Instituto Argentino de Investigaciones de las Zonas Aridas

Pollinators may be declining globally, a matter of concern because animal pollination is required by most of the world's plant species, including many crop plants. Human land use and the loss of native habitats is thought to be an important driver of decline for wild, native pollinators, yet the findings of published studies on this topic have never been quantitatively synthesized. Here we use meta-analysis to synthesize the literature on how bees, the most important group of pollinators, are affected by human disturbances such as habitat loss, grazing, logging, and agriculture. We obtained 130 effect sizes from 54 published studies recording bee abundance and/or species richness as a function of human disturbance. Both bee abundance and species richness were significantly, negatively affected by disturbance. However, the magnitude of the effects was not large. Furthermore, the only disturbance type showing a significant negative effect, habitat loss and fragmentation, was statistically significant only in systems where very little natural habitat remains. Therefore, it would be premature to draw conclusions about habitat loss having caused global pollinator decline without first assessing the extent to which the existing studies represent the status of global ecosystems. Future pollinator declines seem likely given forecasts of increasing land-use change.

Introduced plant populations lose interactions with enemies, mutualists and competitors from their native ranges, and gain interactions with new species, under new abiotic conditions. From a biogeographical perspective, differences in the assemblage of interacting species, as well as in abiotic conditions, may explain the demographic success of the introduced plant populations relative to conspecifics in their native range. Within invaded communities, the new interactions and conditions experienced by the invader may influence both its demographic success and its effects on native biodiversity. Here, we examine indirect effects involving enemies, mutualists and competitors of introduced plants, and effects of abiotic conditions on biotic interactions. We then synthesize ideas building on Darwin's idea that the kinds of new interactions gained by an introduced population will depend on its relatedness to native populations. This yields a heuristic framework to explain how biotic interactions and abiotic conditions influence invader success. We conclude that species introductions generally alter plants' interactions with enemies, mutualists and competitors, and that there is increasing evidence that these altered interactions jointly influence the success of introduced populations.

BACKGROUND: Ecologists and evolutionary biologists are becoming increasingly interested in networks as a framework to study plant-animal mutualisms within their ecological context. Although such focus on networks has brought about important insights into the structure of these interactions, relatively little is still known about the mechanisms behind these patterns. SCOPE: The aim in this paper is to offer an overview of the mechanisms influencing the structure of plant-animal mutualistic networks. A brief summary is presented of the salient network patterns, the potential mechanisms are discussed and the studies that have evaluated them are reviewed. This review shows that researchers of plant-animal mutualisms have made substantial progress in the understanding of the processes behind the patterns observed in mutualistic networks. At the same time, we are still far from a thorough, integrative mechanistic understanding. We close with specific suggestions for directions of future research, which include developing methods to evaluate the relative importance of mechanisms influencing network patterns and focusing research efforts on selected representative study systems throughout the world.

The structure of ecological interaction networks is often interpreted as a product of meaningful ecological and evolutionary mechanisms that shape the degree of specialization in community associations. However, here we show that both unweighted network metrics (connectance, nestedness, and degree distribution) and weighted network metrics (interaction evenness, interaction strength asymmetry) are strongly constrained and biased by the number of observations. Rarely observed species are inevitably regarded as "specialists," irrespective of their actual associations, leading to biased estimates of specialization. Consequently, a skewed distribution of species observation records (such as the lognormal), combined with a relatively low sampling density typical for ecological data, already generates a "nested" and poorly "connected" network with "asymmetric interaction strengths" when interactions are neutral. This is confirmed by null model simulations of bipartite networks, assuming that partners associate randomly in the absence of any specialization and any variation in the correspondence of biological traits between associated species (trait matching). Variation in the skewness of the frequency distribution fundamentally changes the outcome of network metrics. Therefore, interpretation of network metrics in terms of fundamental specialization and trait matching requires an appropriate control for such severe constraints imposed by information deficits. When using an alternative approach that controls for these effects, most natural networks of mutualistic or antagonistic systems show a significantly higher degree of reciprocal specialization (exclusiveness) than expected under neutral conditions. A higher exclusiveness is coherent with a tighter coevolution and suggests a lower ecological redundancy than implied by nested networks.

