This article was downloaded by: [Emilio Guerrieri] On: 29 September 2011, At: 05:56 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
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Description and biological parameters of Ooencyrtus isabellae Guerrieri and Noyes sp. nov. (Hymenoptera: Chalcidoidea: Encyrtidae), a potential biocontrol agent of Zophiuma butawengi (Heller) (Hemiptera: Fulgoromorpha: Lophopidae) in Papua New Guinea Emilio Guerrieri
a b
c
, Catherine W. Gitau , Murray J. Fletcher
b
e
John S. Noyes , Charles F. Dewhurst & Geoff M. Gurr
c d
,
c
a
Institute for Plant Protection, the National Research Council of Italy, 80055, Portici (NA), Italy b
The Natural History Museum, SW7 5BD, London, UK
c
EH Graham Centre for Agricultural Innovation, Charles Sturt University, PO Box 883, Orange, NSW, 2800, Australia d
Orange Agricultural Institute, Department of Trade, Investment, Regional Infrastructure and Services (DTIRIS), Forest Road, Orange, NSW, 2800, Australia e
PNG Oil Palm Research Association, Kimbe 621, West New Britain, Papua New Guinea Available online: 29 Sep 2011
To cite this article: Emilio Guerrieri, Catherine W. Gitau, Murray J. Fletcher, John S. Noyes, Charles F. Dewhurst & Geoff M. Gurr (2011): Description and biological parameters of Ooencyrtus isabellae Guerrieri and Noyes sp. nov. (Hymenoptera: Chalcidoidea: Encyrtidae), a potential biocontrol agent of Zophiuma butawengi (Heller) (Hemiptera: Fulgoromorpha: Lophopidae) in Papua New Guinea, Journal of Natural History, 45:43-44, 2747-2755 To link to this article: http://dx.doi.org/10.1080/00222933.2011.616272
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Journal of Natural History Vol. 45, Nos. 43–44, November 2011, 2747–2755
Description and biological parameters of Ooencyrtus isabellae Guerrieri and Noyes sp. nov. (Hymenoptera: Chalcidoidea: Encyrtidae), a potential biocontrol agent of Zophiuma butawengi (Heller) (Hemiptera: Fulgoromorpha: Lophopidae) in Papua New Guinea Emilio Guerrieria,b* , Catherine W. Gitauc , Murray J. Fletcherc,d , John S. Noyesb , Charles F. Dewhurste and Geoff M. Gurrc a
Institute for Plant Protection, the National Research Council of Italy, 80055 Portici (NA) Italy; The Natural History Museum, SW7 5BD London, UK; c EH Graham Centre for Agricultural Innovation, Charles Sturt University, PO Box 883, Orange, NSW 2800, Australia; d Orange Agricultural Institute, Department of Trade, Investment, Regional Infrastructure and Services (DTIRIS), Forest Road, Orange, NSW 2800, Australia; e PNG Oil Palm Research Association, Kimbe 621, West New Britain, Papua New Guinea
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b
(Received 3 May 2011; final version received 17 August 2011; printed 27 September 2011) The planthopper Zophiuma butawengi (Heller) (= Z. lobulata Ghauri) is a serious pest of coconut and oil palm in Papua New Guinea, causing palm decay known as Finschhafen disorder. Recently, two dominant species of parasitoids emerged from egg masses of this pest, namely Parastethynium maxwelli (Girault) (Hymenoptera: Mymaridae) and an undescribed species of Ooencyrtus Ashmead (Hymenoptera: Encyrtidae). The latter species, here described, appears to be a potential biocontrol agent of Z. butawengi especially in the New Britain Province of Papua New Guinea. Biological features of the new species, i.e. development time and adult longevity, were also calculated to give information that could help in its use in biological control programmes. Keywords: Zophiuma lobulata; Ooencyrtus minor; Ooencyrtus major; Ooencyrtus shakespearei; Ooencyrtus uthetheise
