Plant Protection Quarterly Vol.12(2) 1997 73 decision to shift survey operations to , where the climatic conditions were Biological control of St. John’s wort: past, present considered closer to those of temperate and future Australia, and the chance of finding suit- able thus higher (Wilson 1943). The English work, however, did produce late D.T. Briese, CSIRO Entomology and Co-operative Research Centre for Weed fruits, for in 1939 C. hyperici reappeared in Management Systems, GPO Box 1700, Canberra, ACT 2601, Australia. large numbers at the original release site in Bright and began to spread into new areas (Wilson and Campbell 1943). Biologi- Summary has proven to be effective under certain cal control of St. John’s wort in Australia Work on the biological control of St. conditions, but has not stopped the contin- had commenced. John’s wort ( perforatum L.) in ued spread of the weed (Campbell et al. Australia first commenced almost sev- 1995). The other, the eriophyid mite Phase 2: 1935–1942 enty years ago, and has passed through a Aculus hyperici, was only released in 1990 The shift to southern France in 1935 saw number of discrete phases, leading up to and, while it has yet to realise its full poten- studies concentrate on five potential con- the current program of work. A total of tial, has been attributed with causing con- trol agents (Wilson 1943) (see Table 1), and 15 agents have been studied in some de- siderable reduction in plant vigour at a continued until the onset of World War II tail with a view to introduction, and 12 of number of St. John’s wort infestations forced the field station to close in 1940. these were eventually released. Six (Jupp and Cullen 1996). Wilson (1943) considered the buprestid agents became established, four during This paper looks at the history of intro- root-borer, hyperici and the earlier phases of work in the 1930s to ductions and factors that have led to the chrysomelid defoliator, Chrysolina quad- 1950s and two in the current phase of success or failure of particular agents. The rigemina, to be the two dominant insects work from the mid 1970s on. Two of the current prospects for control are consid- on St. John’s wort stands in southern original agents to establish, the defoliat- ered and the desirability of further intro- France, with the root-borer exerting the ing chrysomelid Chrysolina ductions for biological control of St. John’s greatest impact, and being associated with quadrigemina and C. hyperici, provide wort discussed in the light of available in- large declines in the density of local some degree of control in certain situa- formation on the remaining candidate patches of the weed. Both these insects tions, but are unable to prevent the con- agents. were established relatively easily in 1939– tinued spread of the weed. There is, how- 40 at sites near Bright, Victoria, and ever, some early evidence that the re- History of biological control of St. Mudgee, NSW, and colonies showed early cently released eriophyid mite, Aculus John’s wort in Australia increase and dispersal (Wilson and hyperici, can cause substantial reduction Campbell 1943). Ag. hyperici populations in the vigour of St. John’s wort Phase 1: 1928–1939 built up steadily at the two release sites populations and might therefore im- Although first mooted in 1917, it was not and within two years individual plants prove the overall level of biological con- until 1928 that research actually com- were being killed and the growth of oth- trol. This paper looks at the history of in- menced on the biological control of St. ers restricted by heavy attack (Wilson and troductions of agents into Australia in the John’s wort, with the setting up of a labo- Campbell 1943). Large populations of C. context of changing strategies for bio- ratory in Buckinghamshire, England quadrigemina were also recovered in the logical control of the target weed, and (Currie and Garthside 1932). Eight insects, field in 1942, causing substantial defolia- looks at the potential for further intro- all but one of which were leaf-feeders, tion at the release site as well as dispersing ductions of new agents. Whether further were studied in some detail and eventu- to other areas (Wilson and Campbell work is required, however, depends on ally sent to Australia (Table 1). Three of 1943). The potential of these two beetles, the eventual impact of A. hyperici, and these were not released, however; the along with C. hyperici, was quickly appre- the need for careful evaluation of this two leaf-webbing insects, Lathronympha ciated in the light of the extensive damage agent is stressed. hypericana and Depressaria hypericella, were to roots and local defoliation of infesta- considered unlikely to be effective due to tions of target weed. The other three Introduction the nature of their damage to the target agents imported into Australia were not The biological control project against St. weed, while the English population of the released as they were considered to be not John’s wort, together with those against aphid, Aphis chloris, was sexually-repro- capable of the same levels of damage, and prickly pear and lantana, heralded the ducing and overwintered as an egg work entered a third phase, which was to start of weed biological control in Aus- (Wilson 1938). Cold-requirements for sub- concentrate on the evaluation and large- tralia. Despite this, after almost seventy sequent emergence of nymphs were not scale redistribution of the two chryso- years, the introduction of natural enemies met in Australia, thus preventing its re- melid beetles and the root-borer. The has not yet managed to reduce St. John’s lease. The five defoliating species were re- prospects for successful biological control wort infestations to levels that do not leased in Victoria