Parasitism rate of Plutella xylostella (Lepidoptera: Plutellidae) larvae in greenhouse by Tetrastichus howardi (Hymenoptera: Eulophidae) females at different densities

Taxa de parasitismo de lagartas Plutella xylostella (Lepidoptera: Plutellidae) em estufa por fêmeas de Tetrastichus howardi (Hymenoptera: Eulophidae) em diferentes densidades

Abstract

Parasitoids control insect pests, but their number per host affects their efficiency. The objective of this work was to evaluate the best density of Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) individuals parasitizing fourth instar Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) larvae in greenhouse conditions. These larvae were exposed to parasitism by T. howardi females with 1:1, 3:1, 6:1, 9:1, 12:1, 15:1 and 18:1 parasitoid/host ratios with 10 replications during 96 hours. After this period the larvae were kept on host plants (Brassica oleracea) until pupa formation. Tetrastichus howardi parasitized and reproduced in P. xylostella larvae at all its densities tested, but with higher values, 84% and 10 ± 2.4 individuals, respectively, with 9:1 parasitoids/host. Nine T. howardi females per P. xylostella larvae are the adequate number to manage this insect pest.

Keywords:
biological control; diamondback moth; parasitoids

Resumo

Os parasitoides controlam os insetos pragas, mas o seu número por hospedeiro afeta a sua eficiência. O objetivo deste trabalho foi avaliar a melhor densidade de Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) parasitando o quarto instar de larvas de Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae) em condições de estufa. Estas lagartas foram expostas ao parasitismo por fêmeas T. howardi com densidades 1:1, 3:1, 6:1, 9:1, 12:1, 15:1 e 18:1 de parasitoide/hospedeiro com 10 repetições durante 96 horas. Após este período, as lagartas foram mantidas em plantas hospedeiras (Brassica oleracea) até à formação de pupas. Tetrastichus howardi parasitaram e reproduziram em lagartas P. xylostella em todas as suas densidades testadas, mas com valores mais elevados de 84% e 10 ± 2.4 indivíduos, respectivamente, com 9:1 parasitoides/hospedeiro. Nove fêmeas de T. howardi por lagarta de P. xylostella são o número adequado para controlar está praga de inseto.

Palavras-chave:
controle biológico; traça-diamante; parasitoides

1. Introduction

The endoparasitoid Tetrastichus howardi (Olliff, 1893) (Hymenoptera: Eulophidae) is a potential agent for the biological control of lepidopteran pests. Polyphagy, parasitism of agricultural and forest pests, gregarious, high number of individuals per generation, developing at different temperatures and dispersion favour the use of this natural enemy in the biological control (Favero et al. 2015; Kumar et al. 2016; Favoreto et al. 2021). Tetrastichus howardi developed and emerged from Diatraea saccharalis (Fabricius, 1794) (Lepidoptera: Crambidae) larvae and pupae (Pereira et al., 2015; Rodrigues et al., 2021).

The diamondback moth, Plutella xylostella (Linnaeus, 1758) (Lepidoptera: Plutellidae), is the main pest of cultivated species of the Brassicaceae family (Rezaei et al., 2018). A characteristic that contributes for this pest to have a preference for plants of the Brassicacea family, it is due to the presence of compounds formed from glucosinolates. These compounds are toxic to most insects, however, they stimulate feeding and host plant selection by the insect (Van-Loon et al., 2002). The life cycle of this lepidopteran is short depending on the temperature with several generations per year. This cosmopolitan, polyphagous insect is found globally (Dancau et al., 2018). Its larvae damage leaves and inflorescences of Brassicaceae plants reducing the photosynthetic area with damage reaching up to 100% (Boiça-Júnior et al., 2015; Machekano et al., 2017).

The use of synthetic insecticides to control P. xylostella alters the metabolism of this insect selecting those resistant to the products used (Sarfraz and Keddie, 2005). The natural biological control is an alternative with reports of parasitoid and predator species on P. xylostella in Brassicaceae crops (Karindah et al., 2005; Dancau et al., 2019). In biological control programs which use parasitoid insects, hymenoptera stand out for their wide diversity (Silva et al., 2020) Using mass breeding techniques, evaluating their biological parameters and the release of these parasitoids (Barbosa et al., 2019; Ongaratto et al., 2020).

Studies on the female densities are necessary to increase the efficiency of natural enemies in pest control (Scheiner and Martin, 2020). The best density of parasitoid females to host individuals is important to estimate the number of insects released and that of releasing points of natural enemies in biological control programs (Barbosa et al., 2019).

