Potential predators and parasitoids for conservation biological control in smallholder bean farming tropical ecosystem

A Thesis Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Life Sciences of the Nelson Mandela African Institution of Science and TechnologyConservation biological control (CBC) is an attempt to protect the already existing natural enemies (predators, parasitoids or pathogens) of insect pests within the agricultural systems by manipulating the environment and farming practices to provide the required resources for their survival. This study assessed the major arthropod predators and parasitoids of common bean (Phaseolus vulgaris) insect pests in smallholder bean farming tropical ecosystem and their contribution in pest management, in three elevation zones during 2016 and 2017. The farmers’ knowledge about natural enemies, insect pest and pesticide use was investigated followed by field surveys and experiments to determine the contribution of major predators and parasitoids to pest management in smallholder bean fields. The importance of field margin vegetation to the population of predators and parasitoids was also examined. The study identified a severe lack of knowledge about natural enemies among the smallholder farmers. However, the field survey revealed the existence of a rich community of natural enemies, where a total of 5003 natural enemies were identified out of 13 961 insects collected. The natural enemy abundance differed along the elevation gradient where the high zone was leading with 50.3%, while mid and low zones had 31.7% and 18% respectively. Majority of the natural enemies were sampled along the margin vegetation compared with the bean fields for low (61.1% in margin vs 38.9% in field) and mid (52.1% in margin vs 47.9% in field) zones, but in the high zone they were more abundant within the bean fields (44.6% in margin vs 55.4% field). A dye experiment to monitor their movement revealed high levels of spatial flux (71%) between the two locations. Aphids (Aphis fabae) mortality rates measured by predation and parasitism of sentinel aphids did not significantly differ between the field edges and field centre in all the three elevation zones, indicating the centre of the fields still receive comparable pest control service as the field edge. Parasitoid wasps were the most abundant natural enemy while A. fabae were the most damaging insect pests in the smallholder bean fields. Molecular identification of A. fabae parasitoids revealed 85% primary parasitoids (Aphidius colemani) and two species of secondary parasitoids (Pachyneuron sp., 7% and Charipinae sp., 1%) which may have significant effects in biological pest control. The study revealed the potential predators and parasitoids important for pest control within the smallholder bean fields which can be enhanced through CBC

Crowdsourcing field observations from smallholder farmers in Tanzania using interactive voice response

The term crowdsourcing was first used in 2006 but the approach has been employed in various fields over a much longer period of time. The central idea is to collect information from a large number of people in order to achieve a common goal such as to increase knowledge, solve a problem or enhance the efficiency of a process. In the realm of research, crowdsourcing is closely connected with citizen science in which members of the public are engaged in a scientific project. In C17th England, the naturalist John Ray arranged for a large number of volunteers to collect specimens for him and there are datasets on the phenology of plants, birds and insects in England and in some other countries which provide a continuous record for hundreds of years. A current example of how non-specialists are helping to gather large quantities of biological data is the Breeding Bird Survey run by the British Trust for Ornithology which engages thousands of volunteers to submit records of over 200 bird species each year. Although crowdsourcing has been widely used in environmental monitoring there are few examples of its use in agriculture. This is surprising because there is a tradition of participatory approaches to agricultural research which have been developed in recent decades. The potential for harnessing large numbers of individual farmers to generate information on the performance of crop varieties in different locations was recently demonstrated through a triadic comparison of technologies. This was taken a stage further in a subsequent study in which a total of 12,409 farmers collected data on experimental plots of common bean (Phaseolus vulgaris) in Nicaragua, durum wheat (Triticum durum) in Ethiopia, and bread wheat (Triticum aestivum) in India. The results showed that expected effects of seasonal climatic variables on the performance of the crop varieties occurred and that these were generalizable across growing seasons. The authors concluded that their approach allows for more targeted recommendations for the deployment of crop varieties and that these may differ substantially from recommendations derived from current evaluation procedures in which testing is done at a limited number of sites. Crowdsourcing has tremendous potential for use in insect pest management. Up to date information on the distribution and abundance of insect pests of crops is needed for the development of appropriate management strategies. Field surveys can be used to identify locations where pest levels are high and sequential monitoring may help to establish seasonal patterns of occurrence. Surveys are also useful in monitoring the likely sources of migrant pests and recording their dispersal from these areas. When used in combination with other information such as climatic data, field surveys are an essential element of insect pest forecasting systems. In developing countries, field surveys are generally conducted by agricultural research and extension staff. Their main limitation is that they are labour-intensive and costly to carry out. Since resources of manpower and funds are limited, surveys are carried out infrequently and in restricted locations which may not be representative of the situation over larger areas. As a result national agricultural research and extension systems are constrained by having limited access to accurate information on the status of insect pests in different locations. This makes it difficult for them to respond to new threats such as the recent appearance and spread of the fall armyworm (Spodoptera frugiperda) in Africa where monitoring and early warning systems are crucial for effective control

