MSc (Zoology) / Department of Zoology / See the attached abstract below

PhD (Zoology) / Department of Zoology / Ecosystem services and disservices are important features in agro-ecosystems and both can have relevant economic impacts on farmers. While there has been much research on the value of ecosystem services, especially that of pest control by bats and birds, ecosystem disservices are often overlooked or estimated separately. Both, services and disservices, however, change with landscape and may be supported by natural vegetation. It is hence inevitable to assess them together to uncover their relative value and importance. Habitat loss and fragmentation are major threats to biodiversity and ecosystem services. Agricultural intensification can cause habitat loss and can negatively affect natural ecosystems and their services. However, the removal of natural vegetation can also reduce ecosystem disservices that origin from natural areas. This study focused on the economic trade-off between biocontrol by bats and birds and crop raiding by vervet monkeys in South African macadamia orchards, using vertebrate exclusion experiments. Crop quality and yield were assessed and extrapolated to income values. The study furthermore focused in more detail on the impact of orchard edge habitat and farm management on bats as ecosystem service providers as well as the arthropod community, which can provide both services (pollination, biocontrol) as well as disservices (crop damage). The macadamia industry is highly profitable and plantings are expanding worldwide. South Africa is currently the largest macadamia producer in the world and the study area, Levubu, holds some of the oldest macadamia plantings in the country. The subtropical climate and high annual rainfall make this area an intensively farmed landscape. Levubu lies at the foothills of the Soutpansberg, a centre of biodiversity and patches of natural vegetation wind through orchards of macadamia, avocado, banana and timber. Insect pest pressure is high in the macadamia industry, with several stink bug species (Hemiptera) and two moth species (Lepidoptera) accounting for most of the damage to the crop. Chapter One provides a detailed overlook over the South African macadamia industry, describes the major pest insect species and their impact on the crop and highlights the role of ecosystem services and disservices and the potential importance of remaining natural areas. Over three consecutive seasons, between September 2015 and May 2018, bats, birds and monkeys were excluded, using cages with nets, from a total of 96 macadamia trees. Four treatments were applied (Full, Day, Night, Control) to distinguish between effects of the different functional groups. Exclusions took place at orchard edges with natural or human-modified edge habitat to assess the impact of vicinity to natural vegetation on pest control and crop raiding. Results presented in Chapter Two showed that biocontrol by bats and birds was stronger near natural vegetation and significantly impacted crop quality as well as yield. Effects of bats and birds were still significant at human-modified edges, whereas crop raiding by monkeys is limited to the natural orchard edges. The economic impact analysis shows that the benefits of biocontrol through bats and birds outweighed the income losses due to crop-raiding monkeys. The value of bats and birds was as high as USD 5000 per hectare per year through prevented insect damage and a 60% crop increase. Crop-raiding affected the yield, which dropped by about 26% and resulted in losses of about USD 1500 per hectare. These results highlight the importance of integrating natural areas into agricultural landscapes, even if they incur the risk of being disadvantageous. Farmers need to be made aware of the enormous economic benefits. Effective crop raiding mitigation strategies still need to be researched to avoid negative association with natural areas. These can, however, possibly also limit access for biocntrol agents, like bats and birds and thereby reduce their economic impact. Especially the removal of natural areas or establishment of buffer zones of unpalatable crops between agricultural land and forests is not advisable. Integrative research in agro-ecosystems on trade-offs between a variety of ecosystem services and disservices is necessary in future, rather than assessing them separately. The bat community on macadamia farms was monitored monthly and compared between orchard edges. Stationary bat detectors were placed at each set of exclosures for two consecutive nights a month, automatically recording from sunset to sunrise. Recorded bat calls were identified manually to species level and activity converted to Miller’s activity index, which counts the number of active minutes per species per night. We analysed the activity per feeding guild over season and landscape setting, estimated species richness and diversity (Hill’s numbers) and species turnover between farms, season and landscape setting, using diversity partitioning. The bat community was mostly influenced by seasonality with season turn-over accounting for 21% of total bat diversity (21.25 species). Edge habitat on the other hand only accounted for 5%. We found higher species richness and activity in the high season compared to the low. While there was no difference in diversity in the high season between the two orchard edge types, species diversity at the human-modified edge was lower than in the natural during the low season. Natural habitat might therefore be more important in the low season, while its effect is overwritten by high food availability during the high season. Clutter-edge species furthermore were more active at the natural orchard edges than open-air feeders, which were in turn more active at human-modified edges. Both activities dropped significantly during the low season. Chapter Three concludes that the macadamia landscape is able to support a high bat species diversity, which is affected by seasonal differences, probably due to food availability. Natural areas are important to be maintained to support