Multiple-species introductions of biological control agents against weeds: look before you leap
F.A.C. Impson,1,2 V.C. Moran,1 C. Kleinjan,1 J.H. Hoffmann1 and J.A. Moore2
Summary Biological control practitioners have frequently debated the issues behind single vs multiple species introductions against target weeds. In the case of weed biological control, conventional wisdom is that multiple species should be used on the assumption that several species are more likely to have a greater controlling impact than a single species alone. This debate is rehearsed with reference to the biological control of four species of Australian acacias in South Africa: long-leaved wattle (Acacia longifolia (Andr.) Willd.), golden wattle (Acacia pycnantha Benth.), Port Jackson willow (Acacia saligna (Labill.) H. Wendl.) and rooikrans (Acacia cyclops A. Cunn. ex G. Don), where the impacts of both gall-forming and seed-reducing agents were intended to be additive and possibly synergistic. Evaluation and observations of these specific cases show that multiple-species introductions can be beneficial, but in at least one case (A. cyclops), the wisdom of these releases is questionable and po- tentially even detrimental. This suggests the need for extreme caution when planning multiple-species introductions against a target weed species.
Keywords: multiple species, Acacia, biological control.
Introduction non-target effects (Myers, 1985; Simberloff and Stil- ing, 1996; Callaway et al., 1999; Denoth et al., 2002; For many years, biological control practitioners have Pearson and Callaway, 2005). discussed and debated the merits of releasing multi- For most weed biological control projects, the high- ple as opposed to single species of biological control est levels of ‘success’ have been achieved using mul- agents in weed control programmes. The focus of such tiple agents, either because there has been a cumulative discussion has been multifaceted, either in terms of or synergistic effect of all agents working together the effectiveness of the actual control (Myers, 1985; (e.g. Hoffmann and Moran, 1998) or because as agent Myers et al., 1989; Story et al., 1991; Müller-Schärer numbers are increased, there is likely to be a greater and Schroeder, 1993; Hoffmann and Moran, 1998; An- probability that the most suitable species will be re- derson et al., 2000), competitive interactions between leased, often with a single agent being responsible for agents (Zwölfer, 1973; Ehler and Hall, 1982; Denno the success (Myers, 1985). Alternatively, the introduc- et al., 1995; Woodburn, 1996; Briese, 1997; McEvoy tion of more agents may ultimately provide a higher and Coombs, 2000), the best timing or sequence in probability of biological control over wider geographi- which to introduce agents (Briese, 1991; Syrett et al., cal ranges, due to different agent species performing 1996), or in terms of risk, safety and direct and indirect better under different conditions (DeBach, 1964; Baars and Heystek, 2003; Day et al., 2003). In many cases, new and additional agents are released prematurely, ei- 1 Department of Zoology, University of Cape Town, Rondebosch 7701, South Africa. ther because existing agents have not been adequately 2 Plant Protection Research Institute, Private Bag X5017, Stellenbosch evaluated or because agents have not been provided an 7599, South Africa. opportunity to achieve their full potential (McFadyen, Corresponding author: F.A.C. Impson, Plant Protection Research Insti- 1998; McEvoy and Coombs, 2000). Unfortunately, pre- tute, Private Bag X5017, Stellenbosch 7599, South Africa
26 Multiple-species introductions of biological control agents against weeds: look before you leap ongoing and daunting challenge (Cullen, 1995; Zalucki a related species of gall-forming wasp, Trichilogaster and van Klinken, 2006). signiventris (Girault) (Hymenoptera: Pteromalidae), The biological control programmes against four was released against A. pycnantha during 1987. After invasive Australian Acacia species in South Africa a slow start, when it was believed that the wrong strain are discussed with respect to these issues. They dem- of T. signiventris may have been imported (Dennill and onstrate that although multiple-agent releases are usu- Gordon, 1991), and additional releases in 1992, levels ally beneficial, there are times when this may not be of galling increased dramatically, and the insects be- the case and releases of more than one agent should be came abundant throughout the range of A. pycnantha planned with caution. by 1998. Besides substantial reductions in seed produc- tion due to the wasps, in some cases, extensive galling Biological control of Acacia species in caused collapse of branches and toppling of whole trees (Dennill et al., 1999; Hoffmann et al., 2002). Although South Africa initial indications were that no additional agents would During the last 30 years, biological control has been be required to further reduce seed production, monitor- implemented against nine of the most invasive Aus- ing of pod