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Agricultural growth is particularly effective in improving food security, especially in low income areas [ 38 ], and sustainable intensification is a pathway for realising this [ 2 , 10 , 19 ]. Sustainable intensification includes enhancing or conserving ecosystem services for the role they can play in maintaining and increasing crop production. Ecological intensification is as important in the developing world as it is in the developed world. In addition, the diversity of farming systems in the developing world is greater than the more uniform large-scale and typically intensive agriculture in the developed world.

Sustainable intensification of developing world agriculture must include the billions of farmers that are smallholders [ 19 , 38 ] for whom management guidance for ecological intensification must also work [ 8 ]. However, we show here that there are significant farming-landscape, regional, climatic and economic biases in the evidence base underpinning the likely contribution of regulating ecosystem services to sustainable intensification via quantitative review. The extent to which management interventions derived from research conducted in large-scale farms in developed regions, such as the US and Western Europe, can be generalised to benefit food security in other regions is likely to be limited when there are significant contextual differences in the farming system, climate for example, differences in extremes and modality of temperature and rainfall between temperate and tropical regions and biogeography for example, differences in regional species pools.

Compared to large-scale farming landscapes smallholder-farmed landscapes are much more diverse in terms of local and landscape complexity, management intensity and the interactions between them Additional file 7 : Figure S4. Smallholder landscapes, particularly in areas of subsistence farming, are likely to have a high richness and diversity of crop types, both spatially and temporally [ 16 ]. Also, smallholder landscapes typically will not reach the levels of management intensity that occur in large-scale farms.


If research efforts are concentrated in large-scale systems then we are unlikely to be fully exploring the gradients of farmland landscape complexity and management intensity and their relationship with ecosystem service providers and function. As well as differences between smallholder and large-scale farmed landscapes, there are clearly cultural and contextual differences within the smallholder system for example, coffee agroforestry in humid South-East Asia vs.

However, of the 22 smallholder studies in the quantitative reviews, 16 came from a single context - coffee systems. Coffee is a cash crop, a perennial crop and a stimulant that has no calorific value. Thus, research in these coffee landscapes is of low relevance to landscapes of annual crops that are grown for local consumption and contribute to local food security.

Therefore, we need both an increase in the proportion of smallholder research and also an increase in the diversity of research. All two billion smallholders - two billion decision makers - are unlikely to be served by the same research findings. Moreover, since our expectations of how much research should come from smallholder farmed landscapes were based on the number of smallholder farmers, the results were more significantly biased against smallholder farmed landscapes than they were when our expectations were based on the area of smallholder farmland.

Although the area of smallholder farmland is more relevant to total global food production, we emphasize that the number of smallholders, who constitute a large proportion of the undernourished, would seem to be more relevant to local food security. Thus, the combination of diversity and food insecurity in smallholder systems means that research biases against these systems are all the more acute. Regional biases such as these might pose a problem for generalising to other under-represented regions. The responses of different bee species to disturbance [ 39 , 40 ] and the applicability of a generalised ES relationship for example, the relationship between flower visitation and distance from natural habitat may depend upon the species present in a region.

In some cases, functional groups of service-providing species may be absent or substantially different between regions [ 31 ]. For example, bumblebees Bombus spp. Furthermore, the balance between ecosystem services and dis-services services that reduce productivity or increase production costs, such as herbivory flowing from a natural habitat to a nearby farmland may differ between regions.

Quantitative reviews have often found that natural habitats benefit ecosystem services, such as pollination in nearby farmland [for example, 32]. However, the species that can move from natural habitats into croplands can fundamentally differ between regions.

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Proximity to a natural area in sub-Saharan African and South Asia can expose a farmer to crop-raiding elephants and primates that can reduce crop yields and create human-wildlife conflict. In contrast, in Europe and North America, regions to which research is biased, crop-raiding is a minor problem. When studying the net benefits of natural habitat in certain sub-Saharan African contexts, we might learn that crop raiding an ecosystem disservice tends to outweigh the benefits of enhanced pollination and biological control services on farms near natural habitats. The consequences of crop raiding are likely to impact large landholders less than smallholders, as an individual smallholder can easily lose the majority of their harvest to an elephant or troupe of baboons.

Although ecosystem dis-services could strongly affect the design of sustainable farming landscapes for example, crops that are unpalatable to primates might be used to buffer a habitat with many baboons and monkeys , they are poorly considered in the published literature but see [ 43 ]. Two-thirds of pooled studies came from the temperate region despite tropical croplands occupying a larger area than temperate croplands.

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Obviously, there are profound climatic differences between biomes that shape the assemblages of pollinators and invertebrate pests and their natural enemies. In general, the effects of climate and climate change on pollinators are much better understood than are effects on other groups of ecosystem-service providers [ 44 ], and our analyses reflect this. We show individual quantitative reviews relevant to pollination tend to balance data from tropical and temperate regions whereas biological-control reviews were all significantly and often strongly biased to the temperate zone.

There can be major differences between tropical and temperate biomes in the spatial and temporal availability of resources important for ecosystem-service providers in natural habitats habitats that may enhance ES in nearby crops. For example, the plant community in aseasonal tropical lowland forests has a continuous pollination period throughout the year compared to just late spring and summer in northern temperate forests [ 45 ].

