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Plant Bugs Predators (Hemiptera: Heteroptera: Miridae) with References to Arthropods and Fungi in Brazil

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Plant Bugs Predators (Hemiptera: Heteroptera: Miridae) with References to Arthropods and Fungi in Brazil Anais da Academia Brasileira de Ciências (2019) 91(3): e20181194 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201920181194 www.scielo.br/aabc | www.fb.com/aabcjournal Plant Bugs Predators (Hemiptera: Heteroptera: Miridae) with References to Arthropods and Fungi in Brazil BÁRBARA C.F. NOGUEIRA1, PAULO S.F. FERREIRA1, LÍVIA A. COELHO2, DAVID S. MARTINS2 and BÁRBARA D. BARCELLOS1 1Universidade Federal de Viçosa, Departamento de Biologia Animal, Avenida Peter Henry Rolfs, s/n, 36570-000 Viçosa, MG, Brazil 2Universidade Federal de Viçosa, Departamento de Entomologia, Avenida Peter Henry Rolfs, s/n, 36570-000 Viçosa, MG, Brazil Manuscript received on November 12, 2018; accepted for publication on January 31, 2019 How to cite: NOGUEIRA BCF, FERREIRA PSF, COELHO LA, MARTINS DS AND BARCELLOS BD. 2019. Plant Bugs Predators (Hemiptera: Heteroptera: Miridae) with References to Arthropods and Fungi in Brazil. An Acad Bras Cienc 91: e20181194. DOI 10.1590/0001-3765201920181194. Abstract: The present study demonstrates 30 plant bugs species associated with 50 records of prey and six records of mycophagy for Brazil. The data were compiled from Schuh’s Catalog, the literature, specimens deposited in entomology museums and exemplars from different regions of Brazil sent for identification. Some of the data from the literature used did not presented complete information. This study aims to increase the knowledge of the relationships among plant bugs, prey and fungi and emphasize those species with potential for biological control strategies and pest integrated management. Key words: arthropod, fungi, insect, prey. INTRODUCTION glands (Wheeler 2001), which allow the prey immobilization (Cohen 1996). Plant bugs have a very great ecological importance Plant bugs are among the most important insect due to the high diversity and occurrence in many groups in agriculture because they can act either as zoogeographic regions (Cassis and Schuh 2012). They have a wide feeding behavior varying as plague for crops as well as biological control agents phytophagous, predators, saprophagous and (Henry and Wheeler 1988, Wheeler 2001). Their fungivorous (Henry and Wheeler 1988, Wheeler predation habit is not commonly recognized as they 2001). This happens because their mouthparts do not have the morphological structures used to allow the exploitation of a great variety of food capture prey. However, there are observations in source (Schuh and Slater 1995, Grimaldi and nature about plant bug predating eggs, immature Engel 2005, Gullan 2014), due to the presence of and adult forms of arthropods, and their life cycles digestive enzymes (Boyd et al. 2002) and other may synchronize with those of prey (Schuh and chemical substances released from the salivary Slater 1995, Wheeler 2000, 2001, Shockley and Murray 2006). In addition, records of plant bugs Correspondence to: Bárbara Cristina Félix Nogueira E-mail: [email protected] feeding on dead and disabled invertebrates have ORCid: https://orcid.org/0000-0002-8440-4525 been reported (Wheeler 2001). BIOLOGICAL SCIENCES An Acad Bras Cienc (2019) 91(3) BÁRBARA C.F. NOGUEIRA et al. POTENTIAL PLANT BUGS PREDATORS IN BRAZIL Given the ecological and economic importance regions of the planet (Bonsignore and Vacante of plant bugs, the aim of this study is to increase the 2010). D. fovealis was first recorded in Brazil knowledge about these arthropods in associations in 2010 causing serious damages in strawberry with prey and fungi in Brazil. Additionally, the (Zawadneak et al. 2016). Until now, there is no study intends to emphasize potential species for record of this plant bug attacking strawberry crops biological control. in Brazil. Nevertheless, further studies on the potential of this plant bug as a biological control MATERIALS AND METHODS agent regarding this pest are necessary. The plant bugs Engytatus modestus and All data came from On-line Systematic Catalog Engytatus varians have records of predation on of Plant Bugs (Schuh 2002-2013), Taxonomic Bemisia tabaci (Hemiptera: Aleyrodidae) (Gerling Catalog of the Brazilian Fauna (TCBF), specialized et al. 2001). This Aleyrodidae has a vast geographic literature, information from labels of specimens distribution and was considered pest in more than deposited in the Regional Museum of Entomology 500 agricultural crop species around the world of the Universidade Federal de Viçosa, Minas (Cock 1993). Gerais, Brazil (UFVB), and the National Museum E. modestus is a predator of Dysmicoccus of the Universidade Federal do Rio de Janeiro, brevipes (Hemiptera: Pseudococcidae) (Wheeler