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966 Florida Entomologist 95(4) December 2012

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BIOLOGICAL AND ECOLOGICAL CONSEQUENCES OF DIOLCOGASTER SP. (HYMENOPTERA: BRACONIDAE) PARASITIZING AGARAEA MINUTA

(LEPIDOPTERA: ARCTIIDAE) AND THE EFFECTS ON TWO COSTUS (COSTACEAE) PLANT SPECIES IN BRAZIL

Wagner De Souza TavareS1, geralDo SalgaDo-neTo2, JeSuSa CriSoSTomo legaSpi3, FranCiSCo De SouSa ramalho4, JoSé eDuarDo Serrão5 anD JoSé Cola zanunCio5,*

1Departamento de Fitotecnia, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais State, Brazil2Pós-graduação em Agronomia, Universidade Federal de Santa Maria, 97105-900, Santa Maria,

Rio Grande do Sul State, Brazil

3United States Department of Agriculture - Agricultural Research Service, CMAVE/Florida A&M University - Center for Biological Control, 6383 Mahan Drive, Tallahassee, Florida 32308 USA

4Empresa Brasileira de Pesquisa Agropecuária, Centro Nacional de Pesquisa de Algodão, Unidade de Controle Biológico, 58107-720, Campina Grande, Paraíba State, Brasil

Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-000, Viçosa, Minas Gerais State, Brazil

5Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-000, Viçosa , Minas Gerais State, Brazil

*Corresponding author; E-mail: [email protected]

A pdf file with supplementary material for this article in Florida Entomologist 95(4) (2012) is online at http://purl.fcla.edu/fcla/entomologist/browse

abSTraCT

Costus spicatus (Jacq.) Sw. and Costus spiralis (Jacq.) Roscoe var. spiralis (Costaceae) are economically important plants due to their pharmacological and medicinal properties and ornamental value. These plants are natives from the Brazilian Atlantic Rainforest and are fed upon by Agaraea minuta Schaus, 1892 (Lepidoptera: Arctiidae). This study describes the damage done by A. minuta on C. spicatus and C. spiralis and the biological and ecological aspects of parasitism of A. minuta by Diolcogaster sp. (Hymenoptera: Braconidae). Twenty stems of C. spicatus and C. spiralis with 100 last-instar caterpillars of A. minuta, were col-lected per plant in each of 2 years. The stem heights (F, P > 0.05), leaf lengths (F, P> 0.05), leaf widths (F, P> 0.05) and the number of leaves per stem (F, P > 0.05) of both plant species; number of pupae obtained from caterpillars of A. minuta (F, P > 0.05), adult emergence of this defoliator (F, P > 0.05) and of Diolcogaster sp. (F, P > 0.05) were similar during the 2 study periods. Agaraea minuta fed on C. spicatus and C. spiralis, and Diolcogaster sp. was shown to be a parasitoid suppressor of populations of this defoliator.

Key Words: Arctiidae, biological control, Costaceae, defoliation, parasitoids

reSumo

Costus spicatus (Jacq.) Sw. e Costus spiralis (Jacq.) Roscoe var. spiralis (Costaceae) são plan-tas economicamente importantes devido às suas propriedades farmacológicas e medicinais e valor ornamental. Essas plantas são nativas da Mata Atlântica brasileira e alimento para Agaraea minuta Schaus, 1892 (Lepidoptera: Arctiidae). Esse estudo descreve o dano por A. minuta sobre C. spicatus e C. spiralis e aspectos biológicos e ecológicos de seu parasitismo por Diolcogaster sp. (Hymenoptera: Braconidae). Vinte hastes de C. spicatus e C. spiralis, com 100 lagartas de último estádio de A. minuta, foram coletadas por planta em cada um de dois anos. A altura das hastes (F, P > 0,05), comprimento das folhas (F, P > 0,05), largura das folhas (F, P > 0,05) e o número de folhas por haste (F, P > 0,05) de ambas as espécies de plantas; número de pupas obtidas de lagartas de A. minuta (F, P > 0,05), emergência de adultos desse desfolhador (F, P > 0,05) e de Diolcogaster sp. (F, P > 0,05) foram semelhantes durante os dois períodos de estudo. Agaraea minuta pode se alimentar de plantas de C. spi-catus e C. spiralis, e Diolcogaster sp. mostrou ser um parasitóide supressor de populações desse desfolhador.