Extracts from field margin weeds provide economically viable and environmentally benign pest control compared to synthetic pesticides

Plants with pesticidal properties have been investigated for decades as alternatives to synthetics, but most progress has been shown in the laboratory. Consequently, research on pesticidal plants is failing to address gaps in our knowledge that constrain their uptake. Some of these gaps are their evaluation of their efficacy under field conditions, their economic viability and impact on beneficial organisms. Extracts made from four abundant weed species found in northern Tanzania, Tithonia diversifolia, Tephrosia vogelii, Vernonia amygdalina and Lippia javanica offered effective control of key pest species on common bean plants (Phaseolus vulgaris) that was comparable to the pyrethroid synthetic, Karate. The plant pesticide treatments had significantly lower effects on natural enemies (lady beetles and spiders). Plant pesticide treatments were more cost effective to use than the synthetic pesticide where the marginal rate of return for the synthetic was no different from the untreated control, around 4USD/ha, compared to a rate of return of around 5.50USD/ha for plant pesticide treatments. Chemical analysis confirmed the presence of known insecticidal compounds in water extracts of T. vogelii (the rotenoid deguelin) and T. diversifolia (the sesquiterpene lactone tagitinin A). Sesquiterpene lactones and the saponin vernonioside C were also identified in organic extracts of V. amygdalina but only the saponin was recorded in water extracts which are similar to those used in the field trial. Pesticidal plants were better able to facilitate ecosystem services whilst effectively managing pests. The labour costs of collecting and processing abundant plants near farm land were less than the cost of purchasing synthetic pesticides

Field margin vegetation in tropical African bean systems harbours diverse natural enemies for biological pest control in adjacent crops

Non-crop vegetation around farmland can be valuable habitats for enhancing ecosystem services but little is known of the importance of field margins in supporting natural enemies of insect pests in tropical agriculture. This study was conducted in smallholder bean fields in three elevation zones to assess the importance of field margin vegetation to natural enemy populations and movement to the bean crop for biological pest control. The pests and natural enemies were assessed using different coloured water pan traps (to ensure the capture of insects with different colour preferences) and the interactions of the two arthropod groups with the margin vegetation and their movement to the bean crop were monitored using fluorescent dye. Sentinel plants were used to assess predation and parasitism levels. A total of 5003 natural enemies were captured, more in the field margin than within the bean field for low and mid elevation zones, while in the high elevation zone, they were more abundant within the bean field. Pests were more abundant in the crop than margins for all the elevation zones. The use of a dye applied to margin vegetation demonstrated that common natural enemy taxa moved to the crop during the days after dye application. The proportion of dye-marked natural enemies (showing their origin to be margin vegetation) sampled from the crop suggest high levels of spatial flux in the arthropod assemblage. Aphid mortality rates (measured by prey removal and parasitism levels on sentinel plants) did not differ between the field edges and field centre in any of the three elevation zones, suggesting that for this pest taxon, the centre of the fields still receive comparable pest control service as in the field edges. This study found that field margins around smallholder bean fields are useful habitats to large numbers of natural enemy taxa that move to adjacent crops providing biological pest control service

Characterization of hymenopteran parasitoids of aphis fabae in an African smallholder bean farming system through sequencing of COI 'mini-barcodes'

