Biocontrol introduction

Target pest: Hawkweeds (Pilosella, Hieracium spp.) (Asterales: Asteraceae)

Agent introduced: Macrolabis pilosellae (Diptera: Cecidomyiidae), hieracium gall midge

Imported:

Late-1990s, 2001

Import source:

Switzerland

Import notes:

Landcare Research (2003d) - a mass-rearing programme for M. pilosellae has been underway at Lincoln, Canterbury during the past year to allow widespread releases to begin. Mass-rearing will continue for at least another couple of years.

Smith (2007b) - Macrolabis pilosellae is native to northern Europe. Several shipments were imported into New Zealand from Switzerland by Landcare Research, in conjunction with the Hieracium Control Trust, in the late 1990s for host range testing. Permission to release the gall midges was granted in 2000 and another shipment imported in 2001 to begin a rearing colony.

Landcare Research (2007a) - specimens of M. pilosellae from Switzerland, dated 1999, are present in the Biological Control Voucher Collection of the New Zealand Arthropod Collection [indicating an importation from that source in that year].

Released:

2002

Release details:

Landcare Research (2003d) - the first releases of M. pilosellae were made in February 2002 at two Canterbury, South Island high country stations: Glenthorne (North of Lake Coleridge) and Balmoral (Mackenzie Country). The midges have been subsequently released at 12 sites in the 2002-03 season, at Waiouru in the central North Island (four sites), and in the South Island at Kekerengu (between Blenheim and Kaikoura), Awatere (inland from Kekerengu, 2 sites), Hanmer Springs, Wanaka, Bannockburn (Central Otago) and Alexandra (two sites). Because the adults are fragile and short-lived the best way of releasing them involves planting out infested plants.

Landcare Research (2004b, 2004d) - fifty-three releases made in the year Sep 2003 - Aug 2004, in the areas worst affected by hawkweeds.

Landcare Research (2005d) - forty-nine releases of M. pilosellae were made in the 2004-05 season, bringing the total number of releases so far to 117.

Landcare Research (2006d) - nineteen new releases were made over the summer 2005-06, bringing the total number of releases to 136. Only 5 of these releases have been in the North Island (at Waiouru on the Central Plateau), the rest have been throughout the South Island.

Landcare Research (2007c) - in the year September 2006 - August 2007, M. pilosellae was released at one site.

Smith (2007b) - Macrolabis pilosellae was first released in 2002 and widely released in subsequent years.

Establishment:

Landcare Research (2003d) - plants galled by M. pilosellae have been found at the Glenthorne release site, a year after the February 2002 release, and establishment is looking promising at this early stage.

Landcare Research (2004d) - Macrolabis pilosellae has established in New Zealand. In recent months galls have been found at three sites: Glenthorne Station (Canterbury) and Pisa Station (Otago) in the South Island, and Argo Valley (Waiouru) in the North Island.

Landcare Research (2005d) - releases of M. pilosellae began three years ago and it has now established at 60% of release sites. This insect seems to establish well, as galled leaves were found at 70% of sites where they were first released only a year ago.

Landcare Research (2006d) – Macrolabis pilosellae establishment was confirmed at 92% of the 51 release sites checked over the summer of 2005-06. Monitoring the spread and density of M. pilosellae and the gall wasp Aulacidea subterminalis (also released against hawkweeds) shows M. pilosellae lagging behind A. subterminalis so far. The furthest distance M. pilosellae was found from an original release point was 40 m (compared to up to 160 m for A. subterminalis), though they may have spread further as they are hard to detect, and the highest M. pilosellae density just over one gall per square metre (compared to up to 122 per square metre for A. subterminalis).

Smith (2007b) - established at many sites in both islands but while establishment rates have been high, slow dispersal means that they are not yet widespread.

Landcare Research - (2014c) - common near Waiouru in the central 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 M. pilosellae has established in both the North and the South Islands. In the South Island it was recovered from eight of 11 (73%) of the release sites visited but is still restricted in range, only present near the original release sites; in the North Island it was recovered from 11 of 13 (85%) of the sites visited, dispersing over 10 square kilometres from the original release sites.

Impacts on target:

Landcare Research (2009b) - Macrolabis pillosellae has been shown to reduce 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, M. pilosellae did not establish well enough in the extreme conditions to achieve populations at levels where any impact could be detected in this time frame.

Hayes et al. (2013) - data from a study area on the Central Plateau of the North Island suggest M. pilosellae is reducing mouse-ear hawkweed (Pilosella officinarum, syn Hieracium pilosella) cover by 26% after 10 years and that other vegetation is replacing it.

Landcare Research (2014c) - at Waiouru has reduced host cover by 18% over 6 years; also very damaging in laboratory trials.

