Oil palm (Elaeis guineensis) monoculture may favor insect pests and disease vectors (Gitau et al. 2009). The defoliating caterpillars, Opsiphanes invirae Hübner and Brassolis sophorae L. (Lepidoptera: Nymphalidae), and the crown-leaf borer, Eupalamides cyparissias (Fabricius) (Lepidoptera: Castniidae), affect the development and productivity of this crop in northern Brazil (Vasquez et al. 2008; Ribeiro et al. 2010). Studies involving control methods of these pests are needed.
Trichospilus diatraeae Margabandhu & Cherian (Hymenoptera: Eulophidae) is a pupal parasitoid of many lepidopteran families, such as Arctiidae (Bennett et al. 1987; Paron & Berti-Filho 2000), Crambidae (Bennett et al. 1987), Oecophoridae (Oliveira et al. 2001), Pieridae (Torres-Bauza 1994), Geometridae (Pereira et al. 2008; Zaché et al. 2010; Pastori et al. 2012), Saturniidae (Pastori et al. 2012), Lymantriidae (Zaché et al. 2011a), Riodinidae (Zaché et al. 2011b), Noctuidae and Nymphalidae (Bennett et al. 1987; Zaché et al. 2012).
Female parasitoids must overcome the host's defensive behavior and immune response (Andrade et al. 2010). These factors can affect the biological characteristics and the host choice of parasitoids (Gross 1993; Völkl & Stadler 1996; Farias & Hopper 1999; Walker & Hoy 2003). The objective of this study was to evaluate the potential parasitism of lepidopteran pests of oil palm by T. diatraeae.
Opsiphanes invirae, B. sophorae and E. cyparissias pupae were obtained from oil palms in the district of Tailandia, Pará State, Brazil (S 24° 2.04′ W 48° 08.02′). Trichospilus diatraeae was reared on Tenebrio molitor L. (Coleoptera: Tenebrionidae) pupae at the Federal University of Viçosa, Viçosa, Minas Gerais State, Brazil, at 25 ± 2 °C, 70 ± 10% RH and 12:12 h L:D (Favero 2009). Originally, T. diatraeae was obtained from Thyrinteina arnobia (Stoll) (Lepidoptera: Geometridae) pupae collected on Eucalyptus cloeziana F. Muell. (Myrtales: Myrtaceae) plants (Pereira et al. 2008).
Groups of fifty 2-day old T. diatraeae females were placed inside test tubes (14.5 cm H × 2.0 cm diam) together with one pupa of one of the following hosts: O. invirae, B. sophorae or E. cyparissias, for 48 h. The tubes were closed with cotton and parasitoids females fed with a drop of pure honey applied with a surgical needle on the wall of the test tubes (Pereira et al. 2009).
Trichospilus diatraeae parasitized E. cyparissias (Fig. 1A), B. sophorae (Fig. 1B) and O. invirae pupae (Fig. 1C), with parasitism rates of 90%, 100% and 90%, respectively. Releases of this parasitoid may provide an alternative biological control in oil palm crops, where several species of Lepidoptera pests can occur simultaneously (Ribeiro et al. 2010). However, further studies are needed to assess the mobility and dispersal of T. diatraeae in the field (Zappalà et al. 2012) and determine whether mass release of this parasitoid could interfere with other natural enemies (Charles 2012).
Trichospilus diatraeae developed in pupae of O. invirae and B. sophorae. An average of 447.83 ± 51.52 and 669.00 ± 89.62 parasitoid adults/ pupa were obtained from these hosts, respectively. These results show the potential of this parasitoid to control defoliators and its possible establishment in the field through inoculative releases (Eilenberg et al. 2001). However, T. diatraeae adults did not emerge from E. cyparissias pupae probably because of host defense mechanisms (Gross 1993; Pennacchio & Strand 2006). The number of T. diatraeae females (50) per E. cyparissias pupae may have been insufficient to generate the amount of toxins and immature individuals required to overcome the host defense mechanism (Zaki et al. 1994; Andrade et al. 2010). Encapsulated parasitoids were found inside dissected pupae of E. cyparissias.
Fig. 1.
Eupalamides cyparissias (Lepidoptera: Castniidae) (A), Brassolis sophorae (B) and Opsiphanes invirae (C) (Lepidoptera: Nymphalidae) pupae parasitized by Trichospilus diatraeae (Hymenoptera: Eulophidae).
