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Hexacladia smithii Ashmead, 1891 (Hymenoptera: Encyrtidae) in Panama: first record and new association with Berecynthus hastator (Fabricius, 1798) (Hemiptera: Pentatomidae)

Berecynthus hastator (Fabricius, 1798) is synonym of Berecynthus delirator (Fabricius, 1787) (Grazia and Hildebrant, 1982GRAZIA, J. and HILDEBRANT, R., 1982. Revisão do gênero Berecynthus Stål, 1862 (Heteroptera, Pentatomidae, Pentatomini). Revista Brasileira de Entomologia, vol. 26, no. 2, pp. 173-182.; Rider and Rolston, 1995RIDER, D.A. and ROLSTON, L.H., 1995. Nomenclatural changes in the Pentatomidae (Hemiptera: pentatomidae). Proceedings of the Entomological Society of Washington, vol. 97, pp. 845-855.), whose geographical distribution is limited to the neotropics. Currently, there are records of this species in Bolivia, Brazil, Costa Rica, Colombia, French Guyana, Mexico, Nicaragua, Peru, Puerto Rico, Suriname, Venezuela and Panama (Grazia et al., 2015GRAZIA, J., PANIZZI, A.R., GREVE, C., SCHWERTNER, C.F., CAMPOS, L.A., GABERLOTTO, T.A. and FERNANDES, J.A.M., 2015. Stink bugs (Pentatomidae). In: A.R. PANIZZI and J. GRAZIA, eds. True bugs (Heteroptera) of the Neotropics. Dordrecht: Springer, pp. 681-756. http://dx.doi.org/10.1007/978-94-017-9861-7_22.
http://dx.doi.org/10.1007/978-94-017-986...
; Segarra-Carmona et al., 2015SEGARRA-CARMONA, A.E., FRANQUI, R.A., PEREZ-MARTÍNEZ, H. and MORALES-GRAJALES, A., 2015. New records for stink bugs (Heteroptera: Pentatomidae) in Puerto Rico. The Journal of Agriculture of the University of Puerto Rico, vol. 99, no. 2, pp. 167-178. http://dx.doi.org/10.46429/aupr.v99i2.
http://dx.doi.org/10.46429/aupr.v99i2...
; Cazorla and Moreno, 2020CAZORLA, D. and MORENO, O.M., 2020. Nuevos registros de Pentatomidae (Hemiptera: Heteroptera) en el Estado de Falcón, Venezuela. Revista Nicaraguense Entomologica, vol. 197, pp. 3-54.; Rider, 2021RIDER, D.A., 2021 [viewed 20 December 2021]. Pentatomoidea Home Page [online]. Available from: www.ndsu.edu/pubweb/~rider/Pentatomoidea/index.htm.
www.ndsu.edu/pubweb/~rider/Pentatomoidea...
; Dellapé, 2021DELLAPÉ, G., 2021. New records of neotropical Pentatominae (Heteroptera: Pentatomidae). Entomological Communications, vol. 3, ec03004.; GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
). In Panama B. hastator was reported in Coco Solo, Province of Colon (09º 22’ 21.43” N, 79º 52’ 52.32” W), Puerto Armuelles (08° 39’ 09” N, 82° 07’ 24” W), Bayano (09° 06’ 58” N, 78° 46’ 24” W), Kobe (08º 55’ N, 79º 34’ W), Chorrera (08º 52’ 49” N, 79º 47’ W), Santiago (08º 07’ N, 80º 59’ W), Las Cumbres (09º 06’ N, 79º 32’ W) (Grazia and Hildebrant, 1982GRAZIA, J. and HILDEBRANT, R., 1982. Revisão do gênero Berecynthus Stål, 1862 (Heteroptera, Pentatomidae, Pentatomini). Revista Brasileira de Entomologia, vol. 26, no. 2, pp. 173-182.; GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
). Adults of B. hastator were collected in Panama with light traps and its association with agricultural crops and uncultivated plants was not confirmed (GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
); the voucher specimens were deposited in the collection of Texas A&M University, College Station, Texas, USA; Illinois Natural History Survey Insect Collection, Illinois, USA, and Smithsonian Tropical Research Institute, Panama (GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
). The adults of B. hastator collected in Panama with of light traps and its association with agricultural crops and uncultivated plants were not confirmed (GBIF, 2022GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
). The impact of B. hastator on crops of economic importance is limited; this insect is mentioned as a possible vector of Phytomonas staheli McGhee and McGhee, 1979 (Trypanosomatidae), a possible etiological agent of the “Marchitez Sorpresiva” in species of Arecaceae, among these Cocos nucifera L., Elaeis guineensis Jack (Segeren, 1982SEGEREN, P., 1982 [viewed 20 December 2021]. Preliminary study on the vectors of “Hartrot” disease of coconut in Suriname. Surinaamse Landbouw [online], vol. 30, no. 1, pp. 17-23. Available from: https://www.cabdirect.org/cabdirect/abstract/19826741362
https://www.cabdirect.org/cabdirect/abst...
). In addition, the associations between B. hastator and Gossypium hirsutum L. and Phaseolus sp. (Tellez and Maes, 1991TELLEZ, J. and MAES, J.M., 1991. Policultivo maíz- frijol como elemento de lucha biológica contra Dalbulus maidis (Homoptera: Cicadellidae). II. Influencia sobre plagas de maíz y frijol. Revista Nicaraguense Entomologica, vol. 16, pp. 9-20.), Oryza sativa L. (Krinski, 2014KRINSKI, D., 2014. Artrópodes associados ao arroz de terras altas, Oryza sativa, em Novo Progresso, Estado do Pará: níveis de danos e estratégias para manejo. Paraná: Universidade Federal do Paraná, 326 p. Tese de Doutorado em Zoologia.; Rider, 2021RIDER, D.A., 2021 [viewed 20 December 2021]. Pentatomoidea Home Page [online]. Available from: www.ndsu.edu/pubweb/~rider/Pentatomoidea/index.htm.
www.ndsu.edu/pubweb/~rider/Pentatomoidea...
), Rottboellia cochinchinensis (Lour.) Clayton (Haywood et al., 1994HAYWOOD, P.J., LANCASTERZS, B. and EASTWOOD, D., 1994. Insects associated with, and some diseases of Rottboellia cochinchinensis (Lour.) W.D. Clayton in Guyana. In: Proceedings of 25th Conference, West Indies Sugar Technologists, April 18-21, Belize. Belize: West Indies Sugar Technologists. pp. 101-111.) and Sabal mexicana Mart. (Brailovsky et al., 1992BRAILOVSKY, H., CERVANTES, L. and MAYORGA, C., 1992. Hemiptera: Heteroptera de México XLIV. Biología, Estadíos Ninfales y Fenología de la tribu Pentatomini (Pentatomidae) en la Estación de Biología Tropical “Los Tuxtlas”. Veracruz: Universidad Nacional Autónoma de México, 204 p.) were confirmed.