Palavras Chave: Arctiidae, controle biológico, Costaceae, desfolha, parasitóides

1-17703 p0966-970 Tavares FESdj.indd 966 10/31/12 3:11 PM

Tavares et al.: Diolcogaster sp. Parasitizing Agaraea minuta on Costus spp 967

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The ginger plants, Costus spicatus (Jacq.) Sw. and Costus spiralis (Jacq.) Roscoe var. spiralis (Zingiberales: Costaceae), are plants of economic importance because of their pharmacological and medicinal properties as well as their ornamental value. They are native to the Atlantic Rainforest biome of Brazil. Costus spicatus is an herbaceous species with a hard stem, alternate, invaginate, dark green, hairy leaves and yellow flowers with crimson-colored bracts (Campos et al. 2008). Its rhizomes, leaves, bark, and stems have phar-macological and medical properties, such as diuretic, anti-fever and weight loss (Silva et al. 2008; Quintans et al. 2010). Costus spiralis has tortuous and branched stems, spirally arranged dark green leaves and red, odorless bracts and flowers (Viel et al. 1999; Antunes et al. 2000). This plant is used to manufacture pharmacologi-cal and herbal drugs and has been used in anti-diabetic, antirheumatic, diuretic, sudorific and tonic drugs (Da Silva & Parente 2004; Britto et al. 2011).

Caterpillars of Agaraea minuta Schaus, 1892 (Lepidoptera: Arctiidae) (Suppl. Figs. 1A and 1B), which feed on C. spicatus and C. spiralis, are hairy and active during the d. Its adults are small and light brown in color (Suppl. Figs. 2A, 2B, 2C and 2D) (Watson & Goodger 1986). Two males and 1 female, and 1 male and 1 female of this insect were originally collected in Tabasco (Mexico) and in Las Mercedes (Guatemala), re-spectively (Hampson 1901). In Brazil A. minuta has attracted little attention, probably because until recently it was regarded only as a pest of ornamental plants of minor economic impor-tance.

Species of Diolcogaster (Hymenoptera: Brac-onidae) (Suppl. Figs. 3B, 3C, 3D and 3E) are solitary or gregarious endoparasitoids of Mac-rolepidoptera (Noctuidae, Geometridae and Py-raloidea) and of microlepidopteran leafminer larvae in the native forest of Rio Grande do Sul State, Brazil (Restello & Penteado-Dias 2006). In agricultural settings worldwide they were recorded from caterpillars of Arctiidae, Geome-tridae, Lasiocampidae, Limacodidae, Lymantri-idae, Noctuidae, Notodontidae, Plutellidae, Py-ralidae, Tenthredinidae, and Thaumetopoeidae (Whitfield et al. 2009; Fernández-Triana 2010; Zeng et al. 2011). Color photographs of these or-ganisms and damage to Costus spp. are available online at http://purl.fcla.edu/fcla/entomologist/browse and each figure is designated herein as a Suppl. Fig.

Because of recent interest in the cultivation of Costus spp. there is concern about their pests and how they might be managed. This study de-scribes: 1) the damage that A. minuta caterpillars caused to C. spiralis and C. spicatus plants over 2 consecutive yr, and 2) mortality inflicted by Diol-cogaster sp. on A. minuta.

maTerialS anD meThoDS

Experimental Site

We studied one clump of C. spicatus and one clump of C. spiralis, both of which were approxi-mately, 5 yr old and located in the herbarium of the Federal University of Viçosa (UFV) in Viçosa, Minas Gerais State, Brazil (S 20°45’ W 42°51’ at 651 m asl). The distance between the clumps was 72.4 m. The herbarium was shaded and humid throughout the whole yr; contained fertile soil covered with litter and grew native shrubs and trees of the Brazilian Atlantic Rainforest (Tava-res et al. 2011a, 2011b).

Evaluating Clumps of Costus

The occurrence of lepidopteran defoliators was monitored on the clumps of C. spicatus and C. spiralis (Suppl. Figs. 1A, 1B, 1C, 1D, 1E, 1F, 1G and 1H) in May 2010 and 2011 because of their prior appearance during this month in 2009. The height of the stems, number of leaves per stem and the length and width of the leaves of 20 stems of each species were evaluated in May 2010 and 2011. The experimental design was a randomized block with each stem considered as a replicate (T1- 20 stems of C. spicatus collected in 2010; T2- 20 stems of C. spiralis collected in 2010; T3- 20 stems of C. spicatus collected in 2011 and T4- 20 stems of C. spiralis collected in 2011). The data were submitted to variance analysis (ANOVA) and the means for each species compared be-tween the 2 yr periods using Tukey’s test at the 5% significance level with the computer program SAEG (2007) (Supplier: UFV).

Collecting Agaraea minuta Caterpillars

One hundred last-instar caterpillars of A. minuta (Suppl. Figs. 2G and 2H) per clump of C. spicatus and C. spiralis were collected with a brush in May 2010 and 2011. Caterpillars were placed in plastic pots (20 caterpillars per pot) with 2 leaves of the host plants as food and substrate for pupation and these were changed daily. The petioles of the leaves were moistened to avoid desiccation, and the pots were kept in the Laboratory of Biological Control of Insects (LCBI) of UFV at 25 ± 1 °C at12:12 h L:D and 70 ± 10% RH. Previous studies showed that Di-olcogaster sp. parasitize early larval stages of A. minuta.

