Philippine Journal of Science RESEARCH NOTE 150 (3): 855-859, June 2021 ISSN 0031 - 7683 Date Received: 28 Sep 2020

Thrips (Insecta: Thysanoptera) Species Infesting Garlic (Batanes Red) in Selected Farms in Batanes,

Cecilia P. Reyes* and Maria Katherine Copuyoc

College of Agriculture, State University 3500 Philippines

The study aimed to determine the species of thrips infesting garlic (Batanes Red) in the Department of Agriculture–Batanes Experiment Station (DA-BES) in Ihubok 1, Basco; DA-BES Dibtung, Radiwan, Ivana; and in the Calderon Farm in Radiwan, Ivana, Batanes. Sampling was done in February 2020. A total of 950 adult female thrips were collected from all study sites. The majority of the thrips were collected from DA-BES Farm in Ihubok 1, Basco with 89.89%, followed by the Calderon Farm in Ridawan, Ivana with 5.16%, and DA-BES Farm in Dibtung, Ridawan, Ivana with 4.95%. Thrips were represented by two terebrantian species, namely: Thrips tabaci Lindeman (Thripidae) with 97.37%, Anaphothrips sudanensis Trybom (Thripidae) with 2.32%, and a tubuliferan species Haplothrips gowdeyi (Franklin) (Phlaeothripidae) with 0.31%. T. tabaci was the dominant species in all study sites. A. sudanensis was found in all the study sites but in low number, while H. gowdeyi was present in two DA-BES study sites but absent in the Calderon Farm. This is the first report of A. sudanensis and H. gowdeyi infesting garlic in the Philippines.

Keywords: Anaphothrips sudanensis, Haplothrips gowdeyi, Thrips tabaci

Batanes is located on the northernmost part of the is an introduced variety. Since garlic (Batanes Red) is a Philippines under Region 02 or the , and the promising variety, the DA-BES is eyeing Batanes as one of province is a producer of organic garlic and sweet potato the main sources of planting materials for garlic in line with (Gallibu 2020). The agricultural areas in Batanes are mainly the government's goal to make garlic production sustainable coastal and upland areas, which are utilized for raising in the Philippines; concurrently, the management planned livestock and for growing vegetables and field crops. All to expand the current area of production for garlic (Batanes agricultural lands in Batanes are rainfed, and farmers plant Red) to 500 ha (DA 2018). three garlic (Allium sativum L.) varieties, namely: “Batanes Red,” “Batanes White,” and “ White” (DA 2012). There are over 6,000 species of thrips (Insecta: Thysanoptera) The cropping pattern in Batanes is root crop-garlic-fallow known worldwide (Buckman et al. 2012). Thrips are and crops were grown organically for consumption, and the small insects that feed on leaves, flowers, and fruits of rest of the products are sold in organic food stores in Metro plants using their piercing and sucking mouthparts. Their (de Leon 2014). Garlic (Batanes Red) has bigger body size ranges from 0.5–15 mm with the color varying cloves compared to garlic (Batanes White), but its country from pale yellow, light brown to dark brown, black, or of origin is unknown to local people and they believe it bicolored, and they reproduce asexually or sexually. They cause damage directly through feeding and oviposition on leaves, buds, flowers, and fruits or indirectly through the *Corresponding Author: [email protected] transmission of microbial pathogens (Buckman et al. 2012;

855 Philippine Journal of Science Reyes and Copuyoc: Thrips (Insecta: Thysanoptera) Vol. 150 No. 3, June 2021 Species Infesting Garlic (Batanes Red)

Garcia-Rodriguez et al. 2014). Thrips tabaci Lindeman appropriate control method. The study aimed to identify the – commonly known as onion thrips – is a pest of garlic, species of thrips infesting garlic (Batanes Red) in DA-BES onion, and tobacco in the Philippines (Reyes 1994) and, Ihubok 1, Basco; DA-BES Dibtung, Ridawan, Ivana; and recently, onion thrips tested positive for Garlic Common in the Calderon Farm in Ridawan, Ivana. Latent Virus in Mexico (Garcia-Rodriguez et al. 2014). T. tabaci is also known as the vector of Iris yellow spot virus The study is a part of a two-year project with the goal of of onion and garlic; Garlic common latent virus; Tomato developing a control strategy for garlic thrips. spotted wilt virus of onion, garlic, tomato, potato, and The study was conducted in Ihubok 1, Basco (20.439158°N; other crops; and Tomato yellow fruit ring virus of tomato 121.965264°E) and Dibtung, Radiwan, Ivana (20.351403°N; in many countries (Riley et al. 2011). In addition, T. tabaci 121.930068°E) Farms of the DA-BES; and in the Calderon infestation has been associated with the development Farm in Radiwan, Ivana (20.354352°N; 121.921810°E) of purple blotch disease of onion caused by Alternaria (Figures 1 and 2). The altitude of study sites is approximately porri and Stemphylium vesicarium (McKenzie et al. 1993; 25–57 m above the mean sea level (Google Earth 2020). Leach et al. 2019). Onion thrips is also the vector of Pantoea agglomerans, the causal agent of onion bacterial leaf blight, Thrips were collected from 30 randomly selected garlic and Pantoea ananatis, the causal agent of bacterial center plants of various ages within 300 m2 area of about 500 m2 rot of bulb onion (Grode 2017). In the USA (New York), garlic field in the three study sites through a method that 1–3 thrips larvae per onion leaf require control to prevent involves shaking/tapping on a plastic tray (Aliakbarpour significant yield loss (Nault and Shelton 2010), and accurate and Rawi 2010). Sampling was done from 09:00 AM to identification of thrips is essential in selecting the most 11:00 AM on 12–13 Feb 2020. Specimens were placed

