Teja Tscharntke

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.

Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control

Agricultural intensification has resulted in a simplification of agricultural landscapes by the expansion of agricultural land, enlargement of field size and removal of non-crop habitat. These changes are considered to be an important cause of the rapid decline in farmland biodiversity, with the remaining biodiversity concentrated in field edges and non-crop habitats. The simplification of landscape composition and the decline of biodiversity may affect the functioning of natural pest control because non-crop habitats provide requisites for a broad spectrum of natural enemies, and the exchange of natural enemies between crop and non-crop habitats is likely to be diminished in landscapes dominated by arable cropland. In this review, we test the hypothesis that natural pest control is enhanced in complex patchy landscapes with a high proportion of non-crop habitats as compared to simple large-scale landscapes with little associated non-crop habitat. In 74% and 45% of the studies reviewed, respectively, natural enemy populations were higher and pest pressure lower in complex landscapes versus simple landscapes. Landscape-driven pest suppression may result in lower crop injury, although this has rarely been documented. Enhanced natural enemy activity was associated with herbaceous habitats in 80% of the cases (e.g. fallows, field margins), and somewhat less often with wooded habitats (71%) and landscape patchiness (70%). The similar contributions of these landscape factors suggest that all are equally important in enhancing natural enemy populations. We conclude that diversified landscapes hold most potential for the conservation of biodiversity and sustaining the pest control function.

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.

Habitat Fragmentation, Species Loss, and Biological Control

Fragmentation of habitats in the agricultural landscape is a major threat to biological diversity, which is greatly determined by insects. Isolation of habitat fragments resulted in decreased numbers of species as well as reduced effects of natural enemies. Manually established islands of red clover were colonized by most available herbivore species but few parasitoid species. Thus, herbivores were greatly released from parasitism, experiencing only 19 to 60 percent of the parasitism of nonisolated populations. Species failing to successfully colonize isolated islands were characterized by small and highly variable populations. Accordingly, lack of habitat connectivity released insects from predator control.

Habitat modification alters the structure of tropical host–parasitoid food webs

Global conversion of natural habitats to agriculture has led to marked changes in species diversity and composition. However, it is less clear how habitat modification affects interactions among species. Networks of feeding interactions (food webs) describe the underlying structure of ecological communities, and might be crucially linked to their stability and function. Here, we analyse 48 quantitative food webs for cavity-nesting bees, wasps and their parasitoids across five tropical habitat types. We found marked changes in food-web structure across the modification gradient, despite little variation in species richness. The evenness of interaction frequencies declined with habitat modification, with most energy flowing along one or a few pathways in intensively managed agricultural habitats. In modified habitats there was a higher ratio of parasitoid to host species and increased parasitism rates, with implications for the important ecosystem services, such as pollination and biological control, that are performed by host bees and wasps. The most abundant parasitoid species was more specialized in modified habitats, with reduced attack rates on alternative hosts. Conventional community descriptors failed to discriminate adequately among habitats, indicating that perturbation of the structure and function of ecological communities might be overlooked in studies that do not document and quantify species interactions. Altered interaction structure therefore represents an insidious and functionally important hidden effect of habitat modification by humans.

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.

On the relationship between farmland biodiversity and land-use intensity in Europe

Worldwide agriculture is one of the main drivers of biodiversity decline. Effective conservation strategies depend on the type of relationship between biodiversity and land-use intensity, but to date the shape of this relationship is unknown. We linked plant species richness with nitrogen (N) input as an indicator of land-use intensity on 130 grasslands and 141 arable fields in six European countries. Using Poisson regression, we found that plant species richness was significantly negatively related to N input on both field types after the effects of confounding environmental factors had been accounted for. Subsequent analyses showed that exponentially declining relationships provided a better fit than linear or unimodal relationships and that this was largely the result of the response of rare species (relative cover less than 1%). Our results indicate that conservation benefits are disproportionally more costly on high-intensity than on low-intensity farmland. For example, reducing N inputs from 75 to 0 and 400 to 60 kg ha−1 yr−1 resulted in about the same estimated species gain for arable plants. Conservation initiatives are most (cost-)effective if they are preferentially implemented in extensively farmed areas that still support high levels of biodiversity.

Bottom-up effects of plant diversity on multitrophic interactions in a biodiversity experiment

Biodiversity is rapidly declining, and this may negatively affect ecosystem processes, including economically important ecosystem services. Previous studies have shown that biodiversity has positive effects on organisms and processes across trophic levels. However, only a few studies have so far incorporated an explicit food-web perspective. In an eight-year biodiversity experiment, we studied an unprecedented range of above- and below-ground organisms and multitrophic interactions. A multitrophic data set originating from a single long-term experiment allows mechanistic insights that would not be gained from meta-analysis of different experiments. Here we show that plant diversity effects dampen with increasing trophic level and degree of omnivory. This was true both for abundance and species richness of organisms. Furthermore, we present comprehensive above-ground/below-ground biodiversity food webs. Both above ground and below ground, herbivores responded more strongly to changes in plant diversity than did carnivores or omnivores. Density and richness of carnivorous taxa was independent of vegetation structure. Below-ground responses to plant diversity were consistently weaker than above-ground responses. Responses to increasing plant diversity were generally positive, but were negative for biological invasion, pathogen infestation and hyperparasitism. Our results suggest that plant diversity has strong bottom-up effects on multitrophic interaction networks, with particularly strong effects on lower trophic levels. Effects on higher trophic levels are indirectly mediated through bottom-up trophic cascades.

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.