1 Appendix 2

Appendix 2. Suitability of Gargaphia decoris as a biocontrol agent for woolly nightshade in New Zealand

1. The woolly nightshade problem in New Zealand 2. Scope for biological control in New Zealand 3. Biological control against woolly nightshade in South Africa 4. Determination of the host range of Gargaphia decoris 5. Post-release effects on woolly nightshade in South Africa 6. References

1. The woolly nightshade problem in New Zealand

Distribution The native range of (woolly nightshade) is Argentina, Uruguay, Paraguay and southern Brazil. It is naturalised widely in the Pacific, Indian Ocean islands, India and several southern African countries, and is considered to be an agricultural and environmental weed in New Zealand, South Africa and Australia (ISSG 2006). It has been naturalised in New Zealand since about 1880. It is now abundant in all areas from Taupo northward, but is still uncommon in the Gisborne, Wellington and Tasman regions. It is present in Tasman and Nelson but is not yet regarded as a weed in the remainder of the South Island.

Woolly nightshade thrives throughout the northern parts of the Waikato Region and can be common in other areas. Dense stands occur in the Port Waikato area and on the Coromandel Peninsula. Plants inhabit bush margins, gardens, roadsides, ungrazed wasteland areas, wetlands, and banks of streams. A consistent theme of consultation (Appendix 1) was that woolly nightshade has not yet occupied its available habitat either latitudinally or within its existing range. Woolly nightshade appears to be extending its range southwards and becoming more common (Rahman & Popay 2001). Stanley (2003) records 54,000 of woolly nightshade in the Bay of Plenty Region, but states that 270,000 ha are at risk of invasion. It occupies 245,000 ha in the Auckland Region, but its available habitat is thought to be 345,000 ha (J. Craw ARC pers. comm., Appendix 1). In total, woolly nightshade is thought to occupy 453,000 ha of the Auckland, Waikato and Bay of Plenty regions (Appendix 1).

Biology The biology and ecology of woolly nightshade is well reviewed by Stanley (2003). It is a lowland tree that grows to around 10 m tall, to a stem diameter of 15 cm. Leaves are ovate and entire, 10–25 cm long and 5–10 cm wide, green above and whitish below, and covered with hairs. Leaves have a pungent smell redolent of kerosene. It is moderately tolerant to frost, shade and drought, but requires medium to high soil fertility. Berries are globose, dull yellow, and approximately 1 cm in diameter. Each fruit contains many seeds, and a single plant can produce up to 10 000 seeds annually. Most fruits fall beneath the tree, but the seeds of woolly nightshade are thought to be dispersed widely by birds and possums. Silvereyes and kereru (Hemiphaga novaeseelandiae) have been observed feeding on its fruit (in Stanley 2003), and it seems likely that exotic species such as blackbirds would also carry seeds. A pilot 2 Appendix 2 study by Stanley (2003) suggested that seeds remain viable in the soil for only a few years, but this varies between sites, and longevity may be long at some sites. Seedlings established in summer can bear flowers by autumn (NZPCN 2008). Woolly nightshade tolerates moderate shade, moderate drought (once established) and moderate frost to –5oC (Stanley 2003).

Pest characteristics Woolly nightshade is said to be poisonous, although reported incidences of actual poisoning in New Zealand are very difficult to find. Stanley (2003) reviews this evidence. The dust from the leaf hairs causes respiratory problems if exposure is prolonged, and handling the plants may cause skin irritation and nausea. The green berries contain toxins that could be poisonous, especially to children, although such poisonings have not been recorded. Woolly nightshade is an aggressively invasive and very fast growing plant. Most fruits fall beneath the tree, but plants fruit prolifically from the first year of establishment and viable seed is spread widely by birds. Once a seed source has established, seedlings from it can therefore establish over a wide area. Seedlings establish very quickly and can soon dominate poorly managed and neglected land. In New Zealand it seldom establishes in dense vegetation, but areas particularly at risk include native forest margins, scrub and shrubland areas including prime sites for native forest regeneration, amenity areas such as reserves, shelterbelts and farm woodlots, hill country grazing land, young pine plantations, woodlots, shelterbelts, waste spaces and open areas around urban gardens. Dense stands can overtake pasture, especially in hill country, and impede livestock movement. Woolly nightshade can quickly establish large, dominant stands of plants beneath which little else will grow, impacting plants and , and changing ecosystem structure. Invertebrate communities can be modified (in Stanley 2003). It has been observed that dense woolly nightshade infestations commonly lack understorey plants. This may be because of allelopathic effects (Florentine & Westbrook 2003; van den Bosch et al. 2004), or simply because shading from the large leaves of woolly nightshade preclude successful germination of seedlings. Whatever the reason, while a continuous canopy of woolly nightshade exists, no regeneration of native vegetation can occur in forest margins and gaps. Woolly nightshade produces large numbers of seeds, which have 95% viability. Three-year-old plants have been recorded bearing 10 000 seeds. Seed is spread by birds, but most falls close to the parent. Although woolly nightshade is relatively short lived, the seed bank ensures that woolly nightshade has a strong tendency to replace itself (Bruce Clarkson, pers. comm.).

Where it becomes a dominant land cover, the productivity of the land may be severely reduced, and cultural and traditional values associated with a significant area may also be damaged. Affected parties include private land occupiers, groups responsible for managing significant areas, reserves and roadsides and the general community, which may access significant areas for recreational activities.

Current regulatory requirements It is illegal to sell, propagate, or distribute any parts of woolly nightshade in New Zealand (NPPA 2008).

Regional Pest Management Strategies (RPMS) govern how woolly nightshade management is conducted, and strategies vary between the regions in which it grows. 3 Appendix 2

For example, it is not listed in the pest management strategy for Tasman–Nelson at all, and while woolly nightshade is abundant in Taranaki, the regional council has no rule requiring its destruction; any control is voluntary. Greater Wellington Regional Council ensures that woolly nightshade is totally controlled at all known sites with a view to eventual eradication from the region. It is currently limited to 14 sites, 12 of which have been inactive for several years. Eradication of woolly nightshade from this region is possible (Greater Wellington Regional Council 2008). The weed has limited distribution in Gisborne, and eventual eradication is planned there also. Currently it is landholders’ responsibility to control all woolly nightshade plants on their land. Some regional councils require mandatory removal of all plants from properties at the expense of the occupier, or participation in organised programmes (Hawke’s Bay, Bay of Plenty, Manawatu–Wanganui, parts of Waikato, Auckland and Northland,), while others require clearance from boundaries only (parts of Waikato, Auckland and Northland). Requirements under the RPMSs bind corporate and crown land managers (including DoC and forestry companies) as well as individual occupiers.

