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Biocontrol introduction

Target pest: Uraba lugens (Lepidoptera: Noctuidae), Gum leaf skeletoniser

Agent introduced: Cotesia urabae (Hymenoptera: Braconidae)

Imported:

2006, 2007, 2008, 2010

Import source:

Tasmania, Australia

Import notes:

Berndt et al. (2013) - Cotesia urabae cocoons, reared from U. lugens larvae collected from Eucalyptus in and around Hobart, Tasmania were imported into containment in New Zealand in December 2006, 2007, 2008 and 2010 for host range testing. Each shipment consisted of approximately 200 cocoons. Due to the difficulty and expense of maintaining C. urabae and U. lugens colonies through multiple generations in the laboratory, colonies were maintained only while they were needed for host specificity testing experiments and re-established from shipments each year.

Avila et al. (2013) - 212 C. urabae cocoons were shipped from Tasmania in December 2010 to a containment facility at Rotorua. They were reared there through one generation to provide adults for the first release. Seventy-six cocoons from this second generation were sent to the University of Auckland to continue the culture production for further releases.

Released:

2011

Release details:

On 25 January 2011 37 female and 73 male parasitoids were released at Auckland Domain. An additional 20 females and 40 males were released across 5 sites in Point Chevalier and Grey Lynn, Auckland on 27 January.

Avila et al. (2013) - Cotesia urabae were paired for mating prior to release, and the pair released together, because unmated females (which produce only male offspring) prioritise host attack over mating. The majority of parasitoids were released into sleeve cages containing approximately 30-60 3rd-5th instar U. lugens larvae, although some were released free into the environment The first release was at Auckland Domain on 25 January 2011 [see entry above]. There were two further releases in Auckland Domain, on 14 April and 12 May 2011. Two releases were made at Manukau Memorial Gardens in Auckland, on 28 May and 11 June 2011. Total numbers released at each site: Domain 91 females, 102 males; Memorial Gardens 86 females, 54 males.

Gresham & Withers (2013) - there have been releases [in January 2012 - Gresham et al. (2014)] at Port Whangarei, Northland and Matapihi, Tauranga, Bay of Plenty, both in the North Island, piloting a novel method of releasing parasitised host caterpillars rather than the traditional intensive method of caging parasitoid cocoons or newly emerged adults on infested foliage. Approximately 800 parasitised host larvae were released at Port Whangarei.

Withers et al. (2013) - between 800 and 1000 C. urabae-parasitised U. lugens larvae were released into amenity eucalyptus trees at three sites in Tahunanui, Nelson, South Island on 9 September 2013.

Withers & Gresham (2014) - on 25 February 2014, approximately 450 C. urabae-parasitised U. lugens larvae and 66 adult parasitoids (equal numbers of males and females) were released into two large eucalypt trees at the Park Island Recreation Ground in Orotu Park, Napier, Hawke's Bay, North Island.

Avila, Ehrminger et al. (2016) - it is believed self-introduced populations appeared in Hamilton and Rotorua in the North Island prior to additional small releases in those areas in 2015. A very small release was made in Kerikeri (Northland, North Island) in 2015.

Establishment:

Avila et al. (2013) - the first parasitoid cocoons were found in the field exactly one month after the first release (25 January 2011) at the Auckland Domain. By May 2012, 125 pupal cocoons had been found at the Domain and seven at Manukau Memorial Gardens, at distances up to 60 m, though most no further than 20 m, from the release point. The cocoons found at the Auckland Domain in February-March 2012 can be considered as confirmed field generation cocoons, since the last release made at this site was in May 2011. This shows that C. urabae has successfully overwintered and established, at least initially, in this location.

Gresham & Withers (2013) - establishment has been confirmed at both the Auckland Domain and Manukau Memorial Gardens sites as well as self-dispersal to another site approximately 5 km away. New parasitoid cocoons have been found at the Port Whangarei release site, 14 months post-release, confirming establishment there. Unfortunately, at the Tauranga release site the release tree had been pruned and no evidence of establishment was found.

Gresham et al. (2014) - Cotesia urabae has established at all three original Auckland release sites [Auckland Domain, Manukau Memorial Gardens, Pt Chevalier/Grey Lynn] and has naturally dispersed to six other sites, up to 6 km from original sites. Establishment has been confirmed at the Whangarei and Tauranga release sites, but it is not yet known if the parasitoid has established at Nelson or Napier.

Avila, Ehrminger et al. (2016) - from collections of U. lugens larvae in Napier, Hamilton and Rotorua in January 2016, C. urabae was recovered from three out of five release sites in Napier and was found to be parasitising up to 46% of larvae at one site, and in the release site in Hamilton was parasitising up to 3% of larvae. No parasitoids were collected from the Rotorua site, and with U. lugens populations low in both Rotorua and Nelson it may be that the parasitoid is either not established or present at very low levels there.

