Assessing the non-target impacts of classical biological control agents: is host-testing always necessary?

Release of a biocontrol agent in New Zealand is typically preceded by non-target testing of native or valued species. Nevertheless, if both the target pest and the natural enemy are very different from any native fauna, then there may be no scientific justification for host testing. Gonatocerus ashmeadi (Girault) (Hymenoptera: Mymaridae) is being considered as a biocontrol agent for glassy winged sharpshooter, Homalodisca vitripennis (Germar) (Hemiptera: Cicadellidae), should the pest arrive. An assessment of the potential impact of G. ashmeadi on New Zealand’s Cicadellidae and Membracidae, from published literature data, indicates that none of these insects is at risk, as their eggs will not be recognised by the parasitoid because either their size or location places them outside the parasitoid’s search pattern. Consequently, there is no scientific case for any non-target host-testing to be carried out in containment.     

Parasitism of the lucerne pest Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) and non-target weevils by Microctonus aethiopoides Loan (Hymenoptera: Braconidae) in south-eastern Australia, with an assessment of the taxonomic affinities of non-target hosts of M. aethiopoides recorded from Australia and New Zealand

Abstract  The braconid parasitoid Microctonus aethiopoides Loan has been released in Australia and New Zealand for biological control of the lucerne pest Sitona discoideus Gyllenhal. In New Zealand, the parasitoid attacks a number of endemic weevil species. A survey of Curculionoidea found in and near lucerne in south-eastern Australia was carried out to investigate whether similar non-target parasitism was occurring, and to relate this to levels of parasitism found in the target host, S. discoideus . Some of the original M. aethiopoides release sites were particularly targeted in the survey of 25 sites in Victoria, New South Wales and South Australia. Almost 2500 weevils were collected, of which over 90% were S. discoideus , with the remaining 197 other weevils comprising 29 species found at 15 of the 25 sites. Parasitism of S. discoideus by M. aethiopoides occurred at 12 lucerne sites, with levels ranging from 0 to 25%. A single incidence of parasitism of a species of an Australian native weevil Prosayleus sp. by M. aethiopoides was recorded. No parasitism of any other weevil species was observed. The taxonomic affinities between Sitona and native Australian and New Zealand weevils are discussed, concluding that non-target host range in M. aethiopoides may be determined more by ecological factors than by taxonomic affinities among its hosts.     

Reproductive characteristics of invasive hyperparasitoid Baeoanusia albifunicle have implications for the biological control of eucalypt pest Paropsis charybdis

Hyperparasitoids can impede the establishment of primary parasitoid biological control agents or limit their control capacity. Although modern quarantine practices generally prevent hyperparasitoids being introduced with biological control agents, introductions can occur via natural pathways or accidentally with incoming passengers and cargo. In New Zealand, Baeoanusia albifunicle Girault is a self-introduced hyperparasitoid of Enoggera nassaui Girault, an intentionally introduced control agent of the eucalypt pest Paropsis charybdis Stål. A self-introduced primary parasitoid, Neopolycystus insectifurax (Girault), also parasitises P. charybdis in New Zealand. We assessed B. albifunicle biology to better understand its potential to disrupt P. charybdis control. It was determined that B. albifunicle is an obligate solitary hyperparasitoid with a longer lifespan, lower fecundity and longer generation time than its host. The hyperparasitoid reduced effective parasitism by E. nassaui to <10% in the lab, indicating it may limit control of the first P. charybdis generation by slowing spring population growth. It was confirmed that N. insectifurax is not hyperparasitised by B. albifunicle and therefore has some potential to substitute for any hyperparasitoid-driven decline in E. nassaui.     

