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Pre-selection and biological potential of the egg parasitoid Anaphes inexpectatus for the control of the Eucalyptus snout beetle, Gonipterus platensis

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Abstract

The Eucalyptus snout beetle, Gonipterus platensis (Marelli), causes severe damage to eucalypt plantations in several countries, despite the presence of the parasitoid Anaphes nitens (Girault). Climate and/or host–parasitoid mismatch may explain A. nitens shortcomings in some areas in Portugal, Spain, Chile, South Africa, or Australia. Because additional parasitoids may be needed to achieve reliable control of this pest, Anaphes inexpectatus Huber and Prinsloo, retrieved from field surveys conducted in Tasmania (the pest’s native habitat), was selected for pre-release studies in Portugal. Life history traits of A. inexpectatus and A. nitens were compared at six temperatures (5, 10, 15, 20, 25, and 30 °C), including development times, thermal constants, viability, parasitism, and behaviour. Temperatures ranging from 10 to 20 °C were adequate for development, while at 25 and 30 °C, deleterious effects of temperature were detected, particularly in A. nitens. Development thresholds were similar for A. inexpectatus and A. nitens (6.0 and 5.4 °C, respectively), but A. nitens needed 313 degree-days to complete development, while A. inexpectatus needed 263 degree-days. Globally, A. nitens produced more progeny, parasitised more eggs, and lived longer than A. inexpectatus. Net reproductive rates were higher for A. inexpectatus at lower temperatures (10 and 15 °C), and higher for A. nitens at moderate temperatures (20 and 25 °C). In addition, A. inexpectatus evidenced higher tolerance to the highest temperature tested (30 °C). Anaphes inexpectatus is likely to establish under field conditions and may enhance parasitism of G. platensis.

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References

  • AEMET, IMP, Beus IMP (2011) Iberian climate atlas. Agencia Estatal de Meteorología de España and Instituto de Meteorologia de Portugal. Closas-Orcoyen SL, Madrid

    Google Scholar 

  • Aeschlimann JP, Hopkins DC, Cullen JM, Cavanaugh JA (1989) Importation and release of Anaphes diana Girault (Hym., Mymaridae), a parasitoid of Sitona discoideus Gyllenhal (Col., Curculionidae) eggs in Australia. J Appl Entomol 107:418–423

    Article  Google Scholar 

  • Ahmad R (1978) Note on breeding the argentine stem weevil Hyperodes bonariensis [Col.: Curculionidae] and its egg parasite Patasson atomarius [Hym.: Mymaridae]. Entomophaga 23:161–162

    Article  Google Scholar 

  • Anderson RC, Paschke JD (1969) Additional observations on the biology of Anaphes flavipes (Hymenoptera: Mymaridae), with special reference to the effects of temperature and superparasitism on development. Ann Entomol Soc Am 62:1316–1321

    Article  Google Scholar 

  • Bloem K, Yeargan K (1982) Effects of extreme temperatures on Patasson lameerei survival and oviposition. J Kans Entomol Soc 55:37–45

    Google Scholar 

  • Boivin G, van Baaren J (2000) The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps. Ecol Lett 3:469–474

    Article  Google Scholar 

  • Branco M, Battisti A, Mendel Z (2016) Foliage feeding invasive insects: defoliators and gall makers. In: Paine TD, Lieutier F (eds) Insects and diseases of Mediterranean forest systems. Springer, Dordrecht, pp 211–238

    Chapter  Google Scholar 

  • Campbell A, Frazer BD, Gilbert N, Gutierrez AP, Mackauer M (1974) Temperature requirements of some aphids and their parasites. J Appl Ecol 11:431–438

    Article  Google Scholar 

  • Collins RD, Grafius E (1986) Biology and life cycle of Anaphes sordidatus (Hymenoptera: Mymaridae), an egg parasitoid of the Carrot Weevil (Coleoptera: Curculionidae). Environ Entomol 15:100–105