Figure 1. Map of the Philippines showing the three study sites in the of Batanes, Philippines.

Figure 2. Garlic (Batanes Red) fields in Batanes, Philippines. a) DA-BES Farm, Ihubok 1, Basco; b) DA-BES Farm, Dibtung, Ridawan, Ivana; and c) Calderon Farm in Ridawan, Ivana, Batanes, Philippines.

856 Philippine Journal of Science Reyes and Copuyoc: Thrips (Insecta: Thysanoptera) Vol. 150 No. 3, June 2021 Species Infesting Garlic (Batanes Red) into 5-mL plastic vials containing 70% ethanol and sudanensis Trybom (Thripidae) with 2.32%, and a brought to the laboratory in Cagayan State University tubuliferan species Haplothrips gowdeyi (Franklin) for identification. (Phlaeothripidae) with 0.31% (Figure 3). T. tabaci was the dominant species in all study sites. A. sudanensis Thrips specimens were prepared for microscopic study was found in all the study sites but in low number, while using the techniques of Reyes (1994) and examined H. gowdeyi was present in two DA-BES study sites but under a light compound microscope. The book entitled absent in the Calderon Farm. “Thysanoptera (Hexopoda) of the Philippine Islands” (Reyes 1994) and the online resource Lucid Key Server- This study has proved that Thrips tabaci Lindeman is also Lucid Central (Hoddle et al. 2019) were used as references a major pest of garlic (Batanes Red). T. tabaci is a known for species identification. pest of garlic (Ilocos White) (Reyes 1994), a variety of garlic planted for commercial production in the Philippines A total of 950 adult female thrips were collected from (PSA 2014, 2019). T. tabaci is a highly polyphagous species all study sites (Table 1). The majority of the thrips were of thrips and it attacks at least 25 plant families worldwide collected from DA-BES Farm in Ihubok 1, Basco with (Mound 2007). On the other hand, A. sudanensis is a 89.89%, followed by the Calderon Farm in Ridawan, pest of sugarcane, rice, corn, and various grasses while Ivana with 5.16%, and DA-BES Farm in Dibtung, H. gowdeyi is associated with numerous plants in the Ridawan, Ivana with 4.95%. Thrips were represented Philippines – including “Carabao” mango (Reyes et al. by two terebrantian species, namely: Thrips tabaci 2020). This is the first report of A. sudanensis and H. Lindeman (Thripidae) with 97.37%, Anaphothrips

Table 1. Species of thrips and number of individuals on garlic (Batanes Red) in DA-BES Farm in Ihubok 1, Basco, DA-BES Farm in Dibtung, Ridawan, Ivana, and the Calderon Farm in Ridawan, Ivana, Batanes, Philippines. Species of Thrips Study sites Total number Thrips tabaci Anaphothrips Haplothrips gowdeyi of Thrips per Lindeman sudanensis Trybom (Franklin) site (%) Number of Number of Number of Location Coordinates % % % individuals individuals individuals • DA-BES Farm 20.439158°N; 854 (89.89%) 840 98.36 13 1.52 1 0.12 Ihubok I, Basco 121.965264°E • DA-BES Farm 20.351403°N; 47 42 89.36 3 6.38 2 4.26 Dibtung 121.930068°E (4.95%) Radiwan, Ivana • Calderon Farm, 20.354352°N; 49 43 87.76 6 12.24 0 0.00 Radiwan, Ivana 121.921810°E (5.16%) Total 950 925 97.37 22 2.32 3 0.31

Figure 3. Photomicrographs of thrips infesting garlic (Batanes Red) in Batanes, Philippines. a) Thrips tabaci Lindeman (45x), b) Anaphothrips sudanensis Trybom (45x), and c) Haplothrips gowdeyi (Franklin) (45x).