Table 1. Rules for management of woolly nightshade in regional pest management strategies, and direct costs borne by regional councils

Region Treatment rule Direct annual council expenditure Northland Assistance with community $10,000 (estimate) projects Auckland 1. Occupier control, 2. boundary $260,000 clearance Waikato Mandatory control by occupier $39,600 Bay of Plenty Progressive control by occupiers $171,488 Horizons Mandatory control by occupier $16,360 Hawke’s Bay Eradication by council $20,000 Gisborne Eradication by occupier No estimate Taranaki Voluntary control by occupier No estimate Wellington Eradication by council $6,340 Tasman/Nelson Not designated pest $4,500

Current control methods Details of control methods can be found at http://www.ew.govt.nz/Environmental- information/Plant-and--pests/Plant-pests/Woolly-nightshade/ Where infestations are accessible, and resources allow, woolly nightshade can be successfully controlled by conventional means. Ground disturbance often leads to seedling germination. Plants up to 60 cm tall can be pulled. Taller plants can be cut, and the stumps treated to minimise regrowth. Stanley (2003) also reviews control techniques.

The benefits and costs of woolly nightshade Consultation with regional councils and tāngata whenua indicates that woolly nightshade has no known beneficial attributes or value (Appendix 1). 4 Appendix 2

Woolly nightshade causes non-monetary adverse effects to ecological values in native ecosystems, and to societal well-being in urban environments. It reduces the value of production in pastoral agriculture and forestry, and imposes monetary costs for control.

Woolly nightshade has an Owens score of 24 for ‘biological success’ and ‘effect on ecosystems’ (C. West DoC pers. comm.), and Timmins and MacKenzie (1995) record it as a plant of medium threat to biodiversity values. However, there is virtually no quantitative assessment of the adverse effects of woolly nightshade on plant community dynamics (Van den Bosch 2006). The effects on native ecosystems are not well known (Carol West, DoC, pers. comm.,). Some believe that infestations in forest margins will be out-shaded over time by regenerating native vegetation, while others think that it will replace itself and continue to dominate infested land for a long period (Wendy Mead, Environment Waikato, Bruce Clarkson, University of Waikato, pers. comm., Appendix 1). It is still spreading into un-infested areas. Its management is not considered to be a high priority relative to other weeds although the vulnerability of uninfested areas such as offshore islands or Whanganui National Park are acknowledged (Graeme La Cock, Paul Cashmore, pers comm., Appendix 1). Local authorities invest heavily in woolly nightshade control on reserved land. No information was provided during consultation on the costs of controlling woolly nightshade on the conservation estate.

Woolly nightshade invades poorly or less intensively managed pastoral land, especially hill country areas. It currently infests over 450,000 ha in Bay of Plenty, Waikato and Auckland regions alone, but the breakdown by habitat type is not known. The area of potentially productive pastoral land currently occupied is uncertain. It is also unclear how much infested land would be returned to productive use should biological control of woolly nightshade be successful. The value of lost production cannot be estimated accurately (see Section 7.4.2.1).

Woolly nightshade has spread widely over the upper North Island in the last 10 years, and affects plantation forestry in 3 ways:

1. Woolly nightshade can compete for nutrients and light with young crop trees, although there is little if any data to quantify its impact. If uncontrolled, the weed can hamper growth rate so that it takes three years for a tree to grow 2m (Peter Houston, pers. comm., Appendix 1). Standard site preparation techniques such as over-sowing with grasses and legumes, pre-plant spraying and follow-up spot treatment can control the weed at establishment, at least at some sites (Richard Grimmett, pers. comm., Appendix 1).

It appears that woolly nightshade is sufficiently shade tolerant to accumulate beneath mature plantations. Although experience is limited as yet, the costs of re- establishment of pine seedlings in such forests following harvest could increase due to the hindrance of dead standing trees (Steve Couper, pers. comm., Appendix 1). In one forest where the weed is endemic, the extra costs have been estimated at $15,000 per annum, a massive increase over control requirements to date (Elaine Birk, pers. comm., Appendix 1).

5 Appendix 2

2. Once established, woolly nightshade forms a significant hindrance to silvicultural operations such as thinning, which substantially increases forest management costs (Elaine Birk, pers. comm., Appendix 1). It also grows prolifically on roads and road edges, inhibiting access for harvest and requiring costly spray operations.

3. Forestry companies are required to comply with Regional Pest Management Strategies. This may require the removal of plants from boundaries and public roadsides, or in some regions, more stringent requirements. All require expenditure for which there is no economic return.

It is difficult for foresters to differentiate the expenditure targeted specifically at woolly nightshade management in forests from control costs for other weeds. Just three estimates were obtained during consultation on this proposal. The control of 300ha of woolly nightshade in one region cost $86,000 (Peter Houston, pers. comm., Appendix 1). One company intend to spend over $8,500 on woolly nightshade management this year. In the 4 years 1998 to 2001, Fletcher Challenge Forests spent $92,453 on woolly nightshade control in the 109 ha Welcome Bay Forest alone (Dave Lowry, pers. comm. in Stanley 2003). This level of expenditure impacted on the economics of forestry on that land.

The rules for management of woolly nightshade for the public good protection of environmental and production values are set by regional councils in regional pest management strategies. The costs of that management are allocated to stakeholders differently from region to region (see above), and so it is difficult to estimate regional expenditure. For example, Greater Wellington Regional Council provides ‘service delivery’ to destroy woolly nightshade at all known sites (Table 1, and so the annual cost of $6,340 is well-documented (Wayne Cowan pers. comm., Appendix 1). However, in other regions, responsibility for management (whether boundary or total control) lies largely with occupiers, and the collective costs incurred are poorly known.

