Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-24T07:36:05.208Z Has data issue: false hasContentIssue false

A case of ecological specialization in ladybirds: Iberorhyzobius rondensis (Coleoptera: Coccinellidae), potential biocontrol agent of Matsucoccus feytaudi (Hemiptera: Matsucoccidae)

Published online by Cambridge University Press:  26 March 2014

C. Tavares*
Affiliation:
Centro de Estudos Florestais (CEF), Instituto Superior de Agronomia, University of Lisbon (ISA-UL), Tapada da Ajuda 1349-017 Lisbon, Portugal
H. Jactel
Affiliation:
INRA, UMR1202, BIOGECO, F-33610 Cestas, France Univ Bordeaux, UMR1202, BIOGECO, F-33400 Talence, France
I. van Halder
Affiliation:
INRA, UMR1202, BIOGECO, F-33610 Cestas, France Univ Bordeaux, UMR1202, BIOGECO, F-33400 Talence, France
Z. Mendel
Affiliation:
Department of Entomology, Agricultural Research Organization, 50250 Bet Dagan, Israel
M. Branco
Affiliation:
Centro de Estudos Florestais (CEF), Instituto Superior de Agronomia, University of Lisbon (ISA-UL), Tapada da Ajuda 1349-017 Lisbon, Portugal
*
*Author for correspondence Phone: +351 21 365 3382 Fax: +351 21 365 31 95 E-mail: [email protected]