Development of Trichogramma australicum Girault (Hymenoptera: Trichogrammatidae) in Helicoverpa (Lepidoptera: Noctuidae) host eggs

Abstract Morphological studies of development of the egg parasitoid Trichogramma australicum Girault in the cotton bollworm, Helicoverpa armigera (Hübner), were conducted to provide benchmarks for assessing developmental rates in both natural hosts and artificial diets. Observations of living embryos and histological sections show that embryos proceed rapidly through cleavage and blastoderm formation and show a characteristic pinching or rotation 8 h after deposition. Eggs progressively increase in volume, primarily by increasing in diameter at the widest point. At 29 ± 1°C the duration of the egg stage is 22−24 h, the larval stage 27 h, the prepupal stage 50−52 h, and pupa 85 h. Larvae undergo dramatic shape changes as they ingest food but do not show signs of larval moults, reinforcing observations that there is only one larval instar. Criteria for staging the embryonic and postembryonic development in natural hosts will be used for future studies aimed at developing and refining artificial diets for Trichogramma.     

Potential non-target impact of Microctonus aethiopoides Loan (Hymenoptera: Braconidae) on Cleopus japonicus Wingelmüller (Coleoptera: Curculionidae), a biocontrol agent for putative release to control the butterfly bush Buddleja davidii Franchet in New Zealand

Abstract  Cleopus japonicus Wingelmüller (Coleoptera: Curculionidae) is being considered for release to control buddleia Buddleja davidii in New Zealand. As part of the pre-release testing, Moroccan and Irish biotypes of the solitary endoparasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae) were evaluated for potential non-target impacts on adult C. japonicus should release occur. Laboratory experiments evaluated both the behavioural and physiological suitability of C. japonicus to both biotypes of the parasitoid. Parasitoid behavioural attraction was assessed using the pathenogenic bacterium Serratia marcescens (Enterobactereaceae), as an indicator of ovipositor penetration. Physiological suitability was assessed by comparing parasitism of C. japonicus with the natural hosts of the respective parasitoid biotypes. The parasitoid-bacteria study showed that C. japonicus was behaviourally acceptable to both Moroccan and Irish M. aethiopoides , with the two experiments producing 34% and 8% mortality, respectively. Cleopus japonicus did not support development of either Moroccan or Irish M. aethiopoides biotypes. None of the weevils dissected at the end of the experiment contained immature parasitoids. Comparison between unexposed and parasitoid-exposed C. japonicus found no difference in premature mortality during the experiment nor in the number of fully reproductive females at its conclusion. The results of this study predict that should C. japonicus be released, the potential impact of M. aethiopoides on field populations will be negligible.     

Host preferences ofTrichogrammatoidea bactrae fumata (Hym.: Trichogrammatidae) an egg parasitoid of leafrollers (Lep.: Tortricidae)

Trichogrammatoidea bactrae fumata Nagaraja is a naturally occurring egg parasitoid of some leafrollers in New Zealand kiwifruit orchards. The parasitoid showed a distinct preference for younger host-eggs ofEpiphyas postvittana, in which it achieved a higher rate of successful development. Such a preference is not as apparent withCtenopseustis obliquana. Host-species preference experiments found that the parasitoid rarely attackedPlanotortrix octo, and successful wasp emergence from parasitised eggs of this host was low.Epiphyas postvittana was the preferred host whenT. bactrae fumata was reared on this species. When reared onC. obliquana, the parasitoid showed no preference forE. postvittana orC. obliquana.     

Hyperparasitoids of the gum leaf skeletoniser, Uraba lugens Walker (Lepidoptera: Nolidae), with implications for the selection of a biological control agent for Uraba lugens in New Zealand

Abstract  The hyperparasitoids reared from three species of primary parasitoids of the gum leaf skeletoniser, Uraba lugens Walker (Lepidoptera: Nolidae) collected in South Australia and Tasmania are recorded and discussed. Seven hyperparasitoids were reared. Diatora sp. and ? Paraphylax sp. (Ichneumonidae: Cryptinae); Tetrastichus sp. (Chalcidoidea: Eulophidae); Megadicylus dubius (Girault) (Chalcidoidea: Pteromalidae) and Elasmus sp. (Chalcidoidea: Eulophidae) were reared from Cotesia urabae Austin and Allen (Braconidae: Microgastrinae). Megadicylus dubius , Elasmus sp. and Anastatus sp. (Chalcidoidea: Eupelmidae) were reared from Dolichogenidea eucalypti Austin and Allen (Braconidae: Microgastrinae). Pediobius bruchicida (Rondani) (Chalcidoidea: Eulophidae) was reared from Euplectrus sp. (Chalcidoidea: Eulophidae). This appears to be the first record of the cryptine ichneumonid genus Diatora Förster from Australia. Of the seven hyperparasitoid species reared, only one ( P. bruchicida ) is known to be present in New Zealand. Implications for the selection of a biological control agent for U. lugens in New Zealand are discussed. Some prior misidentifications of associated hyperparasitoids are noted.     

