Biocontrol introduction
Target pest: Sitona discoideus (Coleoptera: Curculionidae), lucerne weevil
Agent introduced: Microctonus aethiopoides Moroccan biotype (Hymenoptera: Braconidae)
Imported:
1982
Import source:
Morocco via New South Wales, Australia
Import notes:
Cameron et al. (1989) - a shipment of 317 M. aethiopoides pupae from New South Wales (it was imported into Australia in 1976 for release against S. discoideus) was received at Lincoln, Canterbury, quarantine laboratory in May 1982. It was reared on S. discoideus through four generations in the laboratory.
Vink et al. (2003), Vink et al. (2012) - Microctonus aethiopoides from Morocco and Greece were released in Australia against Sitona discoideus. The Moroccan strain readily established while establishment of the Greek strain was not confirmed. It was uncertain if the introduction from Australia to New Zealand was the Moroccan or Greek strain, or both, but Morocco was considered most likely. Molecular studies now indicate that the S. discoideus-attacking M. aethiopoides in New Zealand and Australia are all derived from M. aethiopoides specimens that were imported to Australia from Morocco.
Released:
1982
Release details:
Stufkens et al. (1987), Cameron et al. (1989) - released as parasitised weevils (93% - total = 30,450) or adult wasps (7% - total = 2,390) between October 1982 and June 1985 at 17 sites in the South Island. Releases were made in Central Otago (one site - 3,950 parasitised weevils and 40 adult parasitoids), Canterbury (13 sites – 21,800 parasitised weevils and 1,950 parasitoids) and Marlborough (3 sites - 4,700 parasitised weevils and 400 parasitoids).
Ferguson et al. (1994) - Microctonus aethiopoides was released at two sites in Otago; at Earnscleugh (near Alexandria) in 1983, 1984 and 1985 [the releases reported by Stufkens et al. (1987) - see above], and also at Middlemarch in 1985.
Establishment:
Stufkens et al. (1987), Cameron et al. (1989) - Microctonus aethiopoides is successfully established in the South Island. Surveys of 110 lucerne crops in Marlborough, Canterbury and Otago in 1985-86 found the parasitoid at 90 sites (82%) and 24% of adult S. discoideus collected at these sites parasitised.
Ferguson et al. (1994) - in surveys at 88 lucerne stands throughout Otago and Southland in the summer of 1993-94, parasitised S. discoideus were found at 58 sites, with parasitism levels of up to 100% (with mean levels, by region, between 16 and 67%), indicating M. aethiopoides is well established in the southern South Island, including locations where lucerne is only a minor crop.
Barratt et al. (1997), Barratt et al. (2000), Barratt et al. (2007) - parasitism by M. aethiopoides, of both S. discoideus and non-target hosts, has spread to areas outside of the target host habitat (lucerne), in developed pasture and grazed natural grasslands.
Barratt et al. (2000) - Microctonus aethiopoides is now widespread throughout New Zealand wherever S. discoideus is present.
Impacts on target:
Goldson & Proffitt (1986) - a survey carried out throughout 1985 and autumn/early-winter 1986 at a Mid Canterbury site showed 20-30% parasitism of S. discoideus by M. aethiopoides in 1985, which significantly reduced autumn weevil densities and may have reduced the duration of the egg-laying period in spring by 2-3 weeks. Early in the 1986 reproductive season parasitism rates were between 40 and 55%. This variation in parasitism between seasons may result in a corresponding variation in efficacy of M. aethiopoides as a biocontrol agent. Whether the reduction of adult weevil populations through M. aethiopoides parasitism results in the reduction of larval densities is uncertain; because a strong density-dependent mortality occurs at the larval establishment phase, a parasitoid-induced reduction in egg recruitment may simply result in a corresponding reduction in larval competition mortality.
Goldson et al. (1990) - surveys at four lucerne stands in Canterbury 1986-89 showed a peak rate of parasitism (85-100%) of S. discoideus by M. aethiopoides in October-November, moderate (c. 50%) parasitism April-July, with minimal parasitism in August-September and December. A high average rate of parasitism compared to that reported overseas suggests that M. aethiopoides has effectively suppressed S. discoideus in Canterbury dryland lucerne, in spite of the high density-dependent nature of S. discoideus larval establishment which implies the need for a major reduction of egg-laying if economically useful limitation of larval establishment is to occur. The unexpectedly high levels of parasitism observed are attributed to atypical parasitoid development over summer in aestivating S. discoideus adults; as a result it is calculated that M. aethiopoides populations undergo three additional generations.