between 1930 and 1937 looked promising indeed, with Ag. cause unacceptable economic or environ- but with little initial success (Currie and hyperici expected to be the predominant mental damage. Since surveys for poten- Fyfe 1938). By 1938, it was considered that agent (Wilson and Campbell 1943). tial control agents of St. John’s wort first introductions of the two geometrid commenced in 1928, there have been four , Anaitis efformata and A. plagiata, and Phase 3: 1940–1956 distinct phases of work leading to the es- the three chrysomelid beetles, Chrysolina Redistribution of C. hyperici commenced tablishment of six agents in Australia brunsvicensis, C. hyperici and C. varians, on a broad scale in 1940, and of C. (Campbell et al. 1995). Only two of these had failed. Heavy predation on newly re- quadrigemina in 1943. Agencies such as currently appear to have the potential to leased colonies by indigenous natu- CSIRO and the Victorian Department of contribute to the overall control of the ral enemies was considered to be the main Lands and Survey distributed over 10 mil- weed. One species, a defoliating cause of this failure, though unfavourable lion chrysomelid beetles in Victoria (1940– Chrysolina quadrigemina, which established physical conditions were thought to have 51), New South Wales (1941–56), Tasma- in the early 1940s and was widely redis- played a role in the case of the chryso- nia (1943), South Australia (1943–49) and tributed throughout the next two decades, melids (Currie and Fyfe 1938). This led to a Western Australia (1947–53) (Wilson 1960), 74 Plant Protection Quarterly Vol.12(2) 1997 Table 1. Natural enemies of in Australia. Species Mode of action Origin Year released Relative occurrenceA Ref.B Phase 1 Col: Chrysomelidae Chrysolina varians (Schall.) leaf defoliator England 1930–33 did not establish a C. brunsvicensis (Grav.) leaf defoliator England 1930–34 did not establish a C. hyperici (Forster) leaf defoliator England 1930–34 occasional** b Lep: Geometridae Anaitis efformata L. leaf defoliator England 1936–38 did not establish b A. plagiata Guenée leaf defoliator England 1936–38 did not establish b Lep: Eucosmidae Lathronympha hypericana Hubn. leaf webber England not released a Lep: Oecophoridae Depressaria hypericella Hubn. leaf webber England not released a Aphididae Aphis chloris Koch sap sucker England not released a Phase 2 Col: Chrysomelidae Chrysolina quadrigemina (Suffr.) leaf defoliator France 1939 common** c,d Agrilus hyperici (Creutzer) root-borer France 1939–40 rare* c,d Lep: Noctuidae Actinotia hyperici Schiff. leaf defoliator France not released c Dip: Cecidomyiidae Zeuxidiplosus giardi Kieff. leaf-bud galler France not released c Lep: Gelechiidae Aristotelia morphocroma Wals. stem and seed France not released c capsule borer Phase 3 Dip: Cecidomyiidae Zeuxidiplosus giardi Kieff. leaf-bud galler California 1953-54 common* e (ex France) Phase 4 Col: Chrysomelidae Chrysolina hyperici (Forster) leaf defoliator France 1980 uncertain f,g C. quadrigemina (Suffrian) leaf defoliator France 1981 uncertain f,g Lep: Geometridae Anaitis efformata L. leaf defoliator France 1981–83 did not establish h Lep: Noctuidae Actinotia hyperici Schiff. leaf defoliator France 1985–86 did not establish g Buprestidae Agrilus hyperici (Creutzer) root-borer France 1984, 1989 uncertain g Aphididae Aphis chloris Koch sap sucker France 1986–87 common* i Acarina: Eriophyidae Aculus hyperici (Liro) sap sucker France 1990 common* j Lep: Gelechiidae Aristotelia morphocroma Wals. stem and seed France not released capsule borer A *= has caused localised damage, ** = has caused heavy damage at a number of sites. B Sources: a = Currie and Garthside (1932), b = Currie and Fyfe (1938), c = Wilson (1943), d = Wilson and Campbell (1943), e = Wilson (1960), f = Delfosse and Cullen (1981), g = Wapshere (1984), h = Briese (1986), i = Briese and Jupp (1995), j = Jupp and Cullen (1996). with distributions peaking in the late 1940s responsible for one of the classical biologi- Despite the initial steady increase and and early 1950s (Figure 1). By 1951 most of cal control success stories in reducing St. spread, by 1946 both colonies at Mudgee the redistributions were of C. quad- John’s wort to sub-economic levels over and Bright had been over-run by massive rigemina, and these have continued inter- 800 000 ha in 10 years (Huffaker and population build-ups of Chrysolina spp. mittently at lower levels until the present Kennett 1959). During this period, C. These leaf-eating beetles have a much day. As well as internal redistribution, C. quadrigemina proved to be more competi- higher natural rate of increase than Ag. hyperici was sent to New Zealand in 1943, tive than C. hyperici under Australian con- hyperici, and their populations entirely de- where it has contributed significantly to ditions (see Clark 1953), and become the foliated the areas where Ag. hyperici had the control of the weed in some areas dominant species. By the late 1970s, it was been released. The absence of food for (Hancox et al. 1996), and over 600 000 adult ten times more abundant than C. hyperici adult Ag. hyperici would have inhibited beetles of both species of chrysomelid (Shepherd 1984). oviposition and led to overdispersal and sent to California from 1945–47, where The fate of the Ag. hyperici colonies, difficulties in finding mates, with the end C. quadrigemina, in particular, has been unfortunately took another direction. result being the demise of the Bright Plant Protection Quarterly Vol.12(2) 1997 75 1800000 generalist parasitoids, predators and dis- 1600000 eases on the released larvae and eggs (Briese 1986). 