Parasitizing behavior of Cervellus piranga Penteado-Dias (Hymenoptera, Braconidae, Braconinae) on papaya borer weevil Pseudopiazurus obesus Marshall (Coleoptera, Curculionidae)

Parasitizing behavior of Cervellus piranga Penteado-Dias (Hymenoptera, Braconidae, Braconinae) on papaya borer weevil Pseudopiazurus obesus Marshall (Coleoptera, Curculionidae)

Marcos A. B. Moreira^I; Paulo H. G. Zarbin^II; Angélica M. Penteado-Dias^III; Adenir V. Teodoro^I

^IEmbrapa Tabuleiros Costeiros, Av. Beira Mar 3250, Caixa Postal 44, 49025_040 Aracaju-SE, Brasil, E-mail: [e-mail]; [e-mail]

^IIUniversidade Federal do Paraná, Departamento de Química, Caixa Postal 19020, 81531_980 Curitiba-PR, Brasil, E-mail: [e-mail] ^IIIUniversidade Federal de São Carlos, Departamento de Ecologia e Biologia Evolutiva, Caixa Postal 676, 13565_905 São Carlos-SP, Brasil, E-mail: [e-mail]

ABSTRACT

Parasitizing behavior of Cervellus piranga Penteado-Dias (Hymenoptera, Braconidae, Braconinae) on papaya borer weevil Pseudopiazurus obesus Marshall (Coleoptera, Curculionidae). The papaya borer weevil Pseudopiazurus obesus is a pest associated with papaya crops in Brazil and Cervellus piranga is a naturally-occurring parasitoid which may contribute to regulate populations of this pest. We aimed at describing the parasitizing behavior of the parasitoid C. piranga on papaya borer weevil P. obesus larvae under field conditions. The sequence of events related to the parasitizing behavior of C. piranga is similar to other braconid species and includes the location and recognition of the attacked host plant followed by walks on the host plant and touching it with the tip of the antennae and the ovipositor. In the following event, the parasitoid assesses the suitability of the host by speeding up antennae and ovipositor movements. After locating and accepting the host, the parasitoid remains inactive on oviposition aperture sites and starts moving the antennae. Afterwards, the parasitoid inserts its ovipositor and starts cleaning it repeatedly. The female of C. piranga inserts the ovipositor through the hole and lay one egg into the papaya weevil borer. After oviposition, the female cleans continuously both ovipositor and antennae before leaving to forage for a new host.

Keywords: Kairomones; parasitoid; papaya pest; plant volatiles; sinomones.

RESUMO

Comportamento de parasitismo de Cervellus piranga Penteado-Dias (Hymenoptera, Braconidae, Braconinae) sobre a broca-do-mamoeiro Pseudopiazurus obesus Marshall (Coleoptera, Curculionidae). A broca-do-mamoeiro Pseudopiazurus obesus é uma praga de cultivos de mamão no Brasil e Cervellus piranga é um parasitóide que ocorre naturalmente no campo e pode contribuir para a regulação da população desta praga. O objetivo do presente trabalho foi a descrição do comportamento de parasitismo do parasitoide C. piranga sobre larvas da broca-do-mamoeiro P. obesus em condições de campo. A sequência de eventos relacionados ao parasitismo de C. piranga é similar a outras espécies de braconídeos e inclui a localização e o reconhecimento da planta hospedeira atacada, caminhamento na planta e toque desta com as antenas e o ovipositor. No próximo evento, o parasitoide acessa a adequabilidade do hospedeiro através do aumento dos movimentos da antena e do ovipositor. Após localizar e aceitar o hospedeiro, o parasitoide fica imóvel no sítio de oviposição e inicia a movimentar a antena. Em seguida, o parasitoide insere o ovipositor e o limpa repetidamente. A fêmea de C. piranga insere o ovipositor através da abertura e deposita um ovo na broca-do-mamoeiro. Após a oviposição, a fêmea limpa continuamente o ovipositor e a antena e abandona a planta para um novo forrageamento.

Palavras-chave: Cairomônios; parasitoide; praga do mamão; sinomônios; voláteis de plantas.

The papaya borer weevil Pseudopiazurus obesus Marshall, 1922 (Coleoptera, Curculionidae) is a pest associated with papaya crops in the north and northeast regions of Brazil (Moreira et al. 2003). Females of the papaya borer weevil lay their eggs on the papaya trunk into which larvae penetrate after egg hatching causing destruction of meristematic tissues, affecting sap translocation and eventually killing the plant (Farias & Almeida 1995). The larval cycle of the papaya borer weevil takes approximately three months, however we are not aware of any study on the biological aspects of this pest. Since the larvae dwell inside the trunk the use of pesticides is largely inefficient. The use of natural enemies such as parasitoids to control insect pests is an important strategy in integrated pest management programs (Viggiani 2000; Gallo et al. 2002; Moreira et al. 2003).

