Revista de Protección Vegetal Vol. 37, No. 1, January-April, 2022, ISSN: 2224-4697
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CU-ID: https://cu-id.com/2247/v37n1e06
Original Article

Suitability of Ephestia kuehniella (Lepidoptera: Pyralidae) and Aleurodicus cocois (Hemiptera: Aleyrodidae) as food sources for Ceraeochrysa cornuta (Neuroptera: Chrysopidae)

Idoneidad de Ephestia kuehniella (Lepidoptera: Pyralidae) y Aleurodicus cocois (Hemiptera: Aleyrodidae) como fuentes de alimento para Ceraeochrysa cornuta (Neuroptera: Chrysopidae)

iDEliana Maria dos Passos1Empresa de Desenvolvimento Agropecuário de Sergipe (Emdagro), Av. Dr. Carlos Rodrigues da Cruz, s/n, 49080-190, Nossa Sra. do Socorro - SE, Brazil. *✉:bisologa@hotmail.com

iDAdenir Vieira Teodoro2Embrapa Tabuleiros Costeiros, Av. Beira mar, 3250, 49025-040, Aracaju - SE, Brazil. ,3Programa de Pós-Graduação em Agroecologia, Universidade Estadual do Maranhão, Cidade Universitária Paulo VI, s/n, 65054-970, São Luís - MA, Brazil.

iDDanúbia Maria da Costa3Programa de Pós-Graduação em Agroecologia, Universidade Estadual do Maranhão, Cidade Universitária Paulo VI, s/n, 65054-970, São Luís - MA, Brazil.

iDLívia de Almeida Lima4Departamento de Engenharia Florestal da Universidade Federal de Sergipe, Av. Marechal Rondon, s/n, 49100-000, São Cristóvão - SE, Brazil

iDMarcelo da Costa Mendonça2Embrapa Tabuleiros Costeiros, Av. Beira mar, 3250, 49025-040, Aracaju - SE, Brazil. ,5Programa de Pós-Graduação em Biotecnologia Industrial, Universidade Tiradentes, Av. Murilo Dantas, 300, 49032-490, Aracaju - SE, Brazil.


1Empresa de Desenvolvimento Agropecuário de Sergipe (Emdagro), Av. Dr. Carlos Rodrigues da Cruz, s/n, 49080-190, Nossa Sra. do Socorro - SE, Brazil.

2Embrapa Tabuleiros Costeiros, Av. Beira mar, 3250, 49025-040, Aracaju - SE, Brazil.

3Programa de Pós-Graduação em Agroecologia, Universidade Estadual do Maranhão, Cidade Universitária Paulo VI, s/n, 65054-970, São Luís - MA, Brazil.

4Departamento de Engenharia Florestal da Universidade Federal de Sergipe, Av. Marechal Rondon, s/n, 49100-000, São Cristóvão - SE, Brazil

5Programa de Pós-Graduação em Biotecnologia Industrial, Universidade Tiradentes, Av. Murilo Dantas, 300, 49032-490, Aracaju - SE, Brazil.

 

*Correspondence to: Eliana Maria dos Passos, E-mail: bisologa@hotmail.com

ABSTRACT

This study aimed to compare the suitability of Ephestia kuehniella (Zeller, 1879) and Aleurodicus cocois (Curtis, 1846) as food sources for Ceraeochrysa cornuta (Navás, 1925) based on the assessment of the development and reproductive parameters of this predator. For this, E. kuehniella eggs or all developmental stages of A. cocois were used as prey and the effects were evaluated on developmental time, survival, viability, longevity, and fecundity of C. cornuta. Ceraeochrysa cornuta completed its development cycle from larvae to adult in 22 d or in 27 d when it preyed on E. kuehniella or on A. cocois, respectively. This could be explained by longer larval instars for C. cornuta feeding on A. cocois. The larval survival was higher when C. cornuta larvae fed on E. kuehniella than when it fed on A. cocois, increasing progressively from 79.82 % in the first to 97.56 % in the third instar. Although the diets did not influence female longevity, oviposition period and egg viability, the total number of eggs laid per female of C. cornuta was higher when their larvae fed on A. cocois. The results indicate that both E. kuehniella eggs and A. cocois developmental stages are suitable prey for rearing C. cornuta. In addition, this predator showed an outstanding potential for controlling A. cocois.