Consultation with regional councils (Appendix 1) revealed that the direct costs incurred by eight regional councils in the last year for management of the weed on their own land, land inspection, and provision of advice totals $528,000 (Table 1). However, for most of those regions, the cost of compliance with the RPMS lies with the occupier. John Mather (EnvBOP pers. comm., Appendix 1) estimated land/owner/occupier expenditure in the Bay of Plenty region at $240,000 annually.Jack Craw (ARC pers. comm., Appendix 1) reported that the ARC itself treated 500 ha of woolly nightshade last year at a cost of $60,000, but estimated that occupiers, including DoC, treated an additional 30,000 ha. If the control methods and costs are equivalent to those used by ARC, then the cost to occupiers of treating woolly nightshade in the Auckland region would be $3.6m. In addition, land managers such as Ontrack, DoC and Transit New Zealand are required to clear boundaries and verges to comply with the RPMS, and the cost for the region was estimated at $50,000.

District and City Councils also undertake woolly nightshade management in reserved areas, roadsides and other land. These costs have not been estimated, but are likely to be larger than the direct costs of Regional Councils. For the Auckland region, the annual cost to territorial authorities of woolly nightshade control has been estimated at 6 Appendix 2

$80,000 (J. Craw, ARC, pers. comm., Appendix 1). In total, for the Auckland region alone, the annual cost of treatment of woolly nightshade is estimated to be $4million. This is consistent with the summarised cost benefit analysis prepared in 2000 for the Auckland RPMS 2002-2007 (ARC 2001).

Woolly nightshade was the subject of an eradication campaign in the Bay of Plenty region between 1991 and 2003. The total cost of management to the council and to landowners/occupiers has been estimated at $6,000,000 (J. Mather, Env BOP pers. comm., Appendix 1). This has since been modified to a ‘progressive control’ strategy (Stanley 2003).

Cost benefit analyses for woolly nightshade have been conducted as part of the process for developing regional pest management strategies. For example, in the Auckland Region this analysis stated that without intervention, the total NPV of the ‘no control’ scenario was $24,000,000.

2. Scope for biological control in New Zealand The prospects for biological control of S. mauritianum in New Zealand were first summarised by McGregor (1999). Winks et al. (2001) surveyed the invertebrates and fungi associated with woolly mightshade in New Zealand and concluded that no herbivore niches were fully utilised, which offers considerable scope for the introduction of specialised invertebrates as control agents without significant competition from resident species. Similarly, while fungi were ubiquitous in woolly nightshade tissue, the weed did not support a particularly diverse fungal community. They recommended that a classical biological control programme should proceed in New Zealand, that the programme already in existence in South Africa should be reviewed to identify the invertebrates of most value for use in New Zealand, and that host-specific invertebrates chould be introduced following safety-testing. They also concluded that the best approach to the development of a successful biological control programme in New Zealand was to collaborate with South African researchers already actively engaged in such research.

Winks et al. (2001) also surveyed the fauna of predatory on S. mauritianum foliage at 14 sites from Kerikeri to Collingwood that might influence the success of biocontrol agents in New Zealand. Spiders were considered to be common at all sites. Six species of ants were recorded overall, but there were no ants at 25% of sites, no site had more than one species, and five species occurred in only low numbers. Argentine ant (Lipothema humile (Mayr)) was recorded at two sites, and this aggressive species could adversely affect any control agent introduced against woolly nightshade. Otherwise, the initial predation pressure from ants could be expected to be low. Only one mirid bug (Sejanus albisignatus (Knight)), which is known to be predatory, was encountered, and only at two of the 14 sites. Ten species of coccinellid ladybirds were encountered, but the only common species were two specialist predators of mites. Despite the apparent lack of predator diversity and abundance, Winks et al. (2001) stated that the combined effect of these generalist species could inhibit the effectiveness of some potential lepidopteran biocontrol agents (i.e. Gargaphia decoris Drake (, ). This may overestimate the predation risk in New Zealand as G. decoris adults actively defend their young 7 Appendix 2 against predators where diversity and abundance of predatory species is relatively low. No better estimate of predation risk can be made.

Tanybyrsa cumberi (Drake) is the only native true tingid species known in New Zealand (Larivière & Larochelle 2004). It occurs in native habitats over a similar geographic range to woolly nightshade, and is thought to feed on Astelia species. May (1977) observed the emergence of an unidentified mymarid wasp from the eggs of T. cumberi. Neither the host-specificity nor the ecological significance of this wasp is known, and its possible effect on population dynamics of the woolly nightshade lacebug cannot be assessed.

The areas in which S. mauritianum causes problems in South Africa tend to be much warmer than New Zealand. The indicative daily temperatures of the colder sites at which G. decoris has established tend to be comparable with warm New Zealand climates (Table 1). This raises the questions: Can G. decoris survive New Zealand winters? Are summer temperatures in New Zealand sufficient to allow the build- up of damaging populations? Cold winter temperatures were originally suspected of suppressing tingid population growth rates and limiting establishment in cooler climates in South Africa. However, temperature-tolerance trials have revealed that populations from both provenances are cold tolerant. (Hope and Olckers 2008) measured lower lethal temperatures, and probit analysis yielded a LT50 of −9°C for the Argentinian population and −10°C for the Brazilian population. They concluded that the Brazilian population was more cold tolerant than the Argentinian population, but that minimum temperature extremes were not the reason why establishment of G. decoris had failed at many release sites. It is unlikely that G. decoris would encounter such winter temperatures in areas of New Zealand infested with S. mauritianum.

Barker and Byrne (2005) also showed that Brazilian stocks were the more active at low temperature, and it is this provenance that has established at sites in the colder inland regions of KwaZulu-Natal (Table 1). In fact, the rate of establishment of the population of Argentinian provenance along warmer coastal regions has been poorer, but this may be the result of differential predation pressure between the regions (T. Olckers pers. comm.). In mid-2008, G. decoris was discovered at a number of sites that were previously written off as non-establishments, and was found beyond release sites for the first time (T. Olckers pers. comm.). As yet, damaging outbreaks such as that observed near Sabie (see below) have not been found at these sites. The populations crash in winter and it is late in the growing season before populations recover to peak levels. Whether slow population increase is a function of temperature or predation pressure is not known.