1400000 Studies undertaken in Australia indi- 1200000 cated that C. quadrigemina could in fact per- 1000000 form as well under summer rainfall condi- tions as it did in more Mediterranean cli- 800000 mates (Briese 1985), and suggested that 600000 the major factor mitigating against suc- cessful control lay with the ability of the 400000 plant to survive defoliation rather than 200000 with any inherent fault of the insects. The Number of beetles redistributed 0 strong root reserves of established plants 1940 1942 1944 1946 1948 1950 1952 1954 1956 1958 1960 seemed the key to this survival, and it was therefore decided to concentrate remain- Year ing efforts on those agents that could ex- Figure 1. Redistribution of Chrysolina beetles during the third phase of haust these reserves (Table 1). Two agents biological control of St. John’s wort in Australia (data derived from CSIRO previously studied fitted this requirement; the root-borer, Ag. hyperici and the aphid Division of Entomology annual reports). Aphis chloris, which sucks the sap and can exhaust root reserves. New populations of colony of Ag. hyperici and the restriction of and dispersed readily, it did not consist- the root-borer, Ag. hyperici were imported the Mudgee colony to a timbered creek ently develop populations large enough to from France and released, but, as previ- system, where it currently persists pro- contribute significantly to the control of ously, establishment proved difficult. Only tected from competition by C. quad- the weed. The third phase of biological one new colony, at Tuena, appears to have rigemina (Briese 1991a). control thus ended with partial success survived longer than the initial season (P. While Chrysolina spp. were attributed and the knowledge that complementary Jupp personal communication). A. chloris with considerable initial success in control- agents would be needed to find a more readily became established and is now ling St. John’s wort in certain areas, par- sustainable solution in all weed-infested widespread, but causes only localised ticularly those with Mediterranean-type areas. damage (Briese and Jupp 1995). climates (Huffaker 1966), such as Western European work showed that a previ- Australia and South Australia, and in east- Phase 4: 1978–present ously unstudied agent, the eriophyid mite ern Australia where the weed was re- The continuing spread of St. John’s wort Aculus hyperici, was a major controlling placed by competitive pasture species fol- saw pressure mount from landholders for agent in southern France (Wapshere 1984), lowing its reduction by the beetles (L.R. further work on biological control, and a and was apparently not inhibited by Clark 1953), it soon become apparent that fourth phase of work, largely funded by shade. The mite feeds on the sap and over this success was limited by several factors. industry, commenced in 1978. It was con- two to three years gradually exhausts the The absence of competitive plant species sidered that further agents were needed root reserves, leading to progressive to replace the weed following defoliation that would be effective in timbered areas dwarfing and eventual death of the plant. was critical in many areas (N. Clark 1953). and in areas of summer rainfall, were bet- Since introduction and release in Australia While defoliation by the beetles could kill ter synchronised with the climate of in- in 1990, it has caused substantial reduction deep-rooted plants on good soils (N. Clark fested areas, able to damage the weed se- in the vigour of St. John’s wort popula- 1953), in situations where soils were stony verely enough to prevent summer re- tions at many of the initial release sites and or shallow, the plants responded to defo- growth and could achieve control without is currently the subject of a redistribution liation by producing new shoots vegeta- pasture improvement (Delfosse and program (Jupp 1997, Maher et al. 1997). tively from lateral roots (Clark and Clark Cullen 1981, 1982). Some of the agents Having many generations per year and 1952). The boom-bust population cycles of studied earlier were reconsidered (Table being wind-dispersed, the mite has the the beetles tended to provide periods of 1) and further European surveys were un- potential to rapidly build up to damaging respite from herbivore pressure (L.R. dertaken to identify potential agents that levels over a relatively short period. Clark 1953), and this was complicated by might augment the impact of the Hence, this fourth stage of biological con- occasional asynchrony between the onset chrysomelids and provide more continu- trol draws to a conclusion with the prom- of beetle activity after aestivation and ous stress on St. John’s wort (Wapshere ise that, in Ac. hyperici, an agent able to growth of the weed (Huffaker 1966). In 1984). Populations of both Chrysolina spp. apply a more consistent pressure on St. areas with high summer rainfall, St. John’s were collected from regions in France John’s wort infestations in all parts of their wort infestations were able to recover sig- more climatically similar to those parts of range may have been found. nificantly from winter and spring defolia- Australia with summer rainfall patterns tion by the beetles (Huffaker 1966). Fi- and introduced and released at a number Current status of the biological nally, Chrysolina spp. are not tolerant of of sites in south-eastern Australia in 1980– control of St. John’s wort in Australia shaded situations and therefore have been 81 (Delfosse and Cullen 1982). Their status Currently six of the twelve agents re- unable to colonise infestations of the weed remains unknown, however, as it was not leased have become established in Aus- in timbered areas (L.R. Clark 1953). possible to distinguish new from existing tralia (Table 1). One of these, the root- The realisation that Chrysolina spp. populations. The fact that there has been borer Ag. hyperici, while able to