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Biological Control of Cactaceae in South Africa

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Biological Control of Cactaceae in South Africa Biological control of Cactaceae in South Africa I.D. Paterson1*, J.H. Hoffmann2, H. Klein3, C.W. Mathenge4, S. Neser3 & H.G. Zimmermann5 1Department of Zoology and Entomology, Rhodes University, P.O. Box 94, Grahamstown, 6140 South Africa 2Zoology Department, University of Cape Town, Rondebosch, 7700 South Africa 3Agricultural Research Council-Plant Protection Research Institute, Private Bag X134, Queenswood, 0121 South Africa 4Centre for Plants and the Environment, University of Western Sydney (Hawkesbury Campus), Locked Bag 1797, Penrith South DC, NSW 1797 Australia 5Helmuth Zimmermann & Associates (Central), P.O. Box 974, Faerie Glen, 0043 South Africa This review is a summary of developments that have contributed to the success of several biological control programmes against invasive cactus species (Cactaceae) that have been worked on in South Africa over the last 12 years. Six potential biological control agents have been identified for the control of Pereskia aculeata Mill. and molecular studies have identified the origin of the South African P. aculeata population. Host-specificity testing is now required for the three most promising of these agents. The successful biological control programme against Opuntia stricta (Haw.) Haw. has resulted in a change in management strategies against this weed in the Kruger National Park and the control of O. stricta is now almost entirely reliant on biological control. Taxonomic problems associated with the identi- fication of Cylindropuntia fulgida var. fulgida (Engelm.) F.M.Knuth var. fulgida have been resolved and an appropriate cochineal insect (Hemiptera: Dactylopiidae) biotype has been released, resulting in substantial declines in Cyl. fulgida var. fulgida populations. A long-term monitoring programme has been initiated to evaluate the progress of this new cochineal insect biotype. The Harrisia mealybug, Hypogeococcus pungens Granara de Willink (Hemip- tera: Pseudococcidae), which was originally released on Harrisia martinii (Labour.) Britton & Rose has been collected and redistributed onto Cereus jamacaru DC., where it reduces fruit production and leads to the death of both seedlings and large plants. Resolving taxonomic problems to ensure the correct identification of plant species and the most appropriate biological control biotypes have been key issues that have led to the successful control of several cactaceous weed species in South Africa. Key words: cactaceous weeds, Pereskia aculeata, Opuntia stricta, Cylindropuntia fulgida, Cereus jamacaru, cochineal insects, biotypes. INTRODUCTION The first biological control agent deliberately Cactaceae that have biological control agents estab- introduced into South Africa against an invasive lished on them, eight species (53 %) are considered plant was the cochineal insect, Dactylopius to be under substantial biological control (i.e. ceylonicus (Green) (Hemiptera: Dactylopiidae), other forms of management are still needed to for the control of the weed, Opuntia monacantha supplement biological control, but far less, or Haw. (Cactaceae), in 1913 (Lounsbury 1915). less frequently than before), and four species The biological control programme was extremely (27 %) are considered to be under complete bio- successful, reducing the density of the weed to logical control (i.e. no other management inter- negligible levels (Zimmermann et al. 2009). Since ventions are necessary) (Klein 2011). Notable this early success, a further 14 biological-control- successes include the biological control of Opun- agent entities (species or biotypes) have been tia aurantiaca Lindl. (Moran & Annecke 1979; released for the control of 15 cactaceous weed Moran & Zimmermann 1991a), Opuntia ficus-indica species in South Africa. The agents were originally (L.) Mill. (Annecke & Moran 1978; Zimmermann released against eight target species (including & Moran 1991), and Opuntia stricta (Haw.) Haw. O. monacantha) but subsequently became estab- (Hoffmann et al. 1999), which are considered to lished on seven additional cactus species. Of the be under substantial control; and Cylindropun- tia leptocaulis (DC.) F.M.Knuth (Moran & Zimmer- To whom correspondence should be addressed. E-mail: [email protected] mann 1991b), Cylindropuntia fulgida (Engelm.) African Entomology 19(2): 230–246 (2011) Paterson et al.: Biological control of Cactaceae 231 F.M.Knuth var. fulgida, Cereus jamacaru DC. (Klein South Africa (e.g. O. aurantiaca and O. ficus-indica), 1999), and Harrisia martinii (Labour.) Britton & they have also facilitated the control of species that Rose (Klein 1999), which are under complete had not yet become problematic in South Africa control. by providing agents which had