Table 1 Mean daily temperatures in selected New Zealand sites and two cooler sites in South Africa at which G. decoris has established Mean daily max. Mean daily min. New Zealand warmest month coldest month Kaitaia Observatory 23.9 8.6 Kerikeri 24.4 6.6 Dargaville 23.9 6.9 8 Appendix 2

Auckland Albert Park 23.8 8 Tauranga airport 23.9 5 Rotorua airport 23. 3.1 Taupo 23.3 2.2 Hamilton, Ruakura 23.8 3.8 Taumarunui 24.6 2.4 New Plymouth airport 21.8 5.5 Masterton, Waingawa 24 3 Gisborne airport 24.9 4.5 Napier, Nelson Park 24.4 4.4 Palmerston Nth 22.4 4.6 Wellington, Kelburn 20.3 6.2

South Africa Howick, Shafton plantation 25.2 4 Ixopo, Kia ora farm 26.2 6.2

Solanum mauritianum occurs over a very wide geographic and climatic range in South America, including warm-temperate and tropical regions. Countries where the weed occurs in colder climates, e.g. South Africa and New Zealand, have an opportunity to source agents from similar areas, e.g. the southern States of Paraná and Rio Grande do Sol in Brazil. Landcare Research is already working in this region while developing biological control agents for Tradescantia fluminensis Vell. (S. Fowler pers.comm.). The inaccessibility of the native range of suitably adapted agent populations should not therefore limit establishment success in New Zealand.

No summary climate records exist, but the area of South Africa where the current outbreak has been recorded is probably warmer than most if not all areas of New Zealand. The agent has not reached such population levels in areas with climates similar to those in New Zealand. At this stage it is not possible to say whether the outbreak at Sabie is a consequence of this climatic difference, or whether there is simply a time lag between climatic regions in achieving these levels. G. decoris seems to prefer shaded sites as opposed to plants growing in full sun, so forestry and natural forested areas of New Zealand should be well suited for this (T. Olckers pers. comm.).

3. Biological control programme against woolly nightshade in South Africa In South Africa, the plant invades riparian zones, forestry plantations, natural forest, agricultural lands, urban open space and any other disturbed areas (e.g. along roadsides, power lines), particularly in eastern, higher rainfall regions of the country (Henderson 2001). Its success as a weed in South Africa has been attributed to heavy seed-set and long-distance dispersal of seeds by fruit-eating birds (Olckers 1999).

9 Appendix 2

A biological control programme has been in progress in South Africa since 1984 (Olckers 1999, 2009), and the programme has been continuous since 1994. Support for this project in South Africa has been reinforced by promising progress in the biological control of white-edged nightshade and sticky nightshade (Solanum elaeagnifolium and S. sisymbriifolium), which are closely related to woolly nightshade (Olckers et al. 1999). Fifteen agents that attack woolly nightshade have been imported into containment in South Africa for further assessment, but the only control agent to have been released there so far is the lace bug Gargaphia decoris. Permission to release the flowerbud weevil (A. santacruzi Hustache) has been obtained recently.

Other species are under consideration. Olckers et al. (2002) list the insect herbivores associated with species of Solanum in north-eastern Argentina and south-eastern Paraguay, and Pedrosa-Macedo et al. (2003) list the phytophagous arthropods associated with S. mauritianum in Brazil. Olckers (1999) lists 15 of those species that have since been introduced into containment in South Africa since 1984 for evaluation of both effectiveness and safety. Since 1994, this research has been prioritised according to the potential role that those agents might play in limiting the success of S. mauritianum in South Africa (Table 2). The highest priority was given to species that could limit seed set and dispersal, and the flowerbud-feeding weevil Anthonomus santacruzi Hustache was selected for development. Difficulties in culturing and testing this weevil led to the concurrent development of agents with high potential reproductive rates and the ability to generate defoliation and premature leaf-fall, including the leaf-feeding G. decoris, which was the first agent selected for this role. G. decoris has since been released (Olckers 2000), and release of A. santacruzi (Olckers 2003) has just been approved. Several agents are still under consideration, but most of the species listed by Olckers (1999) have been rejected as agents either because the laboratory host-range was too wide to allow release under South African regulations, or because of an inadequate climatic match.

Despite their unsuitability for release in South Africa, the oligophagous nature of some of the agents identified by Pedrosa-Macedo et al. (2003) may permit their use in countries such as New Zealand that have depauperate Solanum floras or where cultivated Solanum species, notably S. melongena, have low economic status (Olckers 2007). Published records and subsequent field surveys in Argentina, Brazil and Paraguay (Olckers et al. 2002; Pedrosa-Macedo et al. 2003) confirm that the stem- boring Nealcidion bicristatum (Bates) (Coleoptera, Cerambycidae) and leaf- sucking lace bug Corythaica cyathicollis (Costa) (Hemiptera, Tingidae) are not sufficiently host-specific for release anywhere in the world. However, others may well be, including the leaf-mining moth, Acrolepia xylophragma (Meyrick) (Lepidoptera, Acrolepiidae), which causes blotch mines that destroy the leaves of young plants growing in shady habitats, and the flea beetle, Acallepitrix sp. nov. (Coleoptera, Chrysomelidae), larvae of which mine in the leaves of woolly nightshade causing premature leaf abscission (Table 2; Olckers 2007). A range of other species have been actively considered as potential control agents for S. mauritianum in South Africa, and could be considered for release in New Zealand (Table 2). Other options may also exist (Pedrosa-Macedo et al. 2003).

Five species of leaf-feeding of the genus Platyphora Gistel (Coleoptera, Chrysomelidae) were introduced into containment in South Africa for evaluation in 1994. These highly specialised species appear to have very narrow host ranges in the 10 Appendix 2 field, but as with many of the potential agents listed in Table 2, their laboratory host ranges were considerably broader and included eggplant, potato and several native Solanum species (Olckers, 2000). Although these results may well be laboratory artefacts, all five Platyphora species were rejected because their sensitivity to food quality and microhabitat made them unlikely to establish widely under South African conditions. These beetles prefer the softer foliage of small plants, seedlings and coppice of S. mauritianum growing in cool, moist and shaded habitats (e.g. plantations, forest margins and clearings) (Olckers 2000). Although the beetles did not appear to cause extensive damage to their host in South Africa (unlike the heavy damage of chrysomelids that control S. elaeagnifolium there) these species could be considered for introduction and evaluation in New Zealand, where the conditions may be more suitable than in South Africa (T. Olckers pers. comm.).

