Introduction
Thrips are important agricultural pests due to the injury caused by larvae and adults on plants. Thrips reported on soybean Glycine max (L.) Merr. (Fabaceae) in various parts of the world include the following species: Caliothrips impurus (Priesner), Caliothrips phaseoli (Hood), Frankliniella fusca (Hinds), Frankliniella insularis (Franklin), Frankliniella occidentalis (Pergande), Frankliniella schultzei (Trybom), Frankliniella tritici (Fitch), Neohydatothrips sp., Scirtothrips dorsalis Hood, Sericothrips occipitales Hood, Sericothrips variabilis (Beach), Taeniothrips sjostedti (Trybom), Thrips palmi Karny and Thrips tabaci Lindeman (Irwin et al., Reference Irwin, Yeargan and Marston1979; Kogan and Turnipseed, Reference Kogan and Turnipseed1987; Higley and Boethel, Reference Higley and Boethel1994; Cabrera et al., Reference Cabrera, Estévez, Vélez, Morales, Viteri and Lugo2006). There are no specific reports of yield losses caused by mechanical injury by thrips on soybean leaves and flowers. However, previous research showed that populations of 16 Echinothrips americanus Morgan thrips per trifolia cause leaf bronzing and chlorosis in soybean seedlings (Viteri et al., Reference Viteri, Cabrera and Estévez2009). Moreover, some thrips species are able to transmit tospovirus (Almeida and Corso, Reference Almeida and Corso1991; Gent et al., Reference Gent, Schwartz and Khosla2004). Bud blight, caused by tobacco ringspot virus (TRSV) transmitted by T. tabaci Lindeman, is reported to affect soybean seed quality in the United States (Kogan and Herzog, Reference Kogan and Herzog1980). Another tospovirus reported in commercial soybean areas in Brazil and the United States is tobacco streak virus (TSV) transmitted by F. schultzei Trybom, F. occidentalis Pergande and T. tabaci Lindeman (Almeida and Corso, Reference Almeida and Corso1991). In Puerto Rico, the potential damage caused by thrips is unknown. However, it is important to identify the thrips species that could affect soybean production and evaluate their damage levels. The objective of this study was to identify thrips species associated with soybean and their abundance in three different ecological zones in Puerto Rico.
Materials and methods
Experimental plots
Sentinel plots were planted in Adjuntas, Isabela and Juana Diaz experimental stations at the University of Puerto Rico. Adjuntas is located 594.4 m above sea level (masl) in the southwest area of the island, latitude N 18°, 10′, 0.474″, and longitude W 066°, 47′, 0.961″. Air temperatures varies from 18 to 24 °C, and the annual precipitation (a.p.) is ~2400 cm. Isabela is located at 128 masl, in the northwest of Puerto Rico, latitude N 18°, 27′, 0.732″ and longitude W 067°, 03′, 0.355″. Air temperature ranges from 22 to 28 °C, and the a.p. is ~2000 mm. Juana Diaz is located 23 masl in the southeast of Puerto Rico, latitude N 18°, 01′, 0.811″ and longitude W 066°, 31′, 0.713″. The temperature ranges between 21 and 30 °C, and the precipitation is ~1100 mm annually. Experimental plots were set in a randomized complete block design replicated four times. Soybean line 2053A was sown on the following dates: 1 February 2007, 22 June 2007, 22 January 2007, 4 April 2007, 11 July 2007, and 18 September 2007. Plots were 31 m × 13 m in Isabela and 22 m × 13 m in Adjuntas and Juana Diaz with a density of approximately 90,000 soybean plants/ha.
Scouting and identification
Thrips were collected from soybean line 2053A in two consecutive plantings in each location during 2007. Thrips species were collected in ten randomly selected plants per plot (ten trifoliates) in bottles containing ethyl alcohol (70%) during V2–R5 growth stages. In the flowering periods (R1–R3), ten blossoms from ten different plants were also inspected. A total of seven evaluations were made for each planting every week. For instance, in Adjuntas, thrips were collected from 17 February 2007 to 30 March 2007 (weeks 1–7) and from 22 June 2007 to 1 August 2007 (weeks 8–14). Flowering occurred during weeks 4–6 and 10–12, respectively. In the case of Isabela, thrips were collected from 6 February 2007 to 20 March 2007 (weeks 1–7) and from 23 July 2007 to 7 September 2007 (weeks 8–14). Flowering occurred during weeks 3–5 and 9–11. In Juana Diaz, thrips were collected from 23 July 2007 to 7 September 2007 (weeks 1–7) and from 4 October 2007 to 14 November 2007 (weeks 8–14). Flowering occurred during weeks 3–5 and 10–12. The insects were cleared using aqueous potassium hydroxide (5%) for 30 s and were mounted on slides with Canada balsam. Slides were dried at 30 °C for 24 h. For the identification of thrips, a taxonomic key for Thysanoptera on DVD was used, and the sex was noted (Mound and Marullo, Reference Mound and Marullo1996; Moritz et al., Reference Moritz, Mound and Goldarazena2004).