Landcare Research (2020e) - 2020 surveys showed 9.5% of hieracium plants at South Island sites where the midge was present were galled by the midge. In a 2006 study up to 33% had been galled by M. pilosellae. The 2006 study also showed that the gall midges had reduced hieracium cover by up to 18% at sites in the North Island, where galling was most intense. It is now known that biocontrol of hieracium is not very effective in the South Island. Although site comparisons over time show that hieracium 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.

Peterson et al. (2020) - despite the establishment of M. pilosellae and Aulacidea subterminalis [hieracium gall wasp, the other biocontrol 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 M. pilosellae, a gall-forming fly, 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:

Hieracium Control Trust (2000) - host range tests [see Syrett et al. (2001) entry below for further details] were completed on 66 test plant species comprising 9 species from the genera Pilosella and Hieracium, 29 species in the family Asteraceae, including the closest relatives to Pilosella and Hieracium among native New Zealand plants, and 28 species from an additional 25 families of plants. Oviposition and larval development tests were carried out in Switzerland, or under insect containment conditions in New Zealand for those plants that could not be grown in Switzerland. No eggs were laid on plants other than Pilosella and Hieracium species, and no larvae survived on any plants other than species in these genera. There are no native plants in the genera Pilosella and Hieracium; they are represented in New Zealand by weedy species introduced from Europe. The host range tests indicate the likelihood that any non-target species will be negatively affected is very low.

Syrett et al. (2001) - host range tests [see Hieracium Control Trust (2000) entry above for further details] 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 M. pilosellae. Gall development, and emergence of new-generation adult M. pilosellae, occurred only on Pilosella species, although two species of this genus tested, P. aurantiaca and P. × stoloniflorum, were unacceptable hosts.

Smith (2007b) - it is extremely unlikely that M. pilosellae will attack plants other than mouse-ear hawkweed (Pilosella officinarum), king devil hawkweed (P. praealta) and field hawkeed (P. caespitosa) [all target species - see Target species note (17 February 2024) entry in 'General comments' section].

Paynter et al. (2015) - surveys of potential non-target hosts the hawkweeds Pilosella aurantiaca (syn Hieracium aurantiacum) and P. praealta (syn H. praealtum), both exotic weeds, [P. officinarum (syn H. pilosella) is listed in this publication as the target weed] showed no feeding on former and minor 'spill-over' feeding on latter.

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 M. pilosellae 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].

EPA Applications:

EPA (1998a) - 26 Aug 1998: application by the Hieracium Control Trust to import into containment a new organism Macrolabis pilosellae (Binne, 1878), for the purpose of testing to determine its suitability as a biological control agent against hieracium. EPA Application # NOC98001, approved with controls 9 Oct 1998.

EPA (2001) - 17 Nov 2000: application by the Hieracium Control Trust to import for release the insects Macrolabis pilosellae (Binnie 1878), Cheilosia urbana (Meigen 1822) and Cheilosia psilophthalma (Becker 1894) for the purpose of biological control of hawkweeds, Hieracium spp. EPA Application #NOR00001, approved without controls 27 Jun 2001.

References

Auckland Regional Council (). The Land 99 http://greensite.arc.govt.nz/library/:70039-2.pdf

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

EPA (1998a). EPA application NOC98001: to import into containment a new organism Macrolabis pilosellae (Binne, 1878), for the purpose of testing to determine its suitability as a biological control agent against hieracium. Environmental Protection Authority website https://www.epa.govt.nz/database-search/hsno-application-register/view/NOC98001

EPA (2001). EPA application 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/database-search/hsno-application-register/view/NOR00001

Hayes L, Fowler SV, Paynter Q, Groenteman R, Peterson P, Dodd S, Bellgard S (2013). Biocontrol of weeds: achievements to date and future outlook. In: Dymond JR (ed) Ecosystem services in New Zealand: conditions and trends. Manaaki Whenua Press, Lincoln, pp 375-385 https://www.landcareresearch.co.nz/__data/assets/pdf_file/0005/77054/2_8_Hayes.pdf

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

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 (2004d). Midges start to bite. What’s New In Biological Control of Weeds? May 2004, 28: 1-2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew28.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 (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 (2007c). Control agents released in 2006/07. What's New In Biological Control of Weeds? August 2007, 41: 2 https://www.landcareresearch.co.nz/assets/Publications/Weed-biocontrol/wtsnew41.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 (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 (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/

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 QE, Fowler SV, Gourlay AH, Peterson PG, Smith LA and Winks CJ (2015). Relative performance on test and target plants in laboratory tests predicts the risk of non-target attack in the field for arthropod weed biocontrol agents. Biological Control 80: 133-142 https://doi.org/10.1016/j.biocontrol.2014.10.007

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 (2007b). Hieracium gall midge: Macrolabis pilosellae. The Biological Control of Weeds Book - Te Whakapau Taru: A New Zealand Guide (Landcare Research) [Updated 2021] https://www.landcareresearch.co.nz/discover-our-research/biodiversity-biosecurity/weed-biocontrol/projects-agents/biocontrol-agents/hieracium-plume-moth-2/

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