Marcelo A. Aizen

A meta-analysis of bees' responses to anthropogenic disturbance

Pollinators may be declining globally, a matter of concern because animal pollination is required by most of the worlds 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.

The Global Stock of Domesticated Honey Bees Is Growing Slower Than Agricultural Demand for Pollination

The prospect that a global pollination crisis currently threatens agricultural productivity has drawn intense recent interest among scientists, politicians, and the general public. To date, evidence for a global crisis has been drawn from regional or local declines in pollinators themselves or insufficient pollination for particular crops. In contrast, our analysis of Food and Agriculture Organization (FAO) data reveals that the global population of managed honey-bee hives has increased approximately 45% during the last half century and suggests that economic globalization, rather than biological factors, drives both the dynamics of the global managed honey-bee population and increasing demands for agricultural pollination services. Nevertheless, available data also reveal a much more rapid (>300%) increase in the fraction of agriculture that depends on animal pollination during the last half century, which may be stressing global pollination capacity. Although the primary cause of the accelerating increase of the pollinator dependence of commercial agriculture seems to be economic and political and not biological, the rapid expansion of cultivation of many pollinator-dependent crops has the potential to trigger future pollination problems for both these crops and native species in neighboring areas. Such environmental costs merit consideration during the development of agriculture and conservation policies.

Long-Term Global Trends in Crop Yield and Production Reveal No Current Pollination Shortage but Increasing Pollinator Dependency

There is evidence that pollinators are declining as a result of local and global environmental degradation [1-4]. Because a sizable proportion of the human diet depends directly or indirectly on animal pollination [5], the issue of how decreases in pollinator stocks could affect global crop production is of paramount importance [6-8]. Using the extensive FAO data set [9], we compared 45 year series (1961-2006) in yield, and total production and cultivated area of pollinator-dependent and nondependent crops [5]. We investigated temporal trends separately for the developed and developing world because differences in agricultural intensification, and socioeconomic and environmental conditions might affect yield and pollinators [10-13]. Since 1961, crop yield (Mt/ha) has increased consistently at average annual growth rates of approximately 1.5%. Temporal trends were similar between pollinator-dependent and nondependent crops in both the developed and developing world, thus not supporting the view that pollinator shortages are affecting crop yield at the global scale. We further report, however, that agriculture has become more pollinator dependent because of a disproportionate increase in the area cultivated with pollinator-dependent crops. If the trend toward favoring cultivation of pollinator-dependent crops continues, the need for the service provided by declining pollinators will greatly increase in the near future.

Invasive Mutualists Erode Native Pollination Webs

Plant–animal mutualisms are characterized by weak or asymmetric mutual dependences between interacting species, a feature that could increase community stability. If invasive species integrate into mutualistic webs, they may alter web structure, with consequences for species persistence. However, the effect of alien mutualists on the architecture of plant–pollinator webs remains largely unexplored. We analyzed the extent of mutual dependency between interacting species, as a measure of mutualism strength, and the connectivity of 10 paired plant–pollinator webs, eight from forests of the southern Andes and two from oceanic islands, with different incidences of alien species. Highly invaded webs exhibited weaker mutualism than less-invaded webs. This potential increase in network stability was the result of a disproportionate increase in the importance and participation of alien species in the most asymmetric interactions. The integration of alien mutualists did not alter overall network connectivity, but links were transferred from generalist native species to super-generalist alien species during invasion. Therefore, connectivity among native species declined in highly invaded webs. These modifications in the structure of pollination webs, due to dominance of alien mutualists, can leave many native species subject to novel ecological and evolutionary dynamics.

ASYMMETRIC SPECIALIZATION: A PERVASIVE FEATURE OF PLANT–POLLINATOR INTERACTIONS

Although specialization in species interactions has usually been equated to reciprocal specialization, asymmetric specialization (i.e., a specialist interacting with a generalist) is also likely. Recent studies have suggested that asymmetric specialization in species interactions could be more common than previously thought. We contrasted patterns of asymmetric specialization observed in 18 plant-pollinator interaction webs with pre- dictions based on null models. We found that asymmetric specialization is common in plant-pollinator interactions, and that its occurrence is more frequent than expected under a simple null model that assumed random interactions among species; furthermore, large assemblages with many pairs of interacting species tend to have more asymmetric inter- actions than smaller assemblages. A second null model, which incorporated a correlation between species frequency of interaction and degree of specialization observed in most data sets produced patterns that were generally closer to those present in the data. At least three kinds of explanations could account for the observed asymmetric specialization, including random interactions among individuals (rather than species), adaptive conse- quences of specialization, and artifacts, such as data aggregation and sampling biases. Future studies should be aimed at understanding the relative importance of each of these alternative explanations in generating asymmetric specialization in species interactions.

