. The use of a visit-based approach is especially important in studies relating interaction network structure and ecosystem function (pollination and/or exploitation of floral resources).

Yearly fluctuations of flower landscape in a Mediterranean scrubland: Consequences for floral resource availability.

Species flower production and flowering phenology vary from year to year due to extrinsic factors. Inter-annual variability in flowering patterns may have important consequences for attractiveness to pollinators, and ultimately, plant reproductive output. To understand the consequences of flowering pattern variability, a community approach is necessary because pollinator flower choice is highly dependent on flower context. Our objectives were: 1) To quantify yearly variability in flower density and phenology; 2) To evaluate whether changes in flowering patterns result in significant changes in pollen/nectar composition. We monitored weekly flowering patterns in a Mediterranean scrubland community (23 species) over 8 years. Floral resource availability was estimated based on field measures of pollen and nectar production per flower. We analysed inter-annual variation in flowering phenology (duration and date of peak bloom) and flower production, and inter-annual and monthly variability in flower, pollen and nectar species composition. We also investigated potential phylogenetic effects on inter-annual variability of flowering patterns. We found dramatic variation in yearly flower production both at the species and community levels. There was also substantial variation in flowering phenology. Importantly, yearly fluctuations were far from synchronous across species, and resulted in significant changes in floral resources availability and composition at the community level. Changes were especially pronounced late in the season, at a time when flowers are scarce and pollinator visitation rates are particularly high. We discuss the consequences of our findings for pollinator visitation and plant reproductive success in the current scenario of climate change.

Body size phenology in a regional bee fauna: a temporal extension of Bergmann's rule.

Bergmann's rule originally described a positive relationship between body size and latitude in warm-blooded animals. Larger animals, with a smaller surface/volume ratio, are better enabled to conserve heat in cooler climates (thermoregulatory hypothesis). Studies on endothermic vertebrates have provided support for Bergmann's rule, whereas studies on ectotherms have yielded conflicting results. If the thermoregulatory hypothesis is correct, negative relationships between body size and temperature should occur in temporal in addition to geographical gradients. To explore this possibility, we analysed seasonal activity patterns in a bee fauna comprising 245 species. In agreement with our hypothesis of a different relationship for large (endothermic) and small (ectothermic) species, we found that species larger than 27.81 mg (dry weight) followed Bergmann's rule, whereas species below this threshold did not. Our results represent a temporal extension of Bergmann's rule and indicate that body size and thermal physiology play an important role in structuring community phenology.

Long-term effects of changing atmospheric pollution on throughfall, bulk deposition and streamwaters in a Mediterranean forest.

The abatement programs implanted in Europe to reduce SO2, NO2 and NH3 emissions are here evaluated by analyzing the relationships between emissions in Spain and neighboring countries and atmospheric deposition in a Mediterranean forest in the Montseny mountains (NE Spain) for the last 3decades. A canopy budget model was applied to throughfall data measured during a period of high emissions (1995-1996) and a period of lower emissions (2011-2013) to estimate the changes in dry deposition over this time span. Emissions of SO2 in Spain strongly decreased (77%) and that was reflected in reductions for nssSO4(2-) in precipitation (65% for concentrations and 62% for SO4(2)-S deposition). A lower decline was found for dry deposition (29%). Spanish NO2 emissions increased from 1980 to 1991, remained constant until 2005, and decreased thereafter, a pattern that was paralleled by NO3(-) concentrations in bulk precipitation at Montseny. This pattern seems to be related to a higher share of renewable energies in electricity generation in Spain in recent years. However, dry deposition increased markedly between 1995 and 2012, from 1.3 to 6.7 kg ha(-1) year(-)(1). Differences in meteorology between periods may have had a role, since the recent period was drier thus probably favoring dry deposition. Spanish NH3 emissions increased by 13% between 1980 and 2012 in Spain but NH4(+) concentrations in precipitation and NH4(+)-N deposition showed a decreasing trend (15% reduction) at Montseny, probably linked to the reduction ammonium sulfate and nitrate aerosols to be scavenged by rainfall. NH4(+)-N dry deposition was similar between the compared periods. The N load at Montseny (15-17 kg ha(-1)y ear(-1)) was within the critical load range proposed for Mediterranean sclerophyllous forests (15-17.5 kg ha(-1) year(-1)). The onset of N saturation is suggested by the observed increasing N export in streamwaters.

