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First record of Heliothrips haemorrhoidalis (Thysanoptera: Thripidae) causing damage on greenhouse strawberries.

Characteristic silvery patches made by thrips (Thysanoptera) were observed on leaves of semi-hydroponic greenhouse strawberries (Fragaria x ananassa Duch.; Rosaceae) 'Camino Real' cultivar, in Curitiba, Parana, Brazil (25.428888[degrees]S; 49.267500[degrees]W), in Sep 2017. Forty-nine adult insects were collected and preserved in AGA solution (1:1:10 parts of glycerin, glacial acetic acid, and ethyl alcohol 60%, respectively). Specimens were slide-mounted (Mound & Kibby 1998) and identified as the greenhouse thrips, Heliothrips haemorrhoidalis (Bouche) (Thysanoptera: Thripidae), based on specialized taxonomic keys (Mound & Marulo 1998; Nakahara et al. 2015).

All specimens obtained were females (Fig. la), with strongly reticulated head sculpture (Fig. lb); 8-segmented antennae, antennal segments III-V and VII-VIII yellow, VI brown in apical half (Fig. 1c); pronotum poligonally reticulate, without long setae; metanotum with a bold and reticulate triangle, median setae short (Fig. 1d); tergites III-IV strongly reticulated, the median setae long and close to each other (Fig. le); wings hyaline, with round apex; and yellowish legs (Fig. 1f). The body color presented variation according to the life stage: recently emerged individuals had the head and thorax dark brown and the abdomen light brown (Fig. 2a), whereas in mature females the abdomen was dark brown, except by the paler segments IX and X (Fig. 2b). According to Bernardo et al. (2005), males are rare in this species, and reproduction is predominately by thelytokous parthenogenesis, where unfertilized eggs produce females (Fig. 2c).

Heliothrips haemorrhoidalis is native from South America, and it is known as highly polyphagous on the leaves of several unrelated plants. It has been reported on several crops, including coffee (Coffea arabica L; Rubiaceae), orange (Citrus aurantium L; Rutaceae), passionfruit (Passiflora caerulea Auct.; Passifloraceae) (Suris & Gonzalez 2008), lime (Citrus aurantiifolia (Christm.) Swingle; Rutaceae), rose (Rosa sp. L; Rosaceae), wild strawberry (Fragaria vesca L; Rosaceae) (Etienne et al. 2015), and avocado (Persea americana Mill.; Lauraceae) (Larral et al. 2018). A greenhouse bioassay was conducted to confirm the damage caused by H. haemorrhoidalis in strawberries. Damage characterization was performed with cage-confined individuals following the methodology described by Non-dillo et al. (2010). Each cage was set up with 1 leaf or 1 semi-ripe strawberry fruit, free from arthropod-induced damage, resulting in a total of 20 replicates for each plant part. Larvae (n = 10) and adults (n = 10) were placed in each cage using a fine paintbrush and kept confined for 72 h. A control was set up with an insect-free cage. Feeding damage was found on leaves and sepals. Thrips are piercing-sucking feeders, piercing the plant surface to feed on chlorophyll and other cell contents from plant tissue (Chhagan & Stevens 2007). As a consequence, silver-colored areas and black spots, due to deposition of excrement, appeared around feeding areas (Fig. 2c). Feces may act as a protective barrier against natural enemies (Denmark & Fasulo 2010) since, after oviposition, H. haemorrhoidalis were observed depositing excrement over the eggs.

Hyaliodocoris insignis (Stal) (Heteroptera: Miridae) and Orius insidiosus (Say) (Hemiptera: Anthocoridae) were observed preying on H. haemorrhoidalis adults and immatures, including larvae, prepupae, and pupae (Fig. 2a, b, f, g, and h). This is the first record of H. insignis preying H. haemorrhoidalis. So far, biological control studies have indicated approximately 10 natural enemies of the greenhouse thrips (CABI 2018). However, a parasitoid, Thripobius semiluteus Boucek (Hymenoptera: Eulophidae), has been considered the most efficient natural enemy for the control of H. haemorrhoidalis (McMurtry 1992; Bernardo et al. 2005; CABI 2018).

Vouchers specimens were deposited in the Padre Jesus Moure Museum, Federal University of Parana, Curitiba, Brazil: H. haemorrhoidalis (DZUP 519163), H. insignis (DZUP 490170), and O. insidiosus (DZUP 490169).

This is the first report of H. haemorrhoidalis causing damage on strawberry crops in the world. Observations of beneficial agents naturally controlling H. haemorrhoidalis populations may provide new perspectives for future biocontrol programs for managing this species.

We thank the Coordination for the Improvement of the Higher Level Personnel (CAPES), National Council for Scientific and Technological Development (CNPq), for the financial support; we are grateful to Paulo Fiuza Ferreira (Federal University of Vicosa) and the Germano Rosado Neto (Federal University of Parana) for identification of Hyaliodocoris insignis and Orius insidiosus, respectively. We also thank BioAgro for providing the seedlings used in experiment.

Summary

Heliothrips haemorrhoidalis (Bouche, 1833) (Thysanoptera: Thripidae), the greenhouse thrips, is reported here for the first time damaging strawberry leaves and sepals (Fragaria x ananassa Duch.; Rosaceae) in the world. Two natural enemies were observed preying on the species: Hyaliodocoris insignis (Stil, 1860) (Heteroptera: Miridae) and Orius insidiosus (Say, 1832) (Hemiptera: Anthocoridae).

