Saul A. Cunningham

Importance of pollinators in changing landscapes for world crops

The extent of our reliance on animal pollination for world crop production for human food has not previously been evaluated and the previous estimates for countries or continents have seldom used primary data. In this review, we expand the previous estimates using novel primary data from 200 countries and found that fruit, vegetable or seed production from 87 of the leading global food crops is dependent upon animal pollination, while 28 crops do not rely upon animal pollination. However, global production volumes give a contrasting perspective, since 60% of global production comes from crops that do not depend on animal pollination, 35% from crops that depend on pollinators, and 5% are unevaluated. Using all crops traded on the world market and setting aside crops that are solely passively self-pollinated, wind-pollinated or parthenocarpic, we then evaluated the level of dependence on animal-mediated pollination for crops that are directly consumed by humans. We found that pollinators are essential for 13 crops, production is highly pollinator dependent for 30, moderately for 27, slightly for 21, unimportant for 7, and is of unknown significance for the remaining 9. We further evaluated whether local and landscape-wide management for natural pollination services could help to sustain crop diversity and production. Case studies for nine crops on four continents revealed that agricultural intensification jeopardizes wild bee communities and their stabilizing effect on pollination services at the landscape scale.

Landscape effects on crop pollination services: are there general patterns?

Pollination by bees and other animals increases the size, quality, or stability of harvests for 70% of leading global crops. Because native species pollinate many of these crops effectively, conserving habitats for wild pollinators within agricultural landscapes can help maintain pollination services. Using hierarchical Bayesian techniques, we synthesize the results of 23 studies - representing 16 crops on five continents - to estimate the general relationship between pollination services and distance from natural or semi-natural habitats. We find strong exponential declines in both pollinator richness and native visitation rate. Visitation rate declines more steeply, dropping to half of its maximum at 0.6 km from natural habitat, compared to 1.5 km for richness. Evidence of general decline in fruit and seed set - variables that directly affect yields - is less clear. Visitation rate drops more steeply in tropical compared with temperate regions, and slightly more steeply for social compared with solitary bees. Tropical crops pollinated primarily by social bees may therefore be most susceptible to pollination failure from habitat loss. Quantifying these general relationships can help predict consequences of land use change on pollinator communities and crop productivity, and can inform landscape conservation efforts that balance the needs of native species and people.

Stability of pollination services decreases with isolation from natural areas despite honey bee visits

Sustainable agricultural landscapes by definition provide high magnitude and stability of ecosystem services, biodiversity and crop productivity. However, few studies have considered landscape effects on the stability of ecosystem services. We tested whether isolation from florally diverse natural and semi-natural areas reduces the spatial and temporal stability of flower-visitor richness and pollination services in crop fields. We synthesised data from 29 studies with contrasting biomes, crop species and pollinator communities. Stability of flower-visitor richness, visitation rate (all insects except honey bees) and fruit set all decreased with distance from natural areas. At 1 km from adjacent natural areas, spatial stability decreased by 25, 16 and 9% for richness, visitation and fruit set, respectively, while temporal stability decreased by 39% for richness and 13% for visitation. Mean richness, visitation and fruit set also decreased with isolation, by 34, 27 and 16% at 1 km respectively. In contrast, honey bee visitation did not change with isolation and represented > 25% of crop visits in 21 studies. Therefore, wild pollinators are relevant for crop productivity and stability even when honey bees are abundant. Policies to preserve and restore natural areas in agricultural landscapes should enhance levels and reliability of pollination services.

A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems

Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture.

EVOLUTIONARY DIVERGENCES IN LEAF STRUCTURE AND CHEMISTRY, COMPARING RAINFALL AND SOIL NUTRIENT GRADIENTS

Leaf structural and chemical characteristics were compared in pairs of species that were phylogenetically independently contrasted along rainfall gradients (10 pairs) or soil nutrient gradients (9 pairs), using perennial plants in New South Wales, Australia. The objective was to test hypotheses regarding leaf attributes that should be successful in sustaining populations in vegetation at lower vs. higher rainfall or lower vs. higher soil nutrients, and especially to assess the proposition that lower rainfall and lower soil nutrients favor similar shifts in leaf attributes, and in this sense can be grouped together as sources of “stress.” Some evolutionary divergences in leaf structure occurred repeatedly toward the lower end of both rainfall and soil nutrient gradients. These include narrower leaves, lower specific leaf area (SLA), thicker lamina, and denser leaf tissue. In other respects, the different resource gradients appeared to favor different leaf attributes. In 8 of 10 contrasts, plants of low-wat...

Seed supply for broadscale restoration: maximizing evolutionary potential.

Restoring degraded land to combat environmental degradation requires the collection of vast quantities of germplasm (seed). Sourcing this material raises questions related to provenance selection, seed quality and harvest sustainability. Restoration guidelines strongly recommend using local sources to maximize local adaptation and prevent outbreeding depression, but in highly modified landscapes this restricts collection to small remnants where limited, poor quality seed is available, and where harvesting impacts may be high. We review three principles guiding the sourcing of restoration germplasm: (i) the appropriateness of using ‘local’ seed, (ii) sample sizes and population characteristics required to capture sufficient genetic diversity to establish self‐sustaining populations and (iii) the impact of over‐harvesting source populations. We review these topics by examining current collection guidelines and the evidence supporting these, then we consider if the guidelines can be improved and the consequences of not doing so. We find that the emphasis on local seed sourcing will, in many cases, lead to poor restoration outcomes, particularly at broad geographic scales. We suggest that seed sourcing should concentrate less on local collection and more on capturing high quality and genetically diverse seed to maximize the adaptive potential of restoration efforts to current and future environmental change.

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.

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.

Depressed pollination in habitat fragments causes low fruit set

In central New South Wales, Australia, flowers of Acacia brachybotrya and Eremophila glabra plants growing in linear vegetation remnants received less pollen than conspecifics in nearby reserves. Pollen supplementation increased fruit production by both species, indicating pollen limitation of fruit set. Together these observations explain why fruit production by these species was depressed in linear–strip populations relative to nearby reserves. This study confirms that habitat fragmentation can lead to decline in pollination and subsequent fruit set in wild plant populations. Disrupted pollination interactions of the kind documented in this study may offer a substantial challenge to the conservation of biodiversity in fragmented landscapes.

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.