Tetrastichus howardi naturally parasitized P. xylostella (Silva-Torres et al., 2010) and the objective was to determine the best density of its females parasiting larvae of this pest in greenhouse conditions.

2. Material and Methods

The experiments were carried out at the Laboratory for Biological Control of Insects (LECOBIOL) and in a greenhouse (22° 19' 80” S, 54° 93' 38” W) of the Faculty of Biological and Environmental Sciences at the Universidade Federal da Grande Dourados in Dourados, Mato Grosso do Sul state, Brazil.

2.1. Laboratory rearing Plutella xylostella

Plutella xylostella larvae were obtained from the LECOBIOL, where this insect is reared in an air-conditioned room, at the temperature of 25 ± 2 °C, 70 ± 10% relative humidity, and a photoperiod of 12 h. Plutella xylostella adults were confined in transparent circular plastic cages (30 cm high and 20 cm in diameter), with a side rectangular opening sealed with a fine nylon mesh, to circulate the air. Adults of this pest were fed a solution of 10% honey in a sponge (10 cm long x 2 cm wide) on the top of the cage. Leaf discs of Brassica oleracea cabbage var. acephala (6 cm in diameter) from local organic producers were distributed on filter paper moistened in distilled water as substrate for the P. xylostella to lay eggs. The egg masses on the leaf discs were removed and placed in a container with a fresh cabbage leaf as food for the newly emerged larvae. Fresh leaves were provided daily until the pupa stage, which were removed from the leaves with the aid of a brush and placed in mating cages (Barros et al., 2012).

The identification of the species Plutella xylostella was made with the aid of a taxonomic identification key.

2.2. Collecting and laboratory rearing T. howardi

Tetrastichus howardi was collected in 2010 at the Experimental Farm of the Universidade Federal da Grande Dourados (UFGD) (22º13'16” S, 54º48'2” W, 530 m) from D. saccharalis pupa in sugarcane stalks. The “voucher specimens” were deposited in the Entomological Collection of the Universidade Federal do Espírito Santo (UFES), Department of Biological Sciences at UFES, 514 Fernando Ferrari Avenue, Biological Sciences Building, Block A, room 216-215, zip code 29.075-919, Vitória, Espirito Santo, Brazil. Archive: 150792 to 150816 to 157187, data available online from Splink. The parasitoid was identified by Prof. Dr. Marcelo Teixeira Tavares (Vargas et al., 2011).

Adults of T. howardi were kept in glass tubes (15 × 2 cm) covered with cotton with a droplet of pure honey. Each D. saccharalis pupae, 24 to 48 h old, were exposed to parasitism by five T. howardi females for 24 h at 25 ± 2 °C, relative humidity (RH) of 70 ± 10% and photophase of 14 h in a climate-controlled chamber. Parasitoids emerged after 18 to 20 days from parasitized host pupae were fed with a droplet of honey and left for 24 hours for mating. Females were individualized after mating and fed to maintain its rearing and/or to perform the bioassays (Vargas et al., 2011).

2.3. Experiment development

Brassica oleracea seedlings, in the second phenological development stage and characterized by less than five true leaves, were acquired from a local retailer in Dourados, Mato Grosso do Sul, Brazil for the greenhouse bioassay. These seedlings were placed in 1L volume vases with a substrate composed of organic fertilizer and soil (dystroferric red oxisol) in the proportion of 1:2. The seedlings were placed in a greenhouse until the third phenological stage, with six to eight true leaves.

The experiment was carried out in a polyethylene greenhouse measuring 6 X 18 m², the vases were on 1.20 m high benches systems arranged randomly spaced at 15 cm, with average temperature and relative humidity of 27.67 ± 2.29 °C and 54.2 ± 4.45%. Four hundred vases were used, containing one cabbage plant at the phenological stage III, and one fourth instar P. xylostella larva each. Wooden stakes were placed at each end of the vase and voile used to prevent larvae to escaping.

The treatments were composed of different densities of T. howardi females per P. xylostella larva on a cabbage plant. Mated and fed 24-hour-old T. howardi females were released into the vases at the densities of 1:1, 3:1, 6:1, 9:1, 12:1, 15:1 and 18:1 parasitoid females per P. xylostella larva. The densities of larvae per plant and of parasitoids per larva were determined through laboratory pre-tests. After 96 hours of parasitism, P. xylostella pupae and larvae were collected using a brush. Larvae were individualized in Petri dishes with cabbage leaves and the pupae in glass tubes (15 cm) covered with cotton and placed in a B.O.D. incubator with controlled temperature, humidity, and photoperiod of 25°C ± 2 ºC, 70 ± 10% and 12 hours, respectively.