Introduction The planthopper Zophiuma butawengi (Heller) (= Z. lobulata Ghauri; Gitau, Fletcher et al. 2011) (Hemiptera: Lophopidae) is considered a serious pest of coconut (Cocos nucifera L.) and oil palm (Elaeis guineensis Jacq.) in Papua New Guinea (PNG) (Ghauri 1967; Smith 1980a,b; Gitau, Gurr et al. 2011). It causes direct damage to palms because of its feeding activity (Smith 1980; Gitau, Gurr et al. 2011) resulting in chlorosis and subsequent necrosis on palm frond leaflets. This damage is known as Finschhafen disorder. During the last years, following field surveys of plant material infested by this pest, there has been a growing interest in the complex of autochthonous natural enemies of the planthopper that could represent a valid alternative to the synthetic pesticides still used to control Zophiuma infestations. Interestingly, high percentages of parasitism by two egg parasitoids, namely Ooencyrtus sp. (Hymenoptera: Encyrtidae) and Parastethynium maxwelli (Girault)
*Corresponding author. Email:
[email protected] ISSN 0022-2933 print/ISSN 1464-5262 online © 2011 Taylor & Francis http://dx.doi.org/10.1080/00222933.2011.616272 http://www.tandfonline.com
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(Hymenoptera: Mymaridae) (Gitau et al., unpublished data) were found. Both these species represent ideal candidates for classical and augmentative releases because they prevent development of the planthopper beyond the egg stage. By examining the material collected in PNG, and comparing it with that deposited at the Natural History Museum in London (UK) and at the Bishop Museum (Honolulu, Hawaii), it was determined that Ooencyrtus sp. was an undescribed species. In the framework of a potential biological control programme against Z. butawengi in PNG, we hereby describe the species and give further information on its biological parameters that could facilitate an efficient control of the pest on coconut and oil palm. These measures could be integrated by interventions of conservation biological control based on the choice and use of nectar-rich plants that provide food for adult wasps and hence encourage their activity as natural enemies of insect pests (Gurr et al. 1998; Baggen et al. 1999, Gitau et al. unpublished data).
Materials and methods Collection of Z. butawengi egg masses Zophiuma butawengi egg masses were collected from coconut, oil palm, betel nut (Areca catechu L.), banana (Musa sp.) and taro leaves (Colocasia sp.) in West New Britain, Milne Bay and Oro provinces of PNG where the planthopper and Finschhafen disorder are prevalent. The collection sites were Dami (5◦ 17’ S, 150◦ 24’ E), Kavui (5◦ 30’ S, 151◦ 02’ E), Numundo (5◦ 30’ S, 151◦ 02’ E), Siki (5◦ 30’ S, 151◦ 02’ E), Hagita (10◦ 19’ S, 150◦ 19’ E), Higaturu (8◦ 44’ S, 148◦ 11’ E), Igora (8◦ 79’ S, 148◦ 13’ E) and Joroba (8◦ 68’ S, 148◦ 43’ E). Leaf fragments bearing egg masses were excised using a pair of scissors or, when on the stem, were carefully scraped off using a clean scalpel blade. Egg masses were placed singly in aerated glass vials. The eggs were transported to the laboratory at the Papua New Guinea Oil Palm Research Association (PNGOPRA) Dami, where they were held at ambient temperatures and humidity (25–30◦ C, 72–93% relative humidity). They were inspected daily for emergence of parasitoids, which were used for the experiments described below. Non-parasitized eggs were used to establish a colony of Z. butawengi in a large holding cage that contained one coconut and one oil palm. Host cultures were occasionally boosted with fieldcollected Z. butawengi nymphs and adults. The eggs obtained from the palms in the holding cage were used as hosts in the study described below, assessing egg to adult development time.
