First Record of Atherigona Reversura Villeneuve (Diptera: Muscidae)
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G Model RBE 91 1–5 ARTICLE IN PRESS Revista Brasileira de Entomologia xxx (2016) xxx–xxx 1 REVISTA BRASILEIRA DE 2 Entomologia A Journal on Insect Diversity and Evolution www.rbentomologia.com Short Communication 3 First record of Atherigona reversura Villeneuve (Diptera: Muscidae) 4 feeding on Bermudagrass (Cynodon dactylon cv. Jiggs, Poaceae) in 5 Brazil: morphological and molecular tools for identification a b a c 6 Q1 Leandro do P. Ribeiro , Alexandre C. Menezes Netto , Felipe Jochims , Kirstern Lica F. Haseyama , d,∗ 7 Claudio J.B. de Carvalho a 8 Q2 Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina, Centro de Pesquisa para Agricultura Familiar, Chapecó, SC, Brazil b 9 Empresa de Pesquisa Agropecuária e Extensão Rural de Santa Catarina, Estac¸ ão Experimental de Videira, Videira, SC, Brazil c 10 Departamento de Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil d 11 Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil 12 a a b s t r a c t 13 r t i c l e i n f o 14 15 Article history: Bermudagrass (Cynodon dactylon cv. Jiggs) is an important food source for dairy cattle in the semi- 16 Received 3 March 2016 intensive milk production systems most often used in southern Brazil. Although many insect pests are 17 Accepted 26 April 2016 associated with feed grasses, we report here the first occurrence of the fly Atherigona (Atherigona) rever- 18 Available online xxx sura Villeneuve, 1936 (Diptera: Muscidae) feeding on bermudagrass in Brazil. This potential pest was 19 Associate Editor: Gustavo Graciolli observed in April 2015 in three localities (Abelardo Luz, Palmitos, and Videira) in western Santa Cata- 20 rina, in southern Brazil. The infested plants had senescent and necrotic terminal leaves that reduced plant 21 Keywords: growth. New growth had to sprout new tillers from basal nodes, which resulted in a reduced plant growth 22 COI gene rate. We also provide a morphological identification key (with figures) for A. (Atherigona) reversura and A. 23 Insect pest 24 Pastures (Acritochaeta) orientalis Schiner, 1868. A molecular identification based on COI is also provided to better differentiate species. 25 Plant–insect interaction © 2016 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 26 Dairy farming has increased recently in Brazil due to changing 2010; Chiaradia et al., 2013), caterpillars (Lepidoptera: Noctuidae) 44 27 market demands (Muniz et al., 2013). Southern Brazil is among (Assunc¸ ão-Albuquerque et al., 2010), and grass bug (Hemiptera: 45 28 the most important milk producing regions and has the great- Miridae) (Chiaradia and Poletto, 2012) were problems for perennial 46 29 est increase in production (Síntese Anual da Agricultura de Santa grasses in southern Brazil. 47 30 Catarina 2012–2013, 2014). Although cattle diets are often sup- We report, for the first time in Brazil, herbivory and dam- 48 31 plemented (especially with corn silage and hay), most farmers age by Atherigona (Atherigona) reversura Villeneuve, 1936 (Insecta, 49 32 use pastures as the main source of feed. Thus, management of Diptera: Muscidae) on bermudagrass Cynodon dactylon cv. Jiggs. 50 33 cultivated pasture is important to ensure constant forage supply This is also the first record of the species in South America. 51 34 and to maintain high levels of productivity while keeping costs Atherigona (Atherigona) reversura larvae were found infesting 52 35 low. bermudagrass in April 2015 in three localities Abelardo Luz 53 ◦ ◦ ◦ ◦ 36 In tropical and subtropical regions, Cynodon grasses (bermuda- (26 39 22 S; 52 12 17 W), Palmitos (27 7 56 S; 53 6 9 W), and 54 −1 ◦ ◦ 37 grass) are very productive (over 20 t ha ), adaptable to regional Videira (27 1 23 S; 51 11 53 W) in the western region of the state 55 38 soil conditions, pest and disease tolerant, and therefore of great of Santa Catarina in southern Brazil. These larvae caused the death 56 39 forage potential (Oliveira et al., 2000; Rodrigues et al., 2006b). Dur- of apical leaves of infected tillers by feeding apically starting at 57 40 ing the last 20 years, bermudagrass became the most important the terminal node and which damages vascular tissue (Fig. 1). 58 41 pasture grass for milk production in southern Brazil, used in more Once larvae begin feeding, senescence and necrosis of the upper 59 42 than 80% of milk farms (Fernandes, 2012). To date, few insect pests, part of tillers occurs, mostly due to the death of the two newest 60 43 including spittlebugs (Hemiptera: Cercopidae) (Lohmann et al., leaves. Feeding this way causes a reduction in plant growth because 61 regrowth must begin through new tillers originating at basal nodes, 62 or the apical node prior to the damage. Thus, feeding by the fly lar- 63 ∗ vae causes a reduction in establishment into new areas as well as 64 Corresponding author. biomass production in areas already established. 