Temperate forests also have higher mean flower longevity and a larger proportion of wind-pollinated plants than aseasonal tropical forests [ 45 ]. As the functional significance flowers providing nectar and pollen of a forest to pollinators differs between and within biomes, this is likely to be the case for other habitats including agricultural land , functions for example, nesting sites and ecosystem service providers too.

As such, interventions for ecological intensification that require manipulating or conserving natural areas in a farming landscape should carefully consider what climate the intervention was derived from and the implications of any functional differences in habitats between derived and target climates see [ 44 ].

This may also reflect a publication bias in that researchers from developed nations may be more likely to publish their work in English-language peer-reviewed journals. The consequences of the overabundance of studies from temperate regions and large-scale landscapes particularly the U. For example, local management options are likely to have more positive effects on service providing insects in agricultural landscapes of intermediate complexity [ 46 — 48 ], but less so in small-scale landscapes comprising many other habitats in addition to agricultural fields [ 39 , 49 — 51 ].

The interaction of local and landscape factors can be important for ES delivery as was the case for flower visitation and production in commercial South African sunflower fields where the enhancement of floral diversity within fields ameliorated the negative effects of isolation from natural habitat [ 52 ]. Cultural species dependent on crop habitats of pollinators and natural enemies might be negatively affected by landscape complexity, whilst ecotone species and dispersers dependent on non-crop habitats might be positively affected [ 22 ]. The most recent reviews relevant to pollination should be commended for considering complexity at multiple spatial-scales.

For example, Garibaldi et al. However, even in recent reviews, smallholding landscapes are not considered explicitly. As such, determining when generalisations can and cannot be applied to a type of smallholder landscapes across multiple regions and thus climates should be a priority for ES science. Quantitative reviews are essential for modelling and predicting ES provisioning in the design of sustainable farming landscapes, for directing the policies required to adapt our current farming practices and advancing ecosystem service theory.

Differences spatial and temporal in management intensity and local complexity between smallholder-farmed and large-scale farming landscapes may cause ecosystem service-providing insects to respond differently to disturbance and management interventions. The high local complexity of smallholder-farmed landscapes could promote beneficial species and, consequently, the ES they provide. Biogeographic differences between regions in terms of climate and service- and disservice-providing species pools may also present problems for the generalisation of findings and application of ecological intensification.

Thus, generalisations from the quantitative reviews included here to smallholder-farmed landscapes and, for biological-control reviews, to tropical landscapes, should be made with caution, especially in regions where little research has been conducted. More specifically, research bias in reviews affects their general application to informing about sustainable intensification. The large number of pollination and biological control studies from temperate large-scale farming landscapes suggests we are well placed to improve ES and trial ecological intensification there.

This problem is greatest in tropical regions with diverse farming landscapes and high agricultural populations, such as South Asia and sub-Saharan Africa, where smallholdings contribute more than a third of the agricultural area Additional file 1 : Table S1.

Investing globally in smallholder research for multiple crops and finding more projects and publications from regions where there is little information such as China, Russia, South Asia and Africa is essential. This is especially the case for research relevant to biological control, which appears more biased than pollination-relevant research.

To increase their global relevance, quantitative reviews investigating landscape or local effects on ES should consider the coverage of their datasets with regards to region, climate and farming landscape. Following on from this, future empirical studies should target smallholder systems, with quantification of climate and complexity in time and at multiple spatial-scales. Classification of existing studies that do not present landscape information could also provide new data and this is becoming easier.

Tropical fruit pests and pollinators : biology, economic importance, natural enemies and control

International collaboration is needed to search for, translate if necessary and disseminate the ES datasets that no doubt exist in the developing world. We suggest that non-English language publications and agricultural institutions that may often be overlooked will be productive. Data regarding the cost of ecosystem dis-services in agricultural areas near protected areas in South Asia or sub-Saharan Africa may already be available from social and developmental disciplines. If so, this should be integrated into current assessments of the net ES value of natural habitats.

Global datasets regarding the structure of farmland are incomplete and inconsistent. Therefore, our estimates of smallholder area in some regions, such as sub-Saharan Africa, were based on limited data and we hope the pending World Census of Agriculture will improve the situation. Furthermore, our classification of landscapes into broad structural categories was necessarily simplistic. From an ES perspective, smallholding landscapes could better be defined using statistical measures of configuration see [ 50 ] and information regarding composition and management. In the face of global climate change and challenges to food security, it is important to understand these issues for diverse environmental conditions and landscapes that fully represent the global farming constituency.

Further investigation of the conditions that characterize smallholder-farmed landscapes would provide crucial information regarding the resilience of such landscapes to environmental disturbance across multiple ecosystem services. Foresight: The Future of Food and Farming. Bruinsma J: The resource outlook to Pretty J: Agricultural sustainability: concepts, principles and evidence. Phil Trans R Soc B. Ecol Soc. Kremen C, Miles A: Ecosystem services in biologically diversified versus conventional farming systems: benefits, externalities, and trade-offs. Email or Customer ID.

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