Parasitoid identification Live parasitoids were killed in 70% ethanol and kept at – 20◦ C until preparation. All parasitoids were critical-point-dried (see Noyes 1982) and mounted on card for further examination. Selected card-mounted specimens were slide mounted following Noyes (1982). One of the paratypes, similar in size to holotype, was selected for drawings. Drawings of the main taxonomic features of the species were prepared using a Zeiss Microscope (Axioskop) with a drawing tube. Type material of morphologically similar species from similar hosts (at the Natural History Museum, London) and locations (at Bishop Museum, Hawaii) were examined. Mounted specimens were identified using available keys and by comparing them with material authoritatively identified
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in collections. Abbreviations used in the text include: BL, longest length of midbasitarsus; EL, eye length in lateral view; EW, eye width in lateral view; FV, minimum frontovertex width; FWL, maximum fore wing length; FWW, maximum fore wing width; GL, gonostylus (third valvula) length; HW, maximum head width; HWL, maximum hind wing length; HWW, maximum hind wing width; MS, the shortest length of malar space; MT, mid-tibia length; OCL, occipital–ocellar line (the shortest distance between posterior ocellus and occipital margin); OD, maximum diameter of posterior ocellus; OL, ovipositor length; OOL, ocular–ocellar line (the shortest distance between posterior ocellus and adjacent eye margin); POL, the shortest distance between posterior ocelli; SL, scape length (excluding radicle); SW, maximum scape width. Adult parasitoid longevity Longevity of males and females was determined under three treatments: honey + water, water alone and nil as control. Newly emerged parasitoids were sexed and held individually in glass vials. Honey was provided as a streak on the wall of the vials and water as a wet cotton-wool swab. Forty-eight individuals in total were tested for each treatment. The experiment was set up at ambient temperatures (25–30◦ C) and relative humidity (72–93%) in the laboratory at PNGOPRA. Parasitoids were monitored at 07.00 h and at 16.00 h daily. Egg to adult development time Newly emerged wasps were held in a vial, which was left under a table lamp for at least 6 hours to allow them to mate. The parasitoids were fed with a cotton-wool swab soaked in water and a streak of honey applied to the wall of the vial. Parasitoids were sexed and 10 females were randomly selected for experiments. Host egg masses were collected from the holding cage and those used in the tests were selected for uniformity of size and egg number. An individual female parasitoid was presented with a newly laid egg mass which was left in the vial for 24 h before removal. Thereafter, the egg mass was kept in the laboratory at PNGOPRA (temperature range of 25–30◦ C and relative humidity of 72–93%). The vials were checked daily for parasitoid and/or nymph emergence. Data analysis ® Data were analysed using GENSTAT (GENSTAT 13.1). Survival analysis was performed on the number of days the adult parasitoids lived. Parasitoids that died prematurely, e.g. those that were trapped in honey, were treated as censored during analysis. Kaplan–Meier estimates of the probability of survival (y-axis) for each treatment at any time (number of days) were plotted. Means, standard errors and 95% confidence intervals (CIs) for development time and number of progeny produced were computed. A 95% CI for the proportion of females emerging was calculated assuming a binomial distribution. Results Ooencyrtus isabellae Guerrieri and Noyes sp. nov
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Diagnosis Female. Overall length 0.85–1 mm; head black, with a green sheen; scape brown with apex yellow, flagellum yellow, last segment of clava dusky; mesoscutum dark green, scutellum basally dark green, distally with golden green reflections; legs white, tarsi yellow; fore wing very weakly uniformly infuscate; basal half of gaster yellow, distal part brown; frontovertex about one-sixth head width; scape about 2.4 times as long as broad, all funicular segments distinctly longer than broad, linear sensilla on F3–F6, clava three-segmented, sutures parallel, sensory area confined to apex; mandible with four teeth; scutellum hardly broader than long, basal two-thirds with sculpture coarser than that on mesoscutum, apical one-third shiny and smooth; fore wing about 2.6 times as long as broad, marginal vein about twice as long as broad, post-marginal vein about half as long as