Key to the New Zealand species of Psyllaephagus Ashmead (Hymenoptera: Encyrtidae) with descriptions of three new species and a new record of the psyllid hyperparasitoid Coccidoctonus psyllae Riek (Hymenoptera: Encyrtidae)

Abstract  This paper records seven species of wasps in the genus Psyllaephagus (Hymenoptera: Encyrtidae) from New Zealand. All of these species are primary parasitoids of psylloids (Hemiptera: Psylloidea). Two are species previously described from New Zealand: P. acaciae Noyes and P. pilosus Noyes. Two are described Australian species which have established recently: P. bliteus Riek and P. gemitus Riek. Three new species are described here, from New Zealand: P. breviramus sp. nov., P. cornwallensis sp. nov. and P. richardhenryi sp. nov. All species are probably Australian in origin. A key to all seven Psyllaephagus species known from New Zealand is provided. An earlier first record of the Australian psyllid hyperparasitoid Coccidoctonus psyllae Riek (Hymenoptera: Encyrtidae), previously first recorded from New Zealand in 2006, is noted.     

Differences in egg parasitism of Chrysophtharta agricola (Chapuis) (Coleoptera: Chrysomelidae) by Enoggera nassaui Girault (Hymenoptera: Pteromalidae) in relation to host and parasitoid origin

Abstract The first instances of egg parasitism of Chrysophtharta agricola , a pest of eucalypt plantations, are recorded. Enoggera nassaui was found parasitising C. agricola egg batches in Tasmania, the Australian Capital Territory (ACT), New South Wales and Victoria: this is the first record of this parasitoid species from Victoria. One instance of Neopolycystus sp. parasitising C. agricola eggs in Victoria was also recorded. Parasitism of egg batches by E. nassaui ranged from 0 to 55% between five geographical populations collected in mainland Australia ( n  = 45), and from 0 to 2% between two populations collected in Tasmania ( n  = 300). For mainland sites at which parasitism was recorded, parasitism rates within sites differed significantly from either population in Tasmania. Reciprocal exposure experiments using one Tasmanian (Florentine Valley) and one parasitised mainland (Picadilly Circus, ACT) population were conducted in the laboratory to examine whether these different parasitism rates were attributable to egg or parasitoid origin. Parasitoids from the ACT parasitised C. agricola eggs of both origins more successfully than parasitoids from Tasmania, with up to 65% wasp emergence compared with 33% from Tasmania. Parasitoid origin significantly affected the number of wasps that emerged from exposed batches, but not the total loss from parasitism.     

The hymenopteran parasitoids of light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) in Australia

Abstract  Epiphyas postvittana (Walker) is a serious pest of a number of horticultural crops including grapes in Australia and New Zealand. This study brings together information on the parasitoid complex associated with E. postvittana that previously was fragmented and largely inaccessible. We include species reared during a 3-year study of the parasitoids of E. postvittana in the vineyards of the Coonawarra region, South Australia, material from several Australian agricultural insect collections and records from the literature. An illustrated key is presented for 25 species of parasitoids and hyperparasitoids associated with E. postvittana , along with information on the taxonomy, identification, distribution and biology of each species. Taxa newly recorded from this host are Perilampus sp. (Perilampidae), and six species of Ichneumonidae: Euceros sp., Labium sp., Netelia sp., Plectochorus sp., Temalucha minuta (Morley) and Eriborus epiphyas sp. n., the latter species being described in full.     