Avila et al. (2023) - releases of C. urabae throughout the upper North Island have resulted in confirmed establishment in various locations from Northland south to the Hawke’s Bay region.

Impacts on non-targets:

Berndt et al. (2010), Hill (2010) - in host range tests C. urabae exhibited attack behaviour on all eight non-target species presented, though only five species (Celama parvitis, Metacrias erichrysa, M. huttoni, Nyctemera annulata, Tyria jacobaeae) were found to contain parasitoids within them upon dissection (indicating successful attack). Parasitoids emerged from larvae and produced cocoons from only two species of non-targets, M. erichrysa and M. huttoni, and none of these successfully developed into adult C. urabae. However, low sample sizes due to difficulties of rearing non-target species resulted in few mathematically significant differences between Uraba lugens and non-targets. Despite these experimental difficulties, results indicate that U. lugens larvae proved to be better hosts than larvae of related Lepidoptera and indicated that the parasitoid is functionally host-specific to this pest and very unlikely to adversely affect populations of other lepidopteran species.

Avila et al. (2014) - retrospective host specificity testing confirmed the native nolid moth Celama parvitis, as a non-host, as no parasitoids emerged from the 52% of caterpillars that survived. However, of those that died during lab rearing, 63% were parasitised by C. urabae, although no parasitoid larvae had developed beyond 2nd instar.

Avila, Withers & Howell (2016a) - laboratory olfactometer trials were carried out with U. lugens and three non-target Lepidoptera and their corresponding host plants and plant-host complexes. The non-target species were the endemic New Zealand magpie moth Nyctemera annulata, the cinnabar moth Tyria jacobaeae, an introduced biocontrol agent (both in the family Erebidae, considered to be relatively closely related to the family Nolidae of the target host U. lugens) and the endemic New Zealand forest looper Pseudocoremia suavis (Geometridae). Although C. urabae was most strongly attracted to U. lugens, it was also attracted to the odours of the non-target Erebidae larvae when tested on their own and when feeding on their host plants, but not to their non-target host plants alone, suggesting in some rare circumstances in the field these non-targets could be attacked by C. urabae. Parasitoids given prior exposure and the opportunity to oviposit within either non-target species were not subsequently more attracted to the Erebidae odours, suggesting that associative learning is unlikely to increase non-target attack. The significantly higher preference for the target species and the lack of associative learning suggests that C. urabae is likely to remain largely host-specific in the field, and the probability of non-target host attack should be quite low, at least when U. lugens is present.

Avila, Withers & Howell (2016b) - retrospective non-target risk assessment was undertaken with two New Zealand endemic species: the magpie moth, Nyctemera annulata and the common forest looper Pseudocoremia suavis, as well as the beneficial biological control agent, the cinnabar moth Tyria jacobaeae. Under no-choice laboratory conditions N. annulata and T. jacobaeae were attacked at a similar rate to the target host U. lugens, though time to attack was significantly faster against the target host. Parasitism of N. annulata under semi-natural field conditions was investigated in field cages; there was significantly lower parasitism of N. annulata than U. lugens, suggesting that non-target impacts on N. annulata in the field are likely to be limited.

Todd et al. (2021) - C. urabae has been found to parasitise early instar Nyctemera annulata larvae at low rates in the field.

Avila et al. (2023) - a 2018-20 field study assessed non-target parasitism by C. urabae using sentinel target (U. lugens) and non-target (Nyctemera annulata) host larvae released, along with the parasitoid, in open-field conditions. Parasitism where target and non-target hosts co-occurred in an overlapping habitat was compared with a habitat supporting only the non-target host. In the overlapping habitat C. urabae was recovered from 22.3% and 3.1% of target and non-target larvae, respectively. In the habitat devoid of the target larvae and its Eucalyptus host only 0.2% of N. annulata (a single individual) was parasitised, suggesting C. urabae had immediately dispersed from release sites devoid of host cues. Nyctemara annulata is a marginal physiological host (all observed parasitism by C. urabae in this trial was from cocoons that did not hatch); however, attacks on this species in the field in this trial mean population impacts cannot be completely ruled out. Nevertheless, this study suggests that the risk posed to N. annulata by C. urabae in habitats without Eucalyptus is likely to be close to zero and that this parasitoid is unlikely to form self-sustaining populations on this host in overlapping habitats. That C. urabae will retain its strong preference for U. lugens in the field is supported by the lack of other evidence of field parasitism by C. urabae of the endemic N. annulata or any other non-target species in New Zealand or Australia, although targeted searching has been limited.

EPA Applications:

EPA (2004) - 9 Jun 2004: application by Scion to import Cotesia urabae, Dolichogenidea eucalypti, Eriborus sp. and Euplectrus sp. into containment for assessment as biocontrol agents of the gum leaf skeletoniser, Uraba lugens. EPA Application # NOC04004, approved with controls 10 Sep 2004.