In summary, despite the questions posed above, experience in South Africa has provided more information about these control agents than is normally available when evaluating novel biocontrol agents. Recent observations (see below), coupled with the extensive information regarding the susceptibility of non-target species, suggest that G. decoris is a valid candidate as a biocontrol agent for S. mauritianum in New Zealand. However, as with all biological control projects, especially against as resilient a target as S. mauritianum, it is unlikely that a single agent will provide adequate control.

The priority for South African researchers has been to limit the development of seed banks, the colonisation of new sites, or the reinvasion of sites where control has been achieved by the development of agents that will limit the dispersal of seed by frugivorous birds. This approach is equally valid in New Zealand. New Zealand has the opportunity to take advantage of the host-range testing of Anthonomus santacruzi that has already been completed in South Africa. However, Olckers (2007) has pointed out that the related A. morticinus may be an alternative, although host-range tests for this species have barely begun. There are indications this species may have the capacity to build to higher population density than its sister species and therefore may be a more effective agent, but this is speculation at present. The agents co-exist in South America, and may have complementary rather than competitive biology.

South African researchers have rejected several potential agents because the host- range of these species was too wide to allow introduction under South African regulations, or because the biology of the species was incompatible with the microhabitats infected by S. mauritianum in South Africa. These conclusions have been drawn specifically for South African conditions, and do not necessarily apply in New Zealand. Olckers (2007) nominates several species that have considerable potential for development as control agents in New Zealand. A number of control agents other than G. decoris therefore appear to have promise for use as control agents in New Zealand.

4. Determination of the host range of Gargaphia decoris Research into the host range of G. decoris first began in South Africa in 1995, and has been the subject of several research papers and reviews. This research is reviewed here, and the original data can be found in the papers presented with the application.

11 Appendix 2

Biological control of of Solanum species poses particular challenges for researchers. New Zealand has only three native species in this genus, S. aviculare, S. laciniatium and S. americanum, but the genus contains a number of vegetable and fruit species that are important in New Zealand, including potato (S. tuberosum) and eggplant (S. melongena). More recently other species have been transferred into the genus Solanum, including tomato (now S. lycopersicum) and tamarillo and pepino (formerly Cyphomandra betaceum and C. muricatum). Assessing the risk to native plants is therefore relatively simple, but the ‘margin of error’ for assessing risk of non-target attack on these economically important species is low. There are other exotic woody Solanum species naturalised in New Zealand, but most are considered minor weeds.

Laboratory tests designed to evaluate the likely field host-range were conducted in South Africa before G. decoris was released there. Plants tested included cultivated species from nine plant families, species from six genera belonging to the Solanaceae, and a range of Solanum species both native and exotic (Olckers 2000). These showed that G. decoris could not survive or reproduce when fed plants outside the genus Solanum, including related crop plants such as cape gooseberry and capsicum. However, these laboratory tests also indicated that G. decoris colonies could survive on species within the genus Solanum other than the target plant, including cultivated eggplant (aubergine) and at least five native South African Solanum species. However, when tests were refined to take account of the full range of discriminatory abilities of the bug, Olckers (2000) concluded that G. decoris displayed very strong feeding and oviposition preferences for the target plant over all test plants. Analyses of the risk of attack on non-target Solanum plants indicated that, with one possible exception, none were likely to suffer more than incidental damage in the field (Olckers 2000; Withers et al. 2002). Olckers (2000) found that eggplant could sustain development and oviposition of G. decoris, but it was a poor host. The number of eggs laid on eggplant in tests was only 5% of that laid on woolly nightshade controls. Eggplant was not used at all when the true host was present. Control agents for other Solanum weeds have been released in South Africa despite similar ambiguous pre- release test results on eggplant, and no attack has been recorded on eggplant since these species were released (Olckers et al. 1995).

Based on these laboratory studies, and in light of previous experience, Olckers (2000) concluded that G. decoris was sufficiently safe to release in South Africa. The results of this study were accepted by the regulatory authorities in South Africa and this bug was released there in February 1999 (Olckers 2000). This conclusion is supported by field observations from South America, where G. decoris has not been recorded on any Solanum species other than S. mauritianum. Surveys at the original release site failed to record the non-target feeding that was observed in the laboratory trials, justifying the decision to release the lace bug in South Africa so far (Olckers & Lotter 2004). However, the rate at which lace bug has encountered non-target hosts is low as yet.

Gargaphia decoris has no pest status, but two related species, G. lunulata Mayr and G. torresi Lima, are pests of vegetable crops such as pumpkins, spinach, beans and sweet potatoes in South America (in Olckers 2000). Several of these plant species were tested, but were not attacked by G. decoris (Olckers 2000).

12 Appendix 2

Withers (2002) undertook a critical review of the research undertaken in South Africa to ensure that the methodology employed was rigorous, and that the list of plants tested was adequate to assess the economic and environmental risks that G. decoris might pose in New Zealand. She felt that the methods were appropriate to the biology of the agent, but that further work should be undertaken to check whether nymphs hatching from eggs laid on test plants could develop there. She concluded that the testing was adequate to show that New Zealand Solanum species would be at negligible risk from G. decoris, but recommended that there should be more detailed research into the risk posed to common eggplant cultivars grown in New Zealand, and to the minor fruit crops pepino and naranjilla, S. quitoense (Withers 2002).

At the request of Landcare Research, the three Solanum species native to New Zealand were tested in South Africa. The results of these tests were reported by Withers et al. (2002). Neither S. laciniatum, S. aviculare (poroporo) nor S. americanum (small-flowered nightshade) supported feeding by nymphs or adults of G. decoris in no-choice tests. S. pseudocapsicum, a weed known as Jerusalem cherry in New Zealand, was also tested, but did not support development. When given a choice of plants species, 97% of placed in tests had left other plants and sought out woolly nightshade within 72 hours.