The braconid Cervellus piranga Penteado-Dias, 2007 (Hymenoptera, Braconidae, Braconinae) is a naturally-occurring parasitoid which may contribute to regulate populations of the papaya borer weevil (Moreira et al. 2003; Penteado-Dias et al. 2007). Parasitism of the papaya borer weevil larvae by C. piranga ranges from 5 to 8% (Moreira et al. 2003). The advantage of parasitoids in comparison with other natural enemies is the ability of reaching the larvae hidden inside the trunk, which is the damaging developmental stage of the papaya weevil borer. However, a diversified community of natural enemies contributes to regulate all developmental stages of the papaya borer weevil (Moreira et al. 2005). Understanding the parasitizing behavior of parasitoids is vital for the establishment of successful biological control programs (Kant et al. 2008) as such knowledge helps to comprehend the multitrophic relationships between these natural enemies, their hosts and the host plant (Santos et al. 2004). Therefore, this work aimed to describe the parasitism behavior of C. piranga on larvae of the papaya borer weevil under field conditions.

We observed the parasitizing behavior of C. piranga on larvae of the papaya borer weevil in two commercial plantations of papaya (2.5 years old plants), located in the Brazilian Northeastern cities of Vera Cruz, in the state of Rio Grande do Norte (6°02'38"S, 35°25'40"W, 92 m above sea level) and Laje, in the state of Bahia (13°09'51"S, 39°25'59"W, 233 m above sea level), in October 2004.

We used a digital camera (Canon A300) to record all steps related to the parasitizing behavior of C. piranga. We chose plants severely attacked by the papaya borer weevil and with activity of the parasitoid C. piranga. Afterwards, we conducted daily observations during four days, between 6:30 and 10:30 am, which was defined based on previous field observations as the main activity period of the parasitoids. The number of observed parasitoids varied and pictures were taken and used to describe and draw the sequence of events related to the parasitizing behavior of C. piranga on larvae of the papaya weevil borer.

The sequence of events related to the parasitizing behavior of C. piranga is similar to other braconid species (Santos et al. 2004; Roux et al. 2005). The location and recognition of the host plant attacked by the papaya borer weevil by the parasitoid C. piranga may be mediated by visual stimuli and chemical signals, mainly sinomones and kairomones (Metcalf & Metcalf 1992). Plant volatiles play a key role in orientating both pest insects and their natural enemies (Vet & Dicke 1992). Parasitoids select habitat and host by means of volatiles recognized by their olfactory apparatus. Volatiles are released in the environment from herbivorous-attacked host plants and from the hosts themselves (Vuorinen et al. 2004; Dannon et al. 2010). Such alellochemicals are used by parasitoids to locate host plants and hosts (Dicke et al. 1990; Metcalf & Metcalf 1992). Therefore, C. piranga may use papaya weevil borer-induced plant volatiles as well as kairomones from feces and regurgitation of the borer to locate the host plant and the host, respectively.

For the recognition of the host plant potentially attacked by the papaya borer weevil, the parasitoid C. piranga walks on the host plant touching it alternatively with the tip of the antennae and the ovipositor. The perception of semiochemicals in interespecific communication is possibly mediated by a synergistic effect of sinomones and kairomones released in the environment (Dicke et al. 1990). Additionally, bracronid parasitoids may detect host visually and the size of the host indicate its suitability for parasitoid fitness (Kant et al. 2008). Sound emitted by larvae and pupae as a result of feeding and movement inside the trunk may also be exploited by the parasitoid in host location through vibrotaxis (Lawrence 1981).

In the following event, the parasitoid assesses the suitability of the host by speeding up antennae and ovipositor movements. Such movements are important for the decision-making process of staying on the host plant or move to another host plant (Richerson & DeLoach 1972). After locating and accepting the host, the parasitoid remains inactive on oviposition aperture sites or on holes bored by larvae of the papaya borer weevil slowly moving the antennae and matching its position to that of the host. Afterwards, the parasitoid inserts its ovipositor and starts cleaning it repeatedly with help of the posterior legs.

The female of C. piranga inserts the ovipositor through the hole and lay one egg into the papaya borer weevil. The parasitoid contracts its abdomen several times during oviposition probably in order to increase egg laying frequency as pointed out by Legaspi et al. (1987). The oviposition process takes 15 to 20 seconds from penetration to retraction of the ovipositor. The parasitoid oviposited only once in each oviposition aperture or hole of bored sites; however, one female was observed laying eggs in other sites of the same plant avoiding, thus, superparasitism. Braconids use oviposition-deterring pheromones or oviposition marker pheromones to avoid intraspecific competition. After oviposition, the female stays inactive by approximately 10 seconds cleaning continuously both ovipositor and antennae before leaving to forage for a new host.

