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Biocontrol introduction

Target pest: Tuberolachnus salignus (Hemiptera: Aphididae), giant willow aphid

Agent introduced: Pauesia nigrovaria (Hymenoptera: Braconidae)

Imported:

2017

Import source:

USA (California)

Import notes:

Scion (2018a, 2018b) - Pauesia nigrovaria was sourced from California, USA. The first collecting trip in October 2017 was unsuccessful; a few small T. salignus colonies were found, but all the aphids brought back to New Zealand died quickly without any parasitoid emergence. For the second trip, the citizen science platform iNaturalist was used to contact Californian-based entomologists, willow enthusiasts and giant willow aphid observers to locate parasitised T. salignus colonies. Consequently, approximately 900 aphids were collected from Oakland, California in December 2018 and imported into containment at Rotorua, Bay of Plenty. Thirty-four P. nigrovaria emerged from these, of which 10 were females. From this importation, six generations and approximately 1,700 individuals of P. nigrovaria have been reared for host range testing.

Released: 2020

Release details:

Scion (2020) - between February and early-June 2020, 23 separate releases were carried out at 15 locations in the lower half of the North Island (from Waikato south) and Marlborough and Westland in the South Island. In total, 458 mated female parasitoids were released. Further releases are planned for 2021.

Scion (2021) - from December 2020 to June 2021 there have been further releases at 17 locations throughout New Zealand, from Northland to Southland. In total, more than 30 releases have been carried out, covering the length and breadth of the country. The release programme has been a New Zealand-wide community effort with releases carried out by beekeepers, caretakers of arboreta, regional council staff and other individuals, who were supplied with mated adults from the Scion rearing colony.

Establishment:

Scion (2020) - at the three earliest release sites (in Bay of Plenty and Manawatu, North Island), where field cages were used, establishment of P. nigrovaria was confirmed by the presence of aphid ‘mummies’ indicating that a new generation had developed.

Scion (2021) - surveys of the central North Island from March through June 2021 found P. nigrovaria to be well-established throughout this region and to have spread considerably, being found as far as 98 km away from the nearest release site, one year later.

Scion (2022) - despite the discovery of hyperparasitism in 2021 [see Scion (2021) entry in 'General comments' section], P. nigrovaria appears to be prevailing, with detections of T. salignus mummies (i.e., parasitised aphids), made primarily during 2022 surveys of the North Island, throughout the island.

Impacts on target:

Scion (2022) - to quantify early impact of P. nigrovaria, giant willow aphid population levels have been measured at five North Island release sites, at the time of release in 2020 and again one and two years later. Overall, aphid abundance has decreased each year, and the proportion of aphid-free trees has increased from 30% at the time of release to 86% two years later. Anecdotal evidence also suggests a drop in aphid numbers and associated issues in 2022 in several locations, particularly those in proximity to release sites.

Impacts on non-targets:

Sopow (2019), Sopow et al. (2021) - almost all known Pauesia species only attack aphids in the subfamily Lachninae (to which T. salignus belongs). New Zealand has no native aphids in this subfamily. Based on this lack of relatedness, their small size and lack of shared hosts with T. salignus, native aphids are considered unlikely to be vulnerable to attack from P. nigrovaria. This was supported by host testing in which none of three native aphid species tested (one in each of the three subfamilies to which all native species belong) were parasitised. Two exotic species present in New Zealand (including one in the subfamily Lachninae) were also tested and not parasitised, strongly indicating that P. nigrovaria is highly host-specific and unlikely to parasitise species other than T. salignus.

General comments:

Sopow (2017) - the specialist parasitoid, Pauesia salignae (Hymenoptera: Braconidae: Aphidiinae), present in Japan, was thought to be suitable as a potential biocontrol agent against the giant willow aphid in New Zealand. However, Scion entomologists have located another more promising species of Aphidiinae, currently unidentified [subsequently identified as Pauesia nigrovaria - see Sopow et al. (2021) entry below] parasitising T. salignus in California, and would like to import both species, if funds allow, into quarantine for assessment. Therefore the application to import potential agents for host range testing [see EPA (2017d) in 'EPA Applications' section] is at the level of sub-family rather than species.