Determinants of spatial distribution in a bee community: nesting resources, flower resources, and body size.

Understanding biodiversity distribution is a primary goal of community ecology. At a landscape scale, bee communities are affected by habitat composition, anthropogenic land use, and fragmentation. However, little information is available on local-scale spatial distribution of bee communities within habitats that are uniform at the landscape scale. We studied a bee community along with floral and nesting resources over a 32 km2 area of uninterrupted Mediterranean scrubland. Our objectives were (i) to analyze floral and nesting resource composition at the habitat scale. We ask whether these resources follow a geographical pattern across the scrubland at bee-foraging relevant distances; (ii) to analyze the distribution of bee composition across the scrubland. Bees being highly mobile organisms, we ask whether bee composition shows a homogeneous distribution or else varies spatially. If so, we ask whether this variation is irregular or follows a geographical pattern and whether bees respond primarily to flower or to nesting resources; and (iii) to establish whether body size influences the response to local resource availability and ultimately spatial distribution. We obtained 6580 specimens belonging to 98 species. Despite bee mobility and the absence of environmental barriers, our bee community shows a clear geographical pattern. This pattern is mostly attributable to heterogeneous distribution of small (<55 mg) species (with presumed smaller foraging ranges), and is mostly explained by flower resources rather than nesting substrates. Even then, a large proportion (54.8%) of spatial variability remains unexplained by flower or nesting resources. We conclude that bee communities are strongly conditioned by local effects and may exhibit spatial heterogeneity patterns at a scale as low as 500-1000 m in patches of homogeneous habitat. These results have important implications for local pollination dynamics and spatial variation of plant-pollinator networks.

The effects of fire on ant trophic assemblage and sex allocation.

Fire plays a key role in ecosystem dynamics worldwide, altering energy flows and species community structure and composition. However, the functional mechanisms underlying these effects are not well understood. Many ground-dwelling animal species can shelter themselves from exposure to heat and therefore rarely suffer direct mortality. However, fire-induced alterations to the environment may change a species' relative trophic level within a food web and its mode of foraging. We assessed how fire could affect ant resource utilization at different scales in a Mediterranean forest. First, we conducted isotopic analyses on entire ant species assemblages and their potential food resources, which included plants and other arthropods, in burned and unburned plots 1 year postfire. Second, we measured the production of males and females by nests of a fire-resilient species, Aphaenogaster gibbosa, and analyzed the differences in isotopic values among workers, males, and females to test whether fire constrained resource allocation. We found that, in spite of major modifications in biotic and abiotic conditions, fire had little impact on the relative trophic position of ant species. The studied assemblage was composed of species with a wide array of diets. They ranged from being mostly herbivorous to completely omnivorous, and a given species' trophic level was the same in burned and unburned plots. In A. gibbosa nests, sexuals had greater δ(15)N values than workers in both burned and unburned plots, which suggests that the former had a more protein-rich diet than the latter. Fire also appeared to have a major effect on A. gibbosa sex allocation: The proportion of nests that produced male brood was greater on burned zones, as was the mean number of males produced per nest with the same reproductive investment. Our results show that generalist ants with relatively broad diets maintained a constant trophic position, even following a major disturbance like fire. However, the dramatically reduced production of females on burned zones compared to unburned zones 1 year postfire may result in considerably reduced recruitment of new colonies in the mid to long term, which could yield genetic bottlenecks and founder effects. Our study paves the way for future functional analyses of fire-induced modifications in ant populations and communities.

Floral advertisement scent in a changing plant-pollinators market.