Goldson et al. (1993) - Microctonus aethiopoides has a significant impact; parasitism of S. discoideus within lucerne paddocks can be 100%, but averages about 50%. Conservatively estimated in 1993 to save farmers $6.8 million p.a. and to have contributed to restoring farmer confidence in growing lucerne.
Barlow & Goldson (1993) - modelling the impact of M. aethiopoides on S. discoideus supports the conclusions of Goldson et al. (1990) [see above] that observed levels of parasitism account for the decline in pest abundance and that the success of biological control in this instance is critically dependent on atypical summer development of the parasitoid.
Cameron et al. (1993) - Microctonus aethiopoides is categorised as exerting “substantial” control (defined as “other control measures are only occasionally required”) over S. discoideus.
Goldson et al. (2020) - no host resistance of S.discoideus to M. aethiopoides (Moroccan strain) in lucerne has been found over the 35 years since the release of the parasitoid. [This observation is made in the context of the collapse of control of Listronotus bonariensis (Argentine stem weevil) by the parthenogenetic Microctonus hyperodae after approximately 14 generations, and concern for the ongoing successful control of Sitona obsoletus (clover root weevil) by the parthenogenetic Microctonus aethiopoides (Irish strain). Microctonus aethiopoides (Moroccan strain), by contrast, reproduces sexually.]
Impacts on non-targets:
Goldson & Proffitt (1991) - during a 1990 trial of an electric blanket to collect Listronotus bonariensis (Argentine stem weevil) over the winter months, unexpectedly high levels of parasistism of this weevil by M. aethiopoides were briefly found: 22-34% in July, though dropping to around 2% August-November. Peak parasitism in weevils obtained by sweep-netting in the same vicinity was much lower, never more than 14% and usually less than 2%, indicating the electric blanket may have selectively attracted parasitised weevils.
McNeill et al. (1993) - opportunist parasitism by M. aethiopoides has been recorded in the New Zealand native weevil Irenimus aequalis.
Ferguson et al. (1994) - in surveys at 88 lucerne stands throughout Otago and Southland in the summer of 1993-94 the following non-target weevils were recorded: 15 native species in the genera Irenimus, Nicaeana, Brachyolus and Capoptes, and three introduced species. Of the natives, seven individuals comprising four species of Irenimus were parasitised; of the introduced weevils, two individuals of Listronotus bonariensis (the pest Argentine stem weevil) and one Rhinocyllus conicus (nodding thistle receptacle weevil, a biocontrol agent introduced against nodding thistle) were parasitised. Parasitism was ostensibly by M. aethiopoides - while the identity was not positively confirmed, characters were consistent with this parasitoid. The capacity of M. aethiopoides to parasitise R. conicus has been demonstrated in the laboratory. Previous studies have shown M. aethiopoides parasitism of L. bonariensis at levels of up to 2% in Canterbury [Goldson & Proffitt (1991) - see above] and up to 5% in Otago, and it has been recorded from the native weevil Irenimus aequalis in Canterbury (South Island) [McNeill et al. (1993) - see above] and Waikato (North Island). Microctonus aethiopoides was released after limited host range testing; the lack of an adequate environment impact assessment study prior to release is of concern.
Barratt et al. (1997) - laboratory host range tests were carried out to investigate potential non-target hosts of M. aethiopoides and surveys conducted to investigate non-target parasitism by this parasitoid in the field. In the laboratory, M. aethiopoides oviposited in 11 of the 12 species to which it was exposed, including all seven native species, and successfully parasitised (completed development in) 9 species, including Rhinocyllus conicus [introduced as a biocontrol of nodding thistle] and all but one native species. (While pre-release host specificity testing for M. aethiopoides was limited, R. conicus was included with apparently no evidence of parasitism.) Laboratory parasitism levels were similar to those achieved in S. discoideus, the target host, although prepupal emergence from native species was about 55% of that which occurred in S. discoideus. In the field M. aethiopoides was found parasitising 10 native species (Nicaeana sp. 1, N. cervina, Irenimus aemulator, I. aequalis, I. albosparsus, I. egens, I.stolidus, I. sp. 53, Nonnotus albicans and Steriphus variabilis) and three non-target introduced species (Rhinocyllus conicus, Listronotus bonariensis [the pest Argentine stem weevil] and Atrichonatus taeniatulus). Parasitism levels ranged from 1.6 to 71.4%. Most of the parasitism was in the agricultural environment, however, 10% of L. bonariensis found at 1,650 m on Coronet Peak, Central Otago, were parasitised by M. aethiopoides. Of the 11 weevil species which were parasitised in the laboratory, three have as yet not been found parasitised in the field: Trachyphloeus porculus, Zenagraphus metallescens (both natives) and Trichosirocalus horridus [introduced as a biocontrol of nodding thistle]. It is apparent that M. aethiopoides is successfully parasitising a range of weevil species in the field; to date, weevils in 7 genera in 3 tribes of 2 subfamilies have been recorded as hosts. The high level of parasitism in some native species in pasture, sometimes distant from lucerne stands, suggests that M. aethiopoides populations may be, to some extent, sustained on native species.
