Biocontrol introduction
Target pest: Uraba lugens (Lepidoptera: Nolidae), gum leaf skeletoniser
Agent introduced: Cotesia urabae (Hymenoptera: Braconidae)
Imported:
2006, 2007, 2008, 2010
Import source:
Tasmania, Australia
Import notes:
Mansfield (2005) - several collections of the U. lugens parasitoids (and potential biocontrol agents) Cotesia urabae, Dolichogenidea eucalypti, Euplectrus sp. and Eriborus sp. (Ichneumonidae) were made in Tasmania and South Australia from November 2004 to January 2005. Dolichogenidea eucalypti did not survive due to a high level of hyperparasitism, but the other three species are now in containment in New Zealand, and host specificity tests have begun with C. urabae and Eriborus sp.
Berry & Mansfield (2006) - natural enemies that attack biocontrol agents can seriously interfere with the effectiveness of the agent. The hyperparasitoids reared from of the four species of primary parasitoids of Uraba lugens collected in South Australia and Tasmania as potential biocontrol agents for U. lugens [see Mansfield (2005) entry above in this section] were identified to determine whether any were already present in New Zealand. Five hyperparasitoid species were reared from C. urabae, but none are known to be present in New Zealand.
Berndt et al. (2007) - Cotesia urabae were reared from U. lugens larvae collected in Hobart, Tasmania, Australia, in November and December 2006. Parasitoid cocoons were shipped into quarantine in New Zealand on 12 December 2006 and a colony maintained on second to fourth instar U. lugens larvae for host range testing [see Berndt (2007) entry below in this section].
Berndt (2007) - since approval to import four parasitoids of Uraba lugens into containment [see EPA (2004) entry in ‘EPA applications’ section below] many problems have been encountered with mating and rearing the parasitoids, and with hyperparasitoid contamination of the parasitoid shipments from Australia. Two of the parasitoids have been ruled out as potential control agents, but progress has been made with Cotesia urabae and Dolichogenidea eucalypti over the past two summers. Hyperparasitoid problems have been solved, and both species have now been reared through three generations in the laboratory. Host range testing of C. urabae is nearly complete for two non-target host species, the exotic pests Spodoptera litura and Helicoverpa armigera [see Berndt et al. (2007) entry in ‘Impacts on non-targets’ section below] and further host range testing on native species is planned for next summer.
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. (2013b) - two hundred and twelve 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. (2013b) - 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. (2013a) - a field study using sentinel host larvae found that U. urabae dispersed up to 20 m away from the release point but parasitism was highest within 5 m of the release site, with 77.1% of parasitoid cocoons recovered from within this radius. A high level of parasitism was observed at the release tree (87.6%), suggesting that most females released may have stayed there. A model developed from the data suggests C. urabae would be able to disperse up to 53 m in one release event.
Avila et al. (2013b) - 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.
Withers (2025) - Cotesia urabae was released into U. lugens-infested sites between 2011 and 2015, and subsequent monitoring showed faster rates of dispersal through the North Island than predicted by experiments [see Avila et al. (2013a) entry above in this section]. The parasitoid has yet to be recovered from the South Island, but it is well established in the North Island.
Impacts on target:
Withers (2025) - sampling from North Island U. lugens populations in both the spring and summer generations have revealed variable C. urabae parasitism rates ranging between zero and 46%. The effectiveness of C. urabae at reducing U. lugens populations remains uncertain. Nuisance outbreaks of the pest in urban areas continue to this day, but to date, no significant defoliation from U. lugens has been recorded in eucalpyt plantations in New Zealand.
Impacts on non-targets:
Mansfield (2005) - host specificity tests have begun with C. urabae against the following non-target moth species: Celama parvitis, Metacrias erichrysa, Nyctemera annulata and Helicoverpa armigera, chosen because they are related to the genus Uraba. Preliminary results show no evidence for attack on these non-target species; however, the testing programme is at a very early stage.
Berndt et al. (2007) - a list of lepidopteran species appropriate for host range testing of potential U. lugens biocontrol agents includes Celama parvitis, the only New Zealand endemic in the same family (Nolidae) as U. lugens, as well as representatives of the related family Arctiidae. Two species of Noctuidae, the pests Helicoverpa armigera and Spodoptera litura, are also included as U. lugens was previously placed in this family. Host range testing methods were developed for C. urabae against the non-target hosts H. armigera and S. litura. Cotesia urabae females showed clear preference for U. lugens over both non-target species. Some females did attempt to attack the non-target species, but no evidence of parasitism was observed when non-target hosts were reared or dissected. The methodology used here was successful and will be used against the other non-target species to be tested.
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 (2013a). Dispersal behavior of the parasitic wasp Cotesia urabae (Hymenoptera: Braconidae): A recently introduced biocontrol agent for the control of Uraba lugens (Lepidoptera: Nolidae) in New Zealand. Biological Control 66(3): 166-172 https://doi.org/10.1016/j.biocontrol.2013.05.008
Avila GA, Berndt LA, Holwell GI (2013b). 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
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Berndt LA, Sharpe A, Withers TM, Kimberley M, Gresham B (2010). Risks to non-target species from potential biological control agent Cotesia urabae against Uraba lugens in New Zealand. Appendix 2, EPA application ERMA200282. Environmental Protection Authority website https://www.epa.govt.nz/assets/FileAPI/hsno-ar/ERMA200281/704d5ff555/Application-Appendix-2.pdf
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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
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Hill R (2010). Application to import and release the parasitoid Cotesia urabae (Hymenoptera: Braconidae) as a biological control agent for gum leaf skeletoniser, Uraba lugens (Lepidoptera: Noctuidae) - ERMA200281 Environmental Protection Authority website https://www.epa.govt.nz/assets/FileAPI/hsno-ar/ERMA200281/0792c97d72/Application-FINAL-2010.04.06.pdf
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Withers TM (2025). Classical biological control of defoliators in Eucalyptus plantations. In: Biological Control of Insect Pests in Plantation Forests (Eds Hurley BP, Lawson SA, Slippers B), Springer 2025, pp 205-221 https://doi.org/10.1007/978-3-031-76495-0
