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Home , Acacia decurrens, Acacia mearnsii, Acacia pycnantha, Neltumius arizonensis

Politics and ecology in the management of alien invasive woody trees: the pivotal role of biological control agents that diminish seed production

V.C. Moran,1 J.H. Hoffmann1 and T. Olckers2

Summary 1. Biological control agents have been established on a total of 22 species of alien, invasive woody trees in (and via Australia in Thailand, Vietnam and Malaysia), South , the United States of America and Hawaii. Fifteen of these tree species (mostly Australian natives) are in . 2. Of the 39 agent species, 38 are (mostly weevils) and one is a pathogen. About 50% of these agents have been released in South Africa. Approximately two-thirds of these agents reduce seed production, directly or indirectly. 3. Usually, pre-dispersal seed mortality will not bring about a reduction in the density of invasive because weed populations can maintain near-saturation densities in spite of impressive depri- vations of their seeds by biocontrol agents. However, when humans intervene to clear adult plants, and where recruited seedlings are systematically and repeatedly destroyed, even modest levels of pre-dispersal seed mortality can translate into substantial savings for weed-control managers. Fewer seeds mean easier management through lower recruitment rates, fewer seedlings, and slower dispersal. 4. In the context of the politics and ecology of alien invasive tree control, agents that reduce seed production can also prove to be decisive in resolving conflicts of interest, and can become key elements in rehabilitation and restoration processes. They have become the first-line of defence in the successful management of alien invasive tree species. 5. We illustrate these points with reference to three very different cases, namely biological control against Sesbania punicea, cyclops and in South Africa. In each case, agents that reduce seeding have played a pivotal role in the biological control campaigns.

Keywords: biological control, invasive trees, management, seed-attacking agents.

Introduction South Africa). Thirty-eight species (and one rust species) have become established as biological control Only about 22 species of alien invasive woody trees agents on trees. About 50% of these agents are estab- have been targeted for biological control. Of these, 3 lished in South Africa, mostly deployed against alien are in the United States of America, 4 in Australia (or Acacia species from Australia (Table 1). About two- via Australia) and 15 in South Africa (Table 1; though thirds of these agents reduce seeding of their host plants an exact species count is not possible because either directly through feeding or laying on, or devel- has formed hybrid communities in Australia and in oping in, the seeds, or indirectly by damaging the repro- ductive parts of the , or variously debilitate the plants, and thus inhibit seed formation. 1 Zoology Department, University of Cape Town, Rondebosch, 7701, Much has been published on seed dynamics (Harper South Africa. 1977, Crawley 1997) and on the dynamics of 2 Plant Protection Research Institute, Cedara, Hilton, 3245, South Africa. plant–herbivore interactions (Crawley 1983). In the Corresponding author: V.C. Moran .

434 Seed-attacking agents in biological control of trees

Table 1. Alien invasive tree species (and their countries of origin) that have been deliberately subjected to biological control. (Shrubs that less commonly become small trees, and large cactus species, are excluded.) The agents that have become established on each of the target tree species, and the countries of introduction, are listed. The data are mostly extracted from Julien and Griffiths (1998), but modified according to more recent information, indi- cated by superscript numerals in the table, as follows: (1) van Klinken, R.D. et al. (2002) and van Klinken, R.D. (2003, pers. comm.); (2) Adair, R. J. (3, 4, 5) Impson, F.A.C.; (6) Olckers, T. (2003, Report of the Plant Protection Research Institute, Pretoria); (7) Center, T.D. et al. (2000); (8) Wheeler, G.S. et al. (2001). Tree species Agents established Countries of introduction Acacia nilotica ssp. indica Bruchidius sahlbergi Australia Prickly acacia (India) (Coleoptera: Bruchidae) Mimosa pigra Acanthoscelides puniceus Australia; to Thailand Giant sensitive plant (tropical America) (Coleoptera: Bruchidae) Acanthoscelides quadridentatus Via Australia (not established); (Coleoptera: Bruchidae) to Thailand, Vietnam Carmenta mimosa Australia; to Vietnam, (Lepidoptera: Sesiidae) Malaysia Chlamisus mimosae Australia (Coleoptera: Chrysomelidae) Coelocephalapion aculeatum Australia (Coleoptera: Apionidae) Coelocephalapion pigrae Australia (Coleoptera: Apionidae) Malacorhinus irregularis Australia (Coleoptera: Chrysomelidae) Neurostrota gunniella Australia (Lepidoptera: Gracillariidae) Parkinsonia aculeata Mimosestes ulkei Australia Palo verde (tropical America) (Coleoptera: Bruchidae) Penthobruchus germaini Australia (Coleoptera: Bruchidae) Rhinacloa callicrates Australia (Hemiptera: Miridae) Prosopis spp. (various hybrids including pallida and velutina) Algarobius prosopis Australia Mesquite (North and Central America) (Coleoptera: Bruchidae) Evippe sp. #11 Australia (Lepidoptera: Gelechiidae) Prosopidopsylla flava 1 Australia (Hemiptera: ) Acacia cyclops Dasineura dielsi 2 South Africa Rooikrans (Australia) (Diptera: Cecidomyiidae) Melanterius servulus South Africa (Coleoptera: Curculionidae) Melanterius maculatus 3 South Africa Silver wattle (Australia) (Coleoptera: Curculionidae) Melanterius maculatus 4 South Africa Green wattle (Australia) (Coleoptera: Curculionidae) Acacia longifolia Melanterius ventralis South Africa Long leaved wattle (Australia) (Coleoptera: Curculionidae) acaciaelongifoliae South Africa (Hymenoptera: Pteromalidae) Melanterius maculatus South Africa Black wattle (Australia) (Coleoptera: Curculionidae) Acacia melanoxylon Melanterius acaciae South Africa Australian blackwood (Australia) (Coleoptera: Curculionidae) Acacia pycnantha Trichilogaster sp. South Africa Golden wattle (Australia) (Hymenoptera: Pteromalidae) Melanterius compactus 5 South Africa Port Jackson willow (Australia) (Coleoptera: Curculionidae) tepperianum South Africa (Fungus: Uredinales) Hakea gibbosa Erytenna consputa South Africa Rock hakea (Australia) (Coleoptera: Curculionidae)