EPA (2010a) - 12 Apr 2010: application by Scion to import and release the parasitoid Cotesia urabae (Hymenoptera: Braconidae) as a biological control agent for gum leaf skeletoniser, Uraba lugens (Lepidoptera: Noctuidae). EPA Application #ERMA200281, approved without controls 1 Jul 2010.

References

Avila G, Ehrminger L, Gresham B, Pugh A, Withers T. (2016). Gumleaf skeletoniser biological control takes a shine to Napier. Forest Health News No. 267, June 2016 https://www.scionresearch.com/__data/assets/pdf_file/0006/47994/FHNews-June2016.pdf

Avila GA, Berndt LA, Holwell GI (2013). First releases and monitoring of the biological control agent Cotesia urabae Austin and Allen (Hymenoptera: Braconidae). New Zealand Entomologist 36 (2): 65-72 https://doi.org/10.1080/00779962.2012.744908

Avila GA, MacDonald FM, Hunt S, Santos K, Alavi M, Pugh AR, Gresham BA, Pearce B, Prache A, Withers TM (2023). Field assessment of parasitism on the New Zealand endemic Nyctemera annulata by Cotesia urabae: can non-target impacts be ruled out? Biocontrol 178, Article Number 105136 http://dx.doi.org/10.2139/ssrn.4184422

Avila GA, Withers TM, Holwell GI (2014). Retrospective host specificity testing of Cotesia urabae to assess the risk posed to the New Zealand nolid moth Celama parvitis (Poster abstract). New Zealand Plant Protection 67: 328

Avila GA, Withers TM, Holwell GI (2016a). Laboratory odour-specificity testing of Cotesia urabae to assess potential risks to non-target species. BioControl 61: 365-377 https://doi.org/10.1007/s10526-016-9716-5

Avila GA, Withers TM, Holwell GI (2016b). Retrospective risk assessment reveals likelihood of potential non-target attack and parasitism by Cotesia urabae (Hymenoptera: Braconidae): A comparison between laboratory and field-cage testing results. Biological Control 103: 108-118 https://doi.org/10.1016/j.biocontrol.2016.08.008

Berndt L. (2010). Biological control of gumleaf skeletoniser - an Update MAF biosecurity New Zealand Update. Issue 78

Berndt L. (2011). Biological control of gumleaf skeletoniser (Uraba lugens) SFF Project Summary http://maxa.maf.govt.nz/sff/about-projects/search/07-042

Berndt LA, Sharpe AM, Gresham BA, Hayes D, Allen GR (2013). Laboratory rearing of Cotesia urabae Austin and Allen (Hymenoptera: Braconidae), a biological control agent of Uraba lugens Walker (Lepidoptera: Nolidae). New Zealand Entomologist 36(1): 1-7 https://doi.org/10.1080/00779962.2012.724929

EPA (2004). EPA application NOC04004: to import Cotesia urabae, Dolichogenidea eucalypti, Eriborus sp. and Euplectrus sp. into containment for assessment as biocontrol agents of the gum leaf skeletoniser, Uraba lugens. Environmental Protection Authority website https://www.epa.govt.nz/database-search/hsno-application-register/view/NOC04004

EPA (2010a). EPA application ERMA200281: to import and release the parasitoid Cotesia urabae (Hymenoptera: Braconidae) as a biological control agent for gum leaf skeletoniser, Uraba lugens (Lepidoptera: Noctuidae). Environmental Protection Authority website https://www.epa.govt.nz/database-search/hsno-application-register/view/ERMA200281

Gresham B, Withers T (2013). Gum leaf skeletoniser biological control update. Forest Health News No. 235, April 2013 https://cdm20044.contentdm.oclc.org/digital/collection/p20044coll2/id/152/rec/126

Gresham BA, Withers TM, Avila GA, Berndt LA (2014). Novel release method proves successful: the gum leaf skeletoniser parasitoid Cotesia urabae establishes at two new locations (Poster abstract). New Zealand Plant Protection 67: 328

Todd JH, Pearce BM, Barratt BIP. (2021). Using qualitative food webs to predict species at risk of indirect effects from a proposed biological control agent. BioControl 66: 45-58, published online 4 Aug 2020. https://doi.org/10.1007/s10526-020-10038-7

Withers T, Gresham B (2014). Cotesia urabae geographic range expanding. Forest Health News No. 245, February 2014 https://cdm20044.contentdm.oclc.org/digital/collection/p20044coll2/id/148/rec/136

Withers T, Gresham B, Watson M (2013). Cotesia urabae released in Nelson. Forest Health News No. 235, September 2013 https://cdm20044.contentdm.oclc.org/digital/collection/p20044coll2/id/150/rec/131