2.4. Data analysis

The experiment was carried out in a completely randomized design (CRD) with seven treatments and a control (no T. howardi females). Fifty replications were used with a cabbage plant and one fourth instar P. xylostella larvae in each one.

Percentage of parasitism (%P) [(P. xylostella larvae with parasitoid emergence + larvae without P. xylostella adult emergence)/(total number of larvae) × 100]; total progeny (parasitoids emerged per parasitized host); emergence (% E) [(P. xylostella larvae with parasitoid emergence)/(number of parasitized larvae) × 100]; progeny per female (progeny of females as a function of the number of females per evaluated density); life cycle duration (development period of immature T. howardi from the day of parasitism to the emergence of its adults); and sex ratio (number of emerged females/number of total emerged adults) were the biological characteristics evaluated per treatment.

Data on the biological characteristics were submitted to analysis of variance (ANOVA) at 5% probability. Values significant were submitted to regression analysis and adjusted according to the model using all significant coefficients, based on the determination coefficient (R2), on the significance of the regression coefficients by the F test (p≤0.05) and on the adaptation to the biological phenomenon studied. The overall average of the data was performed for non-significant data.

3. Results

Tetrastichus howardi females found and parasitized fourth instar larvae of P. xylostella under greenhouse conditions with values of 50%, 62%, 72%, 84%, 78%, 72% and 72% with the densities of 1:1, 3:1, 6:1, 9:1, 12:1, 15:1 and 18:1 parasitoid females per P. xylostella larva, respectively, but it emerged only from this host pupae (Figure 1).

Figure 1
Parasitism percentage of fourth instar Plutella xylostella (Lepidoptera: Plutellidae) caterpillars by Tetrastichus howardi (Hymenoptera: Eulophidae) females at different densities in semi-field conditions.

The characteristics of the parasitized larvae and pupae at all T. howardi female densities were body with losses of bright green coloration, integument dry and rigid and mummified appearance with brown coloration. The color of the P. xylostella pupae was caramel-brown with some immature T. howardi in their interior, usually, encapsulated and melanized, or with malformed individuals of this parasitoid.

The percentages of T. howardi emerged from P. xylostella pupae were similar with the different densities of this parasitoid females with values from 25 to 45.56%.

The duration of the life cycle (egg to adult) of T. howardi varied from 20.67 to 22.75 days with similar values with all the densities of this parasitoid females.

The progeny of T. howardi on P. xylostella varied with the density of this parasitoid with average values of 2.33 to 11.50 offspring per pupa at the densities of 18:1 and 9:1 respectively (Figure 2). The progeny of T. howardi per pupa of P. xylostella in greenhouse varied from six to 20 parasitoids.

Figure 2
Total progeny of Tetrastichus howardi (Hymenoptera: Eulophidae) per pupa of Plutella xylostella (Lepidoptera: Plutellidae) with different densities of females of this parasitoid in semi-field conditions.

The progeny of each T. howardi female per P. xylostella pupae declined as the density of this parasitoid increased with values from 3.00 and 0.16 for the densities of 1:1 and 18:1 parasitoid: host, respectively (Figure 3).

Figure 3
Progeny per Tetrastichus howardi (Hymenoptera: Eulophidae) female with a density of one, three, six, nine, 12, 15 or 18 females of this parasitoid per Plutella xylostella (Lepidoptera: Plutellidae) pupae.

The sex ratio of T. howardi was inversely correlated with its female densities, with a higher value at 1:1 (Figure 4).

Figure 4
Sex ratio (number of females/(number of females + number of males)) of Tetrastichus howardi (Hymenoptera: Eulophidae) with different numbers of females per pupa of Plutella xylostella.

4. Discussion

The percentage of P. xylostella larvae parasitized at all densities of T. howardi females demonstrates the suitability of this host for the development of this parasitoid (Karindah et al., 2005). The success of T. howardi females parasitizing P. xylostella confirms that they overcome the immune defenses of this host as reported for this natural enemy parasitizing D. saccharallis larvae and emerging from pupae of this host (Rodrigues et al., 2021). The parasitism of 50% of the P. xylostella fourth instar larvae by T. howardi in greenhouse at density de 1:1 (T. howardi/ P. xylostella) is lower than the approximately 80% by one female of this natural enemy per fourth instar P. xylostella larva in the laboratory (Tiago, 2018). Difference in the parasitism rate may be due to controlled and confined environment while host location in greenhouse and field conditions is based mainly in chemical signals from plants, besides visual and physical stimuli (shape, texture, or host movement) (Kruidhof et al. 2019).

