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The Role of the Mite Orthogalumna Terebrantis in the Biological Control Programme for Water Hyacinth, Eichhornia Crassipes, in South Africa

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The Role of the Mite Orthogalumna Terebrantis in the Biological Control Programme for Water Hyacinth, Eichhornia Crassipes, in South Africa The role of the mite Orthogalumna terebrantis in the biological control programme for water hyacinth, Eichhornia crassipes, in South Africa A thesis submitted in fulfilment of the requirements for the degree of DOCTOR OF PHILOSOPHY of Rhodes University by DANICA MARLIN December 2010 Abstract Water hyacinth (Eichhornia crassipes) is an aquatic macrophyte originating from the Amazon basin. Due to its beautiful appearance it has been introduced into numerous countries across the world as an ornamental pond plant. It was introduced into South Africa in the early 1900s and has since reached pest proportions in many of the country’s fresh water bodies, causing significant economic and ecological losses. It is now considered to be the worst aquatic weed in South Africa. Efforts to control the spread of the weed began in the early 1970s and there have been some successes. Biological control has been used widely as an alternative to mechanical and chemical controls because it is cost-effective, self-sustaining and environmentally friendly. To date, six biological control agents have been introduced onto water hyacinth in South Africa. However, due to factors such as cold winter temperatures and interference from chemical control, the agent populations are occasionally knocked-down and thus the impact of biological control on the weed population is variable. In addition, many South African water systems are highly eutrophic, and in these systems the plant growth may be accelerated to such an extent that the negative impact of the agents’ herbivory is mitigated. One of the agents established on the weed is the galumnid mite Orthogalumna terebrantis, which originates from Uruguay. In South Africa, the mite was initially discovered on two water hyacinth infestations in the Mpumalanga Province in 1989 and it is now established at 17 sites across the country. Many biological control researchers believe that the mite is a good biological control agent but, prior to this thesis, little quantitative data existed to confirm the belief. Thus, this thesis is a post-release evaluation of O. terebrantis in which various aspects of the mite-plant relationship were investigated to determine the efficacy of the mite and thus better understand the role of the mite in the biological control programme of water hyacinth in South Africa. From laboratory experiments, in which mite densities were lower than densities occurring in the field, it was found that water hyacinth growth is largely unaffected by mite herbivory, except possibly at very high mite densities. When grown in high nutrient conditions the growth of the plant is so great that any affect the mite has is nullified. ii Plant growth is thus more affected by nutrients than by mite herbivory. However, mite feeding was also influenced by water nutrient levels and mite herbivory was greatest on plants grown in high nutrient conditions. The presence of the mite had a positive effect on the performance of the mirid Eccritotarsus catarinensis, such that the interactions of the two agents together had a greater negative impact on the plant’s growth than the individual agents had alone. Furthermore, water hyacinth physiological parameters, such as the plant’s photosynthetic ability, were negatively impacted by the mite, even at the very low mite densities used in the study. Plant growth rate is dependent on photosynthetic ability i.e. the rate of photosynthesis, and thus a decrease in the plant’s photosynthetic ability will eventually be translated into decreased plant growth rates which would ultimately result in the overall reduction of water hyacinth populations. In addition, temperature tolerance studies showed that the mite was tolerant of low temperatures. The mite already occurs at some of the coldest sites in South Africa. Therefore, the mite should be able to establish at all of the water hyacinth infestations in the country, but because it is a poor disperser it is unlikely to establish at new sites without human intervention. It is suggested that the mite be used as an additional biological control agent at sites where it does not yet occur, specifically at cold sites where some of the other, less cold-tolerant, agents have failed to establish. Finally, conditions of where, how many and how often the mite should be distributed to water hyacinth infestation in South Africa are discussed. iii TABLE OF CONTENTS Abstract…………………………………………………………………………………… ii List of figures…………………………………………………………………………….. viii List of tables……………………………………………………………………………… xvii Acknowledgements…………………………………………………………………...... xx Chapter 1: General Introduction…………………………………………………...... 