Keywords: 
alternative prey, cashew whitefly, fecundity, lacewing, natural enemies, survival larval
RESUMEN

Este estudio tuvo como objetivo comparar la idoneidad de Ephestia kuehniella (Zeller, 1879) y Aleurodicus cocois (Curtis, 1846) como fuentes de alimento para Ceraeochrysa cornuta (Navás, 1925), sobre la base de la evaluación de sus parámetros reproductivos y de desarrollo. Para esto, se utilizaron como presa huevos de E. kuehniella o todas las etapas de desarrollo de A. cocois y se evaluaron sus efectos sobre el tiempo de desarrollo, sobrevivencia, viabilidad, longevidad y fecundidad de este depredador. C. cornuta completó su ciclo de desarrollo de larva a adulto en 22 días y en 27 días cuando se alimenta de E. kuehniella y A. cocois, respectivamente. La supervivencia del período larvario fue mayor cuando las larvas de C. cornuta se alimentaron de E. kuehniella en comparación con A. cocois como fuente de alimento, que aumentó progresivamente del 79,82 % en el primero al 97,56 % en el tercer estadio. Aunque las dietas no influyeron en la longevidad de las hembras de esta especie, el periodo de oviposición y la viabilidad de los huevos, así como el número total de huevos puestos por hembra fueron mayores cuando sus larvas se alimentaron de A. cocois. Los resultados indican que tanto los huevos de E. kuehniella como los estados inmaduros de A. cocois son presas adecuadas para la cría de C. cornuta. Adicionalmente, este depredador podría considerarse como un agente de control biológico promisorio para el manejo de A. cocois.

Palabras clave: 
presa alternativa, mosca blanca del anacardo, fecundidad, crisopideo, enemigo natural, supervivencia larval

Received: 23/11/2021; Accepted: 4/2/2022

Declaration of conflict of interest: The authors declare that they have no conflict of interest.

Author Contributions: Eliana Maria dos Passos: Conceptualization, Investigation, Methodology, Writing original draft and writhing review. Adenir Vieira Teodoro: Data curation, Writing original draft. Danúbia Maria da Costa: Writing original draft and writing review. Lívia de Almeida Lima: Investigation. Marcelo da Costa Mendonça: Writing review.

CONTENT

INTRODUCTION

 

Lacewings (Neuroptera: Chrysopidae) are generalist predators considered important biological control agents due to their high reproductive potential, search capacity, ability to explore several habitats and a wide variety of prey (11. Albuquerque GS, Tauber CA, Tauber MJ. Chrysoperla externa and Ceraeochrysa spp.: potential for biological control in the New World tropics and subtropics. In: McEwen PK, New TR, Whittington AE (eds). Lacewings in the crop environment, 1th ed., pp 408-423. Cambridge University Press, 2001., 22. Carvalho CF, Souza B. Métodos de criação e produção de crisopídeos. In VHP Bueno (ed). Controle biológico de pragas: produção massal e controle de qualidade, 2th ed., pp. 77-115. Brasil, Editora UFLA - Universidade Federal de Lavras, 2009.). Ceraeochrysa (Adams, 1982) is one of the most diverse Chrysopidae genera, distributed from Canada to Argentina, but mainly in the Neotropical region, inhabiting open forests and crops (33. Adams PA. Ceraeochrysa, a new genus of Chrysopinae (Neuroptera) (Studies in New World Chrysopidae, Part II). Neuroptera Intl. 1982; 2: 69-75., 44. Brooks SJ, Barnard, PC. The green lacewings of the world: a generic review (Neuroptera: Chrysopidae). Bull Br Mu Nat Hist Entomol. 1990; 59: 117-286., 55. Tauber CA, De León T, Penny N, Tauber MJ. The genus Ceraeochrysa (Neuroptera: Chrysopidae) of America north of Mexico: larvae, adults, and comparative biology. Ann Entomol Soc Am. 2000; 93:1195-1221. DOI: 10.1603/0013-8746(2000)093[1195:TGCNCO]2.0.CO;2 , 66. Freitas S, Penny ND, Adams PA. A revision of the New world genus Ceraeochrysa (Neuroptera: Chrysopidae). Proc Calif Acad Sci. 2009; 60: 503-610. ). The species Ceraeochrysa cornuta (Navás, 1925), synonymous with C. caligata (Banks, 1945) (Neuroptera: Chrysopidae), has proved to be an important biological control agent of agricultural pests (77. Souza JC, Galvão JR, Maia WJMS, Alves Filho PPC, Barbosa AVC. Resposta funcional e capacidade predatória da fase larval de Ceraeochrysa caligata alimentada com Brevicoryne brassicae. Rev Verde. 2015;10 (3): 61-65. DOI:10.18378/rvads.v10i3.3308 , 88. Jumbo LOV, Teodoro AV, Rêgo AS, Haddi K, Galvão AS, Oliveira, EE. The lacewing Ceraeochrysa caligata as a potential biological agent for controlling the red palm mite Raoiella indica. PeerJ. 2019; 7:e7123. DOI:10.7717/peerj.7123 , 99. Palomares-Pérez MPP, Contreras-Bermúdez Y, Grifaldo-Alcántara PF, García-García R E, Bravo-Núñez M, Arredondo-Bernal, HC. Predation capacity and larval development of Ceraeochrysa claveri (Neuroptera: Chrysopidae) fed with Raoiella indica (Acari: Tenuipalpidae). Revista De La Facultad De Ciencias Agrarias UNCuyo 2021; 53(2): 225-231. DOI:10.48162/rev.39.055 ).