The additional research recommended by Withers (2002) has since been completed in a well-executed and well-reported study by Borea (2006), and is about to be published (Olckers & Borea 2009). Four cultivars of S. melongena (eggplant) that are commonly grown in New Zealand (namely ‘Violet Prince’, ‘Black Beauty’, ‘Louisiana Long Green’ and ‘Japanese Long’) were sent to South Africa and grown there, as was S. quitoense (naranjilla) and S. muricatum (pepino dulce). The objectives were to determine the host specificity of G. decoris in relation to New Zealand native and cultivated Solanum species and to quantify the risks to these non-target Solanum species. The host range of G. decoris was determined through both nymphal and adult no-choice tests, adult multi-choice tests, and open-field trials. The test species included one native New Zealand Solanum species (S. aviculare) and six agriculturally important Solanum species including four different cultivars of S. melongena (eggplant). The physiological host range of G. decoris was expected to extend beyond S. mauritianum and this was demonstrated by some non-target plants that supported feeding, development and oviposition in no-choice tests. In contrast, the ecological host range of the insect was expected to be restricted to S. mauritianum and this was verified since G. decoris rarely fed, and did not oviposit, on any of the non-target plants in the choice tests and open-field trials. The calculated risk assessment further proved that G. decoris poses no threat to New Zealand native plants, and little to cultivated Solanum species, including eggplant. Based on the host- specificity tests and the environmental threat posed by the weed, G. decoris should thus be suitable for release in New Zealand. Hill (2007) also reviewed the evidence for host-specificity but reached no new conclusions.

In summary, analysis of the potential economic, environmental and social risk posed by the introduction of G. decoris to New Zealand is complicated by the close relationship between the target host and a range of important crop species. However, comprehensive host-range testing indicates that the risks to these species are low. Of the species tested, S. melongena (eggplant) appeared to be the most at risk. The likelihood of adverse effects from populations persisting on this crop in New Zealand 13 Appendix 2 is considered low because tingids reproduced poorly when fed on this host. The national value of the crop in New Zealand is $1–1.5m, of which approximately 17% is produced under glass. This is a difficult crop to grow in New Zealand, and standard pesticide regimes designed to control existing pests would also control G. decoris. There is some organic production (S. McArthur, Vigour Seed Company, pers. comm.). For these reasons the magnitude of the potential effects of G. decoris introduction on eggplant production in New Zealand are also considered to be small. Overall, the potential economic, environmental and social risks are considered to be low.

The populations of G. decoris used in South Africa were collected from sites that are several hundred kilometres apart. South African researchers are currently testing the comparative host ranges of populations sourced from Argentina and Brazil. This work is not yet completed, but from initial results no differences are expected. The host range testing already completed is therefore adequate to estimate the risk to non-target species in New Zealand (Withers 2002; Withers et al. 2002; Borea 2006; Olckers & Borea 2009).

5. Post-release effects of Gargaphia decoris on woolly nightshade in South Africa Gargaphia decoris was first imported to South Africa from Iguazu Falls, Argentina, in 1995. The insects released from 1999 to 2001 were progeny of this colony. In 2002, a second colony was established from material collected on the First Plateau of Paraná in southern Brazil (Pedrosa-Macedo et al. 2003). This area is cooler than Iguazu Falls, and has a similar climate to the warm-temperate regions in South Africa where S. mauritianum is most invasive. Releases have been made in five South African provinces, with establishment so far confirmed in KwaZulu-Natal, Limpopo and Mpumalanga.

It is now 7 years since G. decoris was first released in South Africa and populations derived from both provenances have established. The insect proved difficult to establish in the first instance, with many early releases failing to establish (Olckers & Lotter 2004). However, observations in 2006–2007 have revealed many established field populations in close proximity to some of the release sites, even ones where releases were deemed to have failed. This suggests that establishment success may well be higher than the 18% of sites reported from KwaZulu-Natal Province, where over 148 000 insects were released at 32 sites (Lotter 2004).

14 Appendix 2

Gargaphia decoris adults

Preliminary trials indicated that 2–4 weeks of sustained herbivory by tingids reduced the leaf, stem and root biomass of potted S. mauritianum plants, with damaged plants containing 33% less biomass than undamaged controls (T. Olckers unpubl. data, pers. comm., see Appendix 1). Until recently damage to weed populations in the field has been only moderate because lace bug populations have remained at low densities and have mostly not reached the high densities needed to inflict severe damage. Whatever the reason, G. decoris has not been regarded as a wholly reliable prospect for successful control of the weed in South Africa, or elsewhere.

In April 2007, an outbreak of G. decoris (of Argentinian provenance) was reported from an invaded forestry plantation near Sabie, in Mpumalanga Province (in NE South Africa). Site-specific climate data are not available, but conditions at the site are thought to be subtropical, with summer rainfall. Observations revealed that large numbers of adults and nymphs had caused severe damage to the S. mauritianum population, which was manifested by extensive and sometimes total defoliation, an absence of fruit and flowers, and even mortality of seedlings and larger trees.

Dr A. Witt of the Plant Protection Research Institute describes the site as follows: ‘What appears to happen is that a gravid female (or females) arrives within a patch and obviously lays eggs. This nucleus then starts growing outwards in more or less a concentric circle. Over time and at any one time you then end up with three zones in a plantation:

1) Centre zone where the females first arrived or where the outbreak started – the plants have lost all of their leaves and depending on the time of the outbreak have no or hardly any flowers or fruit. They have started re-sprouting and they tend to have more new shoots than on unaffected plants – plants tend to push out more lateral shoots if the terminal shoots get damaged. The great thing is that even the leaves on the new shoots had adults and some nymphs on them so they may just be pushed over the edge. We also predict that leaves on these plants will be smaller.

15 Appendix 2

2) Zone just outside of this is much narrower and is more of a transitional zone – plants have lost all or most of their leaves and have no new shoots yet. They look dead but will start putting out new shoots soon – no adults or nymphs in this zone.

3) The next zone falls just outside this and is much wider. In this area the bugweed plants still have most of their leaves but a very large percentage of them are chlorotic. Gargaphia numbers in this zone are very high. We never found plants outside of this zone with no Gargaphia but may have found some had the plantation block been a whole lot bigger.’

Monitoring of the site is in progress to determine whether this damage is an episodic event or will be sustained over time, and to quantify the impact on the weed population. Similar outbreaks have been reported elsewhere in the immediate area.