Geographic Variation in Egg Load of Microctonus hyperodae Loan (Hymenoptera: Braconidae) and its Implications for Biological Control Success

Eight South American geographic populations of the parthenogenic, proovigenic, koinobiont parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae: Euphorinae) were introduced to New Zealand to assist management of the pasture pest Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). Geographic variation in fecundity has been suggested as a reason for the populations' differential successes in establishing in New Zealand. This study investigated whether geographic variation in fecundity was due to corresponding variation in pre-oviposition egg load (other possible sources of fecundity variation include searching efficiency, egg survival and female longevity). Variation in egg load accounted for that in fecundity, but also showed that the variation in fecundity was not as great as it had first appeared. Geographic variation in egg load did not explain the pattern of population establishment observed in New Zealand. Egg load was proportional to parasitoid size and this relationship was stronger in populations originating from west, rather than east, of the Andes. A new method for making parasitoid eggs visible is described.     

A prospective model for the phenology of Microctonus hyperodae (Hymenoptera: Braconidae), a potential biological control agent of argentine stem weevil in New Zealand

A predictive phenological model is described for the parasitoid Microctonus hyperodae, introduced to New Zealand as a potential biological control agent against Argentine stem weevil Listronotus bonariensis. The model is based on development/temperature relationships obtained from experiments on the parasitoid in quarantine prior to its release, allowing early predictions of its phenology in different parts of the target pest's New Zealand range. In particular the model was used to predict the number of parasitoid generations each year, the degree of temporal synchrony between parasitoid adults and the susceptible adult pest stage, the order of parasitism and reproduction in the pest's life cycle as a possible basis for a simplified, discrete host/parasitoid population model, and the likely significance of ecotypic differences in development and diapause characteristics of the parasitoid. These applications demonstrate the potential for simple models to help in climate matching of classical biological control agents and estimation of their interaction with pest dynamics, using data obtainable prior to their introduction and release. In addition the model proved useful as a decision aid during the release programme, by indicating the likely effects of unusual weather and the need or otherwise for further parasitoid releases.     

Systematic mass rearing and release ofMicroctonus hyperodae (Hym.: Braconidae,Euphorinae), a parasitoid of the argentine stem weevilListronotus bonariensis (Col.: Curculionidae) and records of its establishment in New Zealand

The method whereby equal numbers of seven ecotypes of the parasitoidMicroctonus hyperodae Loan (Hymenoptera: Braconidae, Euphorinae) were reared and released is described along with the reasons for doing so. This was achieved by variably intense rearing effort depending on the number of founder females in that particular ecotype. The parasitoid was released in three regions of New Zealand as a control agent of theListronotus bonariensis Kuschel (Col.: Curculionidae), a severe pest of New Zealand pastures. It was later recovered from all three regions.     

Survey of the parasitoids of the tuliptree aphid,Illinoia liriodendri (Hom: Aphididae), in northern California

A survey of the parasitoids ofIllinoia liriodendri (Monell) in northern California conducted from 1988–1990 revealed the presence of 12 primary and 14 hyper-parasitoid species. The most common primary parasitoid wasAphidius polygonaphis (Fitch), which was imported from the eastern United States in the 1970's and is now established throughout the area. New host records were noted forA. ervi Haliday,A. avenaphis (Fitch), Praon occidentale Baker,P. unicum Smith,Diaeretiella rapae M'Intosh,Lysiphlebus testaceipes (Cresson), andMonoctonus nervosus (Haliday) (all Hymenoptera: Braconidae: Aphidiinae), andAphelinus sp. nr.asychis Walker (Hymenoptera: Aphelinidae). The most common hyperparasitoid species werePachyneuron aphidis (Bouché) andAsaphes californicus Girault (both Hymenoptera: Pteromalidae). New hyperparasitoid host records were noted forPachyneuron californicum Girault on Aphidiine and Aphelinidae spp. andCoruna clavata Walker (Hymenoptera: Pteromalidae) onAphelinus sp.     