stigmal vein; mid-tibial spur shorter than corresponding basitarsus; ovipositor slightly longer than mid-tibia, gonostylus as long as mid-tibial spur, second valvifer with three subapical setae. Male. Similar to female except for darker colour, including darker fore wing venation and gaster entirely brown, and wider frontovertex, one-third as broad as head width. Antenna with all funicle segments longer than broad and covered in long setae, clava unsegmented. Description Female (holotype). Length, including ovipositor, 0.95 mm; excluding ovipositor 0.91 mm. Head black with a dark green sheen on frontovertex changing to emerald green towards mouth, anterior part of gena emerald green, posterior part with dark blue green sheen; antenna with radicle and basal two-thirds of scape brown, remaining parts yellow, apex of clava dusky; thorax dark brown with a dark green sheen on mesoscutum and basal half of scutellum, remaining part of scutellum with shiny golden green reflections; tegula dark brown; mesopleuron dark brown with a weak golden purple sheen; legs white except apex of each tibia (especially mid- and hind tibiae) and tarsi yellow; wings virtually hyaline but uniformly weakly infuscate, venation yellow, marginal vein appearing darker; basal half of gaster yellow (up to third tergite), remaining part brown with weak golden green sheen; gonostylus yellow. Head on frontovertex with moderately coarse, regular, polygonally reticulate sculpture of mesh size clearly smaller than eye facet; gena with shallower and more elongate sculpture; ocellar angle about 30◦ ; occipital margin rounded; narrowest point of frontovertex slightly in front of anterior ocellus; region between anterior ocellus and top of scrobes without setae except for those along eye margins; mouth margin covered with white setae; scrobes U-shaped; malar suture conspicuous; antenna (Figure 1A) with scape expanded, 2.4 times as long as broad; all funicular segments distinctly longer than broad, F3–F6 with linear sensilla, clava slender, pointed at apex, sensory area at apex only; mandible (Figure 1B) with four teeth. Relative measurements: HW 40, FV 6.5, OD 2, POL 2, OOL < 1, OCL 6.5, AOL > 4, EL 29.5, EW 26, MS 11, SL 17, SW 7. Thorax with fine, polygonally reticulate sculpture on mesoscutum that is shallower than that on frontovertex; basal half of scutellum with polygonally reticulate sculpture that is deeper than that on mesoscutum, distal half smooth and shiny; setae on mesoscutum thin and longer than those on the basal half of scutellum, setae on the
Journal of Natural History 2751
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A
D E
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Figure 1. Ooencyrtus isabellae Guerrieri and Noyes. Female: (A) antenna; (B) base of forewing; (C) mandible; (D) hypopygium; and. (E) ovipositor. Male: (F) antenna; and (G) genitalia.
remaining part of scutellum increasingly thicker and longer towards its apex; scutellum in profile virtually flat; mesopleuron over-reaching the base of gaster; fore wing venation and setation as in Figure 1C, marginal vein about twice as long as broad, post-marginal vein about half as long as stigmal vein, apex of costal cell with a line of seven or eight setae, linea calva open posteriorly, propodeum with a group of four or five setae around spiracle; mid-tibial spur shorter than corresponding basitarsus. Relative measurements: FWL 100, FWW 38, HWL 69, HWW 15. Hypopygium (Figure 1D) nearly reaching apex of gaster with posterior margin slightly produced medially; ovipositor (Figure 1E) hardly exerted, exerted part much less than one-tenth of length of gaster or about one-sixth of mid-tibial spur; gonostylus as long as mid-tibial spur. Paratype. Funicle with linear sensilla on F3–F6; hypopygium as in Figure 1D; second valvifer (Figure 1E) with three subapical setae. Relative measurements: OL 96, MT 81, GL 23, BL 23.
2752 E. Guerrieri et al. Male. Length 0.55–0.75 mm. Similar to female except for: smaller dimensions; darker colour, including darker fore wing venation and gaster entirely brown; wider frontovertex, one-third as broad as head width; antenna (Figure 1F) with all funicular segments longer than broad and covered in long setae; clava unsegmented; genitalia as in Figure 1(G). phallobase with short parameres, each with two setae, digiti each with a single hook.
Variation Not much in the available material. Female body length varies from 0.85 to 1 mm.
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Hosts All material has been reared from egg masses of Z. butawengi on coconut palm.