How much does agriculture depend on pollinators? Lessons from long-term trends in crop production

BACKGROUND AND AIMS Productivity of many crops benefits from the presence of pollinating insects, so a decline in pollinator abundance should compromise global agricultural production. Motivated by the lack of accurate estimates of the size of this threat, we quantified the effect of total loss of pollinators on global agricultural production and crop production diversity. The change in pollinator dependency over 46 years was also evaluated, considering the developed and developing world separately. METHODS Using the extensive FAO dataset, yearly data were compiled for 1961-2006 on production and cultivated area of 87 important crops, which we classified into five categories of pollinator dependency. Based on measures of the aggregate effect of differential pollinator dependence, the consequences of a complete loss of pollinators in terms of reductions in total agricultural production and diversity were calculated. An estimate was also made of the increase in total cultivated area that would be required to compensate for the decrease in production of every single crop in the absence of pollinators. KEY RESULTS The expected direct reduction in total agricultural production in the absence of animal pollination ranged from 3 to 8 %, with smaller impacts on agricultural production diversity. The percentage increase in cultivated area needed to compensate for these deficits was several times higher, particularly in the developing world, which comprises two-thirds of the land devoted to crop cultivation globally. Crops with lower yield growth tended to have undergone greater expansion in cultivated area. Agriculture has become more pollinator-dependent over time, and this trend is more pronounced in the developing than developed world. CONCLUSIONS We propose that pollination shortage will intensify demand for agricultural land, a trend that will be more pronounced in the developing world. This increasing pressure on supply of agricultural land could significantly contribute to global environmental change.

Global growth and stability of agricultural yield decrease with pollinator dependence

Human welfare depends on the amount and stability of agricultural production, as determined by crop yield and cultivated area. Yield increases asymptotically with the resources provided by farmers’ inputs and environmentally sensitive ecosystem services. Declining yield growth with increased inputs prompts conversion of more land to cultivation, but at the risk of eroding ecosystem services. To explore the interdependence of agricultural production and its stability on ecosystem services, we present and test a general graphical model, based on Jensens inequality, of yield–resource relations and consider implications for land conversion. For the case of animal pollination as a resource influencing crop yield, this model predicts that incomplete and variable pollen delivery reduces yield mean and stability (inverse of variability) more for crops with greater dependence on pollinators. Data collected by the Food and Agriculture Organization of the United Nations during 1961–2008 support these predictions. Specifically, crops with greater pollinator dependence had lower mean and stability in relative yield and yield growth, despite global yield increases for most crops. Lower yield growth was compensated by increased land cultivation to enhance production of pollinator-dependent crops. Area stability also decreased with pollinator dependence, as it correlated positively with yield stability among crops. These results reveal that pollen limitation hinders yield growth of pollinator-dependent crops, decreasing temporal stability of global agricultural production, while promoting compensatory land conversion to agriculture. Although we examined crop pollination, our model applies to other ecosystem services for which the benefits to human welfare decelerate as the maximum is approached.

Beyond species loss: the extinction of ecological interactions in a changing world

Summary 1. The effects of the present biodiversity crisis have been largely focused on the loss of species. However, a missed component of biodiversity loss that often accompanies or even precedes species disappearance is the extinction of ecological interactions. 2. Here, we propose a novel model that (i) relates the diversity of both species and interactions along a gradient of environmental deterioration and (ii) explores how the rate of loss of ecological functions, and consequently of ecosystem services, can be accelerated or restrained depending on how the rate of species loss covaries with the rate of interactions loss. 3. We find that the loss of species and interactions are decoupled, such that ecological interactions are often lost at a higher rate. This implies that the loss of ecological interactions may occur well before species disappearance, affecting species functionality and ecosystems services at a faster rate than species extinctions. We provide a number of empirical case studies illustrating these points. 4. Our approach emphasizes the importance of focusing on species interactions as the major biodiversity component from which the ‘health’ of ecosystems depends.

NULL MODEL ANALYSES OF SPECIALIZATION IN PLANT-POLLINATOR INTERACTIONS

Recent studies have suggested that plant–pollinator interactions may be less specialized than previously thought. We contrasted patterns of specialization observed in five plant–pollinator interaction webs with predictions based on null models. In the five data sets, the observed number of extreme specialists and extreme generalists was significantly higher than the null expectation. This pattern was mostly due to a positive correlation between species frequency of interaction (f) and their estimated degree of generalization (s). After accounting for this association, the expected frequency distribution of degree of specialization generated by the null model closely matched the observed frequency distribution in the five data sets. A second null model, which explicitly incorporated the correlation between f and s, also generated expected frequency distributions of specialization that closely resemble those observed in the data sets. To make progress in understanding the distribution of degree of specializ...

Reconnecting plants and pollinators: challenges in the restoration of pollination mutualisms

Ecological restoration of plant-pollinator interactions has received surprisingly little attention, despite animal-mediated pollination underpinning reproduction of the majority of higher plants. Here, we offer a conceptual and practical framework for the ecological restoration of pollination mutualisms. Through the use of targeted restoration plantings to attract and sustain pollinators and increased knowledge of the ecological requirements of pollinators, we propose that pollination could be successfully restored in degraded ecosystems. The challenge for pollination biologists is to integrate their findings with those of plant restoration ecologists to ensure sustainable pollination in restored ecosystems.