The whitefly Aleurodicus cocois (Curtis, 1846) (Hemiptera: Aleyrodidae) is a key pest of the cashew crop in Brazil. The presence of this pest affects negatively plant development by the suction of sap and nutrients and photosynthesis impairment due to the development of sooty mold on the leaves (1010.Byrne DN, Bellows TS. Whitefly biology. Annu Rev Entomol. 1991; 36: 431-457. DOI:10.1146/annurev.en.36.010191.002243., 1111. Mesquita ALM, Braga Sobrinho R. Pragas do cajueiro. In: Araújo, JPP de (ed). Agronegócio caju: práticas e inovações, pp. 195-215. Brasil, Embrapa, 2013., 1212.Goiana ESS, Dias-Pini NS, Gomes Filho AAH, Vidal Neto FC, Barros LM, Pastori PL, et al. Preferência de clones de cajueiro-anão à mosca-branca e distribuição temporal da praga e seu predador. Brasil, Embrapa Agroindústria Tropical: Boletim de pesquisa e desenvolvimento 123, 2017. http://ainfo.cnptia.embrapa.br/digital/bitstream/item/213060/1/BP-123.pdf ).

Recently, in the northeastern Sergipe state, Brazil, C. cornuta immature stages were found on cashew leaves infested with colonies of A. cocois. Reports of natural predation of A. cocois by other lacewing species, such as Ceraeochrysa sp. and Chrysoperla externa (Hagen, 1861) (Neuroptera: Chrysopidae), on cashew leaves in the northeastern state of Ceará, Brazil (1212.Goiana ESS, Dias-Pini NS, Gomes Filho AAH, Vidal Neto FC, Barros LM, Pastori PL, et al. Preferência de clones de cajueiro-anão à mosca-branca e distribuição temporal da praga e seu predador. Brasil, Embrapa Agroindústria Tropical: Boletim de pesquisa e desenvolvimento 123, 2017. http://ainfo.cnptia.embrapa.br/digital/bitstream/item/213060/1/BP-123.pdf ) suggest these predators as potential biological control agents for this whitefly. Nevertheless, no studies have addressed the importance of A. cocois as food source for C. cornuta.

Eggs of Ephestia (Anagasta) kuehniella (Zeller, 1879) (Lepidoptera: Pyralidae) have been predominantly used as standard food source in biological studies of Chrysoperla, Ceraeochrysa and Leucochrysa species (McLachlan, 1868) (Neuroptera: Chrysopidae), resulting in an adequate development of these predators (1313.Scholtens BG, Solis MA. Annotated check list of the Pyraloidea (Lepidoptera) of America North of Mexico. ZooKeys. 2015; 535: 1-36. DOI: 10.3897/zookeys.535.6086., 1414.Tapajós SJ, Lira R, Silva-Torres CSA, Torres JB, Coitinho RLCB. Suitability of two exotic mealybug species as prey to indigenous lacewing species. Biol Control. 2016; 96: 93-100. DOI: 10.1016/j.biocontrol.2016.02.005 , 1515.Costa SS, Broglio SM, Dias-Pini NS, Santos DS, Santos JM, Duque FJ, et al. Developmental biology and functional responses of Leucochrysa (Nodita) azevedoi fed with different prey. Biocontrol Sci Technol. 2020; 30 (1): 42-50. DOI: 10.1080/09583157.2019.1687644 , 1616.Monteiro NV, Saraiva WVA, Dias NS, Maciel GPS, Vasconcelos JF, Duarte, et al. Aspectos biológicos de Chrysoperla externa visando ao controle biológico da mosca-branca-do-cajueiro. Brasil, Embrapa Agroindústria Tropical: Boletim de Pesquisa e Desenvolvimento 215, 2021. http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1130075 ).