Distribution Papua New Guinea Material examined Holotype. Female, Papua New Guinea, West New Britain, Hoskins, Dami Otto’s Block, 21 m, 5◦ 17’ N 150◦ 24’ E, ex eggs of Zophiuma lobulata on coconut, 5 November 2009 (C. Gitau). Paratypes. Thirty-four females, nine males same data as holotype. Non-type material: 10 females and two males, same data as type material. Holotype, most paratypes and non type material deposited in the Natural History Museum, London, UK; five females and one male paratype are in the Department of Agricultural Entomology and Zoology “Filippo Silvestri”, University of Naples “Federico II” and five females and one male are in Papua ASCU. Etymology The species is named after Isabella Jane Good. Comments Among the known species of Ooencyrtus, O. isabellae appears very close to Ooencyrtus minor (Perkins) and Ooencyrtus major (Perkins) from Queensland, Australia whose type specimens have been examined (Perkins, 1906). All three species have quadridentate mandibles and the females have a completely yellow flagellum with terminal segment slightly dusky, completely white or pale yellow legs and yellow base of gaster. In addition, the three species share an expanded scape clearly less than three times as long as broad. Females of O. isabellae can be separated from those of O. minor and O. major (and several other undescribed species from Australia and PNG) by the relatively narrow frontovertex and the males by the uniformly pale yellow flagellum. Females of other species, including O. minor and O. major, have the frontovertex at least about one-third head width, compared with one-sixth in O. isabellae. Males of
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the other species have the flagellar segments at least partially dark brown whereas in O. isabellae the flagellum is unicolorous pale yellow. Running specimens through the only available key for Indo-Pacific Ooencyrtus (Huang and Noyes, 1994), O. isabellae runs to either O. neptunus Huang and Noyes or to the last couplet including O. shakespearei (Girault) and O. uthetheise (Risbec) with which it shares the coxal colour (never brown), lack of orange-yellow areas on the thorax and the basally orange-yellow gaster. Ooencyrtus isabellae can be separated from all named species by having a quadridentate mandible and frontovertex about one-sixth the head width. In O. neptunus, the mandible is tridentate and the frontovertex is about one-fifth the head width; in O. shakespearei and O. uthetheise the mandible has one small tooth and a broad truncation. In addition, O. shakespeari has the base of the tegula yellow (entirely brown in O. isabellae) whereas O. uthethesiae has the gonostyli entirely black (yellow in O. isabellae).
Adult longevity There was a significant difference between the survivor curves expressing the probability of surviving of the parasitoids after a given interval when provided with honey, water or nil (Figure 2; χ 2 = 122.7; df = 2; P < 0.001). Clearly the longevity of adult parasitoids was markedly enhanced by honey. The 95% CI for median survival time of the parasitoids while feeding on honey were 20.0–25.0 days. There was no difference in survival of the parasitoids between the water and nil treatments The 95% CI for median survival time of the parasitoids when presented with water was 2.0–2.0 whereas for nil, it was 1.5–2.0 days. There was no difference in survival between males and females (χ 2 = 0.746; df = 1; P = 0.388).
Egg to adult development time Mean development time for the parasitoids was 15.45 days with 95% CI 18.67–29.83. Mean total progeny produced was 24 with 95% CI 18.67–29.83. The proportion of females that emerged was 0.716 with 95% CI 0.6870–0.7447.
Discussion There is growing concern about the use of chemicals for the control of insect pests because of problems connected to pollution of the environment and quality of agricultural production. For these reasons environmentally friendly techniques for pest control are generally preferable when reliable and effective. With the introduction of host plants other than coconut that are suitable for Z. butawengi, there has been an increase in numbers of the planthopper (Prior et al. 2001; I. Orrell, personal communication). Current management of these pests, considered a major threat to oil and coconut palms especially for the symptoms known as Finschhafen disorder, is based on repeated application of systemic organophosphate insecticides (targeted trunk injection, TTI), with well-known undesirable adverse effects on the environment. Interestingly field surveys indicated the presence of at least two potential antagonists, both attacking the egg masses, that could replace at least partially the use of pesticides.
1.0
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0.6 0.4 0.0
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Probability of survival
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0.8
Honey Water Nil
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25
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35
Days alive Figure 2. Survivor functions for Ooencyrtus isabellae when fed on honey, water or nil diet.
