Global-scale drivers of crop visitor diversity and the historical development of agriculture.

Understanding diversity in flower-visitor assemblages helps us improve pollination of crops and support better biodiversity conservation outcomes. Much recent research has focused on drivers of crop-visitor diversity operating over spatial scales from fields to landscapes, such as pesticide and habitat management, while drivers operating over larger scales of continents and biogeographic realms are virtually unknown. Flower and visitor traits influence attraction of pollinators to flowers, and evolve in the context of associations that can be ancient or recent. Plants that have been adopted into agriculture have been moved widely around the world and thereby exposed to new flower visitors. Remarkably little is known of the consequence of these historical patterns for present-day crop-visiting bee diversity. We analyse data from 317 studies of 27 crops worldwide and find that crops are visited by fewer bee genera outside their region of origin and outside their family's region of origin. Thus, recent human history and the deeper evolutionary history of crops and bees appear to be important determinants of flower-visitor diversity at large scales that constrain the levels of visitor diversity that can be influenced by field- and landscape-scale interventions.

Experimental habitat fragmentation disrupts nematode infections in Australian skinks.

Habitat conversion and fragmentation threaten biodiversity and disrupt species interactions. While parasites are recognized as ecologically important, the impacts of fragmentation on parasitism are poorly understood relative to other species interactions. This lack of understanding is in part due to confounding landscape factors that accompany fragmentation. Fragmentation experiments provide the opportunity to fill this knowledge gap by mechanistically testing how fragmentation affects parasitism while controlling landscape factors. In a large-scale, long-term experiment, we asked how fragmentation affects a host-parasite interaction between a skink and a parasitic nematode, which is trophically transmitted via a terrestrial amphipod intermediate host. We expected that previously observed amphipod declines resulting from fragmentation would result in decreased transmission of nematodes to skinks. In agreement, we found that nematodes were absent among skinks in the cleared matrix and that infections in fragments were about one quarter of those in continuous forest. Amphipods found in gut contents of skinks and collected from pitfall traps mirrored this pattern. A structural equation model supported the expectation that fragmentation disrupted this interaction by altering the abundance of amphipods and suggested that other variables are likely also important in mediating this effect. These findings advance understanding of how landscape change affects parasitism.

Non-bee insects are important contributors to global crop pollination.

Wild and managed bees are well documented as effective pollinators of global crops of economic importance. However, the contributions by pollinators other than bees have been little explored despite their potential to contribute to crop production and stability in the face of environmental change. Non-bee pollinators include flies, beetles, moths, butterflies, wasps, ants, birds, and bats, among others. Here we focus on non-bee insects and synthesize 39 field studies from five continents that directly measured the crop pollination services provided by non-bees, honey bees, and other bees to compare the relative contributions of these taxa. Non-bees performed 25-50% of the total number of flower visits. Although non-bees were less effective pollinators than bees per flower visit, they made more visits; thus these two factors compensated for each other, resulting in pollination services rendered by non-bees that were similar to those provided by bees. In the subset of studies that measured fruit set, fruit set increased with non-bee insect visits independently of bee visitation rates, indicating that non-bee insects provide a unique benefit that is not provided by bees. We also show that non-bee insects are not as reliant as bees on the presence of remnant natural or seminatural habitat in the surrounding landscape. These results strongly suggest that non-bee insect pollinators play a significant role in global crop production and respond differently than bees to landscape structure, probably making their crop pollination services more robust to changes in land use. Non-bee insects provide a valuable service and provide potential insurance against bee population declines.

Effects of past and present livestock grazing on herpetofauna in a landscape-scale experiment.

Livestock grazing is the most widespread land use on Earth and can have negative effects on biodiversity. Yet, many of the mechanisms by which grazing leads to changes in biodiversity remain unresolved. One reason is that conventional grazing studies often target broad treatments rather than specific parameters of grazing (e.g., intensity, duration, and frequency) or fail to account for historical grazing effects. We conducted a landscape-scale replicated grazing experiment (15,000 km2 , 97 sites) to examine the impact of past grazing management and current grazing regimes (intensity, duration, and frequency) on a community of ground-dwelling herpetofauna (39 species). We analyzed community variables (species richness and composition) for all species and built multiseason patch-occupancy models to predict local colonization and extinction for the 7 most abundant species. Past grazing practices did not influence community richness but did affect community composition and patch colonization and extinction for 4 of 7 species. Present grazing parameters did not influence community richness or composition, but 6 of the 7 target species were affected by at least one grazing parameter. Grazing frequency had the most consistent influence, positively affecting 3 of 7 species (increased colonization or decreased extinction). Past grazing practice affected community composition and population dynamics in some species in different ways, which suggests that conservation planners should examine the different grazing histories of an area. Species responded differently to specific current grazing practices; thus, incentive programs that apply a diversity of approaches rather than focusing on a change such as reduced grazing intensity should be considered. Based on our findings, we suggest that determining fine-scale grazing attributes is essential for advancing grazing as a conservation strategy.

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 Jensen's 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.

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.

