The rice stalk stink bug, Tibraca limbativentris (Stål 1860) (Hemiptera: Pentatomidae), is a major pest of rice in Latin American countries including Argentina, Brazil, Columbia, Ecuador, Peru, Dominican Republic and Venezuela (Fernandes & Grazia 1998; Borges et al. 2006; Pantoja et al. 2007). The few reports of natural enemies associated with T. limbativentris are restricted to egg parasitoids, e.g., Oencyrtus submetallicus (Howard) (Hymenoptera: Encyrtidae), Telenomus podisi Ashmead 1893 (Hymenoptera: Platygastridae) and Trissolcus urichi Crawford 1913 (Hymenoptera: Platygastridae) in northeastern Brazil (State of Maranhão) (Maciel et al. 2007), and T. podisi and T. urichi, in southern Brazil (State of Santa Catarina) (Riffel et al. 2010). With regard to entomopathogens, the fungi Beauveria bassiana (Bals.) Vuill. and Metarhizium anisopliae (Metsch.) have been found on rice stalk stink bugs (RSSB) only after artificial infection (Martins & Lima 1994; Martins et al. 1997; Martins et al. 2004). This work reports the incidence of tachinid flies parasitizing T. limbativentris during the fallow period in southern Brazil.
A total of 60 pairs of RSSB of unknown age were collected from under rice straw after harvest in Jul 2011 in the municipality of Eldorado do Sul, State of Rio Grande do Sul, Brazil (30 02′ S; 51° 23′ W). Each individual was placed in a plastic box (15 × 10 cm) with 10 g of rice straw sterilized with sodium hypochlorite solution (2%), for 30 min, and covered with voile. The bugs were kept under controlled conditions (25 ± 1 C; 60 ± 10% RH; 12:12 h L: D) without food, and inspected daily for pupae, and the straw was moistened with distilled water every 3 d.
The bugs were inspected daily and, whenever present, tachinid pupae were collected and stored under the same controlled conditions in Petri dishes (Ø5 cm), with moistened cotton until the parasitoid emergence. Specimens were deposited in the Entomological Collection of the Museu de Zoologia, Universidade de São Paulo, Brazil (MZSP).
Adults of 2 species of Tachinidae emerged, both belonging to subfamily Phasiinae: Cylindromyia brasiliana (Townsend 1927) (Cylindromyiini) and Phasia (Paraphorantha) sp. (Phasiini). The parasitism by these 2 tachinid species was found only on males of T. limbativentris (35%/total collected). According to Aldrich (1995) and Aldrich & Zhang (2002), sex pheromones of male pentatomids might act as kairomones for the Scelionidae and Tachinidae; which could explain our results.
Cylindromyia brasiliana emerged (13 females and 3 males) from 71.4% of the parasitized bugs. Cylindromyia Meigen, 1803 (Tachinidae, Phasiinae, Cylindromyiini) is a species-rich genus distributed almost worldwide and with 25 species in the Latin America (Guimarães 1976). Several studies report species of this genus parasitizing pentatomid bugs with records in North America (Arnaud 1978; Eger & Ables 1981), South America (Guimarães 1977), Asia (Sâmet et al. 1977; Honda 1985; Nishiyama et al. 1995; Markova 1999; Richter & Markova 1999; Tillman 2008), Europe (Dupuis 1963; Gordún & Tschorsnig 2008), and Australia (Coombs & Khan 1997; Kay 2002). On the other hand, the only host record in South America is for C. porteri (Brèthes 1925) on the pentatomids Acledra albocostata (Spinola 1852) and A. dimidiaticollis (Spinola 1852) in Chile (Guimarães 1971, 1977). This is the first host, T. limbativentris, reported for a tropical South American species of Cylindromyia.
The second tachinid species, Phasia (Paraphorantha) sp., was observed in 28.6% of parasitized bugs, and 4 females and 1 male emerged. Phasia Latreille 1804 (Tachinidae, Phasiinae, Phasiini) is a worldwide distributed genus including about 110 species (Guimarães 1971; Sun & Marshall 2003; O'Hara & Wood 2004). Phasia contains 34 Neotropical species, two of them previously belonging to the genus Paraphorantha Townsend 1915 (now in synonymy with Phasia). The specimens collected in this study were not identified to the species level, but they correspond undoubtedly to a species formerly included in Paraphorantha. The South American Phasia have been recorded as parasitoids of a few species of Pyrrhocoridae, Coreidae and Meloidae (Guimarães 1977). According to Sun & Marshall (2003), Phasia species present low parasitism rates, varying from < 1% to 11% of parasitized individuals.