Barratt et al. (2000) - pasture surveys at three sites in Otago, three in Canterbury and one in Waikato between September 1993 and October 1998 found M. aethiopoides parastising the native weevils Irenimus egens, I. stolidus, I. aemulator, I. aequalis, Nicaeana sp., N. cervina and Steriphus variabilis. Native weevils parasitised by M. aethiopoides were found at all sites, reaching over 30% at the Hamilton (Waikato) site and 50-70% at Kyeburn (Otago). Only at Kyeburn (Otago) were parasitism levels high enough (in I. aemulator and N sp.) to have had a possible impact on the densities of native weevil populations. Parasitism was highest in January, when the mean percentage of native weevils parasitised was about 36%. It is uncertain if M. aethiopoides can sustain itself on non-target species or if native species are attacked by parasitoids which have originated from S. discoideus populations, although it has demonstrated in the laboratory that M. aethiopoides can develop successfully through at least three successive generations of N. cervina.
McNeill et al. (2002) - in surveys between 1992 and 2000 in ryegrass pastures in Canterbury M. aethiopoides was recovered from Listronotus bonariensis (Argentine stem weevil, a pest of ryegrass) at 83% of the 65 sampling sites. Levels of parasitism varied widely up to 18%. In contrast, in surveys between 1992 and 1999 in several North Island regions M. aethiopoides was recovered from L. bonariensis at only 10 of 136 sites. The sites of these recoveries were from Waikato, Bay of Plenty, Taranaki, Manawatu and Northland. Parasitism rates at positive sites averaged 2.2%, with a maximum of 8.4%. In surveys between 1998 and 2000 in Wairarapa, North Island, M. aethiopoides was recovered only twice from 29 collections with a mean parasitism rate of 0.4%. In Canterbury, parasitism of L. bonariensis by M. aethiopoides was negatively correlated with parasitism by Microctonus hyperodae [introduced as a bioncontrol of L. bonariensis in 1991]; parasitism by M. aethiopoides has declined as parasitism by M.hyperodae has increased. Other field studies have showed that the native weevil, Irenimus egens, is preferred as a host by M. aethiopoides over L. bonariensis.
Barratt (2004) - in laboratory host range testing in addition to that reported by Barratt et al. (1997) [see above], three of seven weevil species not tested by Barratt et al. (1997) were parasitised by M. aethiopoides, including two of four native species. Eleven New Zealand native species and five introduced species have been found to be parasitised by M. aethiopoides in the field. Non-target field hosts recorded here but not reported from the field by Barratt et al. (1997) include the native weevil Eugnomus sp.
Barlow et al. (2004) - parasitism levels by M. aethiopoides of up to 30% per year (and averaging 15%) have been recorded in populations of native Nicaeana weevils at Kyeburn in Otago. Modelling the impact of parasitism estimated an 8% population suppression from an average of 15% parasitism. The model also predicted a 35% suppression of populations of these weevils in the Lammerlaw-Rock and Pillar Range area of Otago, where currently parasitism levels are very low (<1%), should parasitism levels there reach an average of 15%.
Barratt et al. (2007) - a field study was carried out at three locations in Otago, South Island, between November 1996 and April 2004 to investigate non-target parasitism by M. aethiopoides over an altitudinal sequence from the target host habitat (lucerne) into native grassland. Seven non-target weevil species were found to be parasitised (Eugnomus sp., Irenimus egens, I. duplex, I. stolidus, Listronotus bonariensis, Nicaeana cervina and N. fraudator). All but L. bonariensis (Argentine stem weevil) are New Zealand natives. Parasitism of nontarget species was approximately 2% overall. Substantial nontarget parasitism was found at only one of the locations, with up to 24% parasitism of the native weevil, Nicaeana fraudator. The data provide no evidence of a population decline of this species over the five years of sampling at that location. This study showed that there are a number of native species that are consistently parasitised in the field by M. aethiopoides in semi-native grassland environments, and confirmed earlier work suggesting that weevils in the genus Nicaeana seem to be particularly susceptible. Still unknown is whether M. aethiopoides is able to complete successive generations entirely on nontarget species outside of the target host environment, or alternatively, to what extent parasitism is contingent on “spillover” from the target environment through the dispersal activity of parasitised S. discoideus.