Biological Aspects of Parasitism of Agaraea minuta by Diolcogaster sp.

The number of pupae and the percentage of adult emergence of A. minuta and the parasit-oids were recorded in a randomized design (T1-



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100 caterpillars of A. minuta collected in 2010 on C. spiralis; T2- 100 caterpillars of A. minuta collected in 2010 on C. spicatus; T3- 100 caterpil-lars of A. minuta collected in 2011 on C. spiralis and T4- 100 caterpillars of A. minuta collected in 2011 on C. spicatus). The pupae obtained were individually put into 50 mL plastic cups sepa-rately per treatment. Each pupa was consid-ered as a replicate. The data were submitted to ANAVA and the means for each plant species and comparisons between the 2 yr periods were ana-lyzed using Tukey’s test at the 5% significance level.

Damage on Clumps of Costus

Stem heights, leaf lengths, leaf widths, and number of leaves per stem for C. spicatus and C. spiralis were measured and the damage (parts fed, aspects after feeding, and viability of stems) done to the clumps by the caterpillars were visu-ally observed during the collection of the cater-pillars in the herbarium (May 2010 and 2011) and in the following month (June 2010 and 2011) in order to quantify the effect of A. minuta cat-erpillars on the plants. The caterpillars were removed after the collections to quantify the parasitism rate in the laboratory, which can af-fect the damage.

Insect Identification

Adults of A. minuta were mounted with en-tomological pins in polystyrene supports and some were sent to Dr. Vitor Osmar Becker, Ui-raçu Institute in Camacan, Bahia State, Brazil, for identification. Individuals of the parasitoid, Diolcogaster sp. (Suppl. Figs. 3B, 3C, 3D and 3E), that had emerged from A. minuta pupa, were transferred to 70% ethanol following identification by M.Sc. Geraldo Salgado-Neto. Voucher specimens were stored at the Regional Entomological Museum of the Federal Univer-sity of Viçosa (UFVB) and at the Entomologi-cal Museum of the Federal University of Santa Maria (UFSM).

reSulTS

Parameters of Clumps of Costus

A comparison of C. spicatus and C. spiralis plants showed that the stem heights, number of leaves per stem and leaf widths and lengths (F, P > 0.05) were similar between treatments (Ta-ble 1).

Pupae and Adults of Agaraea minuta and Lar-val Parasitism by Diolcogaster sp.

The number of pupae (Suppl. Figs. 2E and 2F) obtained from caterpillars collected from plants of C. spicatus and C. spiralis and the adult emer-gence of A. minuta and Diolcogaster sp. (F, P> 0.05) were similar in both yr (Table 2).

Damage on Costus spicatus and Costus spiralis

Caterpillars of A. minuta fed on the apical buds (Suppl. Figs. 1C and 1D) and on the leaves (Suppl. Figs. 1E and 1F) of C. spicatus and C. spiralis, but left the midribs, scarifying them but leaving the epidermis intact. These apical buds and leaves dried quickly becoming light brown and nonviable (Suppl. Figs. 1G and 1H). However, some stems remained green and developed new shoots at the ground level or the apical bud began to grow again. This enabled the plant to survive.

Parasitism on Agaraea minuta Larvae by Diolcogaster sp.

Agaraea minuta caterpillars that had been parasitized produced a cocoon made of white col-ored silk (Suppl. Fig. 3A). Pupation occurred on the abaxial surfaces of the leaves of C. spicatus and C. spiralis as well as on the covers of the plas-tic cups. The silk was wrapped around the leaves causing them to fold and become cone-shaped, which might reduce the photosynthesis rate. On the other hand, this process may lead to a reduc-tion in caterpillar predation. Only one species of parasitoid was found and only a single individual emerged per A. minuta pupa. The caterpillars of A. minuta were of different ages, suggesting that

Table 1. STemS evaluaTeD, STem heighTS (m), leaveS per STem, largeST WiDTh anD greaTer lengTh (Cm) (mean ± SE) oF Costus spiCatus anD Costus spiralis (CoSTaCeae) in apr 2010 anD 2011.

Parameters

Costus spicatus Costus spiralis

2010 2011 2010 2011

Stems evaluated 20 20 20 20Stem heights 1.73 ± 0.28 1.68 ± 0.26 1.44 ± 0.35 1.42 ± 0.33 Leaves/Stem 14.0 ± 3.0 12.0 ± 2.0 22.0 ± 6.0 20.0 ± 5.0 Largest width 18.3 ± 2.7 18.2 ± 2.6 18.3 ± 3.3 18.1 ± 3.1 Greater length 45.6 ± 5.4 45.4 ± 5.3 15.3 ± 2.5 15.1 ± 2.4

Means between the years 2010 and 2011, within each row per plant species did not differ by Tukey’s test at the 5% significance level.