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Table 1. (Continued) Alien invasive tree species (and their countries of origin) that have been deliberately subjected to biological control. (Shrubs that less commonly become small trees, and large cactus species, are excluded.) The agents that have become established on each of the target tree species, and the countries of introduction, are listed. The data are mostly extracted from Julien and Griffiths (1998), but modified according to more recent information, indicated by superscript numerals in the table, as follows: (1) van Klinken, R.D. et al. (2002) and van Klinken, R.D. (2003, pers. comm.); (2) Adair, R. J. (3, 4, 5) Impson, F.A.C.; (6) Olckers, T. (2003, Report of the Plant Protection Research Institute, Pretoria); (7) Center, T.D. et al. (2000); (8) Wheeler, G.S. et al. (2001). Tree species Agents established Countries of introduction Hakea sericea Carposina autologa South Africa Silky hakea (Australia) (Lepidoptera: Carposinidae) Cydmaea binotata South Africa (Coleoptera: Curculionidae) Erytenna consputa South Africa (Coleoptera: Curculionidae) Leptospermum laevigatum Dasineura sp. South Africa Australian myrtle (Australia) (Diptera: Cecidomyiidae) Parectopa thalassias South Africa (Lepidoptera: Gracillariidae) Paraserianthes lophantha Melanterius servulus South Africa Crested wattle (tropics and subtropics) (Coleoptera: Curculionidae) Prosopis spp. (various hybrids including glandulosa and velutina) Algarobius prosopis South Africa Mesquite () (Coleoptera: Bruchidae) arizonensis South Africa (Coleoptera: Bruchidae) Sesbania punicea Neodiplogrammus quadrivittatus South Africa Red sesbania (Argentina, Brazil, Uruguay) (Coleoptera: Curculionidae) Rhyssomatus marginatus South Africa (Coleoptera: Curculionidae) Trichapion lativentre South Africa (Coleoptera: Apionidae) Solanum mauritianum Gargaphia decoris 6 South Africa Bugweed () (Hemiptera: Tingidae) Melaleuca quinquenervia Oxyops vitiosa 7 Florida, U.S.A Paper- tree (Australia) (Coleoptera: Curculionidae) Myrica faya Caloptilia nr schinella Hawaii , U.S.A Fire tree (Azores, Madeira, Canary Islands) (Lepidoptera: Gracillariidae) Schinus terebinthifolius Episimus utilus Hawaii, U.S.A. Brazilian pepper tree (South America) (Lepidoptera: Tortricidae) Lithraeus atronotatus Hawaii, U.S.A (Coleoptera: Bruchidae) Metastigmus transvaalensis 8 Florida, U.S.A (Hymenoptera: Torymidae) context of biological control of weeds, the majority of of the seedlings they generated. Weed populations can studies quantify the actual damage inflicted on the often persist in spite of the destruction of high propor- target plants by the biological control agents (e.g. the tions of their seeds by biological control agents. number of shoots destroyed, or the number of feeding The situation is very different where humans inter- holes in the , and so on). Relatively few studies vene to harvest (see Crawley 1997) or to clear parent quantify the impact of the agents on the population populations of the weed, and where recruited seedlings dynamics of the target weeds (Crawley 1989) or their are systematically and repeatedly pulled out, chopped, effects on the rate of spread of the weeds (Paynter et al. poisoned or burned. Under these circumstances, even 1996). In particular, it has frequently been noted that low levels of seed mortality brought about by biological biological control agents that reduce seed production control agents can reduce seedling densities and slow will usually be ineffective in reducing host-plant densi- rates of spread, which in turn translates into substantial ties (Myers et al. 1990, Cloutier and Watson 1990, savings for weed-control managers in clearing and Myers and Risley 2000). This is because the agents will follow-up operations, and may determine whether or have destroyed a surfeit of seeds that would have not control succeeds. In this paper, we discuss the succumbed to numerous pre- and post-dispersal mortal- pivotal role of seed-destroying agents in the manage- ities anyway, or failed because of the subsequent death ment of invasive trees in South Africa.