Evaluation of the biological control of the pink wax scale Ceroplastes rubens Maskell (Hom., Coccidae) with the introduced parasitoid Anicetus beneficus Ishii & Yasumatsu (Hym., Encyrtidae) in the Central province of Papua New Guinea

Abstract:  In order to evaluate the possibility of a classical biological control of the pink wax scale Ceroplastes rubens (Hom., Coccidae) with the parasitoid Anicetus beneficus (Hym., Encyrtidae), endemic parasitoids were collected (2000/2001) in three provinces in Papua New Guinea and parasitization levels were determined. Eight hymenopteran parasitoid species were identified: Aprostocetus sp. (Eulophidae), Coccophagus sp. (Aphelenidae), five Encyrtidae: Cheiloneurus sp., Coccidocnotus sp., Diversinervus sp., Metaphycus sp., Microterys sp. and Moranila sp. (Pteromalidae). Levels of parasitization were low, varying between 1.4 and 2.8%. A. beneficus was imported from Australia and 1100 specimens were released in spring 2002 at two locations with mango infested by C. rubens (Laloki and Tahira) in the Central Province . A. beneficus did establish at both sites. Six months after release, parasitization levels of C. rubens had increased from 2.8 to 5.9% (P  =  0.05) at Laloki and from 1.8 to 22.2% (P  =  0.01) at Tahira, with A. beneficus being the most frequent parasitoid (69% of all parasitoids). Workers of the ant genus Tapinoma (Dolichoderinae) were frequently collected from infested trees at Laloki, but were not present at Tahira. It is assumed that their presence is at least partly responsible for the lower degree of parasitization and number of A. beneficus at this site. The necessity of further studies is stressed.     

South American Origins of Microctonus hyperodae Loan (Hymenoptera: Braconidae) Established in New Zealand as Defined by Morphometric Analysis

Eight South American geographic populations of the thelytokous parasitoid Microctonus hyperodae Loan (Hymenoptera: Braconidae) were released in New Zealand in 1991 to assist in the suppression of the pasture pest Listronotus bonariensis (Kuschel) (Coleoptera: Curculionidae). With one exception, parasitoids from each South American geographic population were released in equal numbers at each New Zealand release site. It was postulated that the South American geographic population(s) best suited to the conditions encountered at each New Zealand release locality would eventually become prevalent there. A morphometric analysis of adult parasitoids of known South American origins, reported previously, allowed M. hyperodae derived from west of the Andes (i.e. two collection sites in Chile) to be distinguished from parasitoids derived from east of the Andes (i.e. three collection sites in Argentina and one each in Brazil and Uruguay). Parasitoids derived from a fourth site in Argentina (S. C. de Bariloche) could not be clearly discriminated from either the 'east of the Andes' or 'west of the Andes' categories. A morphometric analysis of M. hyperodae adults collected from five of the New Zealand release sites from 1992-1994 is presented in this contribution. The analysis indicated that parasitoids derived from east of the Andes were significantly more prevalent than expected. The possible reasons for the initial success in New Zealand of one or more east of the Andes populations include the greater fecundity of M. hyperodae collected in Uruguay and the likelihood that M. hyperodae from east of the Andes co-evolved more recently with the stock from which New Zealand's L. bonariensis was founded.     

The ant-parasitic genus Rhipipalloidea Girault (Hymenoptera: Eucharitidae), with a description of a new species

The genus Rhipipalloidea Girault (1934 ), from the Australian region is revised. Rhipipalloidea gruberi Girault (1940 ) is synonymised with R. mira Girault 1934 . A new species, R. madangensis , is described from Papua New Guinea. This species is separated from R. mira from Australia by the distinct striation on the head, and ramose, 12-segmented antennae of the females. Males and a host for the genus are described for the first time.     

Plant hosts and parasitoid associations of leaf mining flies (Diptera: Agromyzidae) in the Canberra region of Australia

Abstract  Many leaf mining flies (Diptera: Agromyzidae) are important economic pests of agricultural crops and ornamental plants, and species-rich hymenopteran parasitoid complexes are important in their control. Australian agromyzids are poorly studied, and little is known about their host plants, ecology or natural enemies. We surveyed native and naturalised species of leaf mining flies in Tallaganda National Park, New South Wales and the Australian Capital Territory. Malaise and emergence trapping in Tallaganda yielded 70 agromyzid specimens from six species in four genera: Cerodontha Rondani, Liriomyza Mik, Phytoliriomyza Hendel and Phytomyza Fallen. Of the six species collected, three are Australasian species, two are naturalised species introduced from Europe and one could not be determined to species. The Australian Cerodontha ( Cerodontha ) milleri Spencer represented most of the individuals caught in both Malaise and emergence traps. A total of 163 agromyzid and 98 parasitic wasp specimens were reared from plant samples with agromyzid mines in the Canberra region. Most agromyzids and parasitoids were reared from the weed Sonchus oleraceus L. (Asteraceae). All the agromyzids reared belonged to two introduced species of the genera Phytomyza and Chromatomyia Hardy. The biodiversity of parasitic wasps reared was high with 14 species from seven genera and three families. Hemiptarsenus varicornis (Girault) (Eulophidae), a widespread Old World agromyzid parasitoid, was the most numerous parasitoid reared in our survey.     