Hexacladia smithii Ashmead, 1891 is a gregarious endoparasitoid present in the neotropics which develops in nymphs and adults of some species of Coreidae (Baldin et al., 2010BALDIN, E.L.L., FUJIHARA, R.T., BOIÇA JUNIOR, A.L. and ALMEIDA, M.C., 2010. Parasitismo de percevejos-praga do maracujazeiro no Brasil por Hexacladia smithii Ashmead (Hymenoptera: encyrtidae). Neotropical Entomology, vol. 39, no. 2, pp. 306-307. http://dx.doi.org/10.1590/S1519-566X2010000200025. PMid:20498972.
http://dx.doi.org/10.1590/S1519-566X2010...
), Pentatomidae (Santis, 1979SANTIS, L., 1979. Catálogo de los himénopteros calcidoideos de América al sur de los Estados Unidos. La Plata: Comisión de Investigaciones Científicas, 488 p.; Corrêa-Ferreira et al., 1998CORRÊA-FERREIRA, B.S., NUNES, M.C. and UGUCCIONI, L.D., 1998. Occurrence of Hexacladia smithii Ashmead parasitoid of Euschistus heros (F.) adults in Brazil. Anais da Sociedade Entomológica do Brasil, vol. 27, no. 3, pp. 495-498. http://dx.doi.org/10.1590/S0301-80591998000300022.
http://dx.doi.org/10.1590/S0301-80591998...
) and Scutelleridae (Santis,1980SANTIS, L., 1980. Catálogo de los himenópteros brasileiros de la serie parasitica incluyendo Bethyloidea. Curitiba: Editora da Universidade Federal do Paraná, 187 p.). Records of H. smithii were confirmed in Brazil (Ashmead, 1891ASHMEAD, W.H., 1891. An encyrtid with six-branched antennae. Insect Life, vol. 3, pp. 455-457.), Costa Rica (Noyes, 2010NOYES, J.S., 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute, vol. 84, pp. 1-848.), Nicaragua (Noyes, 2010NOYES, J.S., 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute, vol. 84, pp. 1-848.), Puerto Rico (Noyes, 2010NOYES, J.S., 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute, vol. 84, pp. 1-848.), and Trinidad and Tobago (Burks, 1972BURKS, B.D., 1972. The genus Hexacladia Ashmead (Hymenoptera: encyrtidae). Proceedings of the Entomological Society of Washington, vol. 74, no. 4, pp. 363-371.; Noyes, 2010NOYES, J.S., 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute, vol. 84, pp. 1-848.). Some species of economic importance such as Arvellius albopunctatus (DeGeer, 1773) (Panizzi and Silva, 2010PANIZZI, A.R. and SILVA, J.J., 2010. New records of pentatomids as hosts of Hexacladia smithii Ashmead (Hymenoptera: Encyrtidae) in southern Brazil. Neotropical Entomology, vol. 39, no. 4, pp. 678-679. http://dx.doi.org/10.1590/S1519-566X2010000400034. PMid:20878011.
http://dx.doi.org/10.1590/S1519-566X2010...
), Edessa meditabunda (Fabricius, 1794) (Cuezzo and Fidalgo, 1997CUEZZO, F. and FIDALGO, P., 1997. Hexacladia smithii Ashmead (Hymenoptera: Encyrtidae): a new record for Argentina and two new pentatomid hosts recorded, Antiteuchus variolosus Westwood and Edessa meditabunda F. (Hemiptera: Pentatomidae). Entomologist, vol. 116, no. 1, pp. 11-14.), Euschistus heros (Fabricius, 1798) (Corrêa-Ferreira et al., 1998CORRÊA-FERREIRA, B.S., NUNES, M.C. and UGUCCIONI, L.D., 1998. Occurrence of Hexacladia smithii Ashmead parasitoid of Euschistus heros (F.) adults in Brazil. Anais da Sociedade Entomológica do Brasil, vol. 27, no. 3, pp. 495-498. http://dx.doi.org/10.1590/S0301-80591998000300022.
http://dx.doi.org/10.1590/S0301-80591998...
) and Diceraeus furcatus (Fabricius, 1775) (cited as Dichelops furcatus, Panizzi and Silva, 2010), were parasitized by H. smithii, in the soybean crops (Glycine max L.) and tomato (Solanum lycopersicum L.) (Panizzi and Silva, 2010PANIZZI, A.R. and SILVA, J.J., 2010. New records of pentatomids as hosts of Hexacladia smithii Ashmead (Hymenoptera: Encyrtidae) in southern Brazil. Neotropical Entomology, vol. 39, no. 4, pp. 678-679. http://dx.doi.org/10.1590/S1519-566X2010000400034. PMid:20878011.
http://dx.doi.org/10.1590/S1519-566X2010...
), among others. In Panama, there is limited information on new records of parasitoids and insects-pest of economic importance and the trophic associations they may present. Therefore, the confirmation of the biotic relationship between H. smithii and B. hastator is considered a relevant contribution to strengthening biological control and integrated pest management programs in emerging insects-pest.