65 E-mail: [email protected] (C.J.B. de Carvalho). http://dx.doi.org/10.1016/j.rbe.2016.04.001 0085-5626/© 2016 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Ribeiro, L.d.P., et al. First record of Atherigona reversura Villeneuve (Diptera: Muscidae) feeding on Bermudagrass (Cynodon dactylon cv. Jiggs, Poaceae) in Brazil: morphological and molecular tools for identification. Rev. Brasil. Entomol. (2016). http://dx.doi.org/10.1016/j.rbe.2016.04.001 G Model RBE 91 1–5 ARTICLE IN PRESS 2 L.d.P. Ribeiro et al. / Revista Brasileira de Entomologia xxx (2016) xxx–xxx Fig. 1. (A) Cynodon dactylon cv. Jiggs: showing plant damage. Atherigona (Atherigona) reversura: (B) larvae; (C) puparium; (D) adult. Scale bars = 1 mm. 66 Known elsewhere as the bermudagrass stem maggot (BSM), A. to Atherigona sequences available at GenBank (Table 1). Our objec- 92 67 (Atherigona) reversura was first discovered in the New World in tive in comparing the sequences was to use additional evidence 93 68 southern USA state of Georgia in July 2010 where it was infest- that the species we were dealing was not any other with known 94 69 ing bermudagrass hayfields, pastures and turf and is now found sequences. We also intended to verify if COI data was enough to 95 70 throughout the southeastern United States (Grzywacz et al., 2013). differentiate Atherigona (Atherigona) reversura from other species 96 71 Although the extent of damage varies among cultivars (Ikeda et al., of the genus, especially Atherigona (Acritochaeta) orientalis. We 97 72 1991), BSM causes an average decrease of ∼8% in total dry biomass highlight this analysis is not an inference of the phylogenetic rela- 98 73 of bermudagrass cultivars in the USA (Baxter et al., 2014). Thus, due tionships of the genus, which is very speciose. We also examined 99 74 to this potential problem, A. (Atherigona) reversura should be mon- the Atherigona (Acritochaeta) orientalis voucher that provided the 100 75 itored to assess its establishment and behavior as a potential pest sequence KP161673 to verify its identity. We amplified the COI gene 101 76 of pastures in Brazil. Additional study is also necessary to quan- using Folmer et al. (1994) primers (LCO-1490f and HCO-2198r), 102 77 tify damage by the fly larvae to bermudagrass quality and yield, to the region chosen by DNA Barcoding project as the standard bar- 103 78 develop integrated management. code for most animal groups. DNA was extracted using DNeasy 104 ◦ 79 In the laboratory, under controlled conditions (26 ± 2 C, RH: ± 80 70 10% and photoperiod: 14L:10D hours), larvae were reared and Table 1 List of Atherigona species used in this study with GenBank number. 81 the resulting adults were identified as A. (Atherigona) reversura 82 using the revision of Pont and Magpayo (1995). Adrian C. Pont Species GenBank number 83 (Oxford University Museum of Natural History – UMO) also con- Atherigona (Atherigona) nigritibiella Fan & Liu, 1982 EU627708 84 firmed the species identification by figures and photographs we Atherigona (Acritochaeta) orientalis Schiner, 1868 EU627707 85 sent to him. Voucher specimens were deposited at the Colec¸ ão Atherigona (Acritochaeta) orientalis Schiner, 1868 KP161673 86 Entomológica da Epagri/Cepaf, in Chapecó, and in the Colec¸ ão Ento- Atherigona (Atherigona) oryzae Malloch, 1925 KP161674 Atherigona (Atherigona) reversura Villeneuve, 1936 KT906365 87 mológica Pe. Jesus Santiago Moure, in the Department of Zoology Atherigona (Atherigona) seticauda Malloch, 1926 KJ510607 88 of the Universidade Federal do Paraná, Curitiba (DZUP). Atherigona (Atherigona) theodori Hennig, 1963 KJ510608 89 We also used molecular data to confirm identity and to provide Atherigona (Atherigona) varia (Meigen, 1826) KJ510609 90 another tool to aid in the identification of this pest. Thus, we Cyrtoneuropsis veniseta (Stein, 1904) KJ510614 Cyrtoneuropsis veniseta (Stein, 1904) KP161656 91 provide a partial COI sequence of A. (A.) reversura and compared it Please cite this article in press as: Ribeiro, L.d.P., et al. First record of Atherigona reversura Villeneuve (Diptera: Muscidae) feeding on Bermudagrass (Cynodon dactylon cv. Jiggs, Poaceae) in Brazil: morphological and molecular tools for identification. Rev. Brasil. Entomol. (2016). http://dx.doi.org/10.1016/j.rbe.2016.04.001 G Model RBE 91 1–5 ARTICLE IN PRESS L.d.P. Ribeiro et al. / Revista Brasileira de Entomologia xxx (2016) xxx–xxx 3 105 Blood & Tissue Kit (Qiagen, Valencia, United States) following the program MUSCLE (Edgar, 2004), in MEGA 6.05 (Tamura et al., 2013). 125 106 protocol provided by the manufacturer, with the following modi- GTR + I was the nucleotide substitution model used (chosen by 126 107 fications: the specimen was incubated in proteinase K and buffer JModel Test 2.1.4, Posada, 2008).