and gall loads (in 2004 and 2005) demon- tralian Acacia species in South Africa (Dennill et al., strated that many seed pods were still being produced 1999). Collectively, these programmes have largely despite the damage caused by T. signiventris. been governed by conflicts of interest over desires to The successful combination of the gall former and control the plants whilst continuing to exploit them a seed feeder in the A. longifolia programme paved the commercially for production of tannin, for timber way for a similar approach with A. pycnantha, and in and pulp, for fire wood and for dune binding. Con- 2005, the seed-feeding weevil, Melanterius maculatus sequently, the choice of biological control agents has Lea (Coleoptera: Curculionidae), was released. Al- been restricted, for the most part, to agents that limit though it is still too early to draw conclusions regard- the reproductive output of their hosts, thereby reducing ing the combined impact of the two agents, indications invasiveness but not the useful attributes of the plants. are that both agents will complement each other in re- Four of these acacias have been subject to control by ducing seed loads of A. pycnantha plants as is the case two agent species released sequentially (Table 1), and on A. longifolia. they are the subject of discussion here. Acacia saligna (Labill.) H. Wendl. (Port Jackson wil- Acacia longifolia (Andr.) Willd. (long-leaved wattle): low): Biological control of A. saligna had been recom- The gall-forming wasp, Trichilogaster acaciaelon mended as a priority from the outset of the programme gifoliae Froggatt (Hymenoptera: Pteromalidae), was against the Australian acacias (Neser and Annecke, released on A. longifolia in South Africa during 1982 1973). The gall-forming rust fungus, Uromycladium (Dennill and Donnelly, 1991). The wasps dispersed tepperianum (Sacc.) McAlp. (Urediniales: Ravene- readily and reduced seed production on A. longifolia liaceae), was selected as being a suitably damaging by more than 95%, even causing some suppression of agent in that it could reduce reproductive output and vegetative growth of the plants (Dennill, 1988). How- also weaken the plants and ultimately cause their death ever, there were two situations where T. acaciaelongi (van den Berg, 1977). After its release in 1987, U. tep foliae was not fully effective: (a) in the hot, arid, inland perianum rapidly dispersed throughout the range of A. areas and in the elevated, moist, mist-belt regions of saligna. Long-term evaluation studies demonstrated the country where climatic conditions curb population that the rust was an extremely effective agent, reduc- expansion of the wasps (Dennill and Gordon, 1990) ing population densities of adult trees by up to 85% and (b) A. longifolia plants growing close to rivers do (Wood and Morris, 2007). However, as in the case of not suffer water stress and still produce substantial seed A. longifolia and A. pycnantha, A. saligna was still able loads despite high levels of galling by the wasp (Den- to produce large seed loads before succumbing to the nill et al., 1999). effects of high levels of galling. Although the impact of T. acaciaelongifoliae was Again, the need was recognized for a second agent being studied, a second agent, a seed-feeding weevil, to target the remaining seeds, and another seed-feeding Melanterius ventralis Lea (Coleoptera: Curculionidae), weevil, Melanterius compactus Lea (Coleoptera: Cur- had been proposed for control of A. longifolia and was culionidae), was released against A. saligna in 2001. being tested in quarantine. By 1985, the need for an Although the introduction of M. compactus is relatively additional agent was deemed to be necessary, and the first recent, preliminary monitoring indicates that, like its releases of M. ventralis were made. The seed-feeding counterpart on A. longifolia, the weevils are playing an weevils established readily at release sites and have important supplementary role in curbing the produc- subsequently played an important supplementary role tion of viable seeds on A. saligna. in the suppression of seed production by A. longifolia Acacia cyclops A. Cunn. ex G. Don (rooikrans): A. (Dennill et al., 1999; Donnelly and Hoffmann, 2004). cyclops was the last of the four species under discus- Acacia pycnantha Benth. (golden wattle): Following sion to be subjected to biological control. In the early the success of T. acaciaelongifoliae on A. longifolia, 1990s, there was a strong focus on the Melanterius
