Evidencia de competencia por explotación entre parasitoides de huevos de Spodoptera frugiperda(Lepidoptera: Noctuidae) en el maíz
CHERRE SADE BEZERRA DASILVA1,2, JACI MENDES VIEIRA * 1,2,3, MARTA LOIÁCONO4, CECILIA MARGARÍA4 and JOSÉ ROBERTO POSTALI PARRA2
1Corresponding author.
2 D. Sc. Laboratòrio de Biologia de Insetos, Departamento de Entomologia e Acarologia, Escola Superior de Agricultura "Luiz de Queiroz", Universidade de Sao Paulo (ESALQ/USP). Av. Pádua Dias, 11, Piracicaba-SP, Brazil, 13.418-900. entomologista@gmail.com, jrpparra@usp.br.
3 M. Sc. Laboratòrio de Biologia de Insetos. Departamento de Entomologia e Acarologia. ESALQ/USP, jacimvieira@yahoo.com.br.
4 D. Sc. División Entomología, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata. Address: Paseo del Bosque s/n, B1900FWA, La Plata, Argentina.
Key words: Egg parasitoid. Extrinsic competition. Fall armyworm. Field occurrence. Interference competition.
Resumen: Telenomus remus y Trichogramma spp. (Hymenoptera: Platygastridae, Trichogrammatidae) son parasitoides de huevos del gusano cogollero del maíz (GCM), Spodoptera frugiperda (Lepidoptera: Noctuidae) en Brasil. Mientras que los informes sobre el parasitismo de Trichogramma en huevos de S. frugiperda son relativamente comunes, los registros de T. remus en los cultivos brasileños son escasos. En consecuencia, la literatura sobre la competencia entre T. remus y Trichogramma spp. en campo es poca. En este trabajo, se presenta la presencia simultánea de T. remus, Trichogramma pretiosum y Tr. atopovirilia en huevos del GCM en el cultivo de maíz (Piracicaba, Sao Paulo, Brasil). Los resultados muestran que estas tres especies de parasitoides estuvieron involucradas en competencia exploratoria (interacción indirecta, donde el agotamiento de los recursos por parte de una especie impide que la otra tenga acceso a ellos) por los huevos de S. frugiperda. Sin embargo, teniendo en cuenta que se observó el surgimiento de dos y tres especies de parasitoides de una sola masa de huevos, los resultados sugieren que T. remus , Tr. pretiosum y Tr. atopovirilia también participaron en competencia por interferencia (interacciones directas entre los adultos y/o inmaduros que resultan en cambios en el comportamiento o muerte de los individuos). Ambos tipos de competencia pueden afectar la dinámica poblacional de parasitoides con consecuencias para el control biológico de plagas. Por consiguiente, nuestro trabajo destaca la importancia de investigar la competencia entre T. remus , Tr. pretiosum y Tr. atopovirilia por huevos de S. frugiperda en estudios de laboratorio y campo.
]]> Palabras clave: Parasitoide de huevos. Competencia extrínseca. Cogollero del maíz. Presencia en campo. Competencia por interferencia.Introduction
The fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae), is a key pest of maize in Brazil, as well as the greater Americas. Although its control is based mostly on pesticide sprayings, its biological control by means of augmentative releases of egg parasitoids is promising (Cave 2000; Beserra et al. 2002; Parra and Zucchi 2004; Beserra and Parra 2005). The goal of this work was to collect and identify egg parasitoids of S. frugiperda in maize in order to start laboratory cultures and perform studies to assess their competitiveness and potential as biological controllers of the FAW.