The increasing in the percentage of parasitism up to a density, and a decrease after it is similar to that of T. howardi and other Eulophidae such as Palmistichus elaeisis Delvare & LaSalle and Trichospilus diatraeae Cherian & Margabandhu (Hymenoptera: Eulophidae) without a linear increase in the parasitism percentage as the number of female parasitoid increased (Pastori et al., 2012; Favero et al., 2015; Barbosa et al., 2019). The decline after the optimal parasitoid density could be due to parasitoid females regulating the number of eggs laid after identifying parasitized hosts (Godfray, 1994). The reduction in parasitism can characterize mutual interference when several females forage in the same location with greater interaction between them during host searching (Saini and Sharma, 2018).

The success of females of this parasitoid finding and parasitizing P. xylostella larvae under greenhouse conditions may be due to the process of injecting polydnavirus (PDV) and venom during oviposition, and teratocytes released into the host's hemolymph after the egg hatching as reported for the parasitoid Cotesia vestalis (Haliday) (Hymenoptera: Braconidae). Other parasitoids such as Oomyzus sokolowskii Kurdjumov (Hymenoptera: Eulophidae) release only venom during parasitism, which helps in this process, without affecting the host development (Bai et al., 2011). Tetrastichus howardi, being a parasitoid of the same family as O. sololowskii, may also only release venom during parasitism, which does not prevent the P. xylostella larva from becoming a pupa, and then completing its development into this last host stage.

Morphological characteristics of the pupae are altered and used for identification of parasitismo (Bae and Kim, 2004).The caramel-brown of parasitized pupae is related to the parasitoid invasion into the host’s hemocele with its ovopositor and to the eggs inducing the release of substances generating immune responses and changes in the physiology and color of the host (Meng et al., 2016). The melanization and encapsulation of some parasitoids are due to the host immune defense, while the parasitoid injection, during parasitism, of poisons and other substances can reduce or prevent this process allowing its egg development. The finding of melanized and encapsulated parasitoids indicate that the substances released by the parasitoid did not, in some cases, overcome the host immune response (Meng et al., 2018).

The similar percentages of T. howardi emerged from P. xylostella pupae with all densities of this female parasitoid shows how much the parasitoid can adapt and that the nutrients in the host were sufficient for the development and multiplication of this natural enemy in greenhouse conditions (Harvey et al., 2013; Vargas et al., 2013; Barbosa et al., 2019).

The similar duration of the life cycle (egg to adult) of T. howardi with all its densities per P. xylostella pupae indicates that the food resource available to the immature parasitoid did not affect this parameter as found for this natural enemy with D. saccharallis pupa in the laboratory (Favero et al., 2015). The duration of the life cycle of this parasitoid in P. xylostella was similar to that with D. saccharallis, the original host of this parasitoid. This is important because the short cycle reduces the risk of early mortality of the parasitoid by antagonists, since the parasitoid is defenceless inside the host (Rodrigues et al., 2021).

The lower progeny of T. howardi per P. xylostella pupae at 18:1 parasitoid: host indicates an inadequate density of females per host decreasing oviposition or the survival inside the host pupae (Khatri et al., 2021). The progeny of T. howardi per pupa of P. xylostella in greenhouse from six to 20 parasitoids was lower than that for this parasitoid in the laboratory, four to 28 T. howardi per P. xylostella pupae (Karindah et al., 2005). The pupae of this host is smaller, 0.6 cm long and 4.83 mg in weight (Chagas Filho et al., 2010; Machekano et al. 2017) with a lower number of parasitoid produced per host pupa. Other host pupae such as those of Erinnyis ello (Linnaeus, 1758) (Lepidoptera: Sphingidae) measure between 4 to 6 cm long and with 3,602 mg produced 466 parasitoids each one (Barbosa et al., 2015). The offspring of this parasitoid is related to host size and the food availability (Pyñero et al., 2016).

The highest progeny per female at 1:1 and 3:1 densities of T. howardi and a decrease with higher parasitoid ratio per host female suggests that some female parasitoid decrease the number of eggs laid on the host (Vargas et al., 2013). Another possibility is that the host supports a maximum number of immatures with high mortality over it (Pereira et al., 2015).