cause im- would not solve the St. John’s wort prob- no change in the pattern of impact by portant damage to the weed, is restricted lem on their own led to a renewed and Chrysolina since then suggests that the new to one or possibly two isolated sites. Two successful effort in 1953–54 to import the populations are no more effective than others, the aphid A. chloris and the gall gall midge, Zeuxidiplosis giardi, which galls those introduced earlier. Efforts to re- midge Z. giardi, are relatively widespread terminal shoots and can thus reduce plant introduce the defoliating moths, Actinotia and common without reaching levels able vigour and seed production (Wilson 1960) hyperici and Anaitis efformata, were unsuc- to cause an impact on St. John’s wort infes- (Table 1). Although this insect established cessful, due to the heavy impact of native tations on other than a very limited scale. 76 Plant Protection Quarterly Vol.12(2) 1997 100% infestations supporting populations capa- Impact of Chrysolina populations on St John’s wort ble of causing significant defoliation in any 90% 1 not damaging one year (Figure 2). Population build-ups 2 80% light damage seem to be favoured more by good au- 3 tumn/winter rainfalls, which assure good 70% 4 moderate damage rosette growth and high survival of feed- 5 severe damage 60% ing larvae, than by any effect of summer rainfall on adults (Briese 1985). In less fa- 50% vourable sites, numbers may never reach 40% damaging levels (Figure 3), while in fa- vourable areas, free from many of the 30% original constraints in Europe, populations 20% of the beetle may follow ‘boom–bust’ cy- Percentage of sites surveyed cles, where they increase to a level at 10% which the food resource is destroyed and 0% then crash (Figure 3). 1982 1983 1984 1985 1986 1987 1988 The impact of C. quadrigemina is there- fore somewhat paradoxical. There is Year strong evidence that large amounts of Figure 2. Changes in the proportion of St. John’s wort infestations supporting good pasture lands were recovered from Chrysolina populations and the level of defoliation caused over seven years St. John’s wort infestation through its ac- (1986 was a drought year). tivities (see Figure 4). At present, even though populations fluctuate over the The two leaf-feeding Chrysolina beetles, could not develop in Australia because of years and may attain damaging levels at have had and are both still capable of hav- the different initial population structures no more than 20% of sites (Figure 2), they ing an impact, with C. quadrigemina being of the host weed and the pattern of releases do temporarily reduce infestation densi- the dominant and more effective species. of the two agents (Briese 1991a). With the ties to below economically-damaging lev- The ready establishment of the mite, and wisdom of hindsight, it is possible to argue els (Figure 3). On the other hand, it has its rapid redistribution through the devel- that the initial releases were made too inhibited the development of other opment of networks with community near one another, and that better spacing agents, and in the case of the root-borer, groups (Maher et al.1997) has meant that would have permitted Ag. hyperici to build Ag. hyperici, this may well have prevented there is now a second agent that is wide- up to a critical mass, before there was any a more effective, albeit initially slower, spread and in a position to complement interaction with C. quadrigemina. long-term solution. The risk of competi- the activity of the defoliators. Early indica- Chrysolina quadrigemina was also able to tion by the beetle to Ac. hyperici remains to tions are that it is reducing plant size and outcompete the other leaf-eating beetle, C. be determined. vigour already at some of the release sites, hyperici. It terminates aestivation and com- The most important factor compromis- and close monitoring and evaluation are mences oviposition several weeks earlier ing more effective control by the beetles is needed to ensure that critical data on its than its congener. Thus, early developing the ability of St. John’s wort to regenerate impact are not lost. larval populations of C. quadrigemina can following defoliation in the absence of The structure of the present guild of severely defoliate winter growth before other stress. The mite Ac. hyperici has the control agents is characterised by two fea- larvae of C. hyperici hatch (L. Clark 1953), ability to weaken this capacity through a tures; the competitive superiority of C. giving them a competitive edge. How- sustained depletion of root reserves, and quadrigemina and its dramatic population ever, this has probably been a positive in- may therefore bring some stability to the fluctuations under Australian conditions. teraction for biological control, for by sus- plant-herbivore interactions in Australia In southern Europe, where St. John’s wort taining attack over a longer period, C. (Jupp and Cullen 1996). Apart from com- exists as a metapopulation of small iso- quadrigemina is the more effective control petition by Chrysolina beetles, the spectre lated patches, C. quadrigemina rarely agent (N. Clark 1953). of host-plant resistance to the mite in some reaches densities at which it can com- Chrysolina quadrigemina has recently populations remains a potential long-term pletely defoliate a stand. Here the domi- been implicated as a cause of the failure of threat to its success (Jupp et al. 1997). As nant herbivore is in fact the root-borer, Ag. establishment of the mite, Ac. hyperici, at stressed previously, it is critical that these hyperici (Wilson 1940, Briese 1991b), which some sites where the beetle has defoliated risks be properly evaluated under field can cause the collapse of weed patches areas following release (Jupp and Cullen