Material and methods
We conducted a field survey on May 29th (late autumn) 2010, in a maize plot (1 ha; plants with ca. 90 days after emergence) located at Piracicaba, Sao Paulo, Brazil (22°42’18.57"S 47°38’6.37"W). Fifty-two egg masses (< 18h, ca. 300 eggs) of S. frugiperda were randomly scattered in the plot, with a minimal distance of 10 m from each other. Egg masses were produced in laboratory according to Da Silva and Parra (2013). In an attempt to protect the eggs from predators and direct sunlight, we taped the egg masses inside a collection device, which consisted of a white disposable cup (50 mL) with a punctured bottom and a cotton string (50 cm) passed through it. A knot was made at one extremity of the string in order to prevent the detachment of the cup, while the other extremity was tied to a maize leaf (Fig. 1). The collection devices were recovered two days later and the egg masses were introduced individually into glass tubes (2 x 8 cm) and maintained in incubators (24 ± 1 °C, 70% RH, 14L:10D photoperiod) until parasitoid emergence. In the meantime, caterpillars from non-parasitized eggs were eliminated on a daily basis to prevent injury to the parasitized eggs. Adult females were then individualized, multiplied on eggs of S. frugiperda, and had some adult individuals of their offspring killed in 70% alcohol. The male individuals were set on glass slides with Hoyer’s medium and identified based on the keys developed by Querino and Zucchi (2005), Johnson (1984), Nixon (1937), Nixon (1940) and Chou (1987).
Results and discussion
None of the fifty-two S. frugiperda egg masses exposed to parasitism in field showed any signal of predation (missing eggs or residues of predated eggs). Three species of egg parasitoids were identified: (1) Trichogramma atopovirilia Oatman & Platner, (2) Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae), and (3) Telenomus remus Nixon (Hymenoptera: Platygastridae). The latter species emerged from all 52 egg masses exposed in field, implying that both Trichogrammatids always had to compete with the platygastrid for the same egg masses. Trichogramma pretiosum and Tr. atopovirilia emerged from 19 and 3 egg masses, respectively. Surprisingly, a combination of the three egg parasitoid species was found in one out of the 52 exposed egg masses (Fig. 2).
The fact that T. remus emerged from every egg mass exposed in field suggests a competitive dominance in relation to both Trichogrammatids. Facing such a high dominance, Tr. atopovirilia and Tr. pretiosum simply may have not been able to emerge from T. remus-free egg masses. Alternatively, the fact that the emergences of Tr. atopovirilia and Tr. pretiosum were invariably associated with the emergence of T. remus might be an indication that both Trichogrammatids practice hyperparasitism on T. remus. It has been demonstrated that Tr. pretiosum can develop as facultative hyperparasitoid of T. sphingi (Strand and Vinson, 1984), although Carneiro and Fernandes (2012) found no evidence of emergence of Tr. pretiosum from S. frugiperda eggs previously parasitized by T. remus.
]]> Telenomus remus, Tr. atopovirilia and Tr. pretiosum have been the most cited egg parasitoids of the FAW in Latin America (Cave 2000; Beserra et al. 2002; Parra and Zucchi 2004; Beserra and Parra 2005). Although Telenomus remus was introduced in Brazil 29 years ago, reports on its natural occurrence in field have been very rare, while wild populations of Tr. pretiosum and/or Tr. atopovirilia are often reported (Beserra et al. 2002; Bueno et al. 2009; Bueno et al. 2010). Out of these three species, T. remus has been considered the best candidate for augmentative biological control programs due to their large size, robustness, and ability to reach the inner layers of the FAW egg masses (Cave 2000). Indeed, laboratory studies have demonstrated that T. remus parasitizes eggs of S. frugiperda faster than Tr. pretiosum and, when both species are put together in an arena containing FAW eggs, the majority of the adults emerged are of T. remus (Carneiro and Fernandes 2012). Nevertheless, there are no actual studies exploring the interference and the exploitative competitions among T. remus, Tr. atoporivilia and Tr. pretiosum in field conditions.According to Park (1954), a serious study of interspecific competition should start with proof that competition exists. Our report shows the coexistence of these three egg parasitoid species in the same environment and using the same host species, which implies that they are engaged in a competitive interaction with each other. Other species of Telenomus and Trichogramma have been found sharing host species at the same time/space in Japan and Spain (Cabello 1989; Hirose et al. 1968a; Hirose et al. 1968b). However, we are unaware of previous reports of the coexistence of T. remus, Tr. atopovirilia and Tr. pretiosum in the same environment and especially on the same egg mass. These results are not only evidence that T. remus, Tr. atopovirilia and Tr. pretiosum are engaged in exploitative competition (indirect interaction, where the depletion of resources by one species prevents the other access to it) towards S. frugiperda eggs, but our findings also strongly suggest that the three parasitoids are also displaying interference competition (direct interactions among adults and/or immature individuals resulting in behavioral changes or even death of individuals). Both kinds of competition, combined or not, may have profound implications in the population dynamics (Ricklefs and Miller 2000) of these egg parasitoids and, must be matter of further investigations. Additionally, recent studies (Penaflor et al. 2011a; b) showed that oviposition by S. frugiperda on maize leaves changes the volatile emissions of maize plants, and the authors hypothesize that such changes might constitute chemical signals that attract egg parasitoids of FAW. Our study showed that such signals are not critical for T. remus, Tr. atopovirilia and Tr. pretiosum to successfully find eggs of S. frugiperda in the field, since we attached the egg masses to the collection devices instead of inducing female moths to lay eggs directly on the maize leaves, and even so the parasitoids were able to find the hosts despite the lack of chemical cues released from the maize plants.