The inverse correlation between the parasitoid sex ratio with the number of its females per host pupae agrees with that reported for Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) with the second female of this parasitoid laying fewer eggs than the first, with the sex ratio tending to higher number of males (Campos-Farinha et al., 2000). This suggests that the higher sex ratio with the lower densities 1:1 and 3:1 is due to the lower number of parasitoid larvae inside the host with more food available favoring females. The higher sex ratio with fewer females is important for parasitoids in the field and its release at high sex ratio increases their efficiency (Vacari et al., 2012; Scheiner and Martin, 2020).

This is the first work evaluating the parasitism of P. xylostella larvae by T. howardi females at different densities per host in greenhouse conditions. Tetrastichus howardi, at all densities tested, parasitized P. xylostella larvae, but with higher parasitism rate with nine T. howardi females per P. xylostella larvae.

The use of T. howardi increases the perspectives for biological control programs of P. xylostella in vegetable growing agroecosystems in Brazil. Brassicaceae species are cultivated in small properties, which can be positive for the foraging of T. howardi females.

Acknowledgements

To “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)” for financial support.

References

• BAE, S. and KIM, Y., 2004. Host physiological changes due to parasitism of Braconidae wasp, Cotesia plutellae, on diamondback moth, Plutella xylostella. Comparative Biochemistry and Physiology, vol. 138, no. 1, pp. 39-44. http://dx.doi.org/10.1016/j.cbpb.2004.02.018 PMid:15165569.
  » http://dx.doi.org/10.1016/j.cbpb.2004.02.018
• BAI, S.F., LI, X., CHEN, X.X., CHENG, J.A. and HE, J.H., 2011. Interspecific competition between two endoparasitoids Cotesia vestalis (Hymenoptera: Braconidae) and Oomyzus sokolowskii (Hymenoptera: Eulophidae). Archives of Insect Biochemistry and Physiology, vol. 76, no. 3, pp. 156-167. http://dx.doi.org/10.1002/arch.20399 PMid:21322005.
  » http://dx.doi.org/10.1002/arch.20399
• BARBOSA, R.H., KASSAB, S.O., PEREIRA, F.F., ROSSONI, C., COSTA, D.P. and BERNDT, M.A., 2015. Parasitism and biological aspects of Tetrastichus howardi (Hymenoptera: Eulophidae) on Erinnyis ello (Lepidoptera: Sphingidae) pupae. Ciência Rural, vol. 45, no. 2, pp. 185-188. http://dx.doi.org/10.1590/0103-8478cr20130896
  » http://dx.doi.org/10.1590/0103-8478cr20130896
• BARBOSA, R.H., PEREIRA, F.F., MOTOMIYA, A.V.A., KASSAB, S.O., ROSSONI, C., TORRES, J.B., MUSSURY, R.M. and PASTORI, P.L., 2019. Tetrastichus howardi density and dispersal toward augmentation biological control of sugarcane borer. Neotropical Entomology, vol. 48, no. 2, pp. 323-331. http://dx.doi.org/10.1007/s13744-018-0646-z PMid:30456722.
  » http://dx.doi.org/10.1007/s13744-018-0646-z
• BARROS, R., THULER, R.T. and PEREIRA, F.F., 2012. Técnica de criação de Plutella xylostella (L., 1758) (Lepidoptera: Yponomeutidae). In: D. PRATISSOLI. Técnicas de criação de pragas de importância agrícolas, em dietas naturais Vitória: EDUFES, pp. 65-85.
• BOIÇA-JÚNIOR, A.L., TORRES, A.L., SOUZA, B.H.S., SILVA, A.G. and BARROS, R., 2015. Combination of resistant cultivars, botanical insecticides and biological control for Plutella xylostella management on cabbage. African Journal of Agricultural Research, vol. 10, no. 7, pp. 588-595. http://dx.doi.org/10.5897/AJAR2014.8484
  » http://dx.doi.org/10.5897/AJAR2014.8484