Parasitoids are among the most frequently reported natural enemies of insect pests, particularly aphids. The efficacy of parasitoids as biocontrol agents is influenced by biotic and abiotic factors. For example, hyperparasitoids can reduce the abundance of the primary parasitoids as well as modify their behavior. A field study was conducted at three contrasting elevations on Mount Kilimanjaro, Tanzania, to identify the parasitoids of aphids in smallholder bean farming agroecosystems. Sentinel aphids (Aphis fabae) on potted bean plants (Phaseolus vulgaris) were exposed in 15 bean fields at three elevations for 2 days. The sentinel aphids were then kept in cages in a greenhouse until emergence of the parasitoids, which were collected and preserved in 98% ethanol for identification. Of the 214 parasitoids that emerged from sentinel aphids, the greatest abundance (44.86%) were from those placed at intermediate elevations (1000–1500 m a.s.l), compared to 42.52% from the lowest elevations and only 12.62% from the highest elevation farms. Morphological identification of the parasitoids that emerged from parasitized aphids showed that 90% were Aphidius species (Hymenoptera: Braconidae: Aphidiinae). Further characterization by sequencing DNA ‘mini-barcodes’ identified parasitoids with ≥99% sequence similarity to Aphidius colemani, 94–95% sequence similarity to Pachyneuron aphidis and 90% similarity to a Charipinae sp. in the National Center for Biotechnology Information (NCBI) database. These results confidently identified A. colemani as the dominant primary aphid parasitoid of A. fabae in the study area. A Pachyneuron sp., which was most closely related to P. aphidis, and a Charipinae sp. occurred as hyperparasitoids. Thus, interventions to improve landscapes and farming practice should monitor specifically how to augment populations of A. colemani, to ensure any changes enhance the delivery of natural pest regulation. Further studies are needed for continuous monitoring of the hyperparasitism levels and the dynamics of aphids, primary parasitoids, and secondary parasitoids in different cropping seasons and their implications in aphid control

Knowledge gaps among smallholder farmers hinder adoption of conservation biological control

Conservation biological control uses habitat management to enhance the survival and impact of arthropod natural enemies for pest control. Its advantages are that it relies on native or established invertebrate populations that are adapted to local agricultural ecosystems and conditions. We surveyed 300 farmers in three agro-ecological zones of Kilimanjaro Region, Tanzania to assess farmers’ knowledge of natural enemies, insect pests and pesticide use and ways of accessing agricultural information to identify hurdles to the adoption of conservation biological control measures. Data were collected through face to face interviews using questionnaires and pictures and by using a novel voice-response mobile phone survey. The farmers surveyed regarded almost all insects as pests, with data analyses revealing that 98.7% of farmers were completely unaware of natural enemies. After completing a short training course, however, awareness was transformed, with 80% of farmers recognising beneficial insects and expressing an intention to change farming practices to enhance their survival within the crop. Access to information about synthetic pesticide alternatives was a limiting factor to uptake of biological control measures with 8.7% of farmers reporting no access to agricultural information, while others were mostly dependent on agricultural officers. These findings identified a severe lack of knowledge among smallholder farmers about beneficial insects which will impact adoption of conservation biological control. We recommend improved access to information and knowledge among the technical officers and the smallholder farmers with direct training on agro-ecological intensification for wider adoption of conservation biological control

Beneficial insects are associated with botanically rich margins with trees on small farms

Beneficial insect communities on farms are influenced by site- and landscape-level factors, with pollinator and natural enemy populations often associated with semi-natural habitat remnants. They provide ecosystem services essential for all agroecosystems. For smallholders, natural pest regulation may be the only affordable and available option to manage pests. We evaluated the beneficial insect community on smallholder bean farms (Phaseolus vulgaris L.) and its relationship with the plant communities in field margins, including margin trees that are not associated with forest fragments. Using traps, botanical surveys and transect walks, we analysed the relationship between the floral diversity/composition of naturally regenerating field margins, and the beneficial insect abundance/diversity on smallholder farms, and the relationship with crop yield. More flower visits by potential pollinators and increased natural enemy abundance measures in fields with higher plant, and particularly tree, species richness, and these fields also saw improved crop yields. Many of the flower visitors to beans and potential natural enemy guilds also made use of non-crop plants, including pesticidal and medicinal plant species. Selective encouragement of plants delivering multiple benefits to farms can contribute to an ecological intensification approach. However, caution must be employed, as many plants in these systems are introduced species

Field Margin Vegetation in Tropical African Bean Systems Harbours Diverse Natural Enemies for Biological Pest Control in Adjacent Crops