Here we reported the spontaneous occurrence of T. remus, Tr. pretiosum and Tr. atopovirilia, three egg parasitoids of S. frugiperda, in maize, implying that these wasp species were engaged in exploitative competition and likely involved in interference competition towards eggs of S. frugiperda in field. Since both kinds of competition may affect the population dynamics of parasitoids with consequences to the biological control of pests, our study highlights the importance of determining the outcome of competition among T remus, Tr. pretiosum and Tr. atopovirilia towards eggs of S. frugiperda in laboratory and field studies.
Acknowledgements
We are grateful to Arodi Prado for collaborating with the parasitoid collection in the field; to Mariana Graciano Zério for collaborating with the maintenance of insect colonies in the laboratory; and to Alyssa De La Rosa for the English revision. The first author received a scholarship from Fundagao de Amparo a Pesquisa do Estado de Sao Paulo (process 2007/07054-8). This study was also supported by Secretaría de Ciencia y Técnica de la Universidad Nacional de La Plata, Argentina, processes 11N744 and 11A263 (Dras. Loiacono and Margaria).
Literature cited
BESERRA, E. B.; DIAS, C. T. S.; PARRA, J. R. P. 2002. Distribution and natural parasitism of Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs at different phenological stages of corn. Florida Entomologist 85 (4): 588-593. [ Links ]
BESERRA, E. B.; PARRA, J. R. P. 2005. Impact of the number of Spodoptera frugiperda egg layers on parasitism by Trichogramma atopovirilia. Scientia Agricola 62 (2): 190-193. [ Links ]
]]>BUENO, R. C. O. F.; BUENO, A. F.; PARRA, J. R. P.; VIEIRA, S. S.; OLIVEIRA, L. J. 2010. Biological characteristics and parasitism capacity of Trichogramma pretiosum Riley (Hymenoptera, Trichogrammatidae) on eggs of Spodoptera frugiperda (J. E. Smith) (Lepidoptera, Noctuidae). Revista Brasileira de Entomologia 54 (2): 322-327. [ Links ]
BUENO, R. C. O. F.; PARRA, J. R. P.; BUENO, A. F. 2009. Biological characteristics and thermal requirements of a Brazilian strain of the parasitoid Trichogramma pretiosum reared on eggs of Pseudoplusia includens and Anticarsia gemmatalis. Biological Control 51 (3): 355-361. [ Links ]
CABELLO, T. 1989. Natural enemies of noctuid pests (Lep., Noctuidae) on alfalfa, corn, cotton and soybean crops in southern Spain. Journal of Applied Entomology 108 (1-5): 80-88. [ Links ] CARNEIRO, T. R.; FERNANDES, O.A. 2012. Interspecific interaction between Telenomus remus (Hymenoptera: Platygastridae) and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) on Spodoptera frugiperda (Lepidoptera: Noctuidae) eggs. Anais da Academia Brasileira de Ciencias 84 (4): 1127-35. [ Links ]
CAVE, R. D. 2000. Biology, ecology and use in pest management of Telenomus remus. Biocontrol News and Information 21 (1): 2126. [ Links ]
CHOU, L. Y. 1987. Note on Telenomus remus (Hymenoptera: Scelionidae). Bulletin of the Entomological Society Natural Chung-Hsing University 20: 15-20. [ Links ]