Although studies about suitable food sources for the development and reproduction of C. cornuta are important to determine the predatory potential, the biological cycle of this lacewing was only evaluated on aphids and Spodoptera frugiperda eggs as food sources (Smith, 1797) (Lepidoptera: Noctuidae) (88. Jumbo LOV, Teodoro AV, Rêgo AS, Haddi K, Galvão AS, Oliveira, EE. The lacewing Ceraeochrysa caligata as a potential biological agent for controlling the red palm mite Raoiella indica. PeerJ. 2019; 7:e7123. DOI:10.7717/peerj.7123 , 1717.Nogueira P, Fernandes A, Dias I, Moreira D, Cruz I. Aspectos biológicos de Ceraeochrysa caligata (Banks) (Neuroptera: Chrysopidae) alimentada com ovos frescos de Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). In: Simpósio de Controle Biológico. Brasília, 2007,1p., 1818.Castro ALG, Cruz I, Da Silva I, Paula CDS, Leao ML, Ferreira TE, et al. Biologia de Ceraeochrysa caligata (Banks, 1945) (Neuroptera: Chrysopidae) Alimentada com Schizaphis graminum (Rondani) (Hemiptera: Aphididae). Cadernos de Agroecologia, [S.l.], v 4, n 1, dec 2009. ISSN 2236-7934. Disponível em: http://revistas.aba-agroecologia.org.br/index.php/cad/article/view/4306. Acessado em: 05 de novembro de 2021). This gap of knowledge about potential food sources and their effects on biological parameters of C. cornuta may hamper significant advances regarding its applicability for agricultural pest control.

Therefore, we aimed to compare the suitability of E. kuehniella and A. cocois as food sources for C. cornuta, based on assessment of the development and reproductive parameters of this predator.

MATERIAL AND METHODS

 

Colonies of Ceraeochrysa cornuta

 

The rearing of C. cornuta was established from specimens collected in citrus plantations in the northeastern state of Sergipe (Boquim municipality (11°08'19''S 37° 36'21''W). The specimens were identified by Francisco José Sosa Duque from Federal Rural University of the Amazon. The lacewings used in all experiments had been reared under laboratory conditions (temperature = 26 ± 2 ºC; relative humidity (RH) = 55 ± 10 % and natural photoperiod) for at least five generations. Briefly, adults were kept in PVC tube cages (300 x 300 mm) sitting on plastic plates internally lined with white paper sheets for oviposition. The top of the cage contained a ‘voil’ fabric wrapped by a rubber band. The adults were supplied with water and an artificial diet (i. e., honey and brewer's yeast, 1:1) as food every third day. The paper sheets containing the eggs were transferred to plastic pots in which the newly hatched larvae were fed with E. kuehniella eggs as food source until complete development and formation of the pupae. The eggs of E. kuehniella were obtained from the company Ecotrix biodefensivos.

Developmental time and larval survival of C. cornuta in relation to prey source

 

Eggs of C. cornuta were individually transferred to Elisa plates to avoid larval cannibalism. Subsequently, 137 newly hatched C. cornuta larvae were individually placed in plastic Petri dishes (5.5 cm Ø) containing E. kuehniella eggs ad libitum. Oiti (Licania tomentosa Benth) leaves, which are hairy and waxy, were added to each Petri dish to help lacewings to form the cocoon and protect the pupae. Also, 114 newly hatched C. cornuta were individually transferred to Petri dishes (as described above) containing field-collected cashew leaves heavily infested with eggs, nymphs, and adults of A. cocois. Food sources were daily replaced. The development of each larva, larval survival and pupal viability were daily recorded. The instar change was verified by the presence of exuvias and arrows in the tubers. This experiment was performed under laboratory conditions (temperature = 26 ± 2ºC; relative humidity (RH) = 55 ± 10 % and natural photoperiod).