    Article  Google Scholar 

  • Cordero Rivera A, Santolamazza Carbone S, Andrés JA (1999) Life cycle and biological control of the Eucalyptus snout beetle (Coleoptera, Curculionidae) by Anaphes nitens (Hymenoptera, Mymaridae) in north-west Spain. Agric For Entomol 1:103–109

    Article  Google Scholar 

  • Doutt R, Annecke D, Tremblay E (1976) Biology and host relationships of parasitoids. In: Huffaker C, Messenger P (eds) Theory and practice of biological control. Academic Press, New York, pp 143–168

    Chapter  Google Scholar 

  • Gumovsky A, De Little D, Rothmann S, Jaques L, Mayorga SEI (2015) Re-description and first host and biology records of Entedon magnificus (Girault & Dodd) (Hymenoptera, Eulophidae), a natural enemy of Gonipterus weevils (Coleoptera, Curculionidae), a pest of Eucalyptus trees. Zootaxa 3957:577–584

    PubMed  Google Scholar 

  • Hamilton WD (1967) Extraordinary sex ratios. Science 156:477–488

    Article  CAS  PubMed  Google Scholar 

  • Hance T, van Baaren J, Vernon P, Boivin G (2007) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126

    Article  CAS  PubMed  Google Scholar 

  • Hanks LM, Millar JG, Paine TD, Campbell CD (2000) Classical biological control of the Australian weevil Gonipterus scutellatus (Coleoptera: Curculionidae) in California. Environ Entomol 29:369–375

    Article  Google Scholar 

  • Hardy ICW, Ode PJ, Siva-Jothy MT (2005) Mating systems. In: Jervis MA (ed) Insects as natural enemies: a practical perspective. Springer, Dordrecht, pp 261–298

    Chapter  Google Scholar 

  • Honek A (1996) Geographical variation in thermal requirements for insect development. Eur J Entomol 93:303–312

    Google Scholar 

  • Huber JT (1986) Systematics, biology, and host of the Mymaridae and Mymarommatidae (Insecta: Hymenoptera): 1758–1984. Entomography 4:185–243

    Google Scholar 

  • Huber JT, Prinsloo GL (1990) Redescription of Anaphes nitens (Girault) and description of two new species of Anaphes Halliday (Hymenoptera: Mymaridae), parasite of Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae) in Tasmania. J Aust Entomol Soc 29:333–341

    Article  Google Scholar 

  • Huffaker C, Simmonds F, Laing J (1976) The theoretical and empirical basis of biological control. In: Huffaker C, Messenger P (eds) Theory and practice of biological control. Academic Press, New York, pp 41–78

    Chapter  Google Scholar 

  • Jackson CG (1987) Biology of Anaphes ovijentatus (Hymenoptera: Mymaridae) and its host, Lygus hesperus (Hemiptera: Miridae), at low and high temperatures. Ann Entomol Soc Am 80:367–372

    Article  Google Scholar 

  • Jones W, Jackson C (1990) Mass production of Anaphes iole for augmentation against Lygus hesperus: effects of food on fecundity and longevity. Southwest Entomol 15:463–468

    Google Scholar 

  • Lamb RJ (1992) Developmental rate of Acyrthosiphon pisum (Homoptera: Aphididae) at low temperatures: implications for estimating rate parameters for insects. Environ Entomol 21:10–19

    Article  Google Scholar 

  • Laudien H (1973) Changing reaction systems. In: Precht H, Christophersen J, Hensel H, Larcher W (eds) Temperature and life. Springer, Berlin, pp 355–399

    Google Scholar 

  • Leibee G, Pass B, Yeargan K (1979) Developmental rates of Patasson lameerei [Hym.: Mymaridae] and the effect of host egg age on parasitism. Entomophaga 24:345–348

    Article  Google Scholar 

  • Loch A (2006) Phenology of Eucalyptus weevil, Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae), and chrysomelid beetles in Eucalyptus globulus plantations in south-western Australia. Agric For Entomol 8:155–165