conditions, and this current phase of bio- over a period of several years. Viewed 1996). It appears, though that with its high logical control cannot be viewed as com- simply, this cycle of extinction of patches powers of dispersal and very high rate of plete unless this is done. and the formation of new patches, coupled increase, the mite can recover and reinfest with interpatch migration of various natu- sites within a year (Jupp and Cullen 1996). Future biocontrol work and potential ral enemies, maintains the stability of the While C. quadrigemina initially has the com- control agents? system. In Australia, St. John’s wort can petitive advantage, Ac. hyperici shows re- The need to contemplate a fifth phase of exist as very large, dense infestations. silience to the impact of this competition. work in search for further biological con- With the absence of competing herbivores This interaction will have an important trol agents of St. John’s wort will depend upon introduction, C. quadrigemina was bearing on the long-term impact of the ultimately on whether or not Ac. hyperici able to rapidly build up to levels at which it mite, and it is important that evaluation of lives up to its early promise for the control could defoliate very large areas of the food these releases be made to determine how of the weed. However, it is worth consid- plant. As a consequence C. quadrigemina it develops. ering what shape a further biological con- was able to suppress recently released Chrysolina quadrigemina is to some ex- trol effort might take, both in terms of a neighbouring populations of Ag. hyperici, tent constrained by environmental condi- renewal of work on agents that have al- which has a much slower rate of increase tions (see Briese 1985), and its numbers ready been studied and a search for and (Briese 1991a). Thus, the equilibrium be- tend to fluctuate between years, with evaluation of new potential control agents tween these agents that existed in Europe rarely more than 20% of St. John’s wort (Table 2). Plant Protection Quarterly Vol.12(2) 1997 77 Cassilis Pierce's Creek 5

4 3 2 Chrysolina

damage rating 0 77 78 79 80 81 82 83 84 85 86 87 88 80 81 82 83 84 85 86 87 88 2

0 density -2 Change in weed

Coolah Creek Queanbeyan 5

4 3 2 Chrysolina

damage rating 0 77 78 79 80 81 82 83 84 85 86 87 88 80 81 82 83 84 85 86 87 88 2

0 density -2 Change in weed

Beechworth - timbered Adaminaby - timbered 5

4 3 2 Chrysolina damage rating 0 80 81 82 83 84 85 86 87 88 80 81 82 83 84 85 86 87 88 2

0 density -2 Change in weed

Figure 3. Changes in the impact of Chrysolina beetles and St. John’s wort infestation levels at six sites over a number of years. Chrysolina populations were rated on a scale of 0 to 5 (not present to very high levels of defoliation) and changes in St. John’s wort density between years was indicated on a scale of -2 (severe decline) through 0 (no change) to +2 (heavy increase). The white vertical bars indicate autumn, shaded vertical bars indicate spring. The dark horizontal bar indicates period when weed infestations were sufficient to cause economic damage. The arrows indicate the passage of a fire through the infestation.

The primary causes of the persistence • in addition, it must either withstand or ment of other lepidopteran agents (see of St. John’s wort infestations and the fail- show resilience in the face of competi- Briese 1986), and hence the possibility of ure of adequate biological control are: tion from C. quadrigemina. having a major impact is low. • the ability of the plant to store large Aristotelia morphochroma was considered Given that it is considered one of the nutrient reserves in its root system and for introduction twice previously but was most important natural enemies of St. so recover from drought, fire and at- never released for technical reasons. The John’s wort in southern France (Wilson tack by defoliating agents, main interest in this agent is due to stem 1943, Wapshere 1984, Briese 1991a), there • the ability to regenerate vegetatively die-back caused by the mining of early is some merit in renewing efforts to fur- from horizontal roots, and generation larvae and the direct feeding ther introduce or redistribute the root- • a long-lived seedbank that can lead to on flowers and fruit of later generation lar- borer, Ag. hyperici. Data from North massive germinations under favour- vae (Wilson 1943). Two points mitigate America indicates that Ag. hyperici (origi- able conditions. against this agent being given a high pri- nating from shipments sent from Aus- As a consequence, any future agents must ority in any further work. Firstly, though tralia) can coexist with C. quadrigemina and be able either to: it may serve to limit dispersion, it is not contribute to biological control, once it has • put continual pressure on root reserves clear that direct attack on fruit capsules will been able to establish itself widely until the plant dies, have a significant impact on a plant that (Campbell and McCaffrey 1991). It would • reduce vegetative shooting and/or can also reproduce vegetatively. Secondly, be necessary, though, to reduce or avoid • be able to increase rapidly in response the would be exposed to the same competition from existing Chrysolina to successful large-scale germination range of generalist predators, parasitoids populations during the establishment events and diseases that prevented the establish- phase, which, as indicated earlier, are the 78 Plant Protection Quarterly Vol.12(2) 1997 main reason for the failure of the root- There may, however be an alternative indicate that it is having considerable im- borer to become more widespread in the to Ag. hyperici. nigrifrons (le pact at some of the original release sites in past (Briese 1991a). Certainly, careful site Cerf) is a clearwing moth, the larvae of Western Australia (J. Scott personal com- selection (e.g. shaded areas) and manage- which bore into the roots of their host munication). C. nigrifrons would also have ment (e.g. carefully timed insecticide ap- plants. It is of interest as three species of an advantage over the Ag. hyperici because plications) could be employed to favour this genus have been studied as biological adults of the moth are not leaf feeders and establishment, but given the slow rate of control agents for long-lived perennial hence would not be in direct competition population increase of this insect (Briese plants. One species, C. doryliformis, was re- for food resources with Chrysolina. 