Longevity and reproduction of C. cornuta in relation to prey source

 

After the emergence of adult predators with either prey sources (E. kuehniella or A. cocois), the sex ratio was determined and couples were separately kept in cylindrical PVC tube cages (200 x 200mm). These insects fed on artificial diet and water as previously described, which were replaced every two days. Altogether, 76 couples were randomly formed, however, only 13 couples previously fed on E. kuehniella and 7 couples previously fed on A. cocois remained due to either the absence of viable eggs or early death of females.

Female longevity was daily recorded and males were replaced whenever necessary. Eggs were daily collected, counted, registered, and placed in Elisa plates, and the number of eggs by female, hatching, and egg viability were determined. This experiment was conducted under laboratory conditions (temperature = 28 ± 2ºC; relative humidity (RH) = 50 ± 10 % and natural photoperiod).

Data analysis

 

The data from each experiment were compared by the t-tests (P < 0.05) [Proc TTEST, Method: pooled or satterthwaite, considering the equality of variances] using the SAS software (1919. SAS S, Guide U. SAS Institute Inc. USA; Carry, NC, 2008.). The developmental time of each larval instar, larval and pupal periods, female longevity, oviposition and total number of eggs laid per female of C. cornuta feeding either on E. kuehniella or A. cocois were compared. In addition, the percentage of surviving larvae, the pupal and egg viabilities were compared. The sex ratio was determined by the ratio between the number of females and the total number of adults (males and females) (2020. Silveira Neto S, Nakano O, Bardin D, Villa Nova NA. Manual de ecologia dos insetos. Brasil; Agronômica Ceres, 1976.).

RESULTS AND DISCUSSION

 

Ceraeochrysa cornuta completed its cycle from larva to adult in 27 d when the prey was A. cocois and 22 d when it fed on E. kuehniella eggs. The development time in each larval instar lasted longer when C. cornuta fed on A. cocois, resulting in an increase of 4.76 d in the larval period (t 1. 204 = -21.81, P < 0.0001). Pupal period also lasted longer when C. cornuta fed on A. cocois (t 1. 197 = -2.68, P = 0.0079) (Table 1).

Table 1.  Developmental time of larval instars, and total larval and pupal periods (means ± SE) of Ceraeochrysa cornuta fed on Aleurodicus cocois developmental stages and Ephestia kuehniella eggs. / Tiempo de desarrollo de los estadios larvarios y períodos totales de larvas y pupas (medias ± SE) de Ceraeochrysa cornuta alimentada con estadios de desarrollo de Aleurodicus cocois y huevos de Ephestia kuehniella.
Food source Average time (days)
1st instar 2nd instar 3rd instar Total larvae Pupae
E. kuehniella 3.24 ± 0.05 3.21 ± 0.04 4.99 ± 0.06 11.36 ± 0.06 10.64 ± 0.07
A. cocois 4.40 ± 0.11 4.86 ± 0.15 7.24 ± 0.14 16.12 ± 0.21 10.95 ± 0.09
P 0.0001 0.0001 0.0001 0.0001 0.0079

The survival of larval period, however, was higher for C. cornuta fed on E. kuehniella than on A. cocois as food source (t 1. 249 = 4.85, P < 0.0001), increasing progressively from 79.82 % in the first to 97.56 % in the third instar (Table 2).

Table 2.  Survival (%) of larval instars, total larval period and pupal viability (means ± SE) of Ceraeochrysa cornuta feeding on Aleurodicus cocois developmental stages and Ephestia kuehniella eggs. / Supervivencia (%) de estadios larvarios, período larvario total y viabilidad de pupas (medias ± SE) de Ceraeochrysa cornuta alimentados con estadios de desarrollo de Aleurodicus cocois y huevos de Ephestia kuehniella.
Food source Survival Viability
1st instar 2nd instar 3rd instar Total larvae Pupae
E. kuehniella 98.54 ± 1.03 99.26 ± 0.74 95.52 ± 1.80 93.43 ± 2.12 96.09 ± 1.72
A. cocois 79.82 ± 3.77 90.11 ± 3.15 97.56 ± 1.71 70.17 ± 4.30 93.75 ± 2.72
P 0.0001 0.0056 0.4121 0.0001 0.4680