Trichospilus diatraeae can be reared on pupae of the oil palm defoliator caterpillars, O. invirae and B. sophorae, indicating the potential of this parasitoid for the control of these pests.
ACKNOWLEDGMENTS
We thank “Conselho Nacional de Desenvolvimento Científico e Tecnólogico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)”, “Fundação de Amparo à pesquisa do Estado de Minas Gerais (FAPEMIG)” and “Grupo Agropalma” for financial support.
REFERENCES CITED
1.
G. S. Andrade
,
J. E. Serrão
,
J. C. Zanuncio
,
T. V. Zanuncio
,
G. L. D. Leite
, and
R. A. Polanczyk
2010. Immunity of an alternative host can be overcome by higher densities of its parasitoids
Palmistichus elaeisis and
Trichospilus diatraeae. PLoS One 5(10): 13231.
Google Scholar
2.
F. D. Bennett
,
H. Glenn
,
M. Yaseen
, and
R. M. Baranowski
1987. Records of
Trichospilus diatraeae, an Asian parasite (Hymenoptera: Eulophidae) from the Caribbean and Florida. Florida Entomol. 70: 184–186.
Google Scholar
3.
J. G. Charles
2012. Assessing the non-target impacts of classical biological control agents: is host-testing always necessary? BioControl 57: 619–626.
Google Scholar
4.
J. Eilenberg
,
A. Hajek
, and
C. Lomer
2001. Suggestions for unifying the terminology in biological control. BioControl 46: 387–400.
Google Scholar
5.
A. M. I. Farias
, and
K. R. Hopper
1999. Oviposition behavior of
Aphelinus asychis (Hymenoptera: Aphelinidae) and
Aphidius matricariae (Hymenoptera: Aphidiidae) and defense behavior of their host
Diuraphis noxia (Homoptera: Aphididae). Environ. Entomol. 28: 858–862.
Google Scholar
6.
K. Favero
2009. Biologia e técnicas de criação de
Trichospilus diatraeae (Hymenoptera: Eulophidae) em pupas de
Tenebrio molitor (Coleoptera: Tenebrionidae) e
Diatraea saccharalis (Lepidoptera: Crambidae). Dourados, MS, (Mestrado em Entomologia e Conservação da Biodiversidade) - Universidade Federal da Grande Dourados, 77 p.
Google Scholar
7.
C. W. Gitau
,
G. M. Gurr
,
C. Dewhurst
,
M. J. Fletcher
, and
A. Mitchell
2009. Insect pests and insectvectored diseases of palms. J. Australian Entomol. 48: 328–342.
Google Scholar
8.
P. Gross
1993. Insect behavioral and morphological defenses against parasitoids. Annu. Rev. Entomol. 38: 251–27.
Google Scholar
9.
M. A. S. Oliveira
,
N. T. V. Junqueira,
I. M. Icuma
,
R. T. Alves
,
J. N. S. Oliveira
, and
G. A. Andrade
2001. Incidência de danos da broca do fruto da graviola no Distrito Federal. Comun. Técnol. 51: 01–06.
Google Scholar
10.
P. L. Pastori
,
F. F. Pereira
,
G. S. Andrade
,
R. O. Silva
,
J. C. Zanuncio
, and
A. I. A. Pereira
2012. Reproduction of
Trichospilus diatraeae (Hymenoptera: Eulophidae) in pupae of two lepidopterans defoliators of eucalypt. Rev. Colombiana Entomol. 38: 91–93.
Google Scholar
11.
M. R. Paron
, and
E. Berti Filho
2000. Capacidade reprodutiva de
Trichospilus diatraeae (Hymenoptera: Eulophidae) em pupas de diferentes hospedeiros (Lepidoptera). Sci. Agric. 57: 355–358.
Google Scholar
12.
F. Pennacchio
, and
M. R. Strand
2006. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 51: 233–258.
Google Scholar
13.
F. F. Pereira
,
J. C. Zanuncio
,
M. T. Tavares
,
P. L. Pastori
,
G. C. Jacques
, and
E. F. Vilela
2008. New record of
Trichospilus diatraeae as a parasitoid of the eucalypt defoliator
Thyrinteina arnobia in Brazil. Phytoparasitica 36: 304–306.