The structure of mutualistic networks is likely to result from the simultaneous influence of neutrality and the constraints imposed by complementarity in species phenotypes, phenologies, spatial distributions, phylogenetic relationships, and sampling artifacts. We develop a conceptual and methodological framework to evaluate the relative contributions of these potential determinants. Applying this approach to the analysis of a plant-pollinator network, we show that information on relative abundance and phenology suffices to predict several aggregate network properties (connectance, nestedness, interaction evenness, and interaction asymmetry). However, such information falls short of predicting the detailed network structure (the frequency of pairwise interactions), leaving a large amount of variation unexplained. Taken together, our results suggest that both relative species abundance and complementarity in spatiotemporal distribution contribute substantially to generate observed network patters, but that this information is by no means sufficient to predict the occurrence and frequency of pairwise interactions. Future studies could use our methodological framework to evaluate the generality of our findings in a representative sample of study systems with contrasting ecological conditions.

1. The study of plant-pollinator interactions in a network context is receiving increasing attention. This approach has helped to identify several emerging network patterns such as nestedness and modularity. However, most studies are based only on qualitative information, and some ecosystems, such as deserts and tropical forests, are underrepresented in these data sets. 2. We present an exhaustive analysis of the structure of a 4-year plant-pollinator network from the Monte desert in Argentina using qualitative and quantitative tools. We describe the structure of this network and evaluate sampling completeness using asymptotic species richness estimators. Our goal is to assess the extent to which the realized sampling effort allows for an accurate description of species interactions and to estimate the minimum number of additional censuses required to detect 90% of the interactions. We evaluated completeness of detection of the community-wide pollinator fauna, of the pollinator fauna associated with each plant species and of the plant-pollinator interactions. We also evaluated whether sampling completeness was influenced by plant characteristics, such as flower abundance, flower life span, number of interspecific links (degree) and selectiveness in the identity of their flower visitors, as well as sampling effort. 3. We found that this desert plant-pollinator network has a nested structure and that it exhibits modularity and high network-level generalization. 4. In spite of our high sampling effort, and although we sampled 80% of the pollinator fauna, we recorded only 55% of the interactions. Furthermore, although a 64% increase in sampling effort would suffice to detect 90% of the pollinator species, a fivefold increase in sampling effort would be necessary to detect 90% of the interactions. 5. Detection of interactions was incomplete for most plant species, particularly specialists with a long flowering season and high flower abundance, or generalists with short flowering span and scant flowers. Our results suggest that sampling of a network with the same effort for all plant species is inadequate to sample interactions. 6. Sampling the diversity of interactions is labour intensive, and most plant-pollinator networks published to date are likely to be undersampled. Our analysis allowed estimating the completeness of our sampling, the additional effort needed to detect most interactions and the plant traits that influence the detection of their interactions.

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.

Detailed large-scale information on mammal distribution has often been lacking, hindering conservation efforts. We used the information from the 2009 IUCN Red List of Threatened Species as a baseline for developing habitat suitability models for 5027 out of 5330 known terrestrial mammal species, based on their habitat relationships. We focused on the following environmental variables: land cover, elevation and hydrological features. Models were developed at 300 m resolution and limited to within species' known geographical ranges. A subset of the models was validated using points of known species occurrence. We conducted a global, fine-scale analysis of patterns of species richness. The richness of mammal species estimated by the overlap of their suitable habitat is on average one-third less than that estimated by the overlap of their geographical ranges. The highest absolute difference is found in tropical and subtropical regions in South America, Africa and Southeast Asia that are not covered by dense forest. The proportion of suitable habitat within mammal geographical ranges correlates with the IUCN Red List category to which they have been assigned, decreasing monotonically from Least Concern to Endangered. These results demonstrate the importance of fine-resolution distribution data for the development of global conservation strategies for mammals.

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant-enemy and plant-mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.