1991b) this would require considerable leased in Australia in 1989 for the control Lastuvka and Lastuvka (1995) list H. perf- long-term effort. of docks (Rumex spp.), and recent surveys oratum as its only known host-plant, but C. nigrifrons has not been well studied in its native range. Distribution records indicate 180000 that the main part of this range is in the Balkan peninsula, with pockets in south- 160000 Agent ern Europe, including France and Corsica (Lastuvka and Lastuvka 1995). Prelimi- establishment 140000 nary searches by CSIRO Montpellier staff in the course of other field work have not 120000 located it in mainland France (J-L. Sagliocco personal communication). 100000 Another relatively unknown pair of agents could also provide a complemen- 80000 tary form of attack on St. John’s wort. These are the ceccidomyid gall-midges, Geocrypta braueri Hanl. and G. hypericina 60000 Agricultural land Area infested (ha) Tavares, both apparently restricted to the genus Hypericum and the larvae of which 40000 form galls on the underground shoots of Native forests St. John’s wort (Barnes 1952). Currie and 20000 Garthside (1932) reported that such gall- ing considerably weakened the attacked 0 plant, but did not consider it for introduc- tion into Australia during Phase 1 as they

1880 1890 1900 1910 1920 1930 1940 1950 1960 1970 1980 were unable to rear it. It might well be Year worth reconsidering, however, as, apart from weakening a plant, the galling of Figure 4. Changes in the area of land infested by St. John’s wort in Victoria underground shoots could prevent the with time. The total area is based on data presented in Campbell et al. (1995), vegetative reproduction of St. John’s wort. and the percentage ascribed to forest areas was based on the estimates of This would be an important contribution Shepherd (1984). The figure hypothesises that invasion of agricultural land to reducing infestation densities in Aus- tralia, particularly on shallow soils where was more rapid than that of native forests, and suggests that biological control stands maintain themselves mainly (and associated pasture improvement) was effective in reducing the weed through shoot regrowth from horizontal problem on a large proportion of agricultural areas, but has been unable to roots (up to 90% at a site studied by Briese prevent spread in native forest. 1996). G. braueri occurs in central to

Table 2. Potential biological control agents for St. John’s wort that have not yet been released in Australia Species Mode of action Native range Comments RefA Lep: Gelechiidae Aristotelia morphocroma Wals. stem and seed southern Europe limiting seed production may not a capsule borer greatly improve control Dip: Cecidomyiidae Geocrypta braueri Hanl. root galler northern Europe potential to limit vegetative b reproduction G. hypericina Tavares root galler Spain potential to limit vegetative b reproduction, but rare in Europe Lep: Chamaesphecia nigrifrons (le Cerf) root borer Southern (isolated) can severely damage root system, c and S.E. Europe but rare in Europe Fungi Colletotrichum gloeosporioides anthracnose fungus North America can kill plants, but spore germination d (Penz.) Penz. and Sacc. (Nova Scotia) may have specific moisture requirements Melampsora hypericorum rust fungus Europe can kill plants, but strain needs to e (DC. Wint.) be found for St. John’s wort A Sources: a = Wilson (1943), b = Barnes (1952), c = Lastuvka and Lastuvka (1995), d = Hildebrand and Jensen (1991), e = Bruzzese and Pascoe (1992). Plant Protection Quarterly Vol.12(2) 1997 79 northern Europe, whereas G. hypericina is Conclusion Australia, the Australian Wool Corpora- known from Spain (Barnes 1952), and the In many respects the biological control tion and the Meat Research Corporation. latter species may therefore be better program against St. John’s wort in Aus- adapted to the temperate Australian cli- tralia provides a classic example of how References mate. An attempt by staff from CSIRO the discipline itself has evolved in the past Barnes, H.F. (1952). The gall midges of St. Montpellier to find it in Spain in 1986 was 70 years. Assessments of the success of John’s wort (Hypericum spp.), with de- unsuccessful (J. Cullen personal communi- work in progress and the outcomes of re- scriptions of two new species. Bulletin of cation). leases have led to several changes in ra- Entomological Research 42, 697-705. Finally, pathogens might provide a so- tionale and priorities for agent introduc- Briese, D.T. (1985). A survey to evaluate lution to the need for agents capable of tions. The failures of initial agent introduc- the long-term relationship between rapid population build-up in response to tions from England taught the lesson of a Chrysolina quadrigemina and its host an upsurge of St. John’s wort (McLaren et need for matching climates as closely as weed, St. John’s wort, in south-eastern al. 1997). There are two possibilities, the possible and led to a shift to more Mediter- Australia. Proceedings of the Sixth In- systemic rust, Melampsora hypericorum ranean-type