sensitive species, relying on clutter habitat and natural roosts. Habitat features as well as farm management can also influence arthropod communities. Visual observations took place each month for 20 minutes per tree. Observations were counted and identified to at least order level. Chapter Four concentrates on the impact of orchard edge habitat and insecticide treatment on honey bees (83% of Hymenoptera observations) abundance. Honey bees were the only taxon significantly responding to both variables, with higher abundance close to natural areas and increasing abundance with increasing time since pesticide application. Honey bees furthermore seemed to recover slightly quicker from population crashes after insecticide treatments at natural edges than they did at human-modified edges. Hymenoptera can be highly beneficial to macadamia farmers, as farmers are heavily relying on pollination by honey bees and parasitoids are known to feed on major macadamia pest insect species. These ecosystem service providers were mostly affected by habitat and management practices, which may compromise their ecosystem service provision. Although commercial bee hives are exposed throughout macadamia orchards, they do not appear to fully replace the pollination and biocontrol services provided by feral species, which can be enhanced through resource supplementation by patches of nearby natural vegetation. Chapter Five concludes with emphasizing the general importance of natural vegetation in landscape planning of agricultural areas. This study proved confidently that benefits through ecosystem services largely outweigh negative impacts of ecosystem disservices, both stemming from these natural areas. Through the inclusion, maintenance and restoration of such patches of natural vegetation, farmers can potentially increase the value and effectiveness of biocontrol by bats and birds or other services. Seasonality largely determined bat species diversity, and a general high species diversity was observed in the macadamia landscape, possibly due to a certain degree of landscape heterogeneity and high food availability. Activity patterns of clutter-edge and open-air feeding bats varied with edge habitat, while clutter-dependent bat species / NRF

PhD (Zoology) / Department of Zoology / An ever growing human population and accelerating land use change is associated with the loss of species and their ecosystem services. Agricultural intensification has led to a worldwide threat of extinction to about one quarter of all bat species, despite the valuable ecosystem service of pest control provided by bats. The decline in bat populations is mainly attributed to the loss or fragmentation of habitats, roost sites and feeding opportunities related to agricultural intensification and land use change. Therefore, proactive management of bat communities in agricultural landscapes is essential. South Africa is the world’s largest producer of macadamias and the industry continues to grow. This study gains insight into the habitat use and foraging behaviour of insectivorous bat species on a temporal and spatial scale, in and around macadamia orchards in order to advise management strategies on how to increase bat activity and, possibly, pest control. It also focuses on the preferences of artificial roost sites used by insectivorous bats in macadamia orchards. The diet of insectivorous bat species is especially difficult to study and the least invasive tool to gain information is the study of bat faecal pellets. In order to provide evidence for the consumption of pest insect species by bats and thus incentive to farmers for a more integrated pest management approach (IPM), this study explored molecular approach to insectivorous bat diet analyses using fragment analysis of bat faecal pellets with fluorescent-labelled species-specific primers (designed for the CO I gene). This study was conducted in the subtropical fruit growing area of Levubu, Limpopo province, South Africa between the towns Thohoyandou (22°59'03.7 S, 30°27'12.8 E) and Makhado/Louis Trichardt (23°03'03.6 S, 29°55'12.7 E). Levubu also accounts for the second highest production of macadamia in South Africa. An introduction to the order Chiroptera and into the relevance of insectivorous bat species to agriculture as well as the importance of a more integrated pest management approach (IPM) focusing on bats is provided in Chapter One. Bats were acoustically monitored and light traps were used to catch arthropods during one annual cycle. I sampled five macadamia orchards once a month from September 2015 to August 2016 and used GIS and R to analyse both the general bat activity and foraging bat activity of the two main foraging guilds (open-air/clutter edge guild) in different land use types as well as total bat activity with respect to arthropod abundances. As reported in Chapter Two, results show that the overall clutter edge guild activity (number of passes) decreased with macadamia and orchard (all other fruit) cover in the macadamia high season (December to end of May) and increased with bush cover and distance to settlements (potential roosts) in the macadamia low season (June to end of November). Open-air guild activity increased with fallow cover (uncultivated grassland with scattered trees and shrubs) in the high season. Foraging activity (feeding buzzes) of the clutter edge guild increased with bush cover over the whole year. Total activity (both guilds) increased with abundance of true bugs (Hemiptera), including the main macadamia pests, and bush cover. Macadamia cover has a negative effect on the activity of the clutter edge guild in the high season, with low activity in the orchard center (high cover), and activity increasing in a linear way with decreasing orchard cover at the orchard edge (low cover). These results suggest that the clutter edge guild prefers foraging close to the edges of the orchards rather than in the center, while the open-air guild prefers semi-natural habitats (fallow). When numbers of pest arthropods drop in the macadamia orchards, the natural land use type, bush, becomes a more important