Biocontrol introduction
Target pest: Hawkweeds (Pilosella, Hieracium spp.) (Asterales: Asteraceae)
Agent introduced: Aulacidea subterminalis (Hymenoptera: Cynipidae), hieracium gall wasp
Imported:
1997, 1998, 1999
Import source:
Germany (1997, 1998), Switzerland (1999)
Import notes:
Smith (2007c) - the hieracium gall wasp is native to northern Europe and it was first imported into New Zealand from Switzerland by Landcare Research, in conjunction with the Hieracium Control Trust, in 1997.
Landcare Research (2007a) - specimens of A. subterminalis from Germany, dated 1997 and 1998, and Switzerland, dated 1999, are present in the Biological Control Voucher Collection of the New Zealand Arthropod Collection [indicating importations from those sources in those years].
Released:
1999
Release details:
Syrett et al. (2001) - the first two field releases, each of 100 adult A. subterminalis, were made on 11 February 1999 on Balmoral and Glenrock Stations, in the Mackenzie Basin (Canterbury, South Island). A further 27 releases were made at sites throughout the South Island between November 1999 and February 2000. Eighteen releases comprised 80-150 adult wasps, and nine consisted of 3-6 plants bearing a total of 15-40 galls. The plants were grown in pots and transplanted in the field.
Landcare Research (2001b, 2001c, 2002a, 2002b, 2003b, 2004b, 2005b, 2005d, 2006a, 2008b) - ten releases were made in the South Island in the year Sep 2000 - Aug 2001, 13 releases Sep 2001 - Aug 2002, in both the North and South Islands, 10 releases Sep 2002 - Aug 2003, 20 releases Sep 2003 - Aug 2004, 16 releases Sep 2004 - Aug 2005 (making a total of 98 releases to date), one release Sep 2005 - Aug 2006, one release Sep 2007 - Aug 2008.
Establishment:
Syrett et al. (2001) - Aulacidea subterminalis galls were recovered from two of the six sites checked in April 2000; the remaining sites will be checked in 2001.
Landcare Research (2002b) - Aulacidea subterminalis seems to be establishing well with galls found at just under half of the release sites.
Landcare Research (2003d) - Aulacidea subterminalis has established at 21 out of 52 release sites so far.
Landcare Research (2004c) - established but not yet common in the South Island.
Landcare Research (2005d) - a survey this year [2005] showed A. subterminalis has established at 20% of last year’s release sites, making the overall establishment success rate for all release sites to date 38%. All the galls found were within 50 m of release sites.
Landcare Research (2006d) - Aulacidea subterminalis establishment was confirmed at about a third of the release sites checked over the summer of 2005-06. Monitoring the spread and density of A. subterminalis and the gall midge Macrolabis pilosellae [also released against hawkweeds] shows M. pilosellae lagging behind A. subterminalis so far. The furthest distance A. subterminalis was found from an original release point was 160 m (compared to 40 m for M. pilosellae, though they may have spread further as they are hard to detect), and the highest A. subterminalis density 122 galls per square metre (compared to up to just over one gall per square metre for M. pilosellae).
Landcare Research (2013g) - common at some sites in the South Island and established at one site in the North Island.
Landcare Research (2014c) - established but not yet common in the South Island and has not established yet in the North Island.
Paynter et al. (2018) - abundant at some release sites.
Landcare Research (2019i) - established but still not common in the South Island, and still not established in the North Island.
Landcare Research (2020e), Peterson et al. (2020) - surveys in 2020 at release sites - Canterbury and Otago in the South Island (Marlborough release sites were not visited) and on the Central Plateau of the North Island - showed A. subterminalis has established in both the North and the South Islands, although establishment rate and efficacy differ between the two. In the South Island, gall wasps were recovered from 11 of 12 (92%) of the release sites visited and had dispersed widely from release sites (and are now widespread in Canterbury and Otago), while in the North Island, they were only recovered from three of 20 (15%) of the sites visited, with no evidence of spread from the release sites.
Peterson (2021) - in the South Island, A. subterminalis is widespread in Canterbury and Otago at least, but North Island populations are currently restricted to three sites on the Central Plateau.