climates in France. This area ternational Symposium on Biological (DC.) Wint., and the anthracnose fungus, provided some success, but showed up Control of Weeds, pp. 691-708. Colletotrichum gloeosporioides (Penz.) Penz. further weaknesses in our understanding Briese, D.T. (1986). Factors affecting the and Sacc. M. hypericorum is a monoecious of the system. The need to understand establishment and survival of Anaitis rust that has been described from Hyperi- agent behaviour became apparent with efformata, introduced into Australia for cum spp., including H. perforatum, in Eu- the demonstrated intolerance of Chryso- the biological control of St. John’s wort: rope (Gaumann 1959). Recently, a strain of lina beetles for shaded situations. Com- II. Field trials. Journal of applied Ecology the rust was found causing very heavy plexities of interactions between agent bi- 23, 821-39. damage to tutsan (H. androsaemum) in the ology and weather patterns and competi- Briese, D.T. (1991a). Demographic per- Otway Ranges of southern Victoria tive interactions between agents them- formance in the root-borer, Agrilus (Bruzzese and Pascoe 1992). This strain selves were found to have an influence. hyperici (Coleoptera: Buprestidae), a appears to have been introduced into Aus- The overriding importance of understand- biological control agent of St. John’s tralia illegally, but is highly-specific, fortu- ing the ecology of the target weed, par- wort. Biocontrol Science and Technology 1, nately from a quarantine perspective, but ticularly with respect to differences be- 195-206. unfortunate in that it does not attack H. tween the introduced and native ranges, Briese, D.T. (1991b). Current status of perforatum (E. Bruzzese personal commu- was realised. Such assessments have led to Agrilus hyperici (Coleoptera: nication). Given the ability of this rust to a continual refocussing of the characteris- Buprestidae) released in Australia in be an effective classical biological control tics required for an agent to successfully 1940 for the biological control of St. agent and reduce infestations of a conge- contribute to control of the weed under John’s wort: Lessons for insect intro- neric plant in so spectacular a manner, it Australian conditions. Control at last ductions. Biocontrol Science and Technol- may well be worth the investment to carry seems possible with established agents, ogy 1, 207-15. out European surveys for a strain of M. but should further introductions be neces- Briese, D.T. (1996). Biological control of hypericorum that is virulent against St. sary the types of agents required, and spe- weeds and fire management in pro- John’s wort. cies filling these requirements, have been tected natural areas: are they compat- Various strains of C. gloeosporioides have identified. In a more pragmatic sense, the ible strategies? Biological Conservation 77, been used as mycoherbicides against a program has mirrored the evolution in the 135-41. number of weeds (Templeton 1992) and way biological control technology is trans- Briese, D.T. and Jupp, P.W. (1995). Estab- Hildebrand and Jensen (1991) recently iso- ferred to the end-user; from massive col- lishment, spread and initial impact lated a strain in Novia Scotia, Canada, that lection and redistribution efforts by exten- of Aphis chloris Koch (Hemiptera: was causing natural mortality of an en- sion officers to selected properties (a linear Aphididae), introduced into Australia demic species of Hypericum as well as the flow in which the end-user is a recipient) to for the biological control of St. John’s introduced H. perforatum. Isolates of this the establishment of community-based wort. Biocontrol Science and Technology 5, strain have been subjected to preliminary networks, where the responsibility for 271-85. host-specificity testing at Keith Turnbull rearing and a level of monitoring resides Bruzzese, E. and Pascoe, I.G. (1992). Research Institute in Victoria, and found with the landholder (a feed-back system in Melampsora hypericorum, a rust fungus to not attack a small range of non-target which the end-user is a participant). There with potential in the biological control plants (Shepherd 1995). However, the has also been a philosophical shift in our of tutsan, Hypericum androsaemum. Pro- ability to produce symptoms on wound- view of the role of biological control, away ceedings of the First Weed Control inoculated tomatoes and senescing clover from the idea that natural enemies can by Congress, Volume 2, pp. 101-2. species suggests that release may not be themselves control the weed to the idea Campbell, M.H., Briese, D.T. and Delfosse, approved for safety reasons (McLaren et that introduced agents form part of a E.S. (1995). Hypericum perforatum L. In al. 1997). Attack levels on different range of control options that need to be ‘The Biology of Australian Weeds’, Vol- populations of Australian St. John’s wort integrated in order to develop effective ume 1, eds. R.H. Groves, R.C.H. Shep- also varied, as did the virulence of the fun- weed management strategies. Finally, the herd and R.G. Richardson, pp. 149-68. gal isolates (Shepherd 1995). Shepherd felt history of biological control of St. John’s (R.G. and F.J Richardson, Melbourne). that the fungus had the potential to act as a wort in Australia clearly demonstrates the Campbell, C.L. and McCaffrey, J.P. (1991). classical biocontrol agent as well as a importance of evaluating each step in a Population trends, seasonal phenology mycoherbicide. One particular character- biological control program as it is being and impact of Chrysolina quadrigemina, istic which makes it of interest is the fact carried out. C. hyperici (Coleoptera: Chrysomelidae) that spores can be dispersed by Chrysolina and Agrilus hyperici (Coleoptera: beetles (Morrison 