The developmental periods of predators may be shortened when they feed on high quality preys (2121.Barbosa PRR, Oliveira MD, Giorgi JA, Silva-Torres CSA, Torres JB. Predatory behavior and life history of Tenuisvalvae notata (Coleoptera: Coccinellidae) under variable prey availability conditions. 2014; 97(3): 26-34. DOI:10.1653/024.097.0304 ). Lepidoptera eggs have high nutritional content and foster shorter larval cycles in Ceraeochrysa spp. (1414.Tapajós SJ, Lira R, Silva-Torres CSA, Torres JB, Coitinho RLCB. Suitability of two exotic mealybug species as prey to indigenous lacewing species. Biol Control. 2016; 96: 93-100. DOI: 10.1016/j.biocontrol.2016.02.005 , 2222.Almeida MF, Barros R, Gondim Júnior MGC, Freitas S, Bezerra AL. Biologia de Ceraeochrysa claveri Navás (Neuroptera: Chrysopidae) predando Plutella xylostella (L.) (Lepidoptera: Plutellidae). Cienc Rural. 2009; 39: 313-318. DOI: 10.1590/S0103-84782009000200001., 2323.Oliveira RO, Barbosa VO, Vieira DL, Oliveira FQ, Batista JL, Brito CH. Development and reproduction of Ceraeochrysa cubana (Neuroptera: Chrysopidae) fed with Aleurocanthus woglumi (Hemiptera: Aleyrodidae). Semina: Ciênc Agrár 2016; 37: 17-24. DOI: 10.5433/1679-0359.2016v37n1p17.), including in C. cornuta (1717.Nogueira P, Fernandes A, Dias I, Moreira D, Cruz I. Aspectos biológicos de Ceraeochrysa caligata (Banks) (Neuroptera: Chrysopidae) alimentada com ovos frescos de Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae). In: Simpósio de Controle Biológico. Brasília, 2007,1p., 1818.Castro ALG, Cruz I, Da Silva I, Paula CDS, Leao ML, Ferreira TE, et al. Biologia de Ceraeochrysa caligata (Banks, 1945) (Neuroptera: Chrysopidae) Alimentada com Schizaphis graminum (Rondani) (Hemiptera: Aphididae). Cadernos de Agroecologia, [S.l.], v 4, n 1, dec 2009. ISSN 2236-7934. Disponível em: http://revistas.aba-agroecologia.org.br/index.php/cad/article/view/4306. Acessado em: 05 de novembro de 2021), which is in line with the results of the present study. On the other hand, the development from larva to adult of C. cornuta feeding on A. cocois was accompanied by high larval survival and pupal viability, indicating that this whitefly was also an appropriate prey. As other lacewing species, C. externa also completes its life cycle when it feeds on A. cocois, though with a very low larval survival (35 %) (1616.Monteiro NV, Saraiva WVA, Dias NS, Maciel GPS, Vasconcelos JF, Duarte, et al. Aspectos biológicos de Chrysoperla externa visando ao controle biológico da mosca-branca-do-cajueiro. Brasil, Embrapa Agroindústria Tropical: Boletim de Pesquisa e Desenvolvimento 215, 2021. http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1130075 ).

As with other holometabolic insects, the larval developmental time of C. cornuta is associated with the type of food, while the survival of each instar is influenced by food availability. In fact, the survival of the larval stage increased progressively with the instars when A. cocois was offered as food source. This is because prey consumption by lacewing larvae rely on their search ability and prey handling. For example, the ability of C. cornuta to feed upon Raoiella indica (Hirst,1924) (Acari: Tenuipalpidae) increased with the larval development of the predator (88. Jumbo LOV, Teodoro AV, Rêgo AS, Haddi K, Galvão AS, Oliveira, EE. The lacewing Ceraeochrysa caligata as a potential biological agent for controlling the red palm mite Raoiella indica. PeerJ. 2019; 7:e7123. DOI:10.7717/peerj.7123 ). Eggs of E. kuehniella, on the other hand, are immobile and do not exhibit antipredator behavior, which results in little effort and less energy lost by predators. The pupal viability was not influenced by the diets and the resulting sex ratios for C. cornuta feeding on A. cocois and on E. kuehniella were 0.46 and 0.5, respectively. Adult emergence and the sex ratio are useful parameters to evaluate the suitability of food sources for natural enemies. For this end, both A. cocois and E. kuehniella are suitable preys to C. cornuta emergence. Also, the sex ratios of C. cornuta feeding on both food sources approached that of Ceraeochrysa claveri (Navás, 1911) (0.42) (99. Palomares-Pérez MPP, Contreras-Bermúdez Y, Grifaldo-Alcántara PF, García-García R E, Bravo-Núñez M, Arredondo-Bernal, HC. Predation capacity and larval development of Ceraeochrysa claveri (Neuroptera: Chrysopidae) fed with Raoiella indica (Acari: Tenuipalpidae). Revista De La Facultad De Ciencias Agrarias UNCuyo 2021; 53(2): 225-231. DOI:10.48162/rev.39.055 ) and the ‘ideal’ (1 male:1 female) for sexually reproducing insects.