Adults of B. hastator were randomly collected in 25 tomato plants (S. lycopersicum - Cultivar “IDIAP T-7”) by means of insect aspirators adapted for the capture of parasitoids, during the periods of February 2017, March 2018 and February 2019. The experimental tomato plots of 50 m2 were cultivated in a family farming system located in Cabra, Pacora, Panama (09º 07´ N, 79º 19´ W). Dr. Jocelia Grazia (Universidade Federal do Rio Grande do Sul) made the identification and confirmation of B. hastator. The diagnosis of this species indicates that the genus Berecynthus is close to Dichelops Spinola, Padaeus Stål, Euschistus Dallas (Grazia, 1978GRAZIA, J., 1978. Revisão do gênero Dichelops Spinola, 1837 (Heteroptera, Pentatomidae, Pentatomini). Iheringia. Série Zoologia, vol. 53, pp. 3-119.) and more recently to Diceraeus Dallas (Barão et al., 2020BARÃO, K.R., FERRARI, A. and GRAZIA, J., 2020. Phylogenetic analysis of the Euschistus group (Hemiptera: Pentatomidae) suggests polyphyly of Dichelops Spinola, 1837 with the erection of Diceraeus Dallas, 1851, stat. rev. Austral Entomology, vol. 59, no. 4, pp. 770-783. http://dx.doi.org/10.1111/aen.12489.
http://dx.doi.org/10.1111/aen.12489...
). Berecynthus hastator (Fabricius, 1798) is the only valid species of the genus, characterized by the clypeus longer than mandibular plates, differing from the other closer genera, except Euschistus, that includes some species with clypeus longer. The main differences of Berecynthus are found in the morphology of genitalia for both sexes (Figure 1). Voucher specimens collected in 2017 (3♀, 2♂) and 2018 (2♀, 1♂), were deposited in the collections of the Museum of Invertebrates G.B. Fairchild of University of Panama, Panama and the Laboratory of Entomological Systematics (LES) of the Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil (1♀, 2♂).