foraging habitat and thereby increased the activity of the clutter edge guild. From June 2016 to July 2017, I scanned 31 bat houses, mounted on poles on six macadamia orchards, for bats or any other occupants such as wasps, birds and bees. Twenty-one multichambered bat houses of three slightly different chamber designs were erected on poles, in sets of three. Additionally, five bat houses of the type ‘Rocket box’, four bat houses in sets of two (black and white) and one colony bat house were erected. Bats were counted and visually identified to family or species level. From December 2016 to end of March 2017, three IButtons were installed to record temperature variation between one set of three bat houses. As reported in Chapter Three, results show that the central bat house in the set of three and the black bat house in the set of two had a significantly positive effect on bat house occupancy. There was a significant difference in the mean temperature between the houses in the set of three, with a significant difference in temperature of 0.46°C between the central and the first bat house. The three bat houses erected in sets varied slightly in their chamber design, with the central bathouse having the most chambers (six), while the bat houses to either side had less chambers (four), set at an angle or straight. This and the insulation to either side by the other bat houses is assumingly what caused the central bat house to be on average warmer. The Yellow-bellied house bat (Scotophilus dinganii) was by far the most recorded and the only species observed to co-habitat a bat house with another animal species, in particular honeybees. The study might confirm assumptions in that the microclimate of bat houses, respectively their insulation, sun exposure and color appear to be important factors influencing bat house occupancy. The two preferred bat houses in our study were the black, in the set of black and white, as well as the central, and on average warmest bat house, in the set of three. I collected bat faecal pellets with two different methods between July 2015 and April 2017 to determine the prevalence of pest insects in faecal pellets. Eighteen of the bat houses (in sets of three) on three different farms and two Egyptian slit-faced bat (Nycteris thebaica) roosts were fitted with trays in order to collect pellets from those occupied by bats. I noted occupancy of bat houses to species or family level to keep disturbance minimal. Additionally, I collected pellets from individuals captured by means of mist nets and harp traps. Four of the main pest-insects; the two-spotted stinkbug (Pentatomidae: Bathycoelia distincta), the green vegetable bug (Pentatomidae: Nezara viridula), the macadamia nut borer (Tortricidae: Thaumatotibia batrachopa) and the litchi moth (Tortricidae: Cryptophlebia peltastica), were collected from pheromone traps or after scouting for primer development and optimisation. After extracting DNA from the bat faecal samples the target regions were amplified in a multiplex PCR and fluorescently labelled PCR amplicons were analysed and interpreted. In order to verify multiplex analyses results, all samples were amplified with all four sets of primers in plates and those that produced amplicons were purified and sequenced. As reported in Chapter Four, results show that fragment analyses yielded a total of 63 out of 103 samples tested positive for pest insect species (61%) with a total of 92 positive fragments. Primer specificity could be confirmed to 100% for the sequences obtained for Bathycoelia distincta (26/26) and Nezara viridula (12/12) primers but not for all sequences obtained fot Cryptophlebia peltastica (18/30) and Thaumatotibia batrachopa (1/14) primers. One sample showed no positive fragments but contained a positive sequence for N. viridula. Three samples tested positive for one pest-species fragment but contained a positive sequence for a second pest-species (B. distincta, T. batrachopa and C. peltastica). Adding four positive fragments and one additional positive sequence to the data. This means that sequences of pest insect species were obtained from 54 out of the 103 samples (55.6%) with a total of 73 pest insect sequences. For the high season (December to end of May) a total of 37 positive fragments for the four pest insect species and 24 negative samples were yielded and for the a low season (June to end of November) a total of 36 positive fragments and 15 negative samples. Looking at the pest consumption of the different bat species or families, our results show that all of them foraged on pest insect species. Whereas, all species and families except Myotis bocagii and Rhinolophus simulator (for which N<2) foraged on both the Lepidopteran and Hemipteran pest species. Therefore, all families of bats of which faecal pellets were analysed for this study (Molossidae, Nycteridae, Rhinolophidae and Vespertilionidae) foraged on one or more of the four pest insect species. In summary, Chapter Five concludes that natural and semi-natural vegetation promote bat activity in macadamia orchards, and potentially bats' provision of the ecosystem service of pest control. In times of accelerating land use change, remnants of natural vegetation are important refuges and need to be maintained or restored to conserve bat species and promote their ecosystem services. The study also shows that bat activity might be improved by adding roosting opportunities to orchards. Warm and well-insulated bat houses mounted freestanding on poles and in sets appeared to work best in northern South Africa. Further research on co-habitation of bat houses and displacement behaviour as well as the potential importance of altitude and distance to water is needed. All of the species or families of bats from which faecal pellets were collected have been confirmed to forage on at least one of the four pest insects and the bat species have shown to be much more generalist and presumably opportunistic feeders than previously assumed. Thus, this study provides incentive and advice to farmers for a more integrated pest management approach (IPM). / NRF