Adults and young on a leaf of S. mauritianum

Chlorosis caused by G. decoris 16 Appendix 2

It is unclear why similar outbreaks have not been observed at sites where the tingid is established elsewhere in South Africa, and how this relates to its potential as a control agent in New Zealand. Predation of the eggs and early nymphal instars by several generalist predators has been observed and may well limit population increases, but this effect has not yet been quantified.

In South Africa, S. mauritianum plants support high numbers of generalist predators, notably ants, ladybirds and mirid bugs. A number of these species attack G. decoris and although the adults patrol the young, the eggs and aggregations of early instars appear to be most at risk (T. Olckers and M. Byrne pers. obs.). Several of these prey on the eggs and early nymphal stages of G. decoris and are believed to be reducing their impact in the field. Ants in particular are a major problem (even affecting production in mass-rearing facilities) and can decimate small populations. Ladybirds are also capable of destroying egg batches and aggregations. However, the most effective predators appear to be two species of mirid bug (Miridae).

Until recently the effectiveness of G. decoris as a biological control agent for S. mauritianum in South Africa (and by extension its potential value its New Zealand) was under question, but sentiment has changed. The proportion of South African sites at which tingid populations established was originally thought to be relatively poor, despite very large releases of tingids between 1999 and 2001. However, surveys conducted in the last year suggest that tingids were indeed present at many of these sites, but that populations have only recently grown sufficiently large to be detected. Populations sourced from both Argentina and Brazil appear to have established across a range of habitat types. The value of the agent was also questioned because even at sites where tingids established early, populations had not grown large enough to cause noticeable damage to the target weed. The recent observations in the Sabie region now demonstrate that G. decoris populations can reach high density on leaves, sufficient to cause significant defoliation to S. mauritianum across large areas.

Large plants like woolly nightshade have sufficient root reserves to tolerate occasional defoliation, as its ability to regenerate from cut stumps following mechanical clearance demonstrates. Questions still remain about the future efficacy of this agent. Will the high populations of tingids observed at Sabie now persist, so that regenerating foliage is attacked again and again, or will the outbreaks be episodic, allowing the plant to regain its growth rate and reproductive ability between attacks? Are the outbreak populations near Sabie a forerunner of similar events across the South African range of woolly nightshade as populations build or is this a local phenomenon? Now that we know that high densities of G. decoris can occur at Sabie, what limits the development of large populations elsewhere? In any event, interest in G. decoris as a potentially valuable control agent has been renewed by this recent outbreak and the agent may well have more potential than previously thought.

In late 2007 a massive fire completely destroyed the infestation of woolly nightshade at Sabie, and the damaging G. decoris population with it. This has brought to a close the long-term damage monitoring research at the site.

The predatory fauna of continental areas such as Australia and South Africa is diverse, and predators have been implicated in the relative failure of a number of 17 Appendix 2 biocontrol agents. Against the background of this experience (but without the benefit of detailed population dynamics studies), South African researchers have attributed the slow population increase of G. decoris in South Africa to general predation. The generalist predatory fauna found in non-native habitats in New Zealand is considered to be depauperate by comparison, and (with the obvious exception of the failure of gorse spider mite as a control agent as a result of predation by other mites) predation is not normally considered to be a critical limiter of agent performance in New Zealand (S. Fowler, pers. comm.). It is difficult to predict whether the introduction of a G. decoris into New Zealand will restructure the resident predator fauna, or whether a numerical response will adversely affect the population dynamics of the agent. However, there is also no reason to assume that it will.

There appears to be no reason why the Brazilian strain established in South Africa, or a similar provenance collected in Brazil, should not establish in New Zealand.

Table 2. South American insects introduced into containment in South Africa for consideration as biocontrol agents for Solanum mauritianum. This table is reproduced verbatim from an upcoming book chapter (Olckers 2007).

Insect species Year Origin Damage Outcome Agents that reduce photosynthetic area Corythaica cyathicollis (Costa) 1984 Argentina Sap-sucking Rejected; crop pest (Tingidae) Acrolepia xylophragma 1984– Argentina Leaf-mining Rejected; suitable for other (Meyrick) (Acrolepiidae) 1990 countries? Platyphora species 1994 Argentina & Leaf-chewing Rejected; suitable for other (Chrysomelidae) Brazil countries? Acallepitrix sp. nov. 1994– Argentina & Leaf-mining Rejected; suitable for other (Chrysomelidae) 1998 Brazil countries? Gargaphia decoris Drake 1995, Argentina, Sap-sucking Released; established in (Tingidae) 2002 Brazil field Collabismus notulatus 1995, Argentina Shoot-galling Untested; possibly suitable Boheman (Curculionidae) 1998

Agents that cause structural damage Nealcidion bicristatum (Bates) 1984, Argentina Stem-boring Rejected; crop pest (Cerambycidae) 1995 Adesmus hemispilus (Germar) 1995, Argentina, Stem-boring Untested; possibly suitable (Cerambycidae) 1997 Brazil Conotrachelus squalidus 1995, Argentina & Stem-boring Untested; possibly suitable Boheman (Curculionidae) 1998 Paraguay

Agents that reduce fruit production Anthonomus santacruzi 1995, Argentina & Flowerbud- Cleared for release; releases Hustache (Curculionidae) 1998 Paraguay feeding pending Anthonomus morticinus Clark 1998 Argentina & Flowerbud- Partially tested; probably (Curculionidae) Paraguay feeding suitable 18 Appendix 2

6. References ARC 2001. Excerpt from the Cost Benefit Analysis (2000) for the Auckland Regional Pest Management Strategy 2002-2007.

Barker AL, Byrne MJ 2005. Biotypes and biocontrol: physiological factors affecting the establishment of a South American lace bug, Gargaphia decoris, a biocontrol agent for bugweed, Solanum mauritianum. In: Villet MH (ed.) Proceedings of the XVth Entomological Congress, Entomological Society if Southern Africa, Pretoria, South Africa, 2005, p8.

Florentine SK, Westbrooke ME 2003. Allelopathic potential of the newly emerging weed Solanum mauritianum Scop. (Solanaceae) in the wet tropics of north-east Queensland. Plant Protection Quarterly 18: 23–25.