Non-crop vegetation around farmland can be valuable habitats for enhancing ecosystem services but little is known of the importance of field margins in supporting natural enemies of insect pests in tropical agriculture. This study was conducted in smallholder bean fields in three elevation zones to assess the importance of field margin vegetation to natural enemy populations and movement to the bean crop for biological pest control. The pests and natural enemies were assessed using different coloured water pan traps (to ensure the capture of insects with different colour preferences) and the interactions of the two arthropod groups with the margin vegetation and their movement to the bean crop were monitored using fluorescent dye. Sentinel plants were used to assess predation and parasitism levels. A total of 5003 natural enemies were captured, more in the field margin than within the bean field for low and mid elevation zones, while in the high elevation zone, they were more abundant within the bean field. Pests were more abundant in the crop than margins for all the elevation zones. The use of a dye applied to margin vegetation demonstrated that common natural enemy taxa moved to the crop during the days after dye application. The proportion of dye-marked natural enemies (showing their origin to be margin vegetation) sampled from the crop suggest high levels of spatial flux in the arthropod assemblage. Aphid mortality rates (measured by prey removal and parasitism levels on sentinel plants) did not differ between the field edges and field centre in any of the three elevation zones, suggesting that for this pest taxon, the centre of the fields still receive comparable pest control service as in the field edges. This study found that field margins around smallholder bean fields are useful habitats to large numbers of natural enemy taxa that move to adjacent crops providing biological pest control service

Pesticidal Efficacy of Four Botanical Pesticides on Survival, Oviposition and Progeny Development of Bruchid, Callosobruchus maculatus in Stored Cowpea, Vigna unguiculata

Cowpea (Vigna unguiculata) production is limited by various insect pests that attack and damage the crops both in the field and during storage. Cowpea bruchids, Callosobruchus maculatus are the major insect pests of cowpea which infest the cowpea grains in the field, and then carried into the store where the population builds up rapidly. Chemical insecticide application is one of the management options that has been used for many years to control the insect pests. However, due to the side effects associated with those insecticides, there has been a resurgence need of using botanical pesticides to control insect pests in the field as well as in storage. This review aims to increase an awareness of using selected botanicals (Tephrosia vogelii, Chenopodium ambrosioides, Tithonia diersifolia, Lippia javanica and Vernonia amygdalina) as the cheap, effective and environmental friendly insect pest management strategy against bruchids in stored cowpea. The bioactive compounds from these plants offer great potential of developing botanical pesticides against postharvest insects in stores

Contact and fumigant toxicity of five pesticidal plants against Callosobruchus maculatus (Coleoptera: Chrysomelidae) in stored cowpea (Vigna unguiculata)

Insecticidal activities of five pesticidal plant species, Tephrosia vogelii, Dysphania (Syn: Chenopodium) ambrosioides, Lippia javanica, Tithonia diversifolia and Vernonia amygdalina, which have been reported to control storage pests, were evaluated as leaf powders against Callosobruchus maculatus (Fabricius 1775) in stored cowpea. Their efficacy was compared with the commercial pesticide Actellic dust (pirimiphos-methyl) at the recommended concentration (50 g/90 kg), and with untreated cowpea seeds as a negative control. The plant powders were applied at concentrations of 0.01, 0.1, 1 and 3 g/10 g of cowpea seeds in 250 ml plastic containers (to measure contact toxicity), or 0.005, 0.05, 0.5 and 5 g tied in small muslin cloth bags and hung in 500 ml plastic bottles containing 10 g of cowpea seeds (to measure fumigant toxicity). Mortality of adults, oviposition deterrence, adult emergence, and percent seed damage were recorded. Complete protection of seeds and inhibition of adult emergence were achieved in Actellic dust-treated seeds; contact toxicity using leaf powders of T. vogelii at all concentrations, D. ambrosioides at concentrations of 0.1, 1 and 3 g and L. javanica at concentrations of 1 and 3 g; and fumigant toxicity usingD. ambrosioides at concentrations of 0.5 and 5 g and L. javanica at a concentration of 5 g. Head space analysis of D. ambrosioides and L. javanica identified ascaridole and camphor, respectively, as components that could be responsible for the bioactivity of these plant species. These plants may, therefore, serve as effective but less harmful biopesticide alternatives to Actellic. Conversely, V. amygdalina and T. diversifolia were not effective, indicating that they should not be promoted for controlling bruchids in cowpea