• CAMPOS-FARINHA, A.E.C., CHAUD-NETTO, J. and GOBBI, N., 2000. Biologia reprodutiva de Cotesia flavipes (Cameron) (Hymenoptera: Braconidae). IV. Discriminação entre lagartas parasitadas e não parasitadas de Diatraea saccharalis Fabricius (Lepidoptera: Pyralidae), tempo de desenvolvimento e razão sexual dos parasitoides. Arquivos do Instituto Biológico, vol. 67, no. 2, pp. 229-234.
• CHAGAS FILHO, N.R., BOIÇA-JÚNIOR, A.L. and ALONSO, T.F., 2010. Biologia de Plutella xylostella L. (Lepidoptera: Plutellidae) em cultivares de couve-flor. Neotropical Entomology, vol. 39, no. 2, pp. 253-259. http://dx.doi.org/10.1590/S1519-566X2010000200017 PMid:20498964.
  » http://dx.doi.org/10.1590/S1519-566X2010000200017
• DANCAU, T., HAYE, T., CAPPUCCINO, N. and MASON, P., 2019. Something old, something new: revisiting the diamondback moth (Lepidoptera: Plutellidae) life table after 65 years. Canadian Entomologist, vol. 152, no. 1, pp. 70-88. http://dx.doi.org/10.4039/tce.2019.70
  » http://dx.doi.org/10.4039/tce.2019.70
• DANCAU, T., MASON, G.P. and CAPPUCCINO, N., 2018. Elusively overwintering: a review of diamondback moth (Lepidoptera: Plutellidae) cold tolerance and overwintering strategy. Canadian Entomologist, vol. 150, no. 2, pp. 156-173. http://dx.doi.org/10.4039/tce.2018.2
  » http://dx.doi.org/10.4039/tce.2018.2
• FAVERO, K., PEREIRA, F.P., TORRES, J.B., OLIVEIRA, H.N., KASSAB, S.O. and ZANUNCIO, J.C., 2015. Reproduction of Tetrastichus howardi (Hymenoptera: Eulophidae) in Diatraea saccharalis (Lepidoptera: Crambidae) pupae at different temperatures. The Florida Entomologist, vol. 98, no. 3, pp. 865-869. http://dx.doi.org/10.1653/024.098.0308
  » http://dx.doi.org/10.1653/024.098.0308
• FAVORETO, A.L., PAVANI, R.F., RIBEIRO, M.F., ZANUNCIO, A.J.V., SOARES, M.A., ZANUNCIO, J.C. and WILCKEN, C.F., 2021. Tetrastichus howardi (Hymenoptera: Eulophidae): first report of parasitismo in Oxydia vesulia (Lepidoptera: Geometridae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 8, no. 2, pp. 406-410. http://dx.doi.org/10.1590/1519-6984.228541 PMid:32428093.
  » http://dx.doi.org/10.1590/1519-6984.228541
• GODFRAY, H.C.J., 1994. Parasitoids, behavioral and evolutionary ecology Princeton: University Press. 447 p. http://dx.doi.org/10.1515/9780691207025
  » http://dx.doi.org/10.1515/9780691207025
• HARVEY, J.A., POELMAN, E.H. and TANAKA, T., 2013. Intrinsic inter- and intraspecific competition in parasitoid wasps. Annual Review of Entomology, vol. 58, no. 1, pp. 333-351. http://dx.doi.org/10.1146/annurev-ento-120811-153622 PMid:23092242.
  » http://dx.doi.org/10.1146/annurev-ento-120811-153622
• KARINDAH, S., SUTANTO, S., SISWANTO, E. and SULISTYOWATI, L., 2005. Parasitoid larva-pupa Tetrastichus howardi (Hymenoptera: Eulophidae) pada Pluttella xylostella L. (Lepidoptera: Yponomeutidae) di pertanaman kubis kecamatan batu dan poncokusumo, kabupaten malang. Jurnal Entomologi Indonesia, vol. 2, no. 1, pp. 61-68. http://dx.doi.org/10.5994/jei.2.1.61
  » http://dx.doi.org/10.5994/jei.2.1.61
• KHATRI, D., HE, X.Z. and WANG, Q., 2021. Potential aphid population regulation by Aphidus colemani (Hymenoptera: Aphiidae) in response to host density, parasitoid density, and age. Journal of Economic Entomology, vol. 114, no. 4, pp. 1847-1851. http://dx.doi.org/10.1093/jee/toab090 PMid:34002775.
  » http://dx.doi.org/10.1093/jee/toab090
• KRUIDHOF, H.M., KOSTENKO, O., SMID, H.M. and VET, L.E.M., 2019. Integrating parasitoid olfactory conditioning in augmentative biological control: potential impact, possibilities, and challenges. Frontiers in Ecology and the Environment, vol. 7, pp. 84-91. http://dx.doi.org/10.3389/fevo.2019.00084