The role of carrion in maintaining biodiversity and ecological processes in terrestrial ecosystems.

Carrion provides a resource for a subset of animal species that deliver a critical ecosystem service by consuming dead animal matter and recycling its nutrients. A growing number of studies have also shown various effects of carrion on different plant and microbial communities. However, there has been no review of these studies to bring this information together and identify priority areas for future research. We review carrion ecology studies from the last two decades and summarise the range of spatial and temporal effects of carrion on soil nutrients, microbes, plants, arthropods, and vertebrates. We identify key knowledge gaps in carrion ecology, and discuss how closing these gaps can be achieved by focusing future research on the (1) different kinds of carrion resources, (2) interactions between different components of the carrion community, (3) the ways that ecosystem context can moderate carrion effects, and (4) considerations for carrion management. To guide this research, we outline a framework that builds on the 'ephemeral resource patch' concept, and helps to structure research questions that link localised effects of carrion with their consequences at landscape scales. This will enable improved characterisation of carrion as a unique resource pool, provide answers for land managers in a position to influence carrion availability, and establish the ways that carrion affects the dynamics of species diversity and ecological processes within landscapes.

Density of invasive western honey bee (Apis mellifera) colonies in fragmented woodlands indicates potential for large impacts on native species.

Feral Apis mellifera colonies are widespread globally and cause ecological impacts as pollinators and competitors for food and nesting opportunities. The magnitude of impact depends on their population density, but knowledge of this density is poor. We document feral A. mellifera colonies at 69 per km2 in fragmented Eucalyptus woodlands in Australia, exceeding estimates from elsewhere in the world, and matched only by one other Australian study. We surveyed 52.5 ha of woodland patches with 357 nest boxes installed to provide nesting opportunities for threatened vertebrates. Our sites covered a region of more than 140 km across with repeated surveys over 3 to 6 years. We show that nest box use by feral A. mellifera colonies is influenced by box design (p = 0.042), with weak evidence for an interactive effect of type of vegetation at a site (woodland remnants vs. replanting) and woody cover within 500 m (p = 0.091). At 69 colonies per km2, this density is equivalent to the recommended stocking of hives for pollination of some crops and is therefore likely to influence pollination and lead to competition with other flower visitors. Apis mellifera is also likely to be competing for hollows with cavity dependent native fauna, especially in landscapes where there has been extensive tree removal.

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.

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.

Habitat contrasts reveal a shift in the trophic position of ant assemblages.

1. Trophic structure within a guild can be influenced by factors such as resource availability and competition. While ants occupy a wide range of positions in food webs, and ant community composition changes with habitat, it is not well understood if ant genera tend to maintain their position in the trophic structure, or if trophic position varies across habitats. 2. We used ratios of stable isotopes of carbon and nitrogen to test for differences in the trophic structure and position of assemblages of ants among habitat types. We tested for differences between assemblages in replicate sites of the land use categories: (i) pastures with old large trees; (ii) recently revegetated pastures with small young trees; and (iii) remnant woodlands. Known insect herbivores and predatory spiders provided baselines for herbivorous and predaceous arthropods. Soil samples were used to correct for the base level of isotopic enrichment at each site. 3. We found no significant interactions between land use and ant genus for isotope enrichment, indicating that trophic structure is conserved across land use categories. The fixed relative positions of genera in the trophic structure might be re-enforced by competition or some other factor. However, the entire ant assemblage had significantly lower δ(15) N values in revegetated sites, suggesting that ants feed lower down in the food chain i.e. they are more 'herbivorous' in revegetated sites. This may be a result of the high availability of plant sugars, honeydew and herbivorous arthropod prey. 4. Surprisingly, ants in remnants and pastures with trees displayed similar isotopic compositions. Interactions within ant assemblages are thus likely to be resilient to changes in land use, but ant diets in early successional habitats may reflect the simplicity of communities, which may have comparatively lower rates of saprophagy and predation.

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.

Returning a lost process by reintroducing a locally extinct digging marsupial.

The eastern bettong (Bettongia gaimardi), a medium-sized digging marsupial, was reintroduced to a predator-free reserve after 100 years of absence from the Australian mainland. The bettong may have the potential to restore temperate woodlands degraded by a history of livestock grazing, by creating numerous small disturbances by digging. We investigated the digging capacity of the bettong and compared this to extant fauna, to answer the first key question of whether this species could be considered an ecosystem engineer, and ultimately if it has the capacity to restore lost ecological processes. We found that eastern bettongs were frequent diggers and, at a density of 0.3-0.4 animals ha-1, accounted for over half the total foraging pits observed (55%), with echidnas (Tachyglossus aculeatus), birds and feral rabbits (Oryctolagus cuniculus) accounting for the rest. We estimated that the population of bettongs present dug 985 kg of soil per ha per year in our study area. Bettongs dug more where available phosphorus was higher, where there was greater basal area of Acacia spp. and where kangaroo grazing was less. There was no effect on digging of eucalypt stem density or volume of logs on the ground. While bettong digging activity was more frequent under trees, digging also occurred in open grassland, and bettongs were the only species observed to dig in scalds (areas where topsoil has eroded to the B Horizon). These results highlight the potential for bettongs to enhance soil processes in a way not demonstrated by the existing fauna (native birds and echidna), and introduced rabbit.