Abstract

Specialization is an important attribute of a biological control agent. The maritime pine bast scale, Matsucoccus feytaudi Ducasse (Hemiptera Matsucoccidae), is an invasive species in Southeast France and the North of Italy. Iberorhyzobius rondensis Eizaguirre (Coleoptera: Coccinellidae), is a recently described ladybird species. Both adults and larvae are predaceous, feeding on egg masses of M. feytaudi, and are strongly attracted to M. feytaudi’s sex pheromone. To evaluate the potential of I. rondensis as a biocontrol agent of the scale, we studied its niche breadth and prey range with emphasis on pine forests and hemipterans as tested prey. In this study, I. rondensis was found to achieve complete development only when fed on M. feytaudi egg masses (92.9% survival) and an artificial prey: eggs of Ephestia kuehniella Zeller (27.6% survival). From the 2nd instar onwards, complete development could be achieved using other prey species, although larvae had significantly higher mortality and slower development. In choice tests, M. feytaudi was the preferred prey. Surveys of the ladybird populations in the Iberian Peninsula revealed that it was found exclusively on Pinus pinaster Aiton, the sole host of M. feytaudi. The unusual specialization of I. rondensis, among other predaceous ladybirds, makes it an appropriate candidate for classical biological control of M. feytaudi.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abrams, P.A. & Ginzburg, L.R. (2000) The nature of predation: prey dependent, ratio dependent or neither? Trends in Ecology and Evolution 15, 337341.Google Scholar
Acar, E.B., Medina, J.C., Lee, M.L. & Booth, G.M. (2001) Olfactory behavior of convergent lady beetles (Coleoptera: Coccinellidae) to alarm pheromone of green peach aphid (Hemiptera: Aphididae). Canadian Entomologist 133, 389397.Google Scholar
Ackonor, J. & Mordjifa, D. (1999) Parasitism and predation in Planococcoides njalensis (Laing) (Homoptera: Pseudococcidae) on cacao in Ghana. Tropical Agriculture 76, 269274.Google Scholar
Ben-Dov, Y., Miller, D.R., & Gibson, G.A.P. (2001) ScaleNet, Catalogue Query Results. 13 June 2013. Available online at http://www.sel.barc.usda.gov/scalenet/scalenet.htm Google Scholar
Branco, M., Franco, J.C., Dunkelblum, E., Assael, F., Protasov, A., Ofer, D. & Mendel, Z. (2006) A common mode of attraction of larvae and adults of insect predators to the sex pheromone of their prey (Hemiptera: Matsucoccidae). Bulletin of Entomological Research 96, 179185.Google Scholar
Branco, M., van Halder, I., Franco, J.C., Constantin, R. & Jactel, H. (2011) Prey sex pheromone as kairomone for a new group of predators (Coleoptera: Dasytidae, Aplocnemus spp.) of pine bast scales. Bulletin of Entomological Research 101, 667674.Google Scholar
Bristow, C.M. (1988) What makes a predator specialize? Tree 3, 12.Google Scholar
Burban, C. & Petit, R.J. (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Molecular Ecology 12, 14871495.Google Scholar
Burban, C., Petit, R.J., Carcreff, E. & Jactel, H. (1999) Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Molecular Ecology 8, 15931602.Google Scholar
Caltagirone, L. & Doutt, R. (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Annual Review of Entomology 34, 116.Google Scholar
Causton, C.E., Lincango, M.P. & Poulsom, T.G.A. (2004) Feeding range studies of Rodolia cardinalis (Mulsant), a candidate biological control agent of Icerya purchasi Maskell in the Galapagos islands. Biological Control 29, 315325.CrossRefGoogle Scholar
Chazeau, J. (1981) Biology of Coelophora quadrivittata (Col.: Coccinellidae), predator of Coccus viridis (Hom.: Coccidae) in New-Caledonia. Entomophaga 26, 301312.CrossRefGoogle Scholar
Covassi, M., Binazzi, A. & Toccafondi, P. (1991) Studies on the entomophagous predators of a scale of the genus Matsucoccus Cock. in Italy. I. Faunistical-ecological notes on species observed in pine forests in Liguria and Tuscany. Redia 74, 575597.Google Scholar
Diehl, E., Sereda, E., Wolters, V. & Birkhofer, K. (2013) Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta-analysis. Journal of Applied Ecology 50, 262270.Google Scholar
Dixon, A.F.G. (2000) Insect Predator-Prey Dynamics: Ladybird Beetles and Biological Control. p. 288. New York, USA, Cambridge University Press.Google Scholar
Eizaguirre, S. (2004) Revisión de la tribu Coccidulini en la Península Ibérica (Coleoptera: Coccinellidae) Estudios del Museo de Ciencias Naturales de Álava 18–19, 153170.Google Scholar
EUFORGEN (2009) Distribution map of maritime pine (Pinus pinaster). Available online at www.euforgen.org.Google Scholar
Ferran, A. & Dixon, A.F.G. (1993) Foraging behaviour of ladybird larvae (Coleoptera: Coccinellidae). European Journal of Entomology 90, 383402.Google Scholar
Foldi, A.I. (2004) The Matsucoccidae in the Mediterranean basin with a world list of species (Hemiptera: Sternorrhyncha: Coccoidea). Annales de la Société entomologique de France 40, 145168.Google Scholar
Fowler, S.V. (2004) Biological control of an exotic scale, Orthezia insignis Browne (Homoptera: Ortheziidae), saves the endemic gumwood tree, Commidendrum robustum (Roxb.) DC. (Asteraceae) on the island of St. Helena. Biological Control 29, 367374.Google Scholar
Funk, D.J., Filchak, K.E. & Feder, J.L. (2002) Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116, 251267.Google Scholar
Heidari, M. & Copland, M. (1992) Host finding by Cryptolaemus montrouzieri (Col., Coccinellidae) a predator of mealybugs (Hom., Pseudococcidae). Entomophaga 37, 621625.Google Scholar
Hodek, I. & Honěk, A. (1996) Ecology of Coccinellidae. p. 464. Dordrecht, The Netherlands, Kluwer Academic Publishers.Google Scholar
Hodek, I. & Honěk, A. (2009) Scale insects, mealybugs, whiteflies and psyllids (Hemiptera, Sternorrhyncha) as prey of ladybirds. Biological Control 51, 232243.Google Scholar
Jackson, R.R., Salm, K. & Nelson, X.J. (2010) Specialized prey selection behavior of two East African assassin bugs, Scipinnia repax and Nagusta sp. that prey on social jumping spiders. Journal of Insect Science 10, 119.Google Scholar
Jactel, H., Ménassieu, P. & Burban, C. (1996) Découverte en Corse de Matsucoccus feytaudi Duc (Homoptera: Margarodidae), cochenille du pin maritime. Annals of Forest Science 53, 145152.Google Scholar