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Management of alien invasive trees marginal decline in plant density at only one of the study sites. Sesbania punicea is considered particularly in South Africa vulnerable in this respect because it has no seed banks South Africa has responded to the problems caused by and the trees are relatively short-lived (12–15 years). alien invasive trees (Moran et al. 2000) through the Populations of other species of invasive trees are likely concerted efforts of the Working for Water Programme. to be even less affected by high levels of seed destruc- This ambitious program has been running successfully tion. for several years, and costs about US$50 million per These studies raise the question, again, of whether annum. It employs about 25,000 people who clear inva- biological control agents that reduce seed production, sive trees and other alien plants, mostly from river can ever be successful in controlling trees. If “success” courses and catchments. The task is daunting. For in this context means reductions in the distribution or example, it is estimated that the Klein River in the density of the target plants, then the answer is usually South West Cape (which is about 40 km in length from “no: the self-thinning argument applies”, i.e. even with its mountain sources to the sea), will take 20 years and very high levels of seed destruction, there are still US$4 million to clear (C. Maartens and L. Waller, Cape enough seeds left to replenish the adult plant popula- Nature Conservation, pers. comm.). Weed managers tions. have reached the conclusion that success in clearing The three cases discussed above are apparently alien trees to acceptable densities in South Africa will disappointing from a biological control point of view. be nearly impossible without biological control. Massive reductions in seeding are predicted to have Follow-up operations on regrowth, after parent popula- little impact on invasive plant population densities, tions have been cleared, are crucial and often need to even in the long term. What these bland conclusions continue for many years. It is in this context that seed- hide, however, is the fact that management of the weeds destroying biological control agents have such an is much easier after biological control agents have important role to play in the management of alien inva- reduced the levels of seeding, and hence seedling sive trees. recruitment. Without biological control, manual or other methods of clearing parent populations usually prove to be almost completely futile because of the Management benefits of biological resurgence of seedlings. After biological control using control agents that reduce seed- seed-destroying agents, the reduced levels of seedling production recruitment greatly facilitate control, especially follow- up operations. Recently, Hoffmann et al. (2002) described the effec- The Working for Water Programme has recorded the tiveness of a -forming agent Trichilogaster sp. costs of clearing alien trees from river courses and (Pteromalidae) in reducing seeding in the Australian catchments in South Africa. Each of the many species tree Acacia pycnantha, that has invaded the south- of invasive trees has attendant problems that affect the western parts of South Africa. Galled of costs of clearing. However, on average, the relative A. pycnantha produce no pods, and branches with more costs per unit area can be estimated and these are shown than 10 produce 95% fewer pods (and hence in Table 2. These data illustrate the obvious point that it seeds). The gall-loads on A. pycnantha are enormous is much more expensive (up to 80 times) to clear high and thus, in aggregate, seed reduction is spectacular. densities of mature plants than low densities of seed- Over the last several years, Impson et al. (2000) and lings. This reinforces the imperative to follow-up the Impson (2003) have carefully monitored the effects of original clearing of parent populations as soon, and as the weevil Melanterius servulus on seed destruction in frequently as possible. However, the most significant Acacia cyclops, another highly invasive tree from feature of Table 2 is the evidence that any reduction in Australia. The weevils were originally released at 16 the density of seedlings (that is brought about by sites around the southwestern Cape in 1994. Already, at biological control agents) will result in significant and eight of the sites, seed-destruction is greater than 65% disproportionately favourable reductions in the costs of and at three of the sites the are destroying follow-up control. For example, it is five times more 90–95% of the seeds. costly to clear dense infestations of seedlings (where Hoffmann and Moran (1998) studied the effects of the area covered is between 51–75%) compared with biological control agents on the population dynamics of lighter infestations (of only 6–25%). the invasive South American tree, Sesbania punicea. Thus, if success in biological control means savings They demonstrated that two agents, a bud-feeder, of time and money in clearing and follow-up opera- Trichapion lativentre (Apionidae), and a seed-feeder, tions, then agents that reduce seed production in their Rhyssomatus marginatus (Curculionidae), in combina- target hosts must be deemed to be highly successful. tion, resulted in a 99.7% reduction in seeding by the Seed destruction by biological control agents results in trees. Over a period of 10 years or more, this extremely fewer seeds, fewer seedlings and lower costs of the high level of seed destruction resulted in only a original clearing operations, and these savings are