Fromont M, King S 1992. Characteristics and control methods of 30 weed species affecting conservation land in Northland. Unpublished report. Whangarei, Department of Conservation.

Greater Wellington Regional Council 2008. http://www.gw.govt.nz/section895.cfm

Henderson L 2001. Alien weeds and invasive plants. Plant Protection Research Institute Handbook 12. Cape Town, Agricultural Research Council.

Hope KJ, Olckers T 2008. Confirmation that Gargaphia decoris (Hemiptera:Tingidae) from two South American provenances are equally safe for release against Solanum mauritianum (Solanaceae) in South Africa and New Zealand. Unpublished MS.

Hill RL 2007. A further assessment of the suitability of the tinged bug Gargaphia decoris and other insects as potential biological control agents for woolly nightshade. Unpublished report to Landcare Research. 18p

ISSG (ed.) 2006. Ecology of Solanum mauritianum In: Global Invasive Species database. http://www.issg.org/database/species/ecology.asp?si=209&fr=1&sts

Larivière M-C, Larochelle A 2004. Heteroptera (Insecta: Hemiptera): catalogue. Fauna of New Zealand 50. Lincoln, Manaaki Whenua Press. 330 p.

Lotter WD 2004. The establishment and ecological impact of the leaf-sucking lace bug Gargaphia decoris on Solanum mauritianum in KwaZulu-Natal . M.Tech. thesis, Tshwane Institute of Technology, South Africa. 127 p.

May BM 1977. The immature stages and biology of the lacebug Tanybyrsa cumberi Drake (Heteroptera: Tingidae). Journal of the Royal Society of New Zealand 7: 303– 312.

19 Appendix 2

McGregor PG 1999. Prospects for the biological control of woolly nightshade, Solanum mauritianum (Solanaceae, Solanoideae). Unpublished Landcare Research Report, 18 p.

NPPA 2008. National Pest Plant Accord. http://www.biosecurity.govt.nz/pests- diseases/plants/accord.htm

NZPCN 2008. NZ Plant Conservation Network. Woolly nightshade. http://www.nzpcn.org.nz/exotic_plant_life_and_weeds/detail.asp?WeedID=397

Olckers T 1999. Biological control of Solanum mauritianum Scopoli (Solanaceae) in South Africa: a review of candidate agents, progress and future prospects. African Entomological Memoirs 1: 65–73.

Olckers T 2000. Biology, host-range, and risk assessment of Gargaphia decoris the first agent to be released in South Africa for the biological control of the invasive tree Solanum mauritianum. BioControl 45: 373–388.

Olckers T 2003. Assessing the risks associated with the release of a flowerbud weevil, Anthonomus santacruzi, against the invasive tree Solanum mauritianum in South Africa. Biological Control 28: 302–312.

Olckers, T, 2009. Solanum mauritianum Scopoli (Solanaceae) In: Biological Control of Tropical Weeds using Arthropods, Eds. R. Muniappan, G.V.P. Reddy, and A. Raman. Cambridge University Press. pp. 406-420 (in press).

Olckers T, Borea C 2009. Assessing the risk of releasing a sap-sucking lacebug, Gargaphia decoris, against the invasive tree Solanum mauritianum in New Zealand. BioControl 54: 143-154.

Olckers T, Lotter WD 2004. Possible non-target feeding by the bugweed lacebug, Gargaphia decoris (Tingidae) in South Africa: field evaluations support predictions of laboratory host-specificity tests. African Entomology 12: 283–285.

Olckers T, Zimmerman HG, Hoffman JH 1995. Interpreting ambiguous results of host-specificity tests in biological control of weeds: assessment of two Leptinotarsa species (Chrysomelidae) for the control of Solanum eleagnifolium (Solanaceae) in South Africa. Biological Control 5: 336–344.

Olckers T, Hoffman JH, Moran VC, Impson FAC, Hill MP 1999. The initiation of biological control programmes aganist Solanum elaeagnifolium Cavanilles and S. sisymbriifolium Lamarck (Solanaceae) in South Africa. African Entomological Memoirs 1: 55–63.

Olckers T, Medal JC, Gandolfo DE 2002. Insect herbivores associated with species of Solanum (Solanaceae) in northeastern Argentina and southeastern Paraguay, with reference to biological control of weeds in South Africa and the United States of America. Florida Entomologist 85: 254–260.

20 Appendix 2

Pedrosa-Macedo JH, Olckers T, Vitorino MD, Caxambu MG 2003. Phytophagous arthropods associated with Solanum mauritianum Scopoli (Solanaceae) in the First Plateau of Paraná, Brazil: a cooperative project on biological control of weeds between Brazil and South Africa. Neotropical Entomology 32: 519–522.

Rahman A, Popay I 2001. Review of emerging weed problems in hill country pastures. http://www.maf.govt.nz/mafnet/rural-nz/sustainable-resource-use/land- management/emerging-weeds/emerging-weeds-08.htm

Stanley M 2003. Review of the Woolly Nightshade (Solanum mauritianum) Management Programme in the Bay of Plenty. Landcare Research Contract Report: LC0304/030, 37p.

Timmins SM, MacKenzie IW 1995. Weeds in New Zealand protected natural areas database. New Zealand Department of Conservation, Technical Series 8, 287p.

Van den Bosch E, Ward BG, Clarkson BD 2004. Woolly nightshade (Solanum mauritianum) and its allelopathic effects on New Zealand native Hebe stricta seed germination. New Zealand Plant Protection 57: 98–101.

Winks C, Frohlich J, Fowler S, Gianotti A 2001. Invertebrates and fungi associated with woolly nightshade (Solanum mauritianum, Solanaceae). Landcare Research Contract Report LC0001/157, prepared for three regional councils. 41 p.

Withers T 2002. Gargaphia decoris, a lace bug for the biological control of woolly nightshade, Solanum mauritianum. A retrospective evaluation of the host-range testing. A report prepared for Landcare Research, FRI-1475. 18 p.

Withers TM, Olckers T, Fowler SV 2002. The risk to valued Solanum species in New Zealand from Gargaphia decoris (Hem.:Tingidae), a potential biocontrol agent against wooly nightshade, Solanum mauritianum. New Zealand Plant Protection 55: 90–94.