    Article  Google Scholar 

  • Loch A (2008) Parasitism of the Eucalyptus weevil, Gonipterus scutellatus Gyllenhal, by the egg parasitoid, Anaphes nitens Girault, in Eucalyptus globulus plantations in southwestern Australia. Biol Control 47:1–7

    Article  Google Scholar 

  • Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht

    Google Scholar 

  • Maia AH, Luiz AJ, Campanhola C (2000) Statistical inference on associated fertility life table parameters using Jackknife technique: computational aspects. J Econ Entomol 93:511–518

    Article  Google Scholar 

  • Mansilla Vázquez JP, Pérez Otero R, Salinero Corral MC (1998) Introducción en la Península Ibérica de Anaphes nitens Huber, parásito del defoliador del Eucalipto Gonipterus scutellatus. Montes 51:42–46

    Google Scholar 

  • Mapondera TS, Burgess T, Matsuki M, Oberprieler RG (2012) Identification and molecular phylogenetics of the cryptic species of the Gonipterus scutellatus complex (Coleoptera: Curculionidae: Gonipterini). Aust J Entomol 51:175–188

    Article  Google Scholar 

  • Mayorga SI, Jaques L, Peragallo M (2013) Anaphes tasmaniae, parasitoid of Gonipterus platensis (Marelli, 1926) (Coleoptera: Curculionidae) introduced in Chile. In: 4th international symposium on biological control of arthropods, Pucón, Chile

  • Messenger P, Biliotti E, van den Bosch R (1976) The importance of natural enemies in integrated control. In: Huffaker C, Messenger P (eds) Theory and practice of biological control. Academic Press, New York, pp 543–563

    Chapter  Google Scholar 

  • Reineke A, Thiéry D (2016) Grapevine insect pests and their natural enemies in the age of global warming. J Pest Sci 89:313–328

    Article  Google Scholar 

  • Reis AR, Ferreira L, Tomé M, Araújo C, Branco M (2012) Efficiency of biological control of Gonipterus platensis (Coleoptera: Curculionidae) by Anaphes nitens (Hymenoptera: Mymaridae) in cold areas of the Iberian Peninsula: implications for defoliation and wood production in Eucalyptus globulus. For Ecol Manag 270:216–222

    Article  Google Scholar 

  • SAG (2005) Informativo Fitosanitario Forestal, Nr. 1, July 2005. Servicio Agrícola y Ganadero, Santiago, Chile

  • SAG (2014) Informativo Fitosanitario Forestal, Nr. 9, November 2014. Servicio Agrícola y Ganadero, Santiago, Chile

  • Sahad KA (1984) Biology of Anagrus optabilis (Perkins) (Hymenoptera, Mymaridae), an egg parasitoid of delphacid planthoppers. Esakia 22:129–144

    Google Scholar 

  • Santolamazza-Carbone S, Cordero Rivera A (2003a) Egg load and adaptive superparasitism in Anaphes nitens, an egg parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus. Entomol Exp Appl 106:127–134

    Article  Google Scholar 

  • Santolamazza-Carbone S, Cordero Rivera A (2003b) Superparasitism and sex ratio adjustment in a wasp parasitoid: results at variance with Local Mate Competition? Oecologia 136:365–373

    Article  PubMed  Google Scholar 

  • Santolamazza-Carbone S, Rodríguez-Illamola A, Cordero Rivera A (2006) Thermal requirements and phenology of the Eucalyptus snout beetle Gonipterus scutellatus Gyllenhal. J Appl Entomol 130:368–376

    Article  Google Scholar 

  • Santolamazza-Carbone S, Pestana Nieto M, Pérez Otero R, Mansilla Vázquez P, Cordero Rivera A (2009) Winter and spring ecology of Anaphes nitens, a solitary egg-parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus. Biocontrol 54:195–209

    Article  Google Scholar 

  • Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246

    Article  Google Scholar 

  • Stoner A, Surber DE (1969) Notes on the biology and rearing of Anaphes ovijentatus, a new parasite of Lygus hesperus in Arizona. J Econ Entomol 62:501–502