Figure 1
Berecynthus hastator (Fabricius, 1798) (Hemiptera: Pentatomidae). (a) body, dorsal view; (b) body, ventral view; (c) female genital plate. Photo: Dr. Lurdiana D. Barros.

Adults of B. hasator collected in the experimental plots were separated and transferred to transparent plastic containers (7 cm x 5 cm x 5 cm) with a moistened paper towel at the base of the container and covered with a tulle fabric mesh. Individuals were separated into groups of approximately 10 adults of B. hastator per container, where they were fed peanuts, bean pods and a 90% honey solution, offered in small swabs of cotton. In order to maintain temperature, relative humidity, and constant photoperiod, the insects were transferred to regulated chambers at 28+2 oC, 80% of relative humidity and 12 hours of photophase, located in the laboratory of Biological Pest Control of the Instituto de Innovación Agropecuaria de Panamá (IDIAP), in Chepo, Panama. Adults of H. smithii emerged from B. hastator were identified by Dr. Valmir Costa (Instituto Biológico, Campinas, SP, Brazil) following the key of Noyes (2010)NOYES, J.S., 2010. Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea), 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera, Neuroptera) and ticks (Acari). Memoirs of the American Entomological Institute, vol. 84, pp. 1-848.. This endoparasitoid presents reddish-brown color (Figure 2a) and the basitarsus of mid legs, in both sexes, a line of about 10 stout pegs ventrally. The male´s fore wing, post marginal vein at least 1.5 x as long as stigmal vein (Figure 2b), and the female's fore wing is characterized by the subapical infuscate area broadly connected to median infuscate band, costal cell with less than 10 setae dorsally and at least 2 or 3 setae ventrally, and postmarginal vein clearly longer than stigmal vein (Figure 2c). Voucher specimens (5♀, 3♂) were deposited in the collections of the Museum of Invertebrates G.B. Fairchild of the University of Panama, Panama, and the Oscar Monte Collection of Entomophagous Insects (3♀, 4♂) (IBCBE-007229-007235) of the Instituto Biológico, Campinas, São Paulo, Brazil.