Sopow et al. (2021) – a single parasitoid species was reared from T. salignus individuals imported to New Zealand from California in 2017 [see ‘Import notes’ section]. Surprisingly, morphological examination revealed the parasitoid to be Pauesia nigrovaria rather than P. salignae, previously reported from California and the only known parasitoid of T. salignus. Molecular analysis confirmed P. nigrovaria specimens as distinct from specimens of P. salignae from Japan. This represents a new parasitoid/host association; P. nigrovaria was first described in 1888 as Aphidius nigrovarius and was reported from ‘‘Lachnus sp.’’ (though is highly likely that this host was in fact T. salignus).

Scion (2021) - surveys of the central North Island from March through June 2021 found some hyperparasitism of P. nigrovaria, predominantly by Dendrocerus carpenteri, a generalist hyperparasitoid.

EPA Applications:

EPA (2017d) - 10 Apr 2017: application by The New Zealand Forest Research Institute Ltd (Scion) to import into containment parasitoids of the subfamily Aphidiinae [see Sopow (2017) entry in 'General comments' section], so that they can be evaluated for their potential as biological control agents for giant willow aphid, Tuberolachnus salignus. EPA Application # APP203191, approved with controls 18 Apr 2018.

EPA (2019c) - 24 Jul 2019: application by Scion to import and release the parasitoid wasp, Pauesia nigrovaria, as a biological control agent for the giant willow aphid (Tuberolachnus salignus). EPA Application # APP203853, approved without controls 29 Nov 2019.

References

EPA (2017d). Application to EPA (APP203191) to import into containment parasitoid species (Hymenoptera: Braconidae: Aphidiinae) for assessment as biological control agent of the giant willow aphid, Tuberolachnus salignus. Environmental Protection Authority website https://www.epa.govt.nz/database-search/hsno-application-register/view/APP203191

EPA (2019c). EPA application APP203313: to import and release the parasitoid wasp, Pauesia nigrovaria, as a biological control agent for the giant willow aphid (Tuberolachnus salignus). Environmental Protection Agency website https://www.epa.govt.nz/database-search/hsno-application-register/view/APP203853

Scion (2018a). Citizen science saves the day. Scion Connections 28 (June 2018): 4-5 https://www.scionresearch.com/__data/assets/pdf_file/0018/64107/Scion-Connections-Issue28.pdf

Scion (2018b). Trojan aphids used to import parasitoids. Forest Health News No. 278, January 2018 https://cdm20044.contentdm.oclc.org/digital/collection/p20044coll2/id/203/rec/172

Scion (2020). Release the beast! Management of giant willow aphid newsletter, 2020 https://www.giantwillowaphid.co.nz/__data/assets/pdf_file/0008/71954/GWA_newsletter2020.pdf

Scion (2021). New Zealand wide effort. Management of giant willow aphid newsletter, 2021 https://www.giantwillowaphid.co.nz/__data/assets/pdf_file/0009/78723/GWA_newsletter_2021.pdf

Scion (2022). Tiny wasp appears to be doing its job. Management of giant willow aphid newsletter, 2022 https://www.giantwillowaphid.co.nz/__data/assets/pdf_file/0004/81679/GWA_newsletter_2022.pdf

Sopow S, Wardhaugh C, Turner R, Gresham B, Sutherland R, Woodall G, Withers T. (2021). Host specificity testing of Pauesia nigrovaria (Hymenoptera: Braconidae: Aphidiinae) for classical biological control of Tuberolachnus salignus (Hemiptera: Aphididae: Lachninae) in New Zealand. BioControl 66: 739–751 https://doi.org/10.1007/s10526-021-10107-5

Sopow S. (2017). Application to import aphidiine parasitoids into containment, so that they can be safely evaluated for their potential as biological control agents for giant willow aphid, Tuberolachnus salignus. EPA Application APP203191 http://www.epa.govt.nz/search-databases/HSNO%20Application%20Register%20Documents/APP203191_APP203191_Application%20form_Final.pdf

Sopow S. (2019). EPA application [APP203853] to obtain approval to release new organisms [Pauesia nigrovaria]. Environmental Protection Authority website https://www.epa.govt.nz/assets/FileAPI/hsno-ar/APP203853/66e04c0700/APP203853-Application.pdf