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Post-release evaluation of the biological control programme against Cereus jamacaru De Candolle (Cactaceae), in South Africa A thesis submitted in fulfilment of the requirements for the degree of MASTER OF SCIENCE at RHODES UNIVERISTY By Guy Frederick Sutton January 2017 Abstract Abstract Cereus jamacaru De Candolle (Cactaceae) is an environment-transforming weed of both agricultural and wildlife habitats in South Africa. Weed infestations reduce carrying capacity of the land, and pose a risk to livestock, wildlife and human safety due to the plant’s spiny thorns. The weed is considered to be under complete biological control in South Africa, due to its introduced control agent, Hypogeococcus festerianus Lizer y Trelles (Hemiptera: Pseudococcidae), although observational reports suggest that the level of success achieved is variable. In this thesis, a formal post-release evaluation of this biological control programme was conducted, specifically to determine the efficacy of H. festerianus as a biological control agent, and to identify factors which may limit or constrain the level of success achieved by the control agent. These data were collected with the intention of improving the control of C. jamacaru in South Africa. A field-based study of C. jamacaru population demographics investigated the efficacy of H. festerianus as a biological control agent of the weed, by integrating weed growth, fecundity and survival metrics with C. jamacaru population dynamics and demographic patterns from 8 sites where H. festerianus was present and 14 sites where the control agent was absent. The findings indicated that H. festerianus significantly reduced weed fecundity, which resulted in fewer seedling recruits, and that levels of plant mortality were greater at sites where H. festerianus was present. The reduction in weed fecundity and survival translated into negative population-level consequences for H. festerianus. Weed-population age frequency distributions in the absence of H. festerianus demonstrated a “reverse J-shaped” distribution, indicative of high recruitment rates and population stability, while C. jamacaru populations infected with H. festerianus were described by bell-shaped distributions, and were typified by ii Abstract limited recruitment, or a complete lack thereof. By constraining recruitment and inhibiting self regeneration, H. festerianus appears to regulate populations of C. jamacaru. Predation and parasitism of H. festerianus was believed to be a limiting factor for the biological control programme against C. jamacaru in South Africa, although no formal evaluation of this claim had been undertaken. Accordingly, the assemblage of natural enemies acquired by H. festerianus in South Africa was identified by field-collections of infected H. festerianus gall-material. Further, timed point-count surveys of natural enemies associated with H. festerianus were performed and integrated with the data on the impact of H. festerianus on weed population dynamics to assess the impact of two prominent predaceous taxa on H. festerianus efficacy as a biological control agent. Although H. festerianus had acquired a diverse suite of novel natural enemies in South Africa, this has not prevented the biocontrol agent from having an impact on C. jamacaru populations, although other subtler effects cannot be ruled out. This study showed that biological control efforts employing H. festerianus for the management of C. jamacaru have been successful. Furthermore, these data demonstrated the utility of retrospective analyses in developing and improving the science of biological control, specifically how to improve candidate agent prioritisation, determining how many agents are required for successful biological control, and how to evaluate the success of biological control efforts. Improvements in our theoretical understanding of biological control will undoubtedly reduce costs of biological control programmes, improve success rates, and increase the predictability of biological control. iii Table of Contents Table of Contents Title page...................................................................................................................... i Abstract......................................................................................................................... ii Table of Contents.......................................................................................................... iv List of Figures.............................................................................................................. vii List of Tables................................................................................................................. xi Acknowledgements...................................................................................................... xii Chapter 1 - General Introduction.............................................................................. 1 1.1. Cereus jamacaru De Candolle (Cactaceae)..................................................... 2 1.1.1. Taxonomy................................................................................................ 3 1.1.2. Biology and distribution......................................................................... 4 1.1.3. Invasion, impact and status.................................................................... 6 1.2. Biological control.............................................................................................. 7 1.2.1. Biological control of cactaceous weeds.................................................. 10 1.2.2. Biological control of Cereus j amacaru................................................... 12 1.2.3. Biological control employing Hypogeococcus festerianus..................... 14 1.3. Variable success in biological control................................................................ 15 1.3.1. Plant-insect incompatibility.................................................................... 16 1.3.2. Climate suitability.................................................................................. 19 1.3.3. Predation and parasitism........................................................................ 21 1.4. Aims and rationale............................................................................................... 22 Chapter 2 - Evaluating the efficacy of Hypogeococcus festerianus as a biological control agent of Cereus jamacaru in South Africa..................................................... 24 2.1. Introducti on................................................................................................ 24 iv Table of Contents 2.2. Methods and materials................................................................................. 28 2.2.1. Field survey................................................................................... 28 2.2.2. Data collection.............................................................................. 30 2.2.3. Statistical analyses........................................................................ 30 2.3. Results.......................................................................................................... 32 2.3.1. Between region comparisons of control sites............................. 32 2.3.2. Effect of infestation by Hypogeococcus festerianus...................... 33 2.4. Discussion.................................................................................................... 46 2.5. Conclusions.................................................................................................. 52 Chapter 3 - Natural enemy acquisition by Hypogeococcus festerianus and its implications for biological control of Cereus jamacaru............................................. 54 3.1. Introducti on.................................................................................................. 54 3.2. Methods and materials................................................................................. 58 3.2.1. Natural enemy assemblage associated with Hypogeococcus festerianus............................................................ 59 3.2.2. Association between natural enemies and Hypogeococcus festerianus............................................................ 61 3.2.3. Statistical analyses........................................................................ 62 3.3. Results.......................................................................................................... 64 3.3.1. Natural enemy assemblage composition, structure and diversity.. 64 3.3.2. Predator assemblage..................................................................... 71 3.3.3. Parasitoid assemblage.................................................................. 72 3.3.4. Correlations between natural enemies and Hypogeococcus festerianus........................................................... 73 3.4. Discussion.................................................................................................... 76 3.5. Conclusions.................................................................................................. 86 Chapter 4 - General Discussion.................................................................................. 87 4.1. Defining success in weed biological control................................................ 88 4.2. Setting pre-defined management targets for environmental weeds............. 91 4.3. Developing the science of biological control.............................................. 94 v Table of Contents