Impacts on target:
Klöppell et al. (2003) - in glasshouse and shade house trials, A. subterminalis reduced Pilosella officinarum (mouse-ear hawkweed) stolon growth, whether or not the plants were stressed, indicating that the gall wasp is likely to reduce vegetative reproduction of P. officinarum and therefore may be a successful biocontrol agent.
Landcare Research (2009b) - Aulacidea subterminalis has been shown to reduce mouse-ear hawkweed growth in laboratory trials, but effectiveness in the field is yet to be demonstrated. In a six-year field trial, initiated in 2003, at high country sites in Canterbury and Otago, A. subterminalis did not establish well enough in the extreme conditions to achieve populations at levels where any impact could be detected in this time frame.
Landcare Research (2014c) - impact unknown but reduces stolon length in laboratory trials.
Landcare Research (2020e) - 2020 surveys showed that despite the widespread distribution of A. subterminalis, only 4.5% of hawkweed plants at South Island sites where the wasp was present were galled by the wasp. In a 2006 study less than 1% had been galled by the wasp. Although site comparisons over time show that hawkweed densities have been reduced by 10% in the South Island, this is predominantly attributed to changes in land management practices, such as irrigation, cultivation and reduced grazing pressure, rather than biocontrol.
Landcare Research (2020g) - appears to be having minimal impact.
Peterson et al. (2020), Landcare Research (2021d) - the lack of impact by the gall wasp in the South Island appears to be due to a lack of stolons at the drier, more exposed hieracium sites. Although an average of 67% of stolons are galled by the wasp, only 7% of hieracium plants growing in these environments have stolons, which would severely limit establishment and population growth of the wasp. (In addition, an average of 10% of plants were galled by the hieracium gall midge, Macrolabis pilosellae [the other agent released against hawkweeds that has established].) There has been no overall change in hawkweed cover in the South Island between 2005 and 2020.
Paynter (2024) - factors influencing the success of weed biocontrol agents released and established in New Zealand were investigated. Each agent’s impact on the target weed in New Zealand was assessed as ‘heavy’, ‘medium’, ‘variable’, ‘slight’ or ‘none’, where a ‘heavy’, ‘medium’ or ‘variable’ impact have all been observed to reduce populations or percentage cover of their target weed in all or part of their respective target weed ranges in New Zealand. Results showed that: (i) agents that are highly damaging in their native range were almost invariably highly damaging in New Zealand; (ii) invertebrate agents with a closely related ‘native analogue’ species are susceptible to parasitism by the parasitoids that attack their native analogues and failed to have an impact on the target weed, and (iii) agent feeding guild helped predict agent impact - in particular, agents that only attack reproductive parts of the plant (e.g., seed and flower-feeders) are unlikely to reduce weed populations. Damaging impacts of A. subterminalis, a gall-forming wasp, have not been reported in its native range, it does not have a New Zealand native ecological analogue and its impact in New Zealand is assessed as ‘slight’.
Impacts on non-targets:
Syrett et al. (2001) - host range tests were carried out in Switzerland and in containment in New Zealand. Potential hosts tested included all Pilosella and Hieracium species (family Asteraceae, tribe Cichorieae) naturalised in New Zealand (except H. pollichiae), species chosen from other Cichorieae genera (including New Zealand natives), economically important members of other tribes in the family Asteraceae, more distantly related species (important cultivated and native New Zealand plants) from other families, and host plants of close relatives of A. subterminalis. Galls of A. subterminalis were produced only on Pilosella officinarum (mouse-ear hawkweed) and P. aurantiaca (orange hawkweed); wasps developed through to adult on both species. In its native range in Europe, A. subterminalis galls have been recorded only from P. officinarum, but these host tests show that it could perform equally well on P. aurantiaca, also weedy in New Zealand.
Smith (2007c) - it is extremely unlikely that A. subterminalis will attack plants other than mouse-ear hawkweed (Pilosella officinarum [syn Hieracium pilosella]) and orange hawkweed (P. aurantiaca [syn H. aurantiacum]). The other weedy Pilosella and Hieracium species are unlikely to be attacked.