1995, Jensen et al. 1996), Acknowledgments Buprestidae) associated with Hypericum which are the most abundant insects on St. Jean-Louis Sagliocco drew my attention to perforatum in northern Idaho. Environ- John’s wort in Australia. Such an interac- the potential of the sesiid moth as a control mental Entomology 20, 303-15. tion could lead to synergism between the agent. The work described here has been Clark, L.R. (1953). The ecology of two control agents and provide a novel supported by various bodies at different Chrysomela gemellata Rossi and C. delivery system for the pathogen. times, including the Reserve Bank of hyperici Forst., and their effect on 80 Plant Protection Quarterly Vol.12(2) 1997 St. John’s wort in the Bright District, Symposium on Biological Control of Wilson, F. and Campbell, T.G. (1943). Re- Victoria. Australian Journal of Zoology 1, Weeds, pp. 451-4. cent progress in the entomological 1-69. Jupp, P.W., Briese, D.T. and Cullen, J.M. control of St. John’s wort. Journal of the Clark, L.R. and Clark, N. (1952). A study of (1997). Evidence for variable suscepti- Council for Scientific and Industrial Re- the effect of Chrysomela hyperici Forst. bility of St. John’s wort to Aculus search 16, 45-56. on St. John’s wort in the Mannus Valley, hyperici. Plant Protection Quarterly 12, NSW. Australian Journal of Agricultural 67-70. Research 3, 29-59. Jupp, P.W. and Cullen, J.M. (1996). Ex- Clark, N. (1953). The biology of Hypericum pected and observed effects of the mite, perforatum L. var. angustifolium DC. (St. Aculus hyperici, on St. John’s wort, Hy- John’s wort) in the Ovens Valley, Victo- pericum perforatum, in Australia. Pro- ria, with particular reference to ento- ceedings of the Ninth International mological control. Australian Journal of Symposium on Biological Control of Botany 1, 95-120. Weeds, pp. 365-70. Currie, G.A. and Fyfe, R.V. (1938). The fate Lastuvka, Z. and Lastuvka, A. (1995). ‘An of certain European insects introduced Illustrated Key to European Sesiidae to Australia for the control of weeds. ()’, pp. 128-9. (Brno). Journal of the Council for Scientific and In- Mahr, F.A., Kwong, R.M., McLaren, D.A. dustrial Research 11, 289-301. and Jupp, P.W. (1997). Redistribution Currie, G.A. and Garthside S. (1932). The and present status of the mite, Aculus possibility of the entomological control hyperici. Plant Protection Quarterly 12, of St. John’s wort in Australia – Progress 84-8. report. Pamphlet of the Council for Sci- McLaren, D.A., Bruzzese, E. and Pascoe entific and Industrial Research No. 29, I.G. (1997). The potential of fungal 28 pp. pathogens to control Hypericum species Delfosse, E.S. and Cullen, J.M. (1981). New in Australia. Plant Protection Quarterly activities in the biological control of 12, 81-3. weeds in Australia. III St. John’s wort, Morrison, K.D. (1995). Potential for the Hypericum perforatum. Proceedings of biological control of St. John’s wort, Hy- the Fifth International Symposium on pericum perforatum, with an endemic Biological Control of Weeds, pp. 575-81. pathogen Colletotrichum gloeosporioides Gaumann E. (1959). Die Rostpilze and its vector, a leaf-feeding beetle Mitteleuropas mit besonderer Berück- Chrysolina hyperici: An integrated ap- sichtung de Schweiz. Beitrage für Krypto- proach. M.Sc. Thesis, Acadia University, gamenflora der Schweiz 12, 1407. Canada. Hancox, N.G., Syrett, P. and Scott, R.R. Shepherd, R.C.H. (1984). The present sta- (1986). Biological control of St. John’s tus of St. John’s wort (Hypericum wort (Hypericum perforatum) in New perforatum L.) and its biological control Zealand: A review. Plant Protection agents in Victoria, Australia. Agricul- Quarterly 1, 152-5. ture, Ecosystems and Environment 12, Hildebrand, P.D. and Jensen, K.I.N. (1991). 141-9. Potential for the biological control of St. Shepherd, R.C.H. (1995). A Canadian iso- John’s wort (Hypericum perforatum) with late of Colletotrichum gloeosporioides as a an endemic strain of Colletotrichum potential biological control agent for St. gloeosporioides. Canadian Journal of Plant John’s wort (Hypericum perforatum) in Pathology 13, 60-70. Australia. Plant Protection Quarterly 10, Huffaker, C.B. (1966). A comparison of the 148-51. status of biological control of St. John’s Templeton, G.E. (1992). Use of Colleto- wort in California and Australia. Mushi trichum strains as mycoherbicides. In 29 (supplement), 51-73. ‘Colletotrichum: biology, pathology and Huffaker, C.B. and Kennett, C.E. (1959). A control’, eds. J.A. Bailey, and M.J. Jeger. ten-year study of the vegetational (CABI, Wallingford, UK). changes associated with the biological Wapshere, A.J. (1984). Recent work in the control of Klamath weed Hypericum biological control of Hypericum perforatum L. Journal of Range Manage- perforatum (Guttiferae) for Australia. ment 12, 69-82. Entomophaga 29, 145-56. Jensen, K.I.N., Morrison, K.D. and Reekie, Wilson, F. (1943). The entomological con- E.G. (1996). Integrated biological con- trol of St. John’s wort (Hypericum trol of St. John’s wort (Hypericum perforatum L.) with particular reference perforatum L.): role of Chrysolina hyperici to the insect enemies of the weed in and a host-specific Colletotrichum southern France. Bulletin of Council for gloeosporioides in Atlantic Canada. An- Scientific and Industrial Research No. nual Meeting of the Weed Science Soci- 169, 87 pp. ety of America Abstract. Wilson, F. (1960). A review of the biologi- Jupp, P.W. (1996). The establishment of a cal control of insects and weeds in Aus- distribution network for the mite, Aculus tralia and Australian New Guinea. hyperici, to control St. John’s wort, Hy- Commonwealth Institute of Biological pericum perforatum, in Australia. Pro- Control Technical Communication No. ceedings of the Ninth International 1, 102 pp.