Results
A total of nine genera were found, of which eight species were identified in the three locations. These included Frankliniella cephalica (Crawford), F. schultzei (Trybom), Frankliniella gossypiana Hood, F. insularis (Franklin), Caliothrips phaseoli Hood, Neohydatothrips inversus (Hood), Rhamphothrips sp., Scirtothrips dorsalis Hood and T. palmi Karny. The taxonomic characteristics of C. phaseoli and F. gossypiana have been reported previously because they are a new record for Puerto Rico (Viteri et al., Reference Viteri, Cabrera and Estévez2009).
Frankliniella cefalica
Adults were yellow with eight antennal segments; pedicel antennal segment III with a distinctive collar and convex shape; ocellar setae III arising outside the ocellar triangle; pronotum with anteroangular setae longer than anteromarginal setae; campaniform sensilla absent; tergite VIII with a complete comb of microtrichia.
Frankliniella insularis
Adults were dark brown with eight antennal segments; head longer than wider with ocellar setae III located ahead the ocellar triangle; postocular setae I present; pronotum with anteromarginal setae that were smaller than posteromarginal setae; metanotum with two pairs of media setae in the anterior margin; campaniform sensilla present; tergite VIII with posteromarginal comb of microtrichia moderately long with triangular bases.
Frankliniella schultzei
Adults were brown, although some specimens were yellow with eight antennal segments; ocellar setae III located between the posterior hind ocella; postocular seta I present; pronotum with posteroangular setae that were slightly longer than posteromarginal setae; campaniform sensilla absent; tergite VIII with posteromarginal comb of microtrichia weakly developed.
Neohydatothrips inversus
Adults were yellow with seven antennal segments; antennal segments III and IV with an apical neck developed; ocellar setae III arising outside the ocellar triangle; pronotal blotch outlined by three pairs of spots; forewing with shading where the first vein is complete and the second vein without setae; medial and lateral setae on the metanotum arising in the anterior margin; tergites II–VI with median marginal combs; sternites VI and VII on males with an oval glandular.
Rhamphothrips sp.
Adults were yellow with seven antennal segments; three pairs of visible ocellar setae; mouth cone prolonged to the thorax; pronotum of equal proportion in length and width; forewing first and second veins incomplete; sternites and tergites with craspedum; a pair of jointed setae located in the middle part of sternite VIII.
Scirtothrips dorsalis
Adults were yellow with seven antennal segments; ocellar setae III arising on the middle part of posterior ocella; pronotum with four pairs of posteromarginal setae; a pair of setae located in the middle part of mesonoto; metanoto with medial setae arising behind the anterior margin; campaniform sensilla absent; forewing first vein with three discal setae located in the middle part of the forewing; second vein with two pairs of setae separately; tergites and sternites with dark brown areas; tergites II and VIII covered with rows of fine microtrichia; tergite VIII with posteromarginal comb of microtrichia complete and long.
Thrips palmi
Adults were light yellow with seven antennal segments; ocellar setae III arising outside the ocellar triangle; pronotum with a pair of longer posteroangular setae; forewing first vein incomplete with two or three setae located between the middle and end of the wing; forewing second vein complete with 15 setae; tergite VIII with posteromarginal comb of microtrichia complete and long; discal setae on sternite VIII absent.