27 XII International Symposium on Biological Control of Weeds group of weevils, which were readily available and all of these programmes, the sequence of releases (i.e. a easy to collect and had been shown to be sufficiently gall former preceding a seed feeder) was largely deter- host-specific and damaging to warrant consideration mined by opportunistic and pragmatic considerations. (Impson and Moran, 2004). In 1991, the first release Agents that were readily available, obviously dam- of Melanterius servulus (Pascoe) (Coleoptera: Curcu- aging to the host plant, abundant and easy to collect lionidae) was carried out, followed in 1993 by more and amenable to specificity testing enjoyed priority. In widespread releases. Although the weevils established the case of A. longifolia, the release of two species of successfully, they were relatively slow to build up their agents occurred within 3 years of each other, and it is populations, and dispersal was also limited (Impson et possible that if practical circumstances had been dif- al., 2004; Impson, 2005). Despite this, levels of seed ferent the order of release could have been reversed. damage increased with time at many of the release sites, The cases of A. pycnantha and A. saligna, respectively, with up to 95% seed damage being recorded within 5 are different in the sense that considerable time elapsed years of release at some of the sites. Manual redistri- between the releases of the first and second agents. The bution has been used to compensate for slow rates of reason for this was a conscious decision to evaluate the natural dispersal. impact of the gall formers acting on their own, before In 2001, a proposal was made that a second agent, taking the decision to release a supplementary agent. In a flower-galling midge, Dasineura dielsi Rübsaamen both cases, events were to prove that although the gall (Diptera: Cecidomyiidae), should be released to supple- formers were highly effective, there were more than ment the activities of M. servulus. It was anticipated that sufficient seeds left in the system to maintain popula- the midge would fulfill a complementary role and have tions of the host plants at problematic levels. There was good dispersal abilities, which would thus compensate a clear need for the seed-feeding weevils to reduce the for the problem of slow dispersal rates of the weevil. numbers of viable seeds. At the time, some concerns were expressed regarding The pattern for A. cyclops, however, is different in possible competitive interactions between the two con- that a seed-feeding weevil species was released first, trol agents (i.e. by galling the flowers, the midge would followed several years later by the release of a gall indirectly remove the food source of the weevils), but midge. Again the sequence of release was determined the matter of containing large invasions of A. cyclops by pragmatic and opportunistic circumstances and was was considered a priority and additional restrictive influenced by strong demands for additional control measures against this plant were strongly supported. measures against A. cyclops, particularly in view of the Following the establishment of D. dielsi, the midge slow dispersal rates of M. servulus. The, gall midge, dispersed extremely rapidly (hundreds of kilometers D. dielsi, was not an obvious choice of agent, prima- per year) throughout the range of A. cyclops (J. Moore, rily because of doubts about the effectiveness of gall personal communication, 2003), and with its multivol- midges as biological control agents (Goeden and Louda, tine life cycle, populations of the midge exploded. It 1976; McFadyen, 1985; Wehling and Piper, 1988; Carlson initially appeared that the proverbial ‘silver bullet’ had and Mundal, 1990; Harris and Shorthouse, 1996) and been released, and A. cyclops trees had been all but because from the outset there were some concerns sterilized by the extremely high levels of galling. How- over a potential conflict with M. servulus. Eight years ever, this situation did not persist, and midge popula- elapsed before it was decided that a supplementary tions have become less stable, resulting in considerable agent was needed. variation in the amount of pod set between sites and The A. cyclops programme differs from the others between years (F. Impson, C. Kleinjan and J. Moore, in one other important respect. In the case of A. longi unpublished results). This has obvious implications for folia, A. pycnantha and A. saligna, the gall-forming M. servulus because the weevils may no longer be able agents are essentially univoltine, exert pressure on the to sustain their populations when faced with an unpre- plants and substantially reduce seed production, but in dictable food source, and ultimately, the success of the most circumstances, there are sufficient seeds remain- biological control programme against A. cyclops may ing locally or in a wider area to sustain populations of be compromised. the seed-feeding weevils. In other words, the evidence suggests that the effects of the agents are complemen- Discussion tary. The gall-forming cecidomyiid, D. dielsi, on A. cyclops, by contrast, goes through several generations In these four cases of biological control against imported a year, most of which coincide with the peak flower- Australian acacias, there was a clear rationale, based ing period of the plant (the females lay their eggs in on available knowledge, which governed the pattern the flowers), which initially led to enormous gall loads and sequence of the releases of agents (Table 1), and in and the virtual or complete elimination of pods at sites. each case, the release of two agents has been justified. Subsequently, levels of pod production have been ex- For each of A. longifolia, A. pycnantha and A. tremely variable. Of concern is the possibility that the saligna, a gall-forming agent was released before being fluctuations in pod set will destabilize populations of followed up by a seed-destroying weevil (Table 1). In M. servulus and render the beetles unable to exploit and