Although the influence of nitrogen (N) addition on grassland plant communities has been widely studied, it is still unclear whether observed patterns and underlying mechanisms are constant across biomes. In this systematic review, we use meta-analysis and metaregression to investigate the influence of N addition (here referring mostly to fertilization) upon the biodiversity of temperate mountain grasslands (including montane, subalpine and alpine zones). Forty-two studies met our criteria of inclusion, resulting in 134 measures of effect size. The main general responses of mountain grasslands to N addition were increases in phytomass and reductions in plant species richness, as observed in lowland grasslands. More specifically, the analysis reveals that negative effects on species richness were exacerbated by dose (ha(-1) year(-1) ) and duration of N application (years) in an additive manner. Thus, sustained application of low to moderate levels of N over time had effects similar to short-term application of high N doses. The climatic context also played an important role: the overall effects of N addition on plant species richness and diversity (Shannon index) were less pronounced in mountain grasslands experiencing cool rather than warm summers. Furthermore, the relative negative effect of N addition on species richness was more pronounced in managed communities and was strongly negatively related to N-induced increases in phytomass, that is the greater the phytomass response to N addition, the greater the decline in richness. Altogether, this review not only establishes that plant biodiversity of mountain grasslands is negatively affected by N addition, but also demonstrates that several local management and abiotic factors interact with N addition to drive plant community changes. This synthesis yields essential information for a more sustainable management of mountain grasslands, emphasizing the importance of preserving and restoring grasslands with both low agricultural N application and limited exposure to N atmospheric deposition.

Summary Invasive, alien plants and pollinators have varying effects on their interaction partners, ranging from highly beneficial to strongly detrimental. To understand these contrasting impacts, we review the benefits and costs associated with plant–pollinator interactions and enquire as to how the presence of abundant invaders affects the benefit–cost balance. We provide a conceptual framework that predicts that mutualism shifts to antagonism when invaders increase disproportionally in abundance relative to their interaction partners. This outcome is illustrated by an empirical example of a crop in which flower damage and an associated reduction in fruit quality represent interaction costs of intense visitation by invasive bees. More generally, the extremely high density of invasive flower visitors, such as A pis mellifera and B ombus terrestris , might have population‐ and community‐level consequences by hampering reproduction of native plants while promoting reproduction of alien plants. Furthermore, modification of the structure of pollination networks resulting from intense visitation of native plants by superabundant alien flower visitors in highly invaded communities could predict accentuated interaction costs for many native plants. Owing to their high density and the exclusion of native pollinators, invasive bees, originally introduced for honey production and crop pollination, may negatively impact both the native biota and agriculture.

Mutualisms provide benefits to interacting species, but they also involve costs. If costs come to exceed benefits as population density or the frequency of encounters between species increases, the interaction will no longer be mutualistic. Thus curves that represent benefits and costs as functions of interaction frequency are important tools for predicting when a mutualism will tip over into antagonism. Currently, most of what we know about benefit and cost curves in pollination mutualisms comes from highly specialized pollinating seed-consumer mutualisms, such as the yucca moth-yucca interaction. There, benefits to female reproduction saturate as the number of visits to a flower increases (because the amount of pollen needed to fertilize all the flower's ovules is finite), but costs continue to increase (because pollinator offspring consume developing seeds), leading to a peak in seed production at an intermediate number of visits. But for most plant-pollinator mutualisms, costs to the plant are more subtle than consumption of seeds, and how such costs scale with interaction frequency remains largely unknown. Here, we present reasonable benefit and cost curves that are appropriate for typical pollinator-plant interactions, and we show how they can result in a wide diversity of relationships between net benefit (benefit minus cost) and interaction frequency. We then use maximum-likelihood methods to fit net-benefit curves to measures of female reproductive success for three typical pollination mutualisms from two continents, and for each system we chose the most parsimonious model using information-criterion statistics. We discuss the implications of the shape of the net-benefit curve for the ecology and evolution of plant-pollinator mutualisms, as well as the challenges that lie ahead for disentangling the underlying benefit and cost curves for typical pollination mutualisms.