437 Proceedings of the XI International Symposium on Biological Control of Weeds

Table 2. The average relative costs per unit area of clearing alien invasive tree species (mainly Acacia species, species, Hakea species from Australia and Pinus species from ), at different levels of maturity. The data are a summary of detailed species by species costs that are used by Working for Water to calculate rates of pay for the tree- clearing teams (C. Maartens and L. Waller, Cape Nature Conservation, pers. comm.) Area covered (%) <5 6–25 26–50 51–75 76–100 Seedlings 1 3 7 15 20 Young Plants 3 5 19 43 57 Mature Plants 4 13 26 60 80 multiplied many-fold over the subsequent years of are deployed, selected agent species that attack other follow-up operations. The benefits of biological control parts of the plant should be considered, but only after agents that reduce the levels of seed production by their seeding is controlled, as a first priority. target plants may be summarised as follows: 1. there are fewer seeds (and seed banks) and seed- Acknowledgements lings 2. there are fewer and less expensive follow-ups We gratefully acknowledge the help of Mic Julien and 3. there is less pollution and disturbance during Rieks van Klinken who provided current information clearing operations; there must be a slower spread about biological control of trees in Australia, used in of the invasive plants, although this has seldom Table 1. been satisfactorily demonstrated (Paynter et al. 1996) 4. there will be quicker rehabilitation and easier resto- References ration. Adair, R. (2003) Biological control of invasive Australian Besides these advantages, one of the most compel- Acacia using seed-preventing Cecidomyiidae. Report of the ling “political” benefits of using seed-destroying agents Plant Protection Research Institute. pp. 67–71. Pretoria. against invasive trees is that they help to resolve Center, T.D., Van, T. K., Rayachhetry, M., Buckingham, G.R., conflicts of interest. For example, many invasive trees Dray, F.A., Wineriter, S.A., Purcell, M.F. & Pratt, P.D. are highly problematic in conservation areas, but in (2000) Field colonization of the melaleuca snout (Oxyops vitiosa) in South Florida. Biological Control 19, other areas the same species may be cultivated and 112–123. exploited commercially. Acacia cyclops in South Cloutier, D. & Watson, A.K. (1990) Application of modelling Africa forms widespread, impenetrable infestations to biological weed control. Proceedings of the VII Interna- along the coastal areas in the southwest Cape excluding tional Symposium on Biological Control of Weeds (ed E. S. hundreds of species of native plants, yet it produces a Delfosse) pp. 5–16. Istituto Sperimentale per la Patalogia valuable fuel . Acacia mearnsii is the major Vegetale (MAF), Rome, Italy. conservation problem in riparian and other in Crawley, M.J. (1983) Herbivory: the Dynamics of –plant South Africa, but this species is also the basis of a Interactions. Studies in Ecology, volume 10. Blackwell highly valuable , wood-chip and paper industry Scientific Publications, Oxford. in South Africa. The use of seed-destroying agents Crawley, M.J. (1989) Insect herbivores and plant population against these species does not detract from the benefi- dynamics. Annual Review of Entomology 34, 531–564. cial attributes of the plants, but does reduce their Crawley, M.J. (ed.) (1997) Plant Ecology. Second Edition. Blackwell Science. Oxford. aggressiveness and make them far more manageable. De Loach, C.J. (1981) Prognosis for biological control of weeds With seed-feeding agents we can have our cake and eat in southwestern U.S. rangelands. Proceedings of the V Inter- a piece of it! national Symposium on Biological Control of Weeds, (ed E. S. Delfosse), pp. 175–199. CSIRO, Melbourne. Conclusion Harper, J.L. (1977) Population Biology of Plants. Academic Press, London. There is overwhelming evidence from the studies of Hoffmann, J.H. & Moran, V.C. (1998) The population biological control of invasive trees in South Africa that dynamics of an introduced tree, Sesbania punicea, in South any reduction in seeding levels aids management. Africa, in response to long-term damage caused by different Agents that reduce seed production should always be in combinations of three species of biological control agents. Oecologia 114, 343–348. the front line of the attack (De Loach 1981). As a Hoffmann, J.H., Impson, F.A.C., Moran V.C. & Donnelly, D. general principle in weed biological control we advo- (2002) Biological control of invasive golden wattle trees cate that agents that reduce seed production should take (Acacia pycnantha) by a gall wasp, Trichilogaster sp. priority during the exploration phases and be amongst (Hymenoptera: Pteromalidae), in South Africa. Biological the first agents released. After seed-destroying agents Control 25, 64–73.

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