    Article  Google Scholar 

  • Taylor F (1981) Ecology and evolution of physiological time in insects. Am Nat 117:1–23

    Article  Google Scholar 

  • Tooke FGC (1955) The Eucalyptus snout-beetle, Gonipterus scutellatus Gyll. A study of its ecology and control by biological means. Entomology memoirs. Department of Agriculture, Pretoria

  • Traoré L, Pilon J-G, Fournier F, Boivin G (2006) Adaptation of the developmental process of Anaphes victus (Hymenoptera: Mymaridae) to local climatic conditions across North America. Ann Entomol Soc Am 99:1121–1126

    Article  Google Scholar 

  • Tribe GD (2003) Biological control of defoliating, and phloem- or wood-feeding insects in commercial forestry in southern Africa. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in IPM systems in Africa. CABI Publishing, Wallingford, pp 113–129

    Google Scholar 

  • Tribe GD (2005) The present status of Anaphes nitens (Hymenoptera: Mymaridae), an egg parasitoid of the Eucalyptus snout beetle Gonipterus scutellatus, in the Western Cape Province of South Africa. S Afr For J 203:49–54

    Google Scholar 

  • Trudgill DL, Honek A, Li D, van Straalen NM (2005) Thermal time—concepts and utility. Ann Appl Biol 146:1–14

    Article  Google Scholar 

  • Valente C, Vaz A, Pina J, Manta A, Sequeira A (2004) Control strategy against the Eucalyptus snout beetle, Gonipterus scutellatus Gyllenhal (Coleoptera, Curculionidae), by the Portuguese cellulose industry. In: Borralho N (ed) Proceedings of the IUFRO conference Eucalyptus in a changing world, 11–15 October 2004, Aveiro, pp 37–51

  • Wade MR, Hopkinson JE, Zalucki MP (2008) Influence of food supplementation on the fitness of two biological control agents: a predatory nabid bug and a bollworm pupal parasitoid. J Pest Sci 81:99–107

    Article  Google Scholar 

  • Ward SE, Valente C, Gonçalves C, Polaszek A (2016) Rediscovery and redescription of Centrodora damoni (Girault) (Hymenoptera: Aphelinidae) from Australia, an egg parasitoid of Gonipterus spp (Coleoptera: Curculionidae), after nearly a century. Biodivers Data J. doi:10.3897/BDJ.4.e7766

    Google Scholar 

  • Williams L, Roane TM (2007) Nutritional ecology of a parasitic wasp: food source affects gustatory response, metabolic utilization, and survivorship. J Insect Physiol 53:1262–1275

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors wish to thank Gabriel Dehon, Cristina Marques, Clara Araújo, and Luís Leal for their contribution to develop the present work, and David De Little and Jane Elek for their support during parasitoid collection. We thank Andreia Padrela, Inês Silva, and Sofia Simões for their assistance in laboratory trials. We are indebted to John Huber (Agriculture and Agri-Food, Canada), John LaSalle (CSIRO, Australia), Andrew Polaszek (NHM, United Kingdom), Alex Gumovsky (Schmalhausen Institute of Zoology, Ukraine), Lubomír Masner (Agriculture and Agri-Food, Canada), Bryan Cantrell (Queensland Museum, Australia), and Rolf Oberprieler (CSIRO, Australia) for kindly providing specimen identification. We would also like to thank four anonymous reviewers for valuable comments on the manuscript.

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This study was funded by The Navigator Company and Altri Florestal.

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Correspondence to Carlos Valente.

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Valente, C., Gonçalves, C.I., Reis, A. et al. Pre-selection and biological potential of the egg parasitoid Anaphes inexpectatus for the control of the Eucalyptus snout beetle, Gonipterus platensis . J Pest Sci 90, 911–923 (2017). https://doi.org/10.1007/s10340-017-0839-y

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