There are few reports of tachinid parasitoids in South America pentatomids, e.g., Gymnoclytia paulista (Townsend, 1929) and Beskia aelops Walker 1849 were reported on Oebalus ypsilongriseus (DeGeer, 1773) (Vecchio 1993) in rice crops, and B. aelops was registered parasitizing the small rice stink bug Oebalus poecilus (Dallas 1851) in Guiana (Guimarães 1977; Sutherland & Bahaeally 2002).
This is the first record of C. brasiliana and Phasia (Paraphorantha) sp. as parasitoids on T. limbativentris. These data contribute to the knowledge of natural enemies associated with this stink bug, and may provide further management support to the biological control of T. limbativentris on rice crops.
SUMMARY
Species-level identifications are important to integrated management for sustainable rice production. Adults of T. limbativentris (Stål 1860) (Hemiptera, Pentatomidae) were collected from under the straw during the fallow season of the irrigated rice crop in Eldorado do Sul municipality, State of Rio Grande do Sul, Brazil. Two species of Tachinidae were recorded on the rice stalk stink bug: Cylindromyia brasiliana (Townsend 1927) and Phasia (Paraphorantha) sp. This is the first report of these species parasitizing T. limbativentris under natural conditions.
ACKNOWLEDGMENTS
We express thanks to Capes (PMF) and CNPq (LRR proc. n. 305956/2010-8 and SSN proc. n. 303897/2008-2) and FAPESP (SSN, proc. n. 07/50836-7) for fellowships awarded to the authors.
REFERENCES CITED
1.
J. R. Aldrich
1995. Chemical communication in true bugs and exploitation by parasitoids and commensals, pp. 318–363
In
R. T. Cardé
and
W. J. Bell
[eds.],
Chemical Ecology of Insects II, Chapman & Hall, New York.
Google Scholar
2.
J. R. Aldrich
, and
A. Zhang
2002. Kairomone strains of
Euclytia flava (Townsend), a parasitoid of stink bugs. J. Chem. Ecol. 28: 1565–1582.
Google Scholar
3.
P. H. Arnaud
1978. A host-parasite catalog of North American Tachinidae (Diptera). USDA, Misc. Publ. 1319, Washington, DC. 860 pp.
Google Scholar
4.
M. Borges
,
M. Birkett
,
J. R. Aldrich
,
J. E. Liver
,
M. Chiba
,
Y. Murata
,
R. A. Laumann
,
J. A. Barrigossi
,
J. A. Pickett
, and
M. C. B. Moraes
2006. Sex attractant pheromone from the rice stalk stink bug,
Tibraca limbativentris (Stål). J. Chem. Ecol. 32: 2749–2761.
Google Scholar
5.
M. Coombs
, and
S. A. Khan
1997. New host/parasitoid records for Australian Pentatomidae, Tachinidae and Braconidae. Austral. Entomol. 24: 61–64.
Google Scholar
6.
C. Dupuis
1963. Essai monographique sur les Phasiinae (Diptères Tachinaires parasites d'Hétéroptères). Mem. Mus. Natl. Hist. Nat. (Zoologie) 26: 1–461.
Google Scholar
7.
J. E. Eger Jr., and
J. R. Ables
1981. Parasitism of Pentatomidae by Tachinidae in South Carolina and Texas. Southwest. Entomol. 6: 28–33.
Google Scholar
8.
J. A. M. Fernandes
, and
J. Grazia
1998. Revision of the genus
Tibraca Stål (Heteroptera, Pentatomidae, Pentatominae). Rev. Bras. Zool. 15: 1049–1060.
Google Scholar
9.
E. Gordún
, and
H. P. Tschorsnig
2008. Wirtsbefunde von Phasiinae (Diptera: Tachinidae) aus Wanzen (Hemiptera: Pentatomidae und Scutelleridae) in Nordost-Spanien. Mitt. Entomol. Ver. Stuttgart 43: 41–42.
Google Scholar
10.
J. H. Guimarães
1971. Family Tachinidae (Larvaevoridae)
In A Catalogue of the Diptera of the Americas south of the United States. Museu de Zoologia, Universidade de São Paulo, São Paulo, v.104, 333 pp.
Google Scholar
11.
J. H. Guimarães
1976. A revision of the genus
Cylindromyia Meigen in the Americas South of the United States (Diptera, Tachinidae). Arquivos de Zool. 27: 1–50.
Google Scholar
12.
J. H. Guimarães
1977. Host-parasite and parasite host catalogue of South American Tachinidae (Diptera). Arq. Zool. 40: 1–31.
Google Scholar
13.
K. Honda
1985. A note on
Cylindromyia brassicaria (Fabr.) (Diptera, Tachinidae), a parasite of the sloe bug,
Dolycoris baccarum Linnaeus (Hemiptera, Pentatomidae). Jap. J. Appl. Entomol. Zool. 29: 78–80.
Google Scholar
14.