Morphology and phenology influence plant-pollinator network structure, but whether they generate more stable pairwise interactions with higher pollination success remains unknown. Here we evaluate the importance of morphological trait matching, phenological overlap and specialisation for the spatio-temporal stability (measured as variability) of plant-pollinator interactions and for pollination success, while controlling for species' abundance. To this end, we combined a 6-year plant-pollinator interaction dataset, with information on species traits, phenologies, specialisation, abundance and pollination success, into structural equation models. Interactions among abundant plants and pollinators with well-matched traits and phenologies formed the stable and functional backbone of the pollination network, whereas poorly matched interactions were variable in time and had lower pollination success. We conclude that phenological overlap could be more useful for predicting changes in species interactions than species abundances, and that non-random extinction of species with well-matched traits could decrease the stability of interactions within communities and reduce their functioning.

Abstract In arid zones dominant woody plants are capable of causing changes in microclimate and soil properties likely to affect species composition, as well as the establishment and spatial distribution of plant species. In North American and European deserts species richness appears to be higher under the canopy of shrubs and trees, in contrast with Chilean deserts where it seems to be lower. Since Prosopis flexuosa (Fabaceae, Mimosoideae) is the most conspicuous tree in the central Monte desert, Argentina, we analysed the effect of this species on the composition and abundance of the shrub and herbaceous layers and on soil properties. We considered two mesohabitats: ‘under P. flexuosa canopy’ and ‘intercanopy areas’. In addition, we analysed the differences between two microhabitats under canopies: ‘northern part of the canopy’ and ‘southern part of the canopy’. Results indicate that species composition and soil properties are affected by both mesohabitats and microhabitats. We found a higher number of shrubs under canopies, whereas that of grasses and perennial forbs increased in intercanopy areas. Concentrations of organic matter, nitrogen, potassium and phosphorus, factors limiting biological productivity in Monte desert soils, were significantly higher under than outside P. flexuosa canopies. Electrical conductivity and concentrations of Na+, Ca++, Mg++ were higher in the northern than in the southern microhabitats. No differences in species richness, evenness or diversity were found between mesohabitats or between microhabitats. We conclude that P. flexuosa modifies the spatial pattern of plant species in the shrub and herbaceous layers and the chemical conditions of the soil, generating spatial heterogeneity on different scales. Abbreviations: EC = Electrical conductivity; SAR = Sodium absorption ratio.

Leaf epidermal peels of Arabidopsis (Arabidopsis thaliana) mutants lacking either phototropins 1 and 2 (phot1 and phot2) or cryptochromes 1 and 2 (cry1 and cry2) exposed to a background of red light show severely impaired stomatal opening responses to blue light. Since phot and cry are UV-A/blue light photoreceptors, they may be involved in the perception of the blue light-specific signal that induces the aperture of the stomatal pores. In leaf epidermal peels, the blue light-specific effect saturates at low irradiances; therefore, it is considered to operate mainly under the low irradiance of dawn, dusk, or deep canopies. Conversely, we show that both phot1 phot2 and cry1 cry2 have reduced stomatal conductance, transpiration, and photosynthesis, particularly under the high irradiance of full sunlight at midday. These mutants show compromised responses of stomatal conductance to irradiance. However, the effects of phot and cry on photosynthesis were largely nonstomatic. While the stomatal conductance phenotype of phot1 phot2 was blue light specific, cry1 cry2 showed reduced stomatal conductance not only in response to blue light, but also in response to red light. The levels of abscisic acid were elevated in cry1 cry2. We conclude that considering their effects at high irradiances cry and phot are critical for the control of transpiration and photosynthesis rates in the field. The effects of cry on stomatal conductance are largely indirect and involve the control of abscisic acid levels.