Discussion
Previously, several thrips species on soybeans were identified and reported (Irwin et al., Reference Irwin, Yeargan and Marston1979; Kogan and Turnipseed, Reference Kogan and Turnipseed1987; Higley and Boethel, Reference Higley and Boethel1994; Cabrera et al., Reference Cabrera, Estévez, Vélez, Morales, Viteri and Lugo2006). However, F. cephalica and Rhamphothrips sp. are being reported for the first time on soybean in Puerto Rico. The cucurbitaceous thrip T. palmi was the common species in the three locations surveyed, although F. schultzei was the most abundant species in Juana Diaz. Both these species can transmit tospovirus. Frankliniella schultzei can transmit TSV and TRSV to soybean (Almeida and Corso, Reference Almeida and Corso1991; Mound, Reference Mound, Marullo and Mound2002). In our survey, symptoms related to tospovirus were not observed on the experimental plots. None of the Thysanoptera caused any discernible injury on leaves or flower tissue reported previously in soybean seedlings. This can be attributed to the low populations observed (Viteri et al., Reference Viteri, Cabrera and Estévez2009). In Adjuntas, the most abundant species on leaves were N. inversus and T. palmi. Specimens of Neohydatothrips sp. were reported on soybean in Brazil; however, no damage was observed on the crop. The distribution of this genus in the Caribbean includes Puerto Rico, Dominica and Trinidad in various hosts (Mound and Marullo, Reference Mound and Marullo1996; Monteiro, Reference Monteiro2001; Medina, Reference Medina2003). Thrips palmi is distributed around the world and shows a preference for cucurbitaceous crops (Mound and Marullo, Reference Mound and Marullo1996). On the other hand, F. cephalica, which was found in flowers, has been reported to occur in the Caribbean region, Florida (USA), México, Bermuda and Colombia (Sakimura, Reference Sakimura1986). The hosts include mango, cotton, pigeon peas and peas (Matorell, Reference Matorell1976; Medina, Reference Medina2003). Frankliniella schultzei is reported as a principal vector of TSV on soybean in Brazil (Almeida and Corso, Reference Almeida and Corso1991). In Puerto Rico, some hosts include tomatoes, onions and chrysanthemum (Matorell, Reference Matorell1976). Two females of a Rhamphothrips sp. were observed on soybean leaves and flowers. This genus is particularly common in the Oriental hemisphere, where it makes up one of around ten small species (Mound and Marullo, Reference Mound and Marullo1996). For example, Rhamphothrips pradens Sakimura is reported in Dominican Republic on different hosts. Our specimens, unlike that of R. pradens, showed a pair of medium setae separately on sternite VII. It would be important to identify this species to elucidate its biology, behaviour and principal hosts.
In Isabela, T. palmi was the most abundant species on leaves and flowers. On leaves, a female of S. dorsalis was identified. This specimen is reported as an important pest of chilli in India and of strawberry in Austria (Moritz et al., Reference Moritz, Mound and Goldarazena2004). The damage to soybean is unknown, and more studies are required to determine their potential effect on soybeans.
In Juana Diaz, T. palmi and F. schultzei were the most abundant species on leaves and flowers. In the case of F. schultzei, male specimens were collected in higher proportion on leaves and flowers compared with the other areas, and this may be related to the drier conditions of Juana Diaz (Lewis, Reference Lewis1973). Moreover, the availability of alternate hosts (tomatoes and onions) in Juana Diaz would account for the higher population of F. schultzei compared with Isabela and Adjuntas, where no vegetables are produced. On leaves, a female C. phaseoli was collected, which was reported previously on soybean in Valle de Yaqui (México) and Puerto Rico (Irwin et al., Reference Irwin, Yeargan and Marston1979; Viteri et al., Reference Viteri, Cabrera and Estévez2009). On flowers, a female of F. insularis was collected. The hosts of this species include soybean, crotalaria, pumpkins and broccoli (Matorell, Reference Matorell1976; Cabrera et al., Reference Cabrera, Estévez, Vélez, Morales, Viteri and Lugo2006). Frankliniella gossypiana was observed on leaves and flowers. Since Isabela and Juana Diaz are the major areas of soybean production in Puerto Rico, as expected, high numbers of Terebrantia suborder were observed in these locations, with 66 and 76 specimens, respectively, compared with 21 specimens collected in Adjuntas. T. palmi and F. schultzei are the most common species identified in the soybean production areas during the year. Our data that were obtained from the sentinel plots showed that T. palmi was the most common species in the northwest area (Isabela), and that F. schultzei was the most abundant species in the southeast area (Juana Diaz). However, in commercial soybean production areas in the southeast (Santa Isabel), T. palmi populations were higher than F. schultzei populations. This could be related to the extensive production of cucurbitaceous crops in this area, which increases T. palmi populations (Mound and Marullo, Reference Mound and Marullo1996). Moreover, Juana Diaz is drier with 1150 mm of a.p. than Isabela (2050 mm a.p.) and Adjuntas (2540 mm a.p.), which also favours the development of thrips species (Lewis, Reference Lewis1973).
In summary, our findings stress the need for identification, seasonal distribution surveys and constant monitoring of thrips populations to ensure that appropriate interventions are put in place in Puerto Rico to prevent any direct or indirect damage on soybean.
Acknowledgements
Funding for this project was provided by TSTAR – CSREES Award #2005-34 135-16 283 and USDA Subaward #UF-IFAS 00064385. The authors acknowledge the assistance of Dr Gail Wisler ARS-USDA.