Rio de Janeiro, Brazil (MNRJ). Some of the data 2001), a pantropical pest of pineapple (Silva et al. from the literature used did not presented complete 1968, Scardini 1983, Mau and Kessing 1992). This information. The study also included data from plant bug is a potential agent of biological control many specimens from several regions of Brazil of Liriomyza trifolii (Diptera: Agromyzidae), sent for identification to UFVB. which is a serious pest of a great number of host The data were compiled in the Microsoft Excel plants, including ornamental species (Stegmaier software relating the plant bug species with prey 1966, Spencer 1973). and mycophagy, the associated plant where the The plant bug Campyloneuropsis cincticornis predator and prey were found, and the source of is a predator of Gratiana spadicea (Klug) literature. (Coleoptera: Chrysomelidae), a monophagous RESULTS AND DISCUSSION species that feeds on Solanum sisymbriifolium, an invasive plant of pasture and other important crops Up to date, there was no information grouped (Groth 1989, Mentz and Oliveira 2004). available about the potential occurrences of Some species of plant bugs in Brazil are predation by plant bugs in Brazil. In this study we recorded as family Ortheziidae (Hemiptera: found 30 species of plant bugs with potential prey Sternorrhyncha) predators (Table I): Ambracius and fungi associations were recorded for Brazil, dufouri (Ferreira 1998, Wheeler 2001), Ofellus in all 56 associations, 50 of which were records of guaranianus (Wheeler 2001) and Adhyalochloria prey, six records of mycophagy, of which 18 were inermis preying on Fuchsia regia (Museu Regional associated with plant material (Table I). de Entomologia da Universidade Federal de The plant bug Hyaliodocoris insignis was Viçosa). Species of the Ortheziidae, known as observed preying on Duponchelia fovealis scales, usually constitute serious pests associated (Lepidoptera: Crambidae) (Zawadneak et al. 2016). with plants of economic importance. They occur This Lepidoptera has many registers attacking in most parts of the world mainly in the Neotropics strawberry (Fragaria x ananassa) crops in many and Nearctic regions (Nascimento et al. 1993). An Acad Bras Cienc (2019) 91(3) e20181194 2 | 9 BÁRBARA C.F. NOGUEIRA et al. POTENTIAL PLANT BUGS PREDATORS IN BRAZIL TABLE I Plant bugs predators and mycophagous species in Brazil. Miridae Prey/mycophagy Associated Plant Reference Adhyalochloria inermis Fuchsia regia Hemiptera Ortheziidae Unpublished data (Carvalho, 1985) (Onagraceae) Ferreira (1998), Wheeler Ambracius dufouri Stal, 1860 Hemiptera Ortheziidae (2001) Campyloneuropsis cincticornis Gratiana spadicea (Coleoptera: Wheeler (2001) (Stal, 1860) Chrysomelidae) Campyloneuropsis infumatus Tuta absoluta (Lepidoptera: Solanum lycopersicum Martínez et al. (2014) (Carvalho, 1947) Gelechiidae) (eggs and larva) (Solanaceae) Tuta absoluta (Lepidoptera: Van Lenteren et al. Gelechiidae) (2016) Ceratocapsus dispersus Carvalho Heliothis virescens (Lepidoptera: Wheeler (2001) & Fontes, 1983 Noctuidae) Alabama argilacea (Lepidoptera: Gossypium L. Noctuidae) (eggs and larva) (Malvaceae) Ceratocapsus mariliensis Alabama argilacea (Lepidoptera: Gossypium L. Wheeler (2001) Carvalho & Fontes, 1983 Noctuidae) (eggs and larva) (Malvaceae) Heliothis virescens (Lepidoptera: Noctuidae) Cylapocoris pilosulus Knight, Auricularia Fungus Tree debris Carvalho (1954) 1930 Cylapocoris tiquiensis Carvalho, Auricularia Fungus Tree debris Carvalho (1954) 1954 Schuh (1976), Wheeler Cylapus citus Bergroth, 1922 Pirenomiceto Fungus (2001) Schuh (1976), Wheeler Cylapus ruficeps Bergroth, 1922 Pirenomiceto Fungus (2001) Engytatus modestus (Distant, Liriomyza trifolii (Diptera: Unpublished data 1893) Agromyzidae) Heliothentines (Lepidoptera: Wheeler (2001) Noctuidae). (larva and pulp) Pieris rapae (Lepidoptera: Pieridae) (larva and pulp) Dysmicoccus brevipes (Hemiptera: Ananas comosus Pseudococcidae) (Bromeliaceae) Tupiocoris notatus (Hemiptera: Nicotiana tabacum Miridae) (nimph and adult) (Solanaceae) An Acad Bras Cienc (2019) 91(3) e20181194 3 | 9 BÁRBARA C.F. NOGUEIRA et al. POTENTIAL PLANT BUGS PREDATORS IN BRAZIL TABLE I (continuation). Miridae Prey/mycophagy Associated Plant Reference Solanum lycopersicum Aphids (Solanaceae) Myzus persicae (Hemiptera: Aphidae) Bemisia tabaci (Hemiptera: Gerling et al. (2001) Aleyrodidae) Engytatus varians (Distant, Bemisia tabaci (Hemiptera: Wheeler (2001) 1884) Aleyrodidae) Heliothis virescens (Lepidoptera: Martínez et al. (2014) Noctuidae) (initial stages) Tuta absoluta (Lepidoptera: Gelechiidae) (eggs and larva) Tuta absoluta (Lepidoptera: Van Lenteren et al. Gelechiidae)*** (2016) Fulvius anthocoroides Stal, 1862 Hemiptera Aradidae Alayo (1974) Coleoptera Miriapoda Fungus Tree debris Schuh (1976) Fulvius quadristillatus (Stal, Maes and Carvalho Auricularia Fungus
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