General comments:
Target species note (17 February 2024) - in the 1990s and 2000s, six biocontrol agents were introduced to New Zealand to control hawkweeds, specifically four weedy species that at the time were considered to be in the genus Hieracium (with three of those in the subgenus Pilosella). Subsequently, Pilosella has been recognised as a distinct genus [see Taxonomic note (17 February 2024) entry below]; the four weed species are now classified as Pilosella officinarum (syn Hieracium pilosella) (mouse-ear hawkweed), P. caespitosa (syn H. caespitosum) (field hawkweed), P. praealta (syn H. praealtum) (king devil hawkweed) and H. lepidulum (tussock hawkweed). Of the biocontrol agents, the rust Puccinia hieracia var. piloselloidarum and the gall wasp Aulacidea subterminalis attack only P. officinarum, the plume moth Oxyptilus pilosellae attacks both P. officinarum and P. caespitosa, the gall fly Macrolabis pilosellae attacks all three Pilosella species, and the hover flies Cheilosia urbana and C. psilophthalma attack all four hawkweed species. (All preceding information from Hieracium Control Trust (2000).) Additionally, Syrett et al. (2001) identify a fifth adventive hawkweed, Pilosella aurantiaca (syn Hieracium aurantiacum) (orange hawkweed), as a problem weed in New Zealand, stating it has only recently been regarded as weedy in this country, although it has been here since 1911. Host range trials indicate it will be attacked at significant levels by A. subterminalis and the two Cheilosia species (Syrett et al. 2001).
Taxonomic note (17 February 2024) - at the time that A. subterminalis was introduced to New Zealand, the target weeds (hawkweeds) were all considered to be in the genus Hieracium. Bräutigam & Greuter (2007) note that Pilosella was considered by many authors to be a subgenus of Hieracium but that in recent decades generic recognition of Pilosella had gained increased support. Bräutigam & Greuter (2007) recognise Pilosella as a distinct genus from Hieracium and reclassify the Euro-Mediterranean flora accordingly. Under this classification there are introduced hawkweeds present in New Zealand in both genera (Hieracium and Pilosella) [see Target species note (17 February 2024) entry above].
References
Bräutigam S, Greuter W (2007). A new treatment of Pilosella for the Euro-Mediterranean flora. Willdenowia 37: 123-137 https://doi.org/10.3372/wi.37.37106
Hieracium Control Trust (2000). Application to EPA (NOR00001) to import for release the insects Macrolabis pilosellae (Binnie 1878), Cheilosia urbana Meigen and Cheilosia psilophthalma (Becker 1894) for the purpose of biological control of hawkweeds, Hieracium spp. Environmental Protection Authority website https://www.epa.govt.nz/assets/FileAPI/hsno-ar/NOR00001/6b046d0b38/Application-NOR00001.pdf
Klöppel M, Smith L, Syrett P (2003). Predicting the impact of the biocontrol agent Aulacidea subterminalis (Cynipidae) on growth of Hieracium pilosella (Asteraceae) under differing environmental conditions in New Zealand. Biocontrol Science and Technology (2003) 13(2): 207-218 https://doi.org/10.1080/0958315021000073478
Landcare Research (2001b). Control agents released in 2000/01. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2000/2001. August 2001, 7: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp01.pdf
Landcare Research (2001c). Future eaters. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2000/2001. August 2001, 7: 3 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp01.pdf
Landcare Research (2002a). Control agents released in 2001/02. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2001/2002. August 2002, 8: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp02.pdf
Landcare Research (2002b). News flashes: Two more join the fray. Patua Te Otaota - Weed Clippings. Biological Control of Weeds Annual Review 2001/2002. August 2002, 8: 11 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/weedcp02.pdf
Landcare Research (2003b). Control agents released in 2002/03. What’s New In Biological Control of Weeds? Annual Review. August 2003, 25: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew25.pdf
Landcare Research (2003d). Mighty midget. What’s New In Biological Control of Weeds? May 2003, 24: 1-2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew24.pdf
Landcare Research (2004b). Control agents released in 2003/04. What’s New In Biological Control of Weeds? Annual Review. August 2004, 29: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew29.pdf
Landcare Research (2004c). Who's who in the biological control of weeds. What’s New In Biological Control of Weeds? Annual Review. August 2004, 29: 14-15 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew29.pdf