Most rare species appear to be specialists in plant-pollinator networks. This observation could result either from real ecological processes or from sampling artifacts. Several methods have been proposed to overcome these artifacts, but they have the limitation of being based on visitation data, causing interactions involving rare visitor species to remain undersampled. We propose the analysis of food composition in bee trap nests to assess the reliability of network specialization estimates. We compared data from a plant-pollinator network in the Monte Desert of Villavicencio Nature Reserve, Argentina, sampled by visit observation, and data from trap nests sampled at the same time and location. Our study shows that trap nest sampling was good for estimating rare species degree. The rare species in the networks appear to be more specialized than they really are, and the bias in the estimation of the species degree increases with the rareness. The low species degree of these rare species in the visitation networks results from insufficient sampling of the rare interactions, which could have important consequences for network structure.

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.

A cladistic analysis of Curculionidae was performed using 49 characters (41 from larvae, three from pupae, and five from adults). Illustrations of characters of immatures are provided. The analysis involved 19 terminal units and a hypothetical ancestor determined by the outgroup comparison method used to root the tree. One most parsimonious cladogram was obtained based on the complete data set and the following phylogenetic hypothesis is proposed: Ithycerinae, Microcerinae, and Brachycrinae sensu stricto are broad-nosed weevils placed sequentially at the base of the cladogram. The remaining weevil subfamilies form two major natural groups: one constituted by the sister taxa Rhynchophorinae—Platypodinae; the other with Erirhininae at the base, as sister taxon of the “Curculionidae sensu stricto” which show an unresolved trichotomy involving Curculioninae, Cossoninae—Scolytinae, and the clade including the Entiminae and allied subfamilies. This latter clade of broad-nosed weevils has Thecesterninae at the base; the next branch is Amycterinae, the sister taxon of the clade comprising two groups: one constituted by Aterpinae, Rhytirrhininae, and Gonipterinae; the other is Entiminae whose units form two main clades: one constituted by the sister tribes Pachyrhynchini—Ectemnorhinini, and the other by Alophini, Sitonini, and Entimini. When the analysis was done using only immature characters, results congruent with those based on the complete data set were obtained, except for the placement of Erirhininae. According to the results the hypothesis of monophyly of broad-nosed weevils is not accepted; the Entiminae are justified as monophyletic and their natural classification into tribes is proposed and the phylogenetic position and relationships of higher taxa of Curculionidae are discussed. This paper shows the importance of immature characters in recognition of natural groups and relationships in Curculionidae.

Recent studies of plant-animal mutualistic networks have assumed that interaction frequency between mutualists predicts species impacts (population-level effects), and that field estimates of interaction strength (per-interaction effects) are unnecessary. Although existing evidence supports this assumption for the effect of animals on plants, no studies have evaluated it for the reciprocal effect of plants on animals. We evaluate this assumption using data on the reproductive effects of pollinators on plants and the reciprocal reproductive effects of plants on pollinators. The magnitude of species impacts of plants on pollinators, the reciprocal impacts of pollinators on plants, and their asymmetry were well predicted by interaction frequency. However, interaction strength was a key determinant of the sign of species impacts. These results underscore the importance of quantifying interaction strength in studies of mutualistic networks. We also show that the distributions of interaction strengths and species impacts are highly skewed, with few strong and many weak interactions. This skewed distribution matches the pattern observed in food webs, suggesting that the community-wide organization of species interactions is fundamentally similar between mutualistic and antagonistic interactions. Our results have profound ecological implications, given the key role of interaction strength for community stability.

Abstract Theoretical models of species coexistence between desert mammals have generally been based on a combination of food and microhabitat selection by granivorous rodents. Although these models are applicable in various deserts of the world, they cannot explain resource use by mammals in Neotropical deserts. The present study examines diet composition in a mammal assemblage in the Monte desert, Argentina. The results show that two main strategies are used by these mammals: medium‐sized species (hystricognath rodents: Dolichotis patagonum , Lagostomus maximus , Microcavia australis and Galea musteloides; and an exotic lagomorph: Lepus europaeus ) are herbivores, whereas small‐sized species (a marsupial: Thylamys pusillus; and sigmodontine rodents: Graomys griseoflavus , Akodon molinae , Calomys musculinus , Eligmodontia typus ) are omnivorous. Small mammals also show a tendency towards granivory ( C . musculinus ), insectivory ( A. molinae and T. pusillus ) and folivory ( G. griseoflavus ).