857 Philippine Journal of Science Reyes and Copuyoc: Thrips (Insecta: Thysanoptera) Vol. 150 No. 3, June 2021 Species Infesting Garlic (Batanes Red) gowdeyi infesting garlic in the Philippines. Since the DA- GALLIBU MA. 2020. How agriculture in Batanes thrives BES has a plan to expand the current area of production amid Covid19. Retrieved on 25 Sep 2020 from http:// for garlic (Batanes Red), molecular detection of microbial rfo02.da.gov.ph/2020/09/25/how-agriculture-in-batanes- pathogens associated with T. tabaci, as well as capacity thrives-amid-covid19/ building training on thrips management for farmers and GARCIA-RODRIGUEZ OG, PEREZ-MORENO other stakeholders, are recommended. L, NAVARRO-LEO MI, SALAS-ARAIZA MD, There were three species of thrips infesting garlic (Batanes MARTINEZ-JAIME OA, LEON-GALVAN MF, Red), namely: Thrips tabaci Lindeman, Anaphothrips NUNEZ-PALENIUS HG. 2014. Plant viruses in garlic- sudanensis Trybom, and Haplothrips gowdeyi (Franklin). associated insects. Rev Chap Ser Horti 20(2): 147156. T. tabaci was the dominant species of thrips in all study GOOGLE EARTH 7.3.3.7699. 2020. Ihubok 1, Basco, sites. Majority of the thrips were collected from DA- Batanes 20.439158°N; 121.965264°E elevation 25M; BES Farm in Ihubok 1, Basco, followed by the Calderon Radiwan, Ivana, Batanes 20.351403°N; 121.930068°E Farm in Ridawan, Ivana, and DA-BES Farm in Dibtung, elevation 52M; Dibtung, Radiwan, Ivana, Batanes Ridawan, Ivana. This is the first report of A. sudanensis 20.354352°N; 121.921810°E elevation 57M. 3D map, and H. gowdeyi infesting garlic in the Philippines. Buildings data layer, viewed on 03 July 2020. GRODE AS. 2017. The relationship between onion thrips (Thrips tabaci) and the bacterial pathogens (Pantoea ACKNOWLEDGMENTS agglomerans and Pantoea annanatis) [MS thesis]. Michigan State University, East Lansing, MI. 70p. The assistance of the management and staff of the DA- (ProQuest Dissertations Publishing) BES, Office of the Batanes Provincial Agriculturist, and Cagayan State University is acknowledged with HODDLE MS, MOUND LA, PARIS D. 2019. Thrips much appreciation. The kind assistance of Dr. Freddie of California 2019. Retrieved on 22 Apr 2020 from B. Corsino, Dr. Cesar V. Hostallero, and Mr. Celso https://keyserver.lucidcentral.org/key-server/search.jsp B. Batallones during the conduct of the study is LEACH A, HAY F, HARDING R, DAMANN KC, acknowledged. The project was funded by DA–Bureau NAULT B. 2019. Relationship between onion thrips of Agricultural Research. (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf blight in onion. Ann Appl Biol 176(1): 55–64. DOI: 10.1111/aa b.12558 REFERENCES MCKENZIE CL, CARTWRIGHT B, MILLER ME, EDELSON JV. 1993. Injury to onions by Thrips tabaci ALIAKBARPOUR H, RAWI CSMD. 2010. Diurnal Lindeman (Thysanoptera: Thripidae) and its role in activity of four species of thrips (Thysanoptera: the development of purple blotch. Environ Entomol Thripidae) and efficiencies of three nondestructive 22: 1266–1277. sampling techniques for thrips in mango inflorescenses. J Econ Entom 103(3): 631–640. MOUND LA. 2007. Onion thrips (Thrips tabaci). Retrieved on 18 Aug 2020 from http:www.padil.gov.au BUCKMAN RS, MOUND LA, WHITING MF. 2012. Phylogeny of thrips (Insecta: Thysanoptera) based on NAULT BA, SHELTON AM. 2010. Impact of five molecular loci. Wiley Online Library. Retrieved insecticide efficacy on developing action thresholds on 08 May 2020 from https://doi.org/10.1111/j.1365- for pest management: a case study of onion thrips 3113.2012.00650.x (Thysanoptera: Thripidae) on onion. J Econ Entomol 103: 1315−1326. [DA] Department of Agriculture. 2012. Garlic Production Guide. Regional Field Office 02, Tuguegarao City. 14p. [PSA] Philippine Statistics Authority. 2014. 2013 Cost and returns of garlic production. City, Philippines. [DA] Department of Agriculture. 2018. DA seeks to 68p. expand production of Batanes red garlic. Retrieved on 25 Sep 2020 from https://www.da.gov.ph/da-seeks-to- [PSA] Philippine Statistics Authority. 2019. Crop expand-production-of-batanes-red-garlic/ statistics of the Philippines (2014−2018). , Philippines. 92p. DE LEON DRA. 2014. Batanes regains crop productivity and profit with CPAR. Philstar. 09 Feb 2014. Retrieved REYES CP. 1994. Thysanoptera (Hexapoda) of the on 17 Jun 2020 from https://www.bar.gov.ph/index. Philippine islands. Raffles Bull Zoo 42(2): 107−507. php/news-and-events/5158-2014-01-batanes-cpar