I. R. Kay
2002. Parasitism of
Eysarcoris trimaculatus (Distant) (Hemiptera: Pentatomidae) by two tachinid flies (Diptera: Tachinidae). Austral. Entomol. 29: 21–24.
Google Scholar
15.
A. A. S. MacIel
,
R. N. S. Lemos
,
J. R. Souza
,
V. A. Costa
,
J. A. F. Barrigossi
, and
E. F. Chagas
2007. Parasitismo de ovos de
Tibraca limbativentris Stal (Hemiptera: Pentatomidae) na cultura do arroz no Maranhão. Neotrop. Entomol. 36: 616–618.
Google Scholar
16.
T. O. Markova
1999. New host and distribution data of tachinid flies of subfamily Phasiinae (Diptera, Tachinidae) in Siberia and Russian Far East. — Far East. Entomol. 75: 1–8.
Google Scholar
17.
J. F. S. Martins
, and
M. G. A. Lima
1994. Fungos entomopatogênicos no controle do percevejo-do-colmo do arroz
Tibraca limbativentris Stal: Virulência de isolados de
Metarhizium anisopliae (Metsch.) Sorok. e
Beauveria bassiana (Bals.) Vuill. An. Soc. Entomol. Brasil 23: 39–44.
Google Scholar
18.
J. F. S. Martins
,
M. G. A. Lima
,
M. Botton
,
J. J. Carbonari
, and
E. D. Quintela
1997. Efeito de Isolados de
Metarhizium anisopliae (Metsch.) Sorok. e
Beauveria bassiana (Bals.) Vuill. sobre o Percevejo-do-Colmo do Arroz,
Tibraca limbativentris Stal. An. Soc. Entomol. Brasil 26: 277–283.
Google Scholar
19.
J. F. S. Martins
,
M. Botton
,
J. J. Carbonari
, and
E. D. Quintela
2004. Eficiência de
Metarhizium anisopliae no controle do Percevejo-do-Colmo
Tibraca limbativentris (Heteroptera: Pentatomidae) em lavoura de arroz irrigado. Cien. Rural. 34: 1681–1688.
Google Scholar
20.
M. Nishiyama
,
M. Iwasa
, and
K. Hori
1995. Parasitism by tachinid flies (Diptera, Tachinidae) of heteropterous insects in Tokachi, Hokkaido. Jap. J. Entomol. 63: 159–165.
Google Scholar
21.
J. E. O'Hara
, and
D. M. Wood
2004. Catalogue of the Tachinidae (Diptera) of America north of Mexico. Mem. Entomol. Int. 18: 1–410.
Google Scholar
22.
A. Pantoja
,
M. Triana
,
H. Bastidas
,
C. García
,
D. I. Meija
, and
M. C. Duque
2007. Damage by
Tibraca limbativentris (Hemiptera: Pentatomidae) to rice in Southwestern Colombia. J. Agric. Univ. Puerto Rico 91:11–18.
Google Scholar
23.
V. A. Richter
, and
T. O. Markova
1999. The tachinid species
Cylindromyia umbripennis van der Wulp new to the fauna of Russia (Diptera: Tachinidae). Zoosyst. Rossica. 8: 188.
Google Scholar
24.
C. T. Riffel
,
H. F. Prando
, and
M. I. Boof
2010. Primeiro relate de ocorrência de
Telenomus podisi (Ashmead) e
Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) como parasitóides de ovos do percevejo-do-colmo-do-arroz, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae), em Santa Catarina. Neotrop. Entomol. 39: 447–448.
Google Scholar
25.
K. Sâmet
,
A. Farzâneh
, and
M. Barkhordâri
1977. Primary list of Diptera (Tachinidae) of Iran. J. Entomol. Soc. Iran 4: 83–86.
Google Scholar
26.
X. Sun
, and
S. A. Marshall
2003. Systematics of
Phasia Latreille (Diptera: Tachinidae). Zootaxa, 276: 1–320.
Google Scholar
27.
J. P. Sutherland
, and
V. Bahaeally
2002. Spatio-temporal distribution of
Beskia aelops (Walker) (Diptera: Tachinidae) and its potential for the biocontrol of
Oebalus poecilus (Dallas) (Hemiptera: Pentatomidae). Biocontrol Sci. Technol. 12: 513–517.
Google Scholar
28.
G. Tillman
2008. Populations of stink bugs (Heteroptera: Pentatomidae) and their natural enemies in peanuts. J. Entomol. Sci. 43: 191–207.
Google Scholar
29.
M. C. Vecchio
1993 Parasitoides de adultos de
Oebalus ypsilongriseus (DeGeer, 1773) (Heteroptera: Pentatomidae). An. Soc. Entomol. Brasil 22: 217–219.
Google Scholar