28 Multiple-species introductions of biological control agents against weeds: look before you leap
Table 1. The four species of Australian acacias targeted for biological control in South Africa, using in each case sequen- tial releases of two agent species, all imported from Australia. In certain cases (marked by asterisk), there were previous releases, but they were unsuccessful. Acacia species Agent released Date of Release interval Mode of action References (Mimosaceae) first between agents release (years) A. A. longifolia 1. Trichilogaster 1982 3 Induces extensive Dennill, 1988; (long-leaved wattle) acaciaelongifoliae gall formation Dennill and Donnelly, 1991 2. Melanterius ventralis 1985 Destroys seed Dennill and Donnelly, 1991 B. A. pycnantha 1. T. signiventris 1992* 13 Induces extensive Dennill and Gordon, (golden wattle) gall formation 1991; *Dennill et al., 1999 2. M. maculatus 2005 Destroys seed F. Impson, unpublished results C. A. saligna (Port 1. Uromycladium 1987 14 Induces fungal galls Morris, 1991 Jackson willow) tepperianum on reproductive and vegetative tissue 2. M. compactus 2001 Destroys seed F. Impson, unpublished results D. A. cyclops 1. M. servulus 1993* 8 Destroys seed *Dennill et al., 1999; (rooikrans) Impson, 2005 2. Dasineura dielsi 2001 Induces galling Adair, 2004 of flowers
destroy the surfeit of seeds that develop when D. dielsi cal or prohibitively expensive. Predicting the outcome is less effective. At times when seeds are scarce, the of introductions remains problematic because, fre- situation is further exacerbated by rodent and bird pre- quently, the interacting attributes of the agent, the tar- dation of the seeds. The adult weevils also feed widely get weed and the environment are extremely complex. on the ripening seeds, leaving virtually no seeds that Furthermore, the introduction of each additional agent are in a suitable condition for oviposition. Under these introduces another tier of complexity, complicating the conditions of extreme seed scarcity, the weevil popula- ability to correctly predict outcomes. tions are in danger of becoming extinct locally or even In the case of the releases of a second agent onto A. over wide areas. pycnantha and A. saligna, sufficient time had elapsed It is still too early to predict the long-term outcome between the introductions of the gall formers and the of this programme. Preliminary studies indicate that subsequent decision to release seed feeders; the im- the unstable conditions over the last few years have im- pacts of the gall formers were well understood, and pacted on M. servulus populations at some monitoring a clear need for an additional agent that would target sites, and if this situation persists, it may prove to be residual seed production was identified. In addition, inimical to the biological control programme against A. extensive knowledge of the attributes of Melanterius cyclops in the long term. Alternatively, midge popula- spp. and their potential as biological control agents in tions may ultimately stabilize at levels where sufficient South Africa was available. With A. cyclops, sufficient pods are consistently available at sites. Under such time had elapsed after the introduction of M. servulus conditions, it is anticipated that M. servulus popula- for adequate evaluation of its performance and the tions would build up again and that the actions of D. recognition of its limitations. However, the ability to dielsi and M. servulus could be additive, as it is for the predict the outcome for the midge and its possible in- other Acacia species with two agents. In addition, the teractions with M. servulus was limited. The situation objective of harnessing the high dispersal abilities of with A. cyclops in South Africa highlights the need for D. dielsi would also have been realized. extreme caution when contemplating multiple species Apart from the fact that the introduction of organ- introductions and adds credence to the rule that bio- isms contains inherent risk, the broader ecological con- logical control agents in any situation should only be sequences of introductions have received little attention introduced where circumstances demand and where the and remain poorly understood. Weed biological control best predictions, as a result of experience, intuition or is only contemplated in situations where mechanical modeling, suggest that these multiple species introduc- and/or chemical control of invasive plants is impracti- tions will not worsen the situation.
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