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REYES CP, CAYABYAB BF, COPUYOC MKM. returns of garlic production. Quezon City, Philippines. 2020. Abundance and Diversity of Thrips (Insecta: 68p. Thysanoptera) in Conventional “Carabao” Mango [PSA] Philippine Statistics Authority. 2019. Crop Orchard in Piat, Cagayan, Philippines. Philipp J Sci statistics of the Philippines (2014−2018). Quezon City, 149(4): 1019–1028. Philippines. 92p. RILEY DG, JOSEPH SV, SRINIVASAN R, DIFFIE S. REYES CP. 1994. Thysanoptera (Hexapoda) of the 2011. Thrips vectors of tospoviruses. J Integ Pest Mgt Philippine islands. Raffles Bull Zoo 42(2): 107−507. 1(2): 1−10. REYES CP, CAYABYAB BF, COPUYOC MKM. GALLIBU MA. 2020. How agriculture in Batanes thrives 2020. Abundance and Diversity of Thrips (Insecta: amid Covid19. Retrieved on 25 Sep 2020 from http:// Thysanoptera) in Conventional “Carabao” Mango rfo02.da.gov.ph/2020/09/25/how-agriculture-in-batanes- Orchard in Piat, Cagayan, Philippines. Philipp J Sci thrives-amid-covid19/ 149(4): 1019–1028. GARCIA-RODRIGUEZ OG, PEREZ-MORENO RILEY DG, JOSEPH SV, SRINIVASAN R, DIFFIE S. L, NAVARRO-LEO MI, SALAS-ARAIZA MD, 2011. Thrips vectors of tospoviruses. J Integ Pest Mgt MARTINEZ-JAIME OA, LEON-GALVAN MF, 1(2): 1−10. NUNEZ-PALENIUS HG. 2014. Plant viruses in garlic- associated insects. Rev Chap Ser Horti 20(2): 147156. GOOGLE EARTH 7.3.3.7699. 2020. Ihubok 1, Basco, Batanes 20.439158°N; 121.965264°E elevation 25M; Radiwan, Ivana, Batanes 20.351403°N; 121.930068°E elevation 52M; Dibtung, Radiwan, Ivana, Batanes 20.354352°N; 121.921810°E elevation 57M. 3D map, Buildings data layer, viewed on 03 July 2020. GRODE AS. 2017. The relationship between onion thrips (Thrips tabaci) and the bacterial pathogens (Pantoea agglomerans and Pantoea annanatis) [MS thesis]. Michigan State University, East Lansing, MI. 70p. (ProQuest Dissertations Publishing) HODDLE MS, MOUND LA, PARIS D. 2019. Thrips of California 2019. Retrieved on 22 Apr 2020 from https://keyserver.lucidcentral.org/key-server/search.jsp LEACH A, HAY F, HARDING R, DAMANN KC, NAULT B. 2019. Relationship between onion thrips (Thrips tabaci) and Stemphylium vesicarium in the development of Stemphylium leaf blight in onion. Ann Appl Biol 176(1): 55–64. DOI: 10.1111/aa b.12558 MCKENZIE CL, CARTWRIGHT B, MILLER ME, EDELSON JV. 1993. Injury to onions by Thrips tabaci Lindeman (Thysanoptera: Thripidae) and its role in the development of purple blotch. Environ Entomol 22: 1266–1277. MOUND LA. 2007. Onion thrips (Thrips tabaci). Retrieved on 18 Aug 2020 from http:www.padil.gov.au NAULT BA, SHELTON AM. 2010. Impact of insecticide efficacy on developing action thresholds for pest management: a case study of onion thrips (Thysanoptera: Thripidae) on onion. J Econ Entomol 103: 1315−1326. [PSA] Philippine Statistics Authority. 2014. 2013 Cost and

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