Pupal chambers of the papaya borer weevil parasitized by C. piranga had only one host larvae from which only one parasitoid emerged. We noticed that C. piranga parasitizes only the first instars of the papaya borer weevil suggesting that this parasitoid is a solitary koinobiont laying only one egg per host; however, additional studies are necessary to clarify this behavior.

ACKNOWLEDGMENTS

Angélica M. Penteado-Dias acknowledges financial support from FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) and CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico).

Received 19/4/2011; accepted 26/10/2011

Editor: Sonia Maria Noemberg Lázzari

• Dannon, E. A.; M. Tamò; A. Van Huis & M. Dicke. 2010. Effects of volatiles from Maruca vitrata larvae and caterpillar-infested flowers of their host plant Vigna unguiculata on the foraging behavior of the parasitoid Apanteles taragamae Journal of Chemical Ecology 36: 1083_1091.
• Dicke, M.; M. W. Sabelis; J. Takabayashi; J. Bruin & M. A. Posthumus. 1990. Plant strategies of manipulating predator-prey interactions through allelochemicals: Prospects for application in pest control. Journal of Chemical Ecology 16: 3091_118.
• Farias, A. R. N & A. O. de Almeida. 1995. Ocorrência de Pseudopiazurus obesus em Cruz das Almas, Bahia. Cruz das Almas, EMBRAPA/CNPMF, Mamão em Foco, n. 49, 1 p.
• Gallo, D.; O. Nakano; S. Silveira Neto; R. P. L. Carvalho; G. C. Batista; E. Berti-Filho; J. R. P. Parra; R. A. Zucchi; S. B. Alves & J. D. Vendramin. 2002. Manual de Entomologia Agrícola. São Paulo, Agronômica Ceres, 649 p.
• Kant, R.; W. R. M. Sandanayaka; X. Z. He & Q. Wang. 2008. Effect of host age on searching and oviposition behaviour of Diaeretiella rapae (M'Intosh) (Hymenoptera: Aphidiidae). New Zealand Plant Protection 61: 355_361.
• Lawrence, P.O. 1981. Host vibration _ a cue to host location by the parasite, Biosteres longicaudatus Oecologia 48: 249_251.
• Legaspi, B. A. C.; B. M. Shepard & L. P. Almazan. 1987. Oviposition behavior and development of Goniozus triagulifer Kieffer (Hymenoptera: Bethylidae). Environmental Entomology 16: 1283_1286.
• Metcalf, R. L. & E. R. Metcalf. 1992. Plant kairomones in insect ecology and control. New York, Chapman and Hall, 168 p.
• Moreira, M. A. B.; P. H. G. Zarbin; G. H. Rosado-Neto; M. F. P. Barreto; J. F. Sobrinho & M. A. Borges. 2003. Broca-do-mamoeiro, Pseudopiazurus obesus, Marshall, 1922 (Coleoptera: Curculionidae) e recomendações de controle. Circular Técnica 35, Aracaju, Embrapa: Tabuleiros Costeiros, 4 p.
• Moreira, M. A. B.; P. H. G. Zarbin & M. Fancelli. 2005. Inimigos naturais associados a broca-do-mamoeiro, Pseudopiazurus obesus, Marshall, 1922 (Coleoptera: Curculionidae). Comunicado Técnico 35; Embrapa: Tabuleiros Costeiros, Aracaju-SE.
• Penteado-Dias, A. M.; M. A. B. Barbosa & P. H. G. Zarbin. 2007. A new species of Cervellus Szépligeti (Hymenoptera, Braconidae, Braconinae) with biological notes. Revista Brasileira de Entomologia 51: 8_11.
• Richerson, J. D. & C. J. DeLoach. 1972. Some aspects of host selection by Perilitus coccinellae Annals of the Entomological Society of America 65: 834_839.
• Roux, O.; J. Van Baaren; C. Gers; L. Arvanitakis & L. Legal. 2005. Antennal structure and oviposition behavior of the Plutella xylostella specialist parasitoid: Cotesia plutellae Microscopy Research and Technique 68: 36_44.
• Santos, J. C.; L. R. Viana; F. A. O. Silveira; A. M. Penteado-Dias & W. Fernandes. 2004. Ovipositing behaviour of Compsobracon mirabilis Revista Brasileira de Entomologia 48: 139_140.
• Vet, L. E. M. & M. Dicke. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37: 141_172.
• Viggiani, G. 2000. The role of parasitic Hymenoptera in integrated pest management in fruit orchards. Crop Protection 19: 665_668.
• Vuorinen, T.; A. M. Nerg; M. A. Ibrahim; G. V. P. Reddy & J. K. Holopainen. 2004. Emission of Plutella xylostella induced compounds from cabbages grown at elevated CO₂ and orientation behavior of the natural enemies. Plant Physiology 135: 1984_1992.

Publication Dates

• Publication in this collection
  22 Dec 2011
• Date of issue
  Dec 2011

History

• Received
  19 Apr 2011
• Accepted
  26 Oct 2011