Barratt et al. (2012) – the Moroccan strain of M. aethiopoides (i.e. the Sitona-associated biotype) has been found to attack 19 non-target weevil species in the field in New Zealand, including 14 native species. Most New Zealand non-target hosts are members of the subfamily Entiminae in the tribe Leptopiini. Known non-target field hosts in addition to those reported in the entries above are the natives Irenimus similis and Nicaeana cinerea, and the adventive Listroderes delaiguei. Recent host range surveys in Morocco and Australia indicate the host range in New Zealand is much greater than in either of those countries. In New Zealand the parasitoid was released after limited host-specificity testing; had the Moroccan and Australian data been available, the absence of Leptopiini in Morocco and the record of a native Australian leptopiine host could have indicated that native weevils in this tribe in New Zealand might be at risk of attack by M. aethiopoides.
Ferguson et al. (2016) - at least 14 species of New Zealand native weevils are parasitized by M. aethiopoides in pasture and native tussock grasslands at higher elevations. A trial in high altitude tussock grassland (Lammermoor Range, Central Otago) showed non-target parasitism of native weevils is very low. Evidence suggests that 'spillover' of M. aethiopoides from pasture into this environment probably occurs, and that there is also establishment of local populations of the parasitoid. Low temperatures could be constraining parasitoid populations and therefore parasitism rates; predicted temperature rises with climate change could affect the dynamics of M. aethiopoides parasitism of non-target weevils in such native environments.
Paynter et al. (2022) - a retrospective study compiled previously published laboratory host testing records for M. aethiopoides, Moroccan strain in New Zealand and field host records in New Zealand for those hosts parasitised in the laboratory. In addition, targeted field surveys (focusing on weevils that supported some parasitoid development during host specificity testing but had not previously been confirmed as field hosts) were carried out. Hosts for which rates of field parasitism of more than 10% have been recorded were classified as “major field hosts”. Rates below 10% (considered a conservative threshold) are unlikely to have significant population level impacts on the hosts. Laboratory parasitism has been recorded in 15 of 17 species tested against M. aethiopoides, Moroccan strain. Of those 15 species, eight non-target “major field hosts” and one other non-target field host are recorded. Major field hosts are the natives Chalepistes aequalis (previously lrenimus aequalis), C. egens (I. egens), C. stolidus (I. stolidus), C. tenebricus (l. aemulator), Nicaeana cervina and Steriphus variabilis, and the introduced species Listronotus bonariensis and Rhinocyllus conicus. The other field host is the native Chalepistes similis (Irenimus sp. 3).
References
Barlow ND, Barratt BIP, Ferguson CM, Barron MC (2004). Using models to estimate parasitoid impacts on nontarget host abundance. Environmental Entomology. Vol 33 (4). 941-948 https://academic.oup.com/ee/article/33/4/941/447790
Barlow ND, Goldson SL (1993). A modelling analysis of the successful biological control of Sitona discoideus (Coleoptera: Curculionidae) by Microctonus aethiopoides (Hymenoptera: Braconidae) in New Zealand. Journal of Applied Ecology 30(1): 165-178 https://doi.org/10.2307/2404280
Barratt BIP (2004). Microctonus parasitoids and New Zealand weevils: Comparing laboratory estimates of host ranges to realized host ranges. Assessing Host Ranges of Parasitoids and Predators used for Biological Control; A guide to Best Practice. Van Driesche, R.G. and Reardon, R. (Ed.s) Forest Health Technology Enterprise Team - Morgantown, West Virginia. September 2004. 243p.
Barratt BIP, Evans AA, Ferguson CM, Barker G, McNeill MR, Phillips CB (1997). Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and M. hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Environmental Entomology 26: 694-702 https://doi.org/10.1093/ee/26.3.694
Barratt BIP, Evans AA, Ferguson CM, McNeill MR, Addison P (2000). Phenology of native weevils (Coleoptera: Curculionidae) in New Zealand pastures and parasitism by the introduced braconid, Microctonus aethiopoides Loan (Hymenoptera: Braconidae). NZ Journal of Zoology 27: 93–110 https://www.tandfonline.com/doi/pdf/10.1080/03014223.2000.9518215
Barratt BIP, Ferguson CM, Bixley AS, Crook KE, Barton DM, Johnstone PD (2007). Field parasitism of nontarget weevil species (Coleoptera: Curculionidae) by the introduced biological control agent Microctonus aethiopoides Loan (Hymenoptera: Braconidae) over an altitude gradient. Environmental Entomology 36(4): 826-839 https://doi.org/10.1093/ee/36.4.826
Barratt BIP, Oberprieler RG, Barton DM, Mouna M, Stevens M, Alonso-Zarazaga MA, Vink CJ, Ferguson CM (2012). Could research in the native range, and non-target host range in Australia, have helped predict host range of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a biological control agent introduced for Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in New Zealand? BioControl 57: 735–750 https://doi.org/10.1007/s10526-012-9453-3
Cameron PJ, Hill RL, Bain J, Thomas WP (1989). A Review of Biological Control of Invertebrate Pests and Weeds in New Zealand 1874-1987. Technical Communication No 10. CAB International Institute of Biological Control. DSIR Entomology Division. 424p.