Tavares et al.: Diolcogaster sp. Parasitizing Agaraea minuta on Costus spp 969

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ofthey had originated from eggs laid at different

times, although only the last-instar larvae were collected. At least 2 generations of A. minuta were observed per yr in the field.

The caterpillars of A. minuta showed gregari-ous feeding habits and caused greater damage to the clumps of C. spicatus (Suppl. Fig. 1H) than to those of C. spiralis (Suppl. Fig. 1G), because green tissues remained in some leaves of the lat-ter species. Egg masses of A. minuta were found deposited at the tops of the plants where the cat-erpillars began feeding after hatching. Some feces of these caterpillars remained on damaged leaves but some fell to the soil. All leaves and apical buds of C. spicatus plants were damaged by caterpil-lars after each infestation in the 2 yr study.

DiSCuSSion

Agarea minuta appears to be unaffected by the putative pharmacologically active substances of Costus spp. The roots of Costus spp. are rich in saponins (heterosides from plant secondary metabolism), which are known insect deterrents (Da Silva et al. 1999), but extracts of Costus spp. leaves (without saponins) showed no deterrent ef-fect on insects, for example, after leaves had been offered to Paraponera clavata F., 1775 (Hymenop-tera: Formicidae) (Dyer et al. 2003).

Damage by A. minuta was sufficiently severe to reduce leaf yield, which is used in medical and pharmacological products (Da Silva & Par-ente 2004; Silva et al. 2008; Quintans et al. 2010; Britto et al. 2011). Costus spp. used by the folk medicine are generally cultivated without syn-thetic pesticides. Fresh feces on the leaves or on the soil indicate the presence of caterpillars in the plants. To reduce caterpillar feeding, there is a need to use alternative methods of control such as diversification and crop rotation, trap plants, alternative insecticides, places of refuge for natu-ral enemies, etc.

Agaraea minuta has potential to defoliate C. spicatus and C. spiralis plants, although it dam-ages the former more severely than the latter.

The parasitoid, Diolcogaster sp., could suppress populations of A. minuta, which could result in increased plant biomass.

aCknoWleDgmenTS

We thank the following people and institutions: Dr. Paulus Johannes Maria Maas (Wageningen University, Netherlands) for identifying the variety of Costus spira-lis (Costaceae); Boldsystems.org site for providing the pictures of Agaraea minuta (Lepidoptera: Arctiidae) adults; “Conselho Nacional de Desenvolvimento Cientí-fico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoa-mento de Pessoal de Nível Superior (CAPES)”, and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” for financial support; and Asia Sci-ence Editing of the Republic of Ireland for English cor-rections and editing this manuscript.

reFerenCeS CiTeD

anTuneS, a. D., Da Silva, b. p., anD parenTe, J. p. 2000. Flavonol glycosides from leaves of Costus spiralis. Fitoterapia 71(5): 507-510.

briTTo, r. m., SanToS, a. l., Cruz, J. S., gonDim, a. n. S., lauTon-SanToS, S., lara, a., guaTimoSim, S., vaSCon-CeloS, C. m. l., eSTevame, C. D., DiaS, a. S., oliveira, e. D., lima, a. k., Souza, r. C., anD ConDe-garCia, e. a. 2011. Aqueous fraction from Costus spiralis (Jacq.) Roscoe leaf reduces contractility by impair-ing the calcium inward current in the mammalian myocardium. J. Ethnopharmacol. 138(2): 382-389.

CampoS, v. m., paSin, l. a. a. p., anD barJa, p. r. 2008. Photosynthetic activity and growth analysis of the plant Costus spicatus cultivated under differ-ent light conditions. European Phys. J.-Spec. Top. 153(1): 527-529.

Da Silva, b. p., anD parenTe, J. p. 2004. New steroidal saponins from rhizomes of Costus spiralis. Z. Natur-forsch. (C) 59(1-2): 81-85.

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Table 2. number oF pupae From agaraea minuta (lepiDopTera: arCTiiDae) CaTerpillarS ColleCTeD on Costus spiCatus anD Costus spiralis (CoSTaCeae) planTS anD perCenT oF aDulT emergenCe oF ThiS DeFoliaTor anD oF DiolCo-gaster Sp. (hymenopTera: braConiDae: miCrogaSTrinae).

Parameters

Costus spicatus Costus spiralis

2010 2011 2010 2011

Caterpillars evaluated 100 100 100 100Pupae number 97 98 96 98 Parasitoids - # emerged 89 90 91 93 Adults moths - # emerged 11 10 09 07

Means between the years 2010 and 2011, within each row per plant species did not differ by Tukey’s test at the 5% significance level.



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