Landcare Research (2005b). Control agents released in 2004/2005. What's New In Biological Control of Weeds? Annual Review, August 2005, 33: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew33.pdf
Landcare Research (2005d). Hieracium agents settle in for the long haul. What’s New In Biological Control of Weeds? Annual Review. August 2005, 33: 9 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew33.pdf
Landcare Research (2006a). Control agents released in 2005/06. What’s New In Biological Control of Weeds? Annual Review. August 2006, 37: 11 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew37.pdf
Landcare Research (2006d). Hieracium heroes and heartbreakers. What’s New In Biological Control of Weeds? August 2006, 38: 8 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew38.pdf
Landcare Research (2007a). New Zealand Arthropod Collection (NZAC) Biological Control Voucher Collection. Landcare Research website [Updated 2020] https://www.landcareresearch.co.nz/tools-and-resources/collections/new-zealand-arthropod-collection-nzac/databases-and-holdings/new-t2-landing-page/
Landcare Research (2008b). Control agents released in 2007/08. What’s New In Biological Control of Weeds? August 2008, 45: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew45.pdf
Landcare Research (2009b). Can we hinder high country hieracium? What’s New In Biological Control of Weeds? August 2009, 49: 4-5 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew49.pdf
Landcare Research (2013g). Who’s who in biological control of weeds. What’s New In Biological Control of Weeds? August 2013, 65: 10-11 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/whatsnew65.pdf
Landcare Research (2014c). Who's who in biocontrol of weeds? What's new in biological control of weeds? 69: 10-11 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/WhatsNew69.pdf
Landcare Research (2019i). Who's who in biological control of weeds? Weed Biocontrol: What's New? 89, August 2019 https://www.landcareresearch.co.nz/publications/newsletters/biological-control-of-weeds/weed-biocontrol-issue-89/whos-who-in-biological-control-of-weeds
Landcare Research (2020e). Hieracium biocontrol – 20 years on. Weed Biocontrol: What's New? 93, Aug 2020 https://www.landcareresearch.co.nz/publications/weed-biocontrol/weed-biocontrol-articles/hieracium-biocontrol-20-years-on/
Landcare Research (2020g). Who's who in biological control of weeds? Weed Biocontrol: What's New? 93, Aug 2020. https://www.landcareresearch.co.nz/publications/weed-biocontrol/weed-biocontrol-articles/status-of-agents/
Landcare Research (2021d). Hieracium biocontrol: where to from here? Weed Biocontrol: What's New? 96, May 2021 https://www.landcareresearch.co.nz/publications/weed-biocontrol/weed-biocontrol-articles/hieracium-biocontrol-where-to-from-here/
Paynter Q (2024). Prioritizing candidate agents for the biological control of weeds. Biological Control, Volume 188, January 2024, Article Number 105396 https://doi.org/10.1016/j.biocontrol.2023.105396
Paynter Q, Fowler SV, Groenteman R. (2018). Making weed biological control predictable, safer and more effective: perspectives from New Zealand. BioControl 63: 427–436 (first published online 8 Aug 2017) https://doi.org/10.1007/s10526-017-9837-5 https://link.springer.com/article/10.1007/s10526-017-9837-5
Peterson P (2021). Hieracium gall wasp: Aulacidea subterminalis. The Biological Control of Weeds Book - Te Whakapau Taru: A New Zealand Guide (Landcare Research) [Update of Smith (2007c)] https://www.landcareresearch.co.nz/discover-our-research/biodiversity-biosecurity/weed-biocontrol/projects-agents/biocontrol-agents/hieracium-plume-moth-3/
Peterson P, Smith L, Loxton G (2020). Hieracium biocontrol: 20 year progress report. Landcare Research website, Powerpoint presentation, June 2020 https://www.landcareresearch.co.nz/assets/Events/biosecurity-bonanza/2020/Webinar8_Hieracium-biocontrol-20-year-progress-report.pdf
Smith L (2007c). Hieracium gall wasp: Aulacidea subterminalis. The Biological Control of Weeds Book - Te Whakapau Taru: A New Zealand Guide (Landcare Research) [Updated 2021 - see Peterson (2021)] https://www.landcareresearch.co.nz/discover-our-research/biodiversity-biosecurity/weed-biocontrol/projects-agents/biocontrol-agents/hieracium-plume-moth-3/
Syrett P, Smith L, Grosskopf G, Meurk C (2001). Predicting the likely success of biological control of hawkweeds in New Zealand. Plant Protection Quarterly 16(4): 172-176 https://caws.org.nz/PPQ1617/PPQ%2016-4%20pp172-176%20Syrett.pdf