One of the two, described here for promoting its use in potential biological control programmes, appears particularly promising considering its biological parameters. Female longevity is directly associated with fecundity regardless of whether the species is pre- or synovigenic. Longevity is significantly enhanced by food availability for adults (e.g. honey) suggesting that provision of natural (nectar-rich plants) or artificial (water and honey) sources of food could increase the parasitoids’ efficiency (Baggen et al. 1999; Gitau et al., unpublished data). This perfectly applies to O. isabellae whose longevity nearly doubles in the presence of honey in respect to water. Moreover, it has been recorded that the emergence of O. isabellae in the field has been steady and continuous throughout the year and seasons (Gitau et al., unpublished data) and this makes it impossible to use pesticides at any time during cultivation without direct effects on parasitoid populations. Alternatively, given the high exploitation of the egg masses in the laboratory, inundative control could be pursued to control the populations of Z. butawengi since its appearance in the field. The activity of O. isabellae does not contrast with that of P. maxwelli, but the two seem to occupy different times and niches (Gitau et al. unpublished data). Ooencyrtus isabellae seems more abundant in West New Britain whereas P. maxwelli dominates on mainland PNG (Huber et al. 2011). Indeed, only a small percentage of egg masses (about 5%) was found to be attacked by
Journal of Natural History 2755 the two species and this possibly suggests that a cross-inoculation in the areas where only one species occurs could lead to better control of the pest.
Acknowledgements This paper is an output of a project funded by the Australian Centre for International Agricultural Research (ACIAR) grant CP/2006/063 entitled “Integrated pest management for Finschhafen Disorder of oil palm in Papua New Guinea”. The authors thank PNGOPRA entomology staff for their assistance in collecting egg masses of Zophiuma butawengi from the field.
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References Baggen LR, Gurr GM, Meats A. 1999. Flowers in tri-trophic systems: mechanisms allowing selective exploitation by insect natural enemies for conservation biological control. Entomol exp appl. 91:155–161. Ghauri MSK. 1967. Zophiuma lobulata sp. n. (Lophopidae – Homoptera), a new pest of coconut in New Guinea. Ann Mag Nat Hist. 9:557–561. Gitau CW, Fletcher MJ, Mitchell A, Dewhurst CF, Gurr GM. 2011. A review of the planthopper genus Zophiuma Fennah (Hemiptera: Fulgoromorpha: Lophopidae) with first description of the male of Zophiuma pupillata Stål. Aust J Entomol. 50:86–92. Gitau CW, Gurr GM, Dewhurst CF, Mitchell A, Fletcher MJ, Liefting LW, Cowling A. 2011. Zophiuma lobulata (Hemiptera: Lophopidae) causes Finschhafen disorder of coconut and oil palms. Ann Appl Biol. 158(1):139–148. Gurr GM, van Emden HF, Wratten SD. 1998. Habitat manipulation and natural enemy efficiency: implications for the control of pests. In. Conservation Biological Control (P. Barbosa, ed.), Academic Press, San Diego, pp. 155–183. Huang DW, Noyes JS. 1994. A revision of the Indo-Pacific species of Ooencyrtus (Hymenoptera: Encyrtidae), parasitoids of the immature stages of economically important insect species (mainly Hemiptera and Lepidoptera). Bull Nat Hist Mus (Entomol Ser). 63(1):1–136. Huber JT, Gitau CW, Gurr GM, Dewhurst CF, Fletcher MJ. 2011. Re-description and biology of Parastethynium maxwelli (Hymenoptera: Mymaridae), an egg parasitoid of Zophiuma lobulata (Hemiptera: Lophopidae), and description of a new species of Parastethynium from Indonesia. Zootaxa. 2733:49–62. Noyes JS. 1982. Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). J Nat Hist. 16:315–334. Perkins RCL 1906. Leaf-hoppers and their natural enemies (pt. VIII. Encyrtidae, Eulophidae, Trichogrammatidae). Bull Hawaiian Sugar Planters’ Assoc Exp Stn (Entomol Ser). 1:239–267. Prior R, Solulu T, Laup S, Gende P. 2001. Finschhafen Coconut Disorder in some tree crops in Papua New Guinea. Sci New Guin. 26:61–64. Smith ESC. 1980a. A sickness of coconuts caused by a leafhopper. Harvest 6:202–205. Smith ESC. 1980b. Zophiuma lobulata Ghauri (Homoptera: Lophopidae) and its relation to the Finschhafen coconut disorder in Papua New Guinea. Papua New Guinea Agric J. 31:37–45.