  » http://dx.doi.org/10.3389/fevo.2019.00084
• KUMAR, A., BAITHA, A. and BARELIYA, P.K., 2016. Some biological aspects of pupal parasitoid, Tetrastichus howardi (Olliff) (Hymenoptera: Eulophidae) on Chilo auricilius (Dudgeon) pupae. Current Biotica, vol. 10, no. 2, pp. 170-174.
• MACHEKANO, H., MVUMI, B.M. and NYAMUKONDIWA, C., 2017. Diamondback moth, Plutella xylostella (L.) in Southern Africa: research trends, challenges and insights on sustainable management options. Sustainability, vol. 9, no. 2, pp. 91-114. http://dx.doi.org/10.3390/su9020091
  » http://dx.doi.org/10.3390/su9020091
• MENG, E., QIAO, T., TANG, B., HOU, Y., YU, H. and CHEN, Z., 2018. Effects of ovarian fluid, venom and egg surface characteristics of Tetrastichus brontispae (Hymenoptera: Eulophidae) on the immune response of Octodonta nipae (Coleoptera: Chrysomelidade). Journal of Insect Physiology, vol. 109, pp. 125-137. http://dx.doi.org/10.1016/j.jinsphys.2018.07.006 PMid:30025717.
  » http://dx.doi.org/10.1016/j.jinsphys.2018.07.006
• MENG, E., TANG, B., HOU, Y., CHEN, X., CHEN, J. and YU, X.Q., 2016. Altered immune function of Octodonta nipae (Maulik) to its pupal endoparasitoid, Tetrastichus brontispae Ferrière. Comparative Biochemistry and Physiology, vol. 198, pp. 100-109. http://dx.doi.org/10.1016/j.cbpb.2016.04.001 PMid:27101988.
  » http://dx.doi.org/10.1016/j.cbpb.2016.04.001
• ONGARATTO, S., PINTO, K.J., MÂNICA-BERTO, R., NÖRNBERG, S.D., GONÇALVES, R.S., GARCIA, M.S. and NAVA, D.E., 2020. Influence of the host diet on the performance of Doryctobracon areolatus (Hymenoptera: braconidae). Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 80, no. 4, pp. 727-734. http://dx.doi.org/10.1590/1519-6984.217968 PMid:31778480.
  » http://dx.doi.org/10.1590/1519-6984.217968
• PASTORI, P.L., FAGUNDES-PEREIRA, F., SANTOS-ANDRADE, G., OLIVEIRA-SILVA, R., COLA-ZANUNCIO, J. and AZEVEDO-PEREIRA, A.Í., 2012. Reproduction of Trichospilus diatraeae (Hymenoptera: Eulophidae) in pupae of two lepidopterans defoliators of eucalypt. Revista Colombiana de Entomologia, vol. 38, no. 1, pp. 91-93. http://dx.doi.org/10.25100/socolen.v38i1.8927
  » http://dx.doi.org/10.25100/socolen.v38i1.8927
• PEREIRA, F.F., KASSAB, S.O., CALADO, V.R.F., VARGAS, E.L., OLIVEIRA, H.N. and ZANUNCIO, J.C., 2015. Parasitism and emergence of Tetrastichus howardi (Hymenoptera: Eulophidae) on Diatraea saccharalis (Lepidoptera: Crambidae) larvae, pupae and adults. The Florida Entomologist, vol. 98, no. 1, pp. 377-380. http://dx.doi.org/10.1653/024.098.0164
  » http://dx.doi.org/10.1653/024.098.0164
• PYÑERO, N.G., PEREIRA, F.F., GOMES-BORGES, F.L., ROSSONI, C., SILVA, A.S. and KASSAB, S.O., 2016. Multiplicar Tetrastichus howardi (Hymenoptera: Eulophidae) en la oruga de la seda afecta su biología? Acta Biologica Colombiana, vol. 21, no. 1, pp. 186-193. http://dx.doi.org/10.15446/abc.v21n1.47999
  » http://dx.doi.org/10.15446/abc.v21n1.47999
• REZAEI, M., KARIMZADEH, J. and SHAKARAMI, J., 2018. Size of interacting resource-host-parasitoid populations influences mass rearing of Cotesia vestalis. Journal of Entomological Research Society, vol. 20, no. 3, pp. 23-32.
• RODRIGUES, A., PEREIRA, F.F., BARBOSA, P.R.R., SILVA-TORRES, C.S.A. and TORRES, J.B., 2021. Parasitism behavior of Tetrastischus howardi (Hymenoptera: Eulophidae) on larvae and pupae of sugarcane borers. Journal of Insect Behavior, vol. 34, no. 3, pp. 1-11. http://dx.doi.org/10.1007/s10905-021-09770-4