Google Scholar
14.
F. F. Pereira
,
J. C. Zanuncio
,
J. E. Serräo
,
H. N. Oliveira
,
K. Fávero
, and
E. L. V. Grance
2009. Progênie de
Palmistichus elaeisis Delvare & LaSalle (Hymenoptera: Eulophidae) parasitando pupas de
Bombyx mori L. (Lepidoptera: Bombycidae) de diferentes idades. Neotrop. Entomol. 38: 660–664.
Google Scholar
15.
R. C. Ribeiro
,
W. P. Lemos
,
A. S. Bernardino
,
J. Buecke
, and
A. A. Müller
2010. Primeira ocorrência de
Alcaeorrhynchus grandis (Dallas) (Hemiptera: Pentatomidae) predando lagartas desfolhadoras do dendezeiro no Estado do Pará. Neotrop. Entomol. 39: 131–132.
Google Scholar
16.
J. A. Torres-Bauza
1994. Hymenopterous parasitoids of
Dismorfia spio (Pieridae: Dismorphiinae). J. Lepidopt. Soc. 48: 266.
Google Scholar
17.
J. Vasquez
,
C. Delgado
,
G. Couturier
,
K. Mejia
,
L. Freitas
, and
D. Castillo
2008. Pest insects of the palm tree
Mauritia flexuosa L.f., dwarf form, in Peruvian Amazonia. Fruits 63: 227–238.
Google Scholar
18.
W. Völkl
, and
B. Stadler
1996. Colony orientation and successful defense behavior in the conifer aphid,
Schizolachnus pineti. Entomol. Exp. Appl. 78: 197– 200.
Google Scholar
19.
A. M. Walker
, and
M. A. Hoy
2003. Responses of
Lipoplexis oregmae (Hymenoptera: Aphidiidae) to different instars of
Toxoptera citricida (Homoptera: Aphididae). J. Econ. Entomol. 96: 1685–1692.
Google Scholar
20.
F. N. Zaki
,
G. Elsaadany
,
A. Gomaa
, and
M. Saleh
1994. Some biological factors affecting the production of the larval parasitoid
Bracon brevicornis Wesm. (Hymenoptera: Braconidae). J. Appl. Entomol. 118: 413–418.
Google Scholar
21.
B. Zaché
,
C. F. Wilcken
,
R. R. Da Costa
, and
E. P. Soliman
2010.
Trichospilus diatraeae Cherian & Margabandhu, 1942 (Hymenoptera: Eulophidae), a new parasitoid of
Melanolophia consimilaria (Lepidoptera: Geometridae). Phytoparasitica 38: 355–357.
Google Scholar
22.
B. Zaché
,
C. F. Wilcken
,
R. R. C. Zaché
, and
N. M. Souza
2012. New occurrence of
Trichospilus diatraeae (Hymenoptera: Eulophidae) as a parasitoid of
Spodoptera cosmioides Walker, 1858 (Lepidoptera: Noctuidae) in Brazil. Biota Neotrop. 12: 1–4.
Google Scholar
23.
B. Zaché
,
R. R. C. Zaché
,
E. P. Soliman
, and
C. F. Wilcken
2011a. Evaluation of
Trichospilus diatraeae (Hymenoptera: Eulophidae) as parasitoid of the eucalyptus defoliator
Euselasia eucerus (Lepidoptera: Riodinidae). Intl. J. Trop. Insect Sci. 20: 1–5.
Google Scholar
24.
B. Zaché
,
R. R. C. Zaché
,
N. M. Souza
,
T. K. R. Dias
, and
C. F. Wilcken
2011b. New record of
Trichospilus diatraeae margabandhu & cherian, 1942 (Hymenoptera: Eulophidae) parasitizing
Sarsina violascens (Herrich-Schaeffer, 1856) (Lepidoptera: Lymantriidae) in Brazil. J. Plant. Protect. Res. 51: 420–422.
Google Scholar
25.
L. Zappalá
,
O. Campolo
,
S. B. Grande
,
F. Saraceno
,
A. Biondi
,
G. Siscaro
, and
V. Palmeri
2012. Dispersal of
Aphytis melinus (Hymenoptera: Aphelinidae) after augmentative releases in citrus orchards. European J. Entomol. 109: 561–568.
Google Scholar