Ingolf Steffan-Dewenter

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.

SCALE-DEPENDENT EFFECTS OF LANDSCAPE CONTEXT ON THREE POLLINATOR GUILDS

Most ecological processes and interactions depend on scales much larger than a single habitat, and therefore it is important to link spatial patterns and ecological processes at a landscape scale. Here, we analyzed the effects of landscape context on the distribution of bees (Hymenoptera: Apoidea) at multiple spatial scales with respect to the following hypotheses: (1) Local abundance and diversity of bees increase with increasing proportion of the surrounding seminatural habitats. (2) Solitary wild bees, bumble bees, and honey bees respond to landscape context at different spatial scales. We selected 15 landscape sectors and determined the percentage of seminatural habitats and the diversity of habitat types at eight spatial scales (radius 250-3000 m) by field inspections and analyses of vegetation maps using two Geographic Information Systems. The percentage of semi- natural habitats varied between 1.4% and 28%. In the center of each landscape sector a patch of potted flowering plants (four perennial and two annual species) was placed in the same habitat type, a grassy field margin adjacent to cereal fields. In all, 865 wild bee individuals and 467 honey bees were observed and an additional 475 individuals were caught for species identification. Species richness and abundance of solitary wild bees showed a close positive correlation with the percentage of seminatural habitats at small scales up to 750 m, whereas bumble bees and honey bees did not respond to landscape context at these scales. In contrast, honey bees were correlated with landscape context at large scales. The densities of flower-visiting honey bees even increased with decreasing proportion of seminatural habitats at a radius of 3000 m. We are not aware of any empirical studies showing contrasting foraging patterns related to landscape context at different spatial scales. We conclude (1) that local landscape destruction affects solitary wild bees more than social bees, possibly changing mutualistic plant-pollinator and competitive wild bees- honey bees interactions and (2) that only analyses of multiple spatial scales may detect the importance of the landscape context for local pollinator communities.

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.

Extinction debt: a challenge for biodiversity conservation

Local extinction of species can occur with a substantial delay following habitat loss or degradation. Accumulating evidence suggests that such extinction debts pose a significant but often unrecognized challenge for biodiversity conservation across a wide range of taxa and ecosystems. Species with long generation times and populations near their extinction threshold are most likely to have an extinction debt. However, as long as a species that is predicted to become extinct still persists, there is time for conservation measures such as habitat restoration and landscape management. Standardized long-term monitoring, more high-quality empirical studies on different taxa and ecosystems and further development of analytical methods will help to better quantify extinction debt and protect biodiversity.

Effects of habitat isolation on pollinator communities and seed set

Abstract Destruction and fragmentation of natural habitats is the major reason for the decreasing biodiversity in the agricultural landscape. Loss of populations may negatively affect biotic interactions and ecosystem stability. Here we tested the hypothesis that habitat fragmentation affects bee populations and thereby disrupts plant-pollinator interactions. We experimentally established small ”habitat islands” of two self-incompatible, annual crucifers on eight calcareous grasslands and in the intensively managed agricultural landscape at increasing distances (up to 1000 m) from these species-rich grasslands to measure effects of isolation on both pollinator guilds and seed set, independently from patch size and density, resource availability and genetic erosion of plant populations. Each habitat island consisted of four pots each with one plant of mustard (Sinapis arvensis) and radish (Raphanus sativus). Increasing isolation of the small habitat islands resulted in both decreased abundance and species richness of flower-visiting bees (Hymenoptera: Apoidea). Mean body size of flower-visiting wild bees was larger on isolated than on nonisolated habitat islands emphasizing the positive correlation of body size and foraging distance. Abundance of flower-visiting honeybees depended on the distance from the nearest apiary. Abundance of other flower visitors such as hover flies did not change with increasing isolation. Number of seeds per fruit and per plant decreased significantly with increasing distance from the nearest grassland for both mustard and radish. Mean seed set per plant was halved at a distance of approximately 1000 m for mustard and at 250 m for radish. In accordance with expectations, seed set per plant was positively correlated with the number of flower-visiting bees. We found no evidence for resource limitation in the case of mustard and only marginal effects for radish. We conclude that habitat connectivity is essential to maintain not only abundant and diverse bee communities, but also plant-pollinator interactions in economically important crops and endangered wild plants.

Fruit set of highland coffee increases with the diversity of pollinating bees

The worldwide decline of pollinators may negatively affect the fruit set of wild and cultivated plants. Here, we show that fruit set of the self–fertilizing highland coffee (Coffea arabica) is highly variable and related to bee pollination. In a comparison of 24 agroforestry systems in Indonesia, the fruit set of coffee could be predicted by the number of flower–visiting bee species, and it ranged from ca. 60% (three species) to 90% (20 species). Diversity, not abundance, explained variation in fruit set, so the collective role of a species–rich bee community was important for pollination success. Additional experiments showed that single flower visits from rare solitary species led to higher fruit set than with abundant social species. Pollinator diversity was affected by two habitat parameters indicating guild–specific nesting requirements: the diversity of social bees decreased with forest distance, whereas the diversity of solitary bees increased with light intensity of the agroforestry systems. These results give empirical evidence for a positive relationship between ecosystem functions such as pollination and biodiversity. Conservation of rainforest adjacent to adequately managed agroforestry systems could improve the yields of farmers.

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.

Habitat fragmentation causes immediate and time‐delayed biodiversity loss at different trophic levels

Intensification or abandonment of agricultural land use has led to a severe decline of semi-natural habitats across Europe. This can cause immediate loss of species but also time-delayed extinctions, known as the extinction debt. In a pan-European study of 147 fragmented grassland remnants, we found differences in the extinction debt of species from different trophic levels. Present-day species richness of long-lived vascular plant specialists was better explained by past than current landscape patterns, indicating an extinction debt. In contrast, short-lived butterfly specialists showed no evidence for an extinction debt at a time scale of c. 40 years. Our results indicate that management strategies maintaining the status quo of fragmented habitats are insufficient, as time-delayed extinctions and associated co-extinctions will lead to further biodiversity loss in the future.

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.

Functional group diversity of bee pollinators increases crop yield

Niche complementarity is a commonly invoked mechanism underlying the positive relationship between biodiversity and ecosystem functioning, but little empirical evidence exists for complementarity among pollinator species. This study related differences in three functional traits of pollinating bees (flower height preference, daily time of flower visitation and within-flower behaviour) to the seed set of the obligate cross-pollinated pumpkin Cucurbita moschata Duch. ex Poir. across a land-use intensity gradient from tropical rainforest and agroforests to grassland in Indonesia. Bee richness and abundance changed with habitat variables and we used this natural variation to test whether complementary resource use by the diverse pollinator community enhanced final yield. We found that pollinator diversity, but not abundance, was positively related to seed set of pumpkins. Bees showed species-specific spatial and temporal variation in flower visitation traits and within-flower behaviour, allowing for classification into functional guilds. Diversity of functional groups explained even more of the variance in seed set (r2=45%) than did species richness (r2=32%) highlighting the role of functional complementarity. Even though we do not provide experimental, but rather correlative evidence, we can link spatial and temporal complementarity in highly diverse pollinator communities to pollination success in the field, leading to enhanced crop yield without any managed honeybees.