Plant-pollinator systems may be considered as biological markets in which pollinators choose between different flowers that advertise their nectar/pollen rewards. Although expected to play a major role in structuring plant-pollinator interactions, community-wide patterns of flower scent signals remain largely unexplored. Here we show for the first time that scent advertisement is higher in plant species that bloom early in the flowering period when pollinators are scarce relative to flowers than in species blooming later in the season when there is a surplus of pollinators relative to flowers. We also show that less abundant flowering species that may compete with dominant species for pollinator visitation early in the flowering period emit much higher proportions of the generalist attractant ß-ocimene. Overall, we provide a first community-wide description of the key role of seasonal dynamics of plant-specific flower scent emissions, and reveal the coexistence of contrasting plant signaling strategies in a plant-pollinator market.

The dimensionality of ecological networks.

How many dimensions (trait-axes) are required to predict whether two species interact? This unanswered question originated with the idea of ecological niches, and yet bears relevance today for understanding what determines network structure. Here, we analyse a set of 200 ecological networks, including food webs, antagonistic and mutualistic networks, and find that the number of dimensions needed to completely explain all interactions is small ( < 10), with model selection favouring less than five. Using 18 high-quality webs including several species traits, we identify which traits contribute the most to explaining network structure. We show that accounting for a few traits dramatically improves our understanding of the structure of ecological networks. Matching traits for resources and consumers, for example, fruit size and bill gape, are the most successful combinations. These results link ecologically important species attributes to large-scale community structure.

Uncoupling the effects of seed predation and seed dispersal by granivorous ants on plant population dynamics.

Secondary seed dispersal is an important plant-animal interaction, which is central to understanding plant population and community dynamics. Very little information is still available on the effects of dispersal on plant demography and, particularly, for ant-seed dispersal interactions. As many other interactions, seed dispersal by animals involves costs (seed predation) and benefits (seed dispersal), the balance of which determines the outcome of the interaction. Separate quantification of each of them is essential in order to understand the effects of this interaction. To address this issue, we have successfully separated and analyzed the costs and benefits of seed dispersal by seed-harvesting ants on the plant population dynamics of three shrub species with different traits. To that aim a stochastic, spatially-explicit individually-based simulation model has been implemented based on actual data sets. The results from our simulation model agree with theoretical models of plant response dependent on seed dispersal, for one plant species, and ant-mediated seed predation, for another one. In these cases, model predictions were close to the observed values at field. Nonetheless, these ecological processes did not affect in anyway a third species, for which the model predictions were far from the observed values. This indicates that the balance between costs and benefits associated to secondary seed dispersal is clearly related to specific traits. This study is one of the first works that analyze tradeoffs of secondary seed dispersal on plant population dynamics, by disentangling the effects of related costs and benefits. We suggest analyzing the effects of interactions on population dynamics as opposed to merely analyzing the partners and their interaction strength.

Plant-pollinator networks: adding the pollinator's perspective.

Pollination network studies are based on pollinator surveys conducted on focal plants. This plant-centred approach provides insufficient information on flower visitation habits of rare pollinator species, which are the majority in pollinator communities. As a result, pollination networks contain very high proportions of pollinator species linked to a single plant species (extreme specialists), a pattern that contrasts with the widely accepted view that plant-pollinator interactions are mostly generalized. In this study of a Mediterranean scrubland community in NE Spain we supplement data from an intensive field survey with the analysis of pollen loads carried by pollinators. We observed 4265 contacts corresponding to 19 plant and 122 pollinator species. The addition of pollen data unveiled a very significant number of interactions, resulting in important network structural changes. Connectance increased 1.43-fold, mean plant connectivity went from 18.5 to 26.4, and mean pollinator connectivity from 2.9 to 4.1. Extreme specialist pollinator species decreased 0.6-fold, suggesting that ecological specialization is often overestimated in plant-pollinator networks. We expected a greater connectivity increase in rare species, and consequently a decrease in the level of asymmetric specialization. However, new links preferentially attached to already highly connected nodes and, as a result, both nestedness and centralization increased. The addition of pollen data revealed the existence of four clearly defined modules that were not apparent when only field survey data were used. Three of these modules had a strong phenological component. In comparison to other pollination webs, our network had a high proportion of connector links and species. That is, although significant, the four modules were far from isolated.