  » http://dx.doi.org/10.1007/s10905-021-09770-4
• SAINI, A. and SHARMA, P.L., 2018. Functional response and mutual interference of Cotesia vestalis (Hymenoptera: Braconidae) on Plutella xylostella (Lepidoptera: Plutellidae). Journal of Entomological Science, vol. 53, no. 2, pp. 162-170. http://dx.doi.org/10.18474/JES17-36.1
  » http://dx.doi.org/10.18474/JES17-36.1
• SARFRAZ, M. and KEDDIE, B.A., 2005. Conserving the efficacy of insecticides against Plutella xylostella (L.) (Lepidoptera: plutellidae). Journal of Applied Entomology, vol. 129, no. 3, pp. 149-157. http://dx.doi.org/10.1111/j.1439-0418.2005.00930.x
  » http://dx.doi.org/10.1111/j.1439-0418.2005.00930.x
• SCHEINER, C., and MARTIN, E. A., 2020. Spatiotemporal changes in landscape crop composition differently affect density and seasonal variability of pests, parasitoids and biological pest control in cabbage. Agriculture, Ecosystems and Environment, vol. 301, pp. 107051. https://doi.org/10.1016/j.agee.2020.107051
  » https://doi.org/10.1016/j.agee.2020.107051
• SILVA, G.S., JAHNKE, S.M. and JOHNSON, N.F., 2020. Riparian forest fragments in rice fields under different management: differences on hymenopteran parasitoids diversity. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 80, no. 1, pp. 122-132. http://dx.doi.org/10.1590/1519-6984.194760 PMid:31066765.
  » http://dx.doi.org/10.1590/1519-6984.194760
• SILVA-TORRES, C.S.A., PONTES, I.V.A.F., TORRES, J.B. and BARROS, R., 2010. New records of natural enemies of Plutella xylostella (L) (Lepidoptera: Plutellidae) in Pernambuco, Brazil. Neotropical Entomology, vol. 39, no. 5, pp. 835-838. http://dx.doi.org/10.1590/S1519-566X2010000500028 PMid:21120399.
  » http://dx.doi.org/10.1590/S1519-566X2010000500028
• TIAGO, E.F., 2018. Biologia comparada de Tetrastichus howardi, Trichospilus diatraeae e Palmistichus elaeisis (Hymenoptera: Eulophidae) em lagartas e pupas de Plutella xylostella (Lepidoptera: Plutellidae) Dourados: Universidade Federal da Grande Dourados, 97 p. Tese de Doutorado em Entomologia e Conservação da Biodiversidade.
• VACARI, A.M., BORTOLI, S.A. and TORRES, J.B., 2012. Relationship between predation by Podisus nigrispinus and developmental phase and density of its prey, Plutella xylostella. Entomologia Experimentalis et Applicata, vol. 145, no. 1, pp. 30-37. http://dx.doi.org/10.1111/j.1570-7458.2012.01310.x
  » http://dx.doi.org/10.1111/j.1570-7458.2012.01310.x
• VAN-LOON, J.J.A., WANG, C.Z., NIELSEN, J.K., GOLS, R. and QIU, Y.T., 2002. Flavonoids from cabbage are feeding stimulants for diamondback moth larvae additional to glucosinolates: chemoreception and behaviour. Entomologia Experimentalis et Applicata, vol. 104, no. 1, pp. 27-34. http://dx.doi.org/10.1046/j.1570-7458.2002.00987.x
  » http://dx.doi.org/10.1046/j.1570-7458.2002.00987.x
• VARGAS, E. L., PEREIRA, F. F., CALADO, V. R. F., GLAESER, D. F., RODRIGUES B. A. C., and SILVA, N.V., 2013. Densidade de fêmeas de Trichospilus diatraeae (Hymenoptera: Eulophidae) em pupas de Diatraea saccharalis (Lepidoptera: Crambidae). Sitientibus série Ciências Biológicas, vol. 13, pp. 1-7. https://doi.org/10.13102/scb227
  » https://doi.org/10.13102/scb227
• VARGAS, E.L., PEREIRA, F.F. and TAVARES, M.T., 2011. Record of Tetrastichus howardi (Hymenoptera: Eulophidae) parasitizing Diatraea sp. (Lepidoptera: Crambidae) in sugarcane crop in Brazil. Entomotrópica, vol. 26, no. 3, pp. 143-146.

Publication Dates

• Publication in this collection
  07 Oct 2022
• Date of issue
  2022

History

• Received
  25 Apr 2022
• Accepted
  25 Aug 2022