proved to be suc- Factors that have contributed to the success of cessful in Australia, e.g. H. martinii (Hoffmann biological control of Cactaceae in South Africa 1995). include unusual aspects of the biology of the In this paper, the biological control programmes plants and of the cactophagous insects. The taxo- against weeds in the family Cactaceae that have nomic isolation and characteristic morphology been worked on since 1999 in South Africa are and anatomy of the Cactaceae have resulted in reviewed, including the selection of potential adaptations in their insect herbivores which in biological control agents for Pereskia aculeata Mill., turn have resulted in almost no cactophagous recent research on Cylindropuntia fulgida var. insects being able to feed on any plant species fulgida, long-term post-release evaluations on outside of the family (Mann 1969; Moran 1980). O. stricta, and some observations on the biological Because there are no native Cactaceae in the Old control of Cereus jamacaru. Species of Cactaceae World, with the possible exception of Rhipsalis that have not been worked on in the past 12 years baccifera (J.Müller) Stern, oligophagous cacto- are not included as they were dealt with in previous phages can be used for biological control without reviews (Annecke & Moran 1978; Moran & Annecke risk to non-target native or commercial plants (but 1979; Moran & Zimmermann 1991a,b; Zimmer- see below), thereby considerably broadening mann & Moran 1991; Klein 1999). the pool of suitable agents that are available. The increasing commercial importance of some cactus PERESKIA ACULEATA species such as O. ficus-indica, Opuntia robusta Wendel and Hylocereus species (Cactaceae) in Pereskia aculeata (Barbados gooseberry, pereskia) is South Africa has hampered efforts to extend a primitive creeping cactus with well developed biological control of cactus weeds, especially for leaves and woody stems and branches (Fig. 1). The species in the genus Opuntia. This is not a new plant is armed with paired, hooked thorns at the phenomenon. The introduction of Cactoblastis leaf-bases on the young, green shoots and clusters cactorum Berg. (Lepidoptera: Pyralidae: Phyci- of long spines which develop progressively on tinae) into South Africa in 1933 was opposed older,woody stems (Henderson 1995). Flowers are initially on the grounds that the larvae would creamy-white and have creamy-white stamen damage Opuntia plants which were providing filaments in South Africa, and either creamy-white fruit and fodder for commercial gain. It eventually or purple stamen filaments in the native distribu- took a parliamentary decision, in the early 1900s, tion (Leuenberger 1986; Paterson et al. 2009). The to allow release of the moth on the grounds that fruits are yellow and spiny when immature, but as the losses caused by O. ficus-indica far exceeded the fruit ripens the spines are lost and the fruit any gains that were derived from this and related changes to an orange colour (Leuenberger 1986). cactus species (Annecke & Moran 1978; van Sittert Pereskia aculeata is native to parts of Central 2002; Zimmermann et al. 2009). The success of America and the Caribbean as well as to southeast- C. cactorum in Australia helped sway opinion in ern Brazil and northern Argentina (Leuenberger favour of its release in South Africa (Pettey 1948; 1986). It was first recorded in South Africa in the Annecke & Moran 1978; Beinart 2003). Cape Town Botanical Gardens in 1858 (McGibbon The historical successes of many biological control 1858) and has become naturalized in areas around programmes around the world have benefited Cape Town and in Gauteng, Mpumalanga and from collaboration in the transfer of successful Limpopo provinces. It has also naturalized along agents between countries sharing common prob- the eastern coast of the country in the Eastern lems. This approach has been especially promi- Cape Province and KwaZulu-Natal Province, nent between Australia and South Africa in the where it is particularly invasive and abundant in case of the biological control of Cactaceae (Moran forests and coastal vegetation (Fig. 2) (Henderson & Zimmermann 1984; Zimmermann et al. 2009). 2001). The plant overgrows and kills indigenous Not only have these exchanges assisted in the coastal and forest flora, sometimes even causing control of already widespread cactus species in large trees to collapse under the weight of the 232 African Entomology Vol. 19, No. 2, 2011 X 2/3 Fig. 1. Pereskia aculeata. (Drawn by G. Condy; first published in Henderson (1995), ARC-Plant Protection Research Institute, Pretoria.) infestation (Moran & Zimmerman 1991b, Paterson regenerate. Herbicides are not translocated within et al. 2011). It was declared a weed in 1979, Procla- the plant’s tissues so all parts of the plant must be mation R35 (1979), and under the
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