Figure 2
Hexacladia smithii (Ashmead, 1891ASHMEAD, W.H., 1891. An encyrtid with six-branched antennae. Insect Life, vol. 3, pp. 455-457.) (Hymenoptera: Encyrtidae. (a) body, lateral view; (b) male fore wing; (c) female fore wing. Photo: Dr. Valmir A. Costa.

The circular holes caused by the emergence of adults of H. smithii in the abdomen of adults of B. hastator and the quantification of emerged adults of H. smithii allowed to calculate the rate of (%) natural parasitism.

% Parasitism = [(Total Parasitized Adults / Total Collected Adults) 100]

The natural parasitism of H. smithii in adults of B. hastator, over the years 2017, 2018 and 2019, was 39.13% (9/23), 56.25% (9/16), 38.09% (8/21), respectively. Therefore, the first report of H. smithii is considered a new trophic association between this endoparasitoid and B. hastator, for Panama. No damage caused by adults of B. hastator were observed on tomato plants. The data submitted by GBIF (2022)GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
indicated that in Panama the collection of B. hastator were made by means of light traps, thus the trophic association “S. lycopersicum - B. hastator” was not confirmed. Noyes (2019)NOYES, J.S., 2019 [viewed 15 April 2022]. Universal Chalcidoidea Database, 2019 [online]. Available from: https://www.nhm.ac.uk/our-science/data/chalcidoids/database/.
https://www.nhm.ac.uk/our-science/data/c...
confirmed that there were no previous records of H. smithii in Panama, information that was validated by GBIF (2022)GLOBAL BIODIVERSITY INFORMATION FACILITY – GBIF, 2022 [viewed 30 January 2022]. Spermacoce verticillata L.. Available from: https://www.gbif.org/species/2918574.
https://www.gbif.org/species/2918574...
. The relevance of the information presented strengthens the Pentatomidae species management programs, based on the adaptation and colonization of H. smithii, in the agroecological zones of Panama.

Acknowledgments

B. Zachrisson (corresponding author) thanks the Sistema Nacional de Investigación (SNI) of the Secretaría Nacional de Ciencia, Tecnología e Innovación (SENACYT) of Panama for the grant (SNI-19-2020) and the financial support, allowing the conduction of this research. V.A. Costa thanks the INCT-Hympar (Instituto Nacional de Ciência e Tecnologia dos Hymenoptera Parasitoides, CNPq Process 465562/2014-0) for financial support. J. Grazia thanks to CNPq for the fellowship grant (PQ #310747/2020-1) and to L.D. Barros for the photos of B. hastator.

References

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  • BALDIN, E.L.L., FUJIHARA, R.T., BOIÇA JUNIOR, A.L. and ALMEIDA, M.C., 2010. Parasitismo de percevejos-praga do maracujazeiro no Brasil por Hexacladia smithii Ashmead (Hymenoptera: encyrtidae). Neotropical Entomology, vol. 39, no. 2, pp. 306-307. http://dx.doi.org/10.1590/S1519-566X2010000200025 PMid:20498972.
    » http://dx.doi.org/10.1590/S1519-566X2010000200025
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    » http://dx.doi.org/10.1111/aen.12489
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Publication Dates

  • Publication in this collection
    13 June 2022
  • Date of issue
    2024

History

  • Received
    18 Apr 2022
  • Accepted
    30 May 2022
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