Potential for classical biological control of the potato bug Closterotomus norwegicus (Hemiptera: Miridae): description, parasitism and host specificity of Peristenus closterotomae sp. n. (Hymenoptera: Braconidae)

The potato bug, Closterotomus norwegicus (Gmelin) (Hemiptera: Miridae) is an introduced pest of lucerne, white clover and lotus seed crops in New Zealand and a key pest of pistachios in California, USA. Efforts were made to identify potential biological control agents of C. norwegicus in Europe. A total of eight parasitoids, including six primary parasitoids from the genus Peristenus (Hymenoptera: Braconidae) and two hyperparasitoids from the genus Mesochorus (Hymenoptera: Ichneumonidae), were reared from C. norwegicus nymphs collected in various habitats in northern Germany. With a proportion of more than 85% of all C. norwegicus parasitoids, Peristenus closterotomae (Hymenoptera: Braconidae), a new species, was the most dominant parasitoid, whereas other parasitoid species only occurred sporadically. Peristenus closterotomae did not fit in the keys to any described species and is described as new to science. Parasitism caused by P. closterotomae was on average 24% (maximum 77%). To assess the host specificity of parasitoids associated with C. norwegicus, the parasitoid complexes of various Miridae occurring simultaneously with C. norwegicus were studied. Peristenus closterotomae was frequently reared from Calocoris affinis (Herrich-Schaeffer), and a few specimens were reared from Calocoris roseomaculatus (De Geer) and the meadow plant bug, Leptopterna dolobrata (Linnaeus) (all Hemiptera: Miridae). The remaining primary parasitoids associated with C. norwegicus were found to be dominant in hosts other than C. norwegicus. Whether nymphal parasitoids may potentially be used in a classical biological control initiative against the potato bug in countries where it is introduced and considered to be a pest is discussed.     

Early impact of endoparasitoid Microctonus hyperodae (Hymenoptera: Braconidae) after its establishment in Listronotus bonariensis (Coleoptera: Curculionidae) populations of northern New Zealand pastures

The South American curculionid Listronotus bonariensis (Kuschel) is an important pest of pastures in New Zealand. Population census data were gathered for L. bonariensis in northern New Zealand pastures during 1980-1983 in the absence of parasitism and again in 1991-1996 after the introduction and establishment of the braconid parasitoid Microctonus hyperodae Loan as a biological control agent. M. hyperodae achieved high rates of parasitism, with 75-90% of overwintering L. bonariensis parasitized within 3 yr of the parasitoid establishing at a site. Multistratum analysis of variance (ANOVA), with allowance for variation in host plant resource (numbers of Neotyphodium-free grass tillers), indicated reduction in the abundance of L. bonariensis life stages in the early part of life cycle. Although providing evidence for suppression of L. bonariensis, these analyses indicated the regulatory role of M. hyperodae was weak because L. bonariensis populations continued to exhibit marked intergenerational variability in abundance. Analyses of life tables indicated larval + pupal survival contributed most to intergenerational changes in abundance, irrespective of presence or absence of M. hyperodae. However, the density dependence of the stage survivals was modified in the presence of the parasitoid, with loss of density-dependent mortality in overwintering adults and increased density dependence in population natality. Regression analyses indicated dual contribution of parasitism and host plant resource to regulation of population natality and population trend in L. bonariensis. We conclude that M. hyperodae is a useful adjunct to host plant resistance in reducing the economic status of L. bonariensis populations in northern New Zealand pastures.