Jałoszyński, P. & Olszanowski, Z. (2013) Specialized feeding of Euconnus pubicollis (Coleoptera: Staphylinidae: Scydmaeninae) on oribatid mites: prey preferences and hunting behaviour. European Journal of Entomology 110, 339353.CrossRefGoogle Scholar
Kalushkov, P. & Hodek, I. (2001) New essential aphid prey for Anatis ocellata and Calvia quatuordecimguttata (Coleoptera: Coccinellidae). Biocontrol Science and Technology 11, 3539.Google Scholar
Katsanis, A., Babendreier, D., Nentwig, W. & Kenis, M. (2013) Intraguild predation between the invasive ladybird Harmonia axyridis and non-target European coccinellid species. BioControl 58, 7383.Google Scholar
Koch, R. & Galvan, T. (2008) Bad side of a good beetle: the North American experience with Harmonia axyridis . pp. 2335 in Roy, H. & Wajnberg, E. (Eds) From Biological Control to Invasion: the Ladybird Harmonia axyridis as a Model Species. Netherlands, Springer.Google Scholar
Majumder, J. & Agarwala, B. (2013) Biology and population dynamics of giant ladybird predator Anisolemnia dilatata (F.) (Coleoptera: Coccinellidae): a specialized predator of woolly aphids of bamboo plants in Northeast India. World Journal of Zoology 8, 5561.Google Scholar
Matsuki, M. & MacLean, S.F. Jr (1994) Effects of different leaf traits on growth rates of insect herbivores on willows. Oecologia 100, 141152.Google Scholar
Mendel, Z., Blumberg, D., Zehavi, A. & Weissenberg, M. (1992) Some polyphagous Homoptera gain protection from their natural enemies by feeding on the toxic plants Spartium junceum and Erythrina corallodendrum (Leguminosae). Chemoecology 3, 118124.Google Scholar
Mendel, Z., Assael, F., Zeidan, S. & Zehavi, A. (1998) Classical biological control of Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) in Israel. Biological Control 12, 151157.Google Scholar
Obata, S. (1986) Mechanisms of prey finding in the aphidophagous ladybird beetle, Harmonia axyridis [Coleoptera: Coccinellidae]. Entomophaga 31, 303311.Google Scholar
Obrycki, J.J. & Kring, T.J. (1998) Predaceous Coccinellidae in biological control. Annual Review of Entomology 43, 295321.Google Scholar
Pekár, S. (2004) Predatory behavior of two european ant-eating spiders (Araneae, Zodariidae). Journal of Arachnology 32, 3141.Google Scholar
Ponsonby, D. & Copland, M. (1995) Olfactory responses by the scale insect predator Chilocorus nigritus (F.) (Coleoptera: Coccinellidae). Biocontrol Science and Technology 5, 8394.Google Scholar
Pope, R.D. (1981) ‘ Rhyzobius ventralis’ (Coleoptera: Coccinellidae), its constituent species, and their taxonomy and historical roles in biological control. Bulletin of Entomological Research 71, 1932.Google Scholar
Ragab, M.E. (1995) Adaptation of Rodolia cardinalis (Mulsant) (Col., Coccinellidae) to Icerya aegyptiaca (Douglas) (Hom., Margarodidae) as compared with Icerya purchasi Mask. Journal of Applied Entomology 119, 621623.Google Scholar
Raimundo, A., Canepari, C., Mendel, Z., Branco, M. & Franco, C. (2006) Iberorhyzobius Raimundo & Canepari gen. nov., for Coccidula rondensis Eizaguirre (Coleoptera: Coccinellidae). Zootaxa 1312, 4958.Google Scholar
Ricci, C. (1986) Seasonal food preferences and behavior of Rhyzobius litura . pp. 119123 in Hodek, I. (Ed.) Ecology of Aphidophaga. Dordrecht, The Netherlands, Academia, Prague & Dr. W.Junk.Google Scholar
Richards, A.M. (1981) Rhyzobius ventralis (Erichson) and R. forestieri (Mulsant) (Coleoptera: Coccinellidae), their biology and value for scale insect control. Bulletin of Entomological Research 71, 3346.Google Scholar
Richards, A.M. (1985) Biology and defensive adaptations in Rodatus major (Coleoptera: Coccinellidae) and its prey, Monophlebulus pilosior (Hemiptera: Margarodidae). Journal of Zoology 205, 287295.Google Scholar
Riom, J. & Gerbinot, B. (1977) Étude biologique et écologique de la cochenille du pin maritime Matsucoccus feytaudi Ducasse, 1942 (Coccoidea, Margarodidae, Xylococcinae) dans le Sud-Est de la France. 1. Biologie générale et phénologie. Annales de Zoologie Ecologie Animale 9, 1150.Google Scholar
Scriber, J.M. (2010) Integrating ancient patterns and current dynamics of insect–plant interactions: taxonomic and geographic variation in herbivore specialization. Insect Science 17, 471507.Google Scholar
Short, B.D. & Bergh, J.C. (2004) Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia Apple Orchards. Journal of Economic Entomology 97, 813819.Google Scholar
Sloggett, J.J. & Majerus, M.E.N. (2000) Habitat preferences and diet in the predatory Coccinellidae (Coleoptera): an evolutionary perspective. Biological Journal of the Linnean Society 70, 6388.Google Scholar
Stathas, G.J. (2000) Rhyzobius lophanthae prey consumption and fecundity. Phytoparasitica 28, 203211.CrossRefGoogle Scholar
Strand, M.R. & Obrycki, J.J. (1996) Host specificity of insect parasitoids and predators. BioScience 46, 422429.Google Scholar
Thompson, A.J.J.N. (1995) Trade-offs and the evolution of host specialization. Evolutionary Ecology 9, 8292.Google Scholar
Toccafondi, P., Covassi, M. & Pennacchio, F. (1991) Studies on the entomophagous predators of scale insects of the genus Matsucoccus Cock. in Italy. II Bio-ethological notes on Rhyzobius chrysomeloides (Herbst) in pine forests of Liguria (Coleoptera: Coccinellidae). Redia 74, 599620.Google Scholar
Van Lenteren, J., Bale, J., Bigler, F., Hokkanen, H. & Loomans, A. (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of. Entomology 51, 609634.Google Scholar
Vantaux, A., Roux, O., Magro, A., Ghomsi, N.T., Gordon, R.D., Dejean, A. & Orivel, J. (2010) Host-Specific Myrmecophily and Myrmecophagy in the Tropical Coccinellid Diomus thoracicus in French Guiana. Biotropica 42, 622629.Google Scholar
Vieira, L., Salom, S., Montgomery, M. & Kok, L. (2013) Field-cage evaluation of the survival, feeding and reproduction of Laricobius osakensis (Coleoptera: Derodontidae), a predator of Adelges tsugae (Hemiptera: Adelgidae). Biological Control 66, 195203.Google Scholar
Wiegmann, B., Mitter, C. & Farrell, B. (1996) Diversification of carnivorous parasitic insects: extraordinary radiation or specialized dead end? American Naturalist 142, 737754.Google Scholar