DA SILVA, C. S. B.; PARRA, J. R. P. 2013. New method for rearing Spodopterafrugiperda in laboratory shows that larval cannibalism is not obligatory. Revista Brasileira de Entomologia 57 (3): 347349. [ Links ]
HIROSE, Y.; SHIGA, M.; NAGASUJI, F. 1968a. Interspecific relations among three hymenopterous egg parasites of the pine moth, Dendrolimus spectabilis Butler (Lepidoptera: Lasiocampidae) in the Japanese black pine forest. II. Spatial interspersion of the two egg parasites, Trichogramma dendrolimi and Telenomus dendrolimi in the pine crown. Journal of the Faculty of Agriculture, Kyushu University 14 (3): 459-472. [ Links ]
HIROSE, Y.; SHIGA, M.; NAGASUJI, F. 1968b. Interspecific relations among three hymenopterous egg parasites of the pine moth, Dendrolimus spectabilis Butler (Lepidoptera: Lasiocampidae) in the Japanese blackpine forest. I. Methods of the study and general sketches of the biology of the host and parasites. Journal of the Faculty of Agriculture, Kyushu University 14 (3): 449-458. [ Links ]
JOHNSON, N. F. 1984. Systematics of Nearctic Telenomus: classification and revisions of the podisi and phymatae species groups (Hymenoptera: Scelionidae). Bulletin of the OhioBiological Survey, New Series 6 (3): 1-113. [ Links ]
NIXON, G. E. J. 1937. Some Asiatic Telenominae (Hym., Proc-totrupoidea). Annals and Magazine of Natural History 10 (20): 444-475. [ Links ]
NIXON, G. E. J. 1940. New species of Proctotrupoidea. Annals and Magazine of Natural History 11 (6): 497-512. [ Links ]
PARK, T. 1954. Experimental studies of interspecies competition .2. Temperature, humidity, and competition in 2 species of Tribolium. Physiological Zoology 27 (3): 177-238. [ Links ]
PARRA, J. R. P.; ZUCCHI, R. A. 2004. Trichogramma in Brazil: feasibility of use after twenty years of research. Neotropical Entomology 33 (3): 271-281. [ Links ]
PENAFLOR, M. F. G. V.; ERB, M.; MIRANDA, L.A.; WERNEBURG, A. G.; BENTO, J. M. S. 2011a. Herbivore-induced plant volatiles can serve as host location cues for a generalist and a specialist egg parasitoid. Journal of Chemical Ecology 37 (12): 1304-1313. [ Links ]
PENAFLOR, M. F. G. V; ERB, M.; ROBERT, C. A.; MIRANDA, L. A.; WERNEBURG, A. G.; DOSSI, F. C.; TURLINGS, T. C.; BENTO, J. M. S. 2011b. Oviposition by a moth suppresses constitutive and herbivore-induced plant volatiles in maize. Planta 234 (1): 207-15. [ Links ]
QUERINO, R. B.; ZUCCHI, R. A. 2005. An illustrated key to the species of Trichogramma (Hymenoptera: Trichogrammatidae) of Brazil. Zootaxa 1073: 37-60. [ Links ]
RICKLEFS, R. E.; MILLER, G. L. 2000. Ecology, W. H. Freeman and Company, New York. [ Links ]
STRAND, M. R.; VINSON, S. B. 1984. Facultative hyperparasitism by the egg parasitoid Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Annals of the Entomological Society of America 77 (6): 679-686. [ Links ]
Received: 3-Dec-2014
Accepted: 10-Dec-2015
Suggested citation:
]]> DASILVA, C. S. B.; VIEIRA, J. M.; LOIÁCONO, M.; MARGARÍA, C.; PARRA, J. R. P. 2015. Evidence of exploitative competition among egg parasitoids of Spodoptera frugiperda (Lepidoptera: Noctuidae) in maize. Revista Colombiana de Entomología 41 (2): 184-186. Julio - Diciembre 2015. ISSN 0120-0488.]]>