1 1.1. Invasive alien plants……………………………………………………….. 1 1.2. Biological control of aquatic plants………………………………………. 3 1.2.1. Globally……………………………………………………………………… 3 1.2.2. South Africa…………………………………………………………………. 4 1.3. Water hyacinth: Eichhornia crassipes …………………………………... 5 1.3.1. History and distribution…………………………………………………….. 5 1.3.2. Biology……………………………………………………………………….. 7 1.3.3. Impact on the environment………………………………………………… 8 1.3.4. Utilisation……………………………………………………………………. 9 1.3.5. Biological control of water hyacinth in South Africa…………………….. 10 1.4. Mites (Acari) as agents for pest reduction………………………………. 12 1.5. Orthogalumna terebrantis ………………………………………………... 15 1.5.1. Introduction………………………………………………………………….. 15 1.5.2. History and distribution…………………………………………………….. 16 1.5.3. Biology……………………………………………………………………….. 16 1.5.4. Feeding damage and effect on water hyacinth………………………….. 18 1.5.5. Natural enemies of Orthogalumna terebrantis………………………...... 19 1.5.6. Present status of Orthogalumna terebrantis in South Africa…………... 20 1.6. Aims of thesis………………………………………………………………. 21 Chapter 2: The impact of herbivory by different densities of Orthogalumna terebrantis on water hyacinth growth parameters and leaf chlorophyll content………………………………………………………. 23 2.1. Introduction…………………………………………………………………. 23 2.2. Materials and methods……………………………………………………. 26 2.2.1. Experimental set-up………………………………………………………... 26 iv 2.2.2. Leaf chlorophyll determination……………………………………………. 27 2.2.3. Feeding damage determination…………………………………………… 29 2.2.4. Statistical analyses…………………………………………………………. 29 2.3. Results……………………………………………………………………… 30 2.3.1. Plant growth parameters…………………………………………………... 31 2.3.2. Leaf chlorophyll content……………………………………………………. 39 2.3.3. Mite damage to the leaf surface area…………………………………….. 42 2.3.4. Effect of mite herbivory on the plant growth parameters………………. 47 2.3.5. Summary of results………………………………………………………… 48 2.4. Discussion………………………………………………………………...... 49 2.4.1. Effect of mite herbivory on the plant growth parameters………………. 49 2.4.2. Effect of mite herbivory on the leaf chlorophyll content………………… 53 2.4.3. Effect of mite herbivory on the leaf surface area damaged……………. 54 2.5. Conclusion………………………………………………………………..... 55 Chapter 3: The impact of nutrients and herbivory by Orthogalumna terebrantis on water hyacinth growth parameters and leaf chlorophyll content………………………………………………………. 57 3.1. Introduction…………………………………………………………………. 57 3.2. Materials and methods……………………………………………………. 61 3.2.1. Experimental set-up………………………………………………………... 61 3.2.2. Feeding damage determination…………………………………………… 63 3.2.3. Leaf chlorophyll content……………………………………………………. 63 3.2.4. Statistical analyses…………………………………………………………. 64 3.3. Results……………………………………………………………………… 65 3.3.1. Effect of nutrients on the plant growth parameters……………………... 65 3.3.2. Effect of mite herbivory on the plant growth parameters………………. 72 3.3.3. Effect of nutrients and herbivory on the leaf chlorophyll content……… 74 3.3.4. Effect of nutrients on mite herbivory……………………………………… 75 3.3.5. Effect of nutrients and time on mite development, based on gallery 78 lengths……………………………………………………………………….. 3.4. Discussion………………………………………………………………...... 79 3.5. Conclusion………………………………………………………………..... 82 Chapter 4: Interactions of three biological control agents of water hyacinth and their impact on the plant…………………………………………... 84 4.1. Introduction…………………………………………………………………. 84 4.2. Materials and methods……………………………………………………. 89 4.2.1. Pilot studies…………………………………………………………………. 89 4.2.2. Interaction study……………………………………………………………. 92 4.3. Results……………………………………………………………………… 95 4.3.1. Pilot studies…………………………………………………………………. 95 4.3.2. Interaction study……………………………………………………………. 104 4.4. Discussion………………………………………………………………...... 112 4.5. Conclusion………………………………………………………………..... 122 v Chapter 5: Photosynthetic performance of water hyacinth as affected by Orthogalumna terebrantis herbivory…………………………………. 124 5.1. Introduction…………………………………………………………………. 124 5.2. Materials and methods……………………………………………………. 131 5.2.1. Experimental set-up………………………………………………………... 131 5.2.2. Feeding intensity measurements…………………………………………. 132 5.2.3. Photosynthetic gas exchange…………………………………………...... 132 5.2.4. Chlorophyll-a fluorescence………………………………………………… 133 5.2.4.1. The JIP-test…………………………………………………….. … 133 5.2.5. Leaf chlorophyll content and biomass……………………………………. 134 5.2.6. Statistical analyses…………………………………………………………. 136 5.3. Results………………………………………………………………………….. 136 5.3.1. Photosynthetic gas exchange…………………………………………...... 136 5.3.2. Chlorophyll-a fluorescence………………………………………………… 139 5.3.3. Leaf chlorophyll content and biomass……………………………………. 143 5.4. Discussion……………………………………………………………………… 144 5.5. Conclusion……………………………………………………………………... 149 Chapter 6: Thermal tolerance of Orthogalumna terebrantis and the effect of temperature on its establishment in South Africa…………………. 150
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