Key Words: Fragaria x ananassa; greenhouse thrips; leaf damage; natural enemies

Sumario

Heliothrips haemorrhoidalis (Bouche, 1833) (Thysanoptera: Thripidae), o tripes-das-casas-de-vegetacao, e relatado pela primeira vez danificando folhas e sepalas de morangueiro (Fragaria x ananassa Duch.; Rosaceae) no mundo. Dois inimigos naturais foram observados predando a especie: Hyaliodocoris insignis (Stal, 1860) (Heteroptera: Miridae) e Orius insidiosus (Say, 1832) (Hemiptera: Anthocoridae).

Palavras Chave: Fragaria x ananassa; tripes-das-casas de-vegetacao; dano foliar; inimigos naturais

References Cited

Bernardo U, Viggiani G,Sasso R. 2005. Biological parameters of Thripobius semiluteus Boucek (Hym., Eulophidae), a larval endoparasitoid of Heliothrips haemorrhoidalis (Bouche) (Thysan., Thripidae). Journal of Applied Entomology 129: 250-257.

CABI (Centre for Agriculture and Biosciences International). 2018. Heliothrips haemorrhoidalis (black tea thrips). Wallingford, Oxfordshire, United Kingdom. https://www.cabi.org/isc/datasheet/26818 (last accessed 18 May 2019).

Chhagan A, Stevens PS. 2007. Effect of temperature on the development, longevity and oviposition of greenhouse thrips (Heliothrips haemorrhoidalis) on lemon fruit. New Zealand Plant Protection 60: 50-55.

Denmark HA, Fasulo TR. 2010. Greenhouse thrips, Heliothrips haemorrhoidalis (Bouche) Insecta: Thysanoptera: Thripidae). UF/IFAS Publication EENY-75. University of Florida, Gainesville, Florida, USA. https://entnemdept.ifas.ufl.edu/creatures/orn/thrips/greenhouse_thrips.htm (last accessed 18 May 2019).

Etienne J, Ryckewaert P, Michel B. 2015. Thrips (Insecta: Thysanoptera) of Guadeloupe and Martinique: updated check-list with new information on their ecology and natural enemies. Florida Entomologist 98: 298-304.

Larral P, Ripa R, Funderburk J, Lopez E. 2018. Population abundance, phenology, spatial distribution and a binominal sampling plan for Heliothrips haemorrhoidalis (Thysanoptera: Thripidae) in avocado. Florida Entomologist 101: 166-171.

McMurtry JA. 1992. The role of exotic natural enemies in the biological control of insect and mite pests of avocado in California, pp. 247-252, In Proceedings of the Second World Avocado Congress, 21-26 Apr 1991, Orange, California, USA.

Mound LA, Kibby G. 1998. Thysanoptera: An Identification Guide, 2nd edition. CAB International, Wallingford, Oxfordshire, United Kingdom.

Mound LA, Marullo R. 1998. Thysanoptera: An Identification Guide. 2nd edition. CAB International, Wallingford, Oxfordshire, United Kingdom.

Nakahara S, O'donnell CA, Mound LA. 2015. Heliothrips haemorrhoidalis and its relatives, with one new species and one new genus (Thysanoptera: Thripidae). Zootaxa 4021: 578-584.

Nondillo A, Redaelli LR, Pinent SMJ, Botton M. 2010. Caracterizacao das injurias causadas por Frankliniella occidentalis no morangueiro. Ciencia Rural 40: 820-826.

Suris M, Gonzalez C. 2008. Especies de trips asociadas a hospedantes de interes en las provincias habaneras: II. Plantas frutales. Revista de Proteccion Vegetal 23: 85-89.

Mireli Trombin de Souza (1,2,*), Michele Trombin de Souza (1,2), Launa Bianca Dybas Ivankio (1), Bruna Caroline Durau (1), Leticia Tamara Maleski (1), and Maria Aparecida Cassilha Zawadneak (1,2)

(1) Federal University of Parana, Department of Basic Pathology, Federal University of Parana, Caixa Postal 19031, 81531-980, Curitiba, Parana, Brazil; E-mail: mirelitrombin@gmail.com (M. T. S.); mictrombin@gmail.com (M. T. S); laudybas@gmail.com (L. B. D. I.); brudurau535@gmail.com (B. C. D.); Ieticial9.maleski@gmail.com (L. T. M.); mazawa@ufpr.br (M. A. C. Z.)

(2) Postgraduate Program in Agronomy, Department of Phytotechnology and Plant Health, Federal University of Parana, Curitiba, Parana, Brazil.

(*) Corresponding author; E-mail: mirelitrombin@gmail.com

Caption: Fig. 1. Morphological characteristics of Heliothrips haemorrhoidalis: (a) female, (b) head and pronotum reticulated, (c) antennae, (d) mesonotum, metanotum, and tergite I-II reticulated, (e) tergites III-VI, and (f) forewing and leg.

Caption: Fig. 2. Heliothrips haemorrhoidalis and its damage in strawberry plants: (a) teneral female, (b) mature female, (c) egg, (d) damage on leaves, (e) leaf chlorosis and fecal specks, (f) larva, (g) pre-pupa, and (h) pupa.

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Author:Souza, Mireli Trombin de; Souza, Michele Trombin de; Ivankio, Launa Bianca Dybas; Durau, Bruna Carol
Publication:Florida Entomologist
Geographic Code:3BRAZ
Date:Sep 1, 2019
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