Effects of digging by a native and introduced ecosystem engineer on soil physical and chemical properties in temperate grassy woodland.

Temperate grasslands and woodlands are the focus of extensive restoration efforts worldwide. Reintroduction of locally extinct soil-foraging and burrowing animals has been suggested as a means to restore soil function in these ecosystems. Yet little is known about the physical and chemical effects of digging on soil over time and how these effects differ between species of digging animal, vegetation types or ecosystems. We compared foraging pits of a native reintroduced marsupial, the eastern bettong (Bettongia gaimardi) and that of the exotic European rabbit (Oryctolagus cuniculus). We simulated pits of these animals and measured pit dimensions and soil chemical properties over a period of 2 years. We showed that bettong and rabbit pits differed in their morphology and longevity, and that pits had a strong moderating effect on soil surface temperatures. Over 75% of the simulated pits were still visible after 2 years, and bettong pits infilled faster than rabbit pits. Bettong pits reduced diurnal temperature range by up to 25 °C compared to the soil surface. We did not find any effects of digging on soil chemistry that were consistent across vegetation types, between bettong and rabbit pits, and with time since digging, which is contrary to studies conducted in arid biomes. Our findings show that animal foraging pits in temperate ecosystems cause physical alteration of the soil surface and microclimatic conditions rather than nutrient changes often observed in arid areas.

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.

Advances in pollination ecology from tropical plantation crops.

Although ecologists traditionally focus on natural ecosystems, there is growing awareness that mixed landscapes of managed and unmanaged systems provide a research environment for understanding basic ecological relationships on a large scale. Here, we show how tropical agroforestry systems can be used to develop ideas about the mechanisms that influence species diversity and subsequent biotic interactions at different spatial scales. Our focus is on tropical plantation crops, mainly coffee and cacao, and their pollinators, which are of basic ecological interest as partners in an important mutualistic interaction. We review how insect-mediated pollination services depend on local agroforest and natural habitats in surrounding landscapes. Further, we evaluate the functional significance of pollinator diversity and the explanatory value of species traits, and we provide an intercontinental comparison of pollinator assemblages. We found that optimal pollination success might be best understood as a consequence of niche complementarities among pollinators in landscapes harboring various species. We further show that small cavity-nesting bees and small generalist beetles were especially affected by isolation from forest and that larger-bodied insects in the same landscapes were not similarly affected. We suggest that mixed tropical landscapes with agroforestry systems have great potential for future research on the interactions between plants and pollinators.

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.

Predicting the economic impact of an invasive species on an ecosystem service.

Quantifying the impact of alien invasive species on ecosystem services is an essential step in developing effective practices and policy for invasive species management. Here we develop a stochastic bioeconomic model that enables the economic impact of an invasive pest to be estimated before its arrival, based on relatively poorly specified ecological and economic parameters. We developed the model by using a hypothetical invasion of the varroa bee mite (Varroa destructor) into Australia and the negative flow-on effects that it would have on pollination by reducing honey bee populations, giving rise to a loss of pollination services, reduced crop yields, and additional production costs. If the mite were to continue to be prevented from entering the country over the next 30 years, we estimate that the economic costs avoided would be U.S. $16.4-38.8 million (Aus $21.3-50.5 million) per year. We suggest that current invasion response funding arrangements in Australia, which do not acknowledge these avoided damages, require amendment.

Deconstructing pollinator community effectiveness.

Effective pollination is a complex, context-dependent phenomenon determined by both species-level and community-level factors. While pollinator communities are constituted by interacting organisms in a shared environment, these factors are often simplified or overlooked when quantifying species-level pollinator effectiveness alone. Here, we review the recent literature on pollinator effectiveness to identify the pros and cons of existing methods and outline three important areas for future research: plant-pollinator interactions, heterospecific pollen transfer and variation in pollination outcomes. We conclude that pollinator community effectiveness needs to be acknowledged as a key property of pollination effectiveness in order to fully account for the suite of plant, pollinator and environmental factors known to influence different stages of successful pollination.

Farming Approaches for Greater Biodiversity, Livelihoods, and Food Security.

Scientists and policy-makers globally are calling for alternative approaches to conventional intensification of agriculture that enhance ecosystem services provided by biodiversity. The evidence reviewed here suggests that alternative approaches can achieve high crop yields and profits, but the performance of other socioeconomic indicators (as well as long-term trends) is surprisingly poorly documented. Consequently, the implementation of conventional intensification and the discussion of alternative approaches are not based on quantitative evidence of their simultaneous ecological and socioeconomic impacts across the globe. To close this knowledge gap, we propose a participatory assessment framework. Given the impacts of conventional intensification on biodiversity loss and greenhouse gas emissions, such evidence is urgently needed to direct science-policy initiatives, such as the United Nations (UN) 2030 Agenda for Sustainable Development.