Cameron PJ, Hill RL, Bain J, Thomas WP (1993). Analysis of importations for biological control of insect pests and weeds in New Zealand. Biocontrol Science and Technology 3(4): 387-404
Ferguson CM, Kean JM, Barton DM & Barratt BIP (2016). Ecological mechanisms for non-target parasitism by the Moroccan ecotype of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) in native grassland. Biological Control 96: 28-38
Ferguson CM, Roberts GM, Barratt BIP, Evans AA, Popay AJ (1994). The distribution of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae) in southern South Island Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) populations. Proceedings of the New Zealand Plant Protection Conference 47: 261-265 https://journal.nzpps.org/index.php/pnzppc/article/view/11108/10958
Goldson SL, Barker GM, Chapman HM, Popay AJ, Stewart AV, Caradus JR, Barratt BIP. (2020). Severe insect pest impacts on New Zealand pasture: the plight of an ecological outlier. Journal of Insect Science 20(2): 1–17
Goldson SL, Proffitt JR (1896). The seasonal behaviour of the parasite Miroctonus aethiopoides and its effect on sitona weevil. Proceedings of the New Zealand Weed and Pest Control Conference 39: 122-125 https://journal.nzpps.org/index.php/pnzwpcc/article/view/9393/9225
Goldson SL, Proffitt JR (1991). Use of an electric blanket for winter field collection of Argentine stem weevil, Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). New Zealand Entomologist 14(1): 44–47
Goldson SL, Proffitt JR, McNeill MR (1990). Seasonal biology and ecology in New Zealand of Microctonus aethiopoides (Hymenoptera: Braconidae), a parasitoid of Sitona spp. (Coleoptera: Curculionidae), with special emphasis on atypical behaviour. Journal of Applied Ecology 27(2): 703-722 https://doi.org/10.2307/2404313
Goldson SL, Proffitt JR, Muscroft-Taylor KE (1993). The economic value of achieving biological control of Sitona discoideus. Proceedings of a New Plant Protection: Costs, Benefits and Trade Implications. Suckling, D.M. and Popay, A.J. (Eds) Zealand Plant Protection Society Symposium, Christchurch, New Zealand 1993. 161p
McNeill MR, Kean JM, Goldson SL (2002). Parasitism by Microctonus aethiopoides on a novel host, Listronotus bonariensis, in Canterbury pastures. New Zealand Plant Protection 55: 280-286 https://journal.nzpps.org/index.php/nzpp/article/view/3953/3781
McNeill MR, Phillips CB, Goldson SL (1993). Diagnostic characteristics and biology of three Microctonus spp. (Hymenoptera: Braconidae, Euphorinae) parasitoids of weevils (Coleoptera: Curculionidae) in New Zealand pasture and lucerne. New Zealand Entomologist 16(1): 39-44 https://doi.org/10.1080/00779962.1993.9722648
Paynter Q, Barton DM, Ferguson CM, Barratt BIP (2022). Relative risk scores generated from laboratory specificity tests predict non-target impacts of Microctonus spp. parasitoids in the field. Biological Control, Volume 170, July 2022, 104927 https://doi.org/10.1016/j.biocontrol.2022.104927
Stufkens MW, Farrell JA, Goldson SL (1987). Establishment of Microtonus aethiopoides, a parasitoid of the sitona weevil in New Zealand. Proceedings of the New Zealand Weed and Pest Control Conference 40: 31-35 https://journal.nzpps.org/index.php/pnzwpcc/article/view/9939/9771
Vink CJ, Barratt BIP, Phillips CB, Barton DM (2012). Moroccan specimens of Microctonus aethiopoides spice our understanding of genetic variation in this internationally important braconid parasitoid of adult weevils. BioControl 57: 751–758 https://doi.org/10.1007/s10526-012-9450-6
Vink CJ, Phillips CB, Mitchell AD, Winder LM, Cane RP (2003). Genetic variation in Microctonus aethiopoides (Hymenoptera: Braconidae). Biological Control 28(2): 251-264 https://doi.org/10.1016/S1049-9644(03)00103-8