The diets also did not influence the longevity of females, oviposition period and viability of eggs. However, the total number of eggs laid by female was higher for C. cornuta feeding on A. cocois than on E. kuehniella (t 1, 18 = -2.54, P = 0.0405) (Table 3). In addition, C. cornuta larvae feeding on A. cocois laid 823.57 ± 146.58 eggs per female. This high oscillation in the number of eggs laid possibly reflect the nutritional variation of the different biological stages of the whitefly.

Table 3.  Period of oviposition, female longevity, total number of eggs laid per female (means ± SE) and egg viability (%) (means ± SE) of Ceraeochrysa cornuta feeding on Aleurodicus cocois developmental stages and Ephestia kuehniella eggs. / Período de oviposición, longevidad de la hembra, número total de huevos puestos por hembra (media ± SE) y viabilidad del huevo (%) (media ± SE) de Ceraeochrysa cornuta alimentada con huevos de Aleurodicus cocois y Ephestia kuehniella
Food source Female longevity Oviposition Total number of eggs Egg viability
E. kuehniella 56.92 ± 3.41 43.23 ± 3.33 441.92 ± 31.79 52.45 ± 3.52
A. cocois 63.14 ± 6.61 51.71 ± 6.58 823.57 ± 146.58 57.19 ± 7.21
P 0.3643 0.2140 0.0405 0.5128

The oviposition of C. cornuta feeding on E. kuehniella (441.92 ± 31.79) are consistent with that found in other species of Ceraeochrysa. For instance, C. claveri and Ceraeochrysa cubana (Hagen,1861) laid 467.7 ± 0.52 and 476.2 ± 3.21 eggs, respectively, when they fed on eggs from other lepidopteran species (2222.Almeida MF, Barros R, Gondim Júnior MGC, Freitas S, Bezerra AL. Biologia de Ceraeochrysa claveri Navás (Neuroptera: Chrysopidae) predando Plutella xylostella (L.) (Lepidoptera: Plutellidae). Cienc Rural. 2009; 39: 313-318. DOI: 10.1590/S0103-84782009000200001., 2323.Oliveira RO, Barbosa VO, Vieira DL, Oliveira FQ, Batista JL, Brito CH. Development and reproduction of Ceraeochrysa cubana (Neuroptera: Chrysopidae) fed with Aleurocanthus woglumi (Hemiptera: Aleyrodidae). Semina: Ciênc Agrár 2016; 37: 17-24. DOI: 10.5433/1679-0359.2016v37n1p17.).

Other authors also found an even higher oviposition (1,629.4 ± 200.46) of Ceraeochrysa everes (Banks, 1920) feeding on eggs of E. kuehniella (1414.Tapajós SJ, Lira R, Silva-Torres CSA, Torres JB, Coitinho RLCB. Suitability of two exotic mealybug species as prey to indigenous lacewing species. Biol Control. 2016; 96: 93-100. DOI: 10.1016/j.biocontrol.2016.02.005 ). The oviposition difference between C. cornuta and C. everes may be related to differential species-specific capacities, as well as the quality of food offered to the prey E. kuehniella, which determines eggs nutrition contents. In this regard, changes in diets provided to E. kuehniella influenced the developmental time of the larval and pupal stages, sex ratio and pupal viability of C. cubana (2424.Nunes G S, Silva ITFA, Barbosa VO, Dantas TAV, Oliveira R, Batista JL. Influência da alimentação de Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) no desenvolvimento de Ceraeochrysa cubana Hagen (Neuroptera: Chrysopidae). EntomoBrasilis. 2017; 10 (1): 14-18. DOI: 10.12741/ebrasilis.v10i1.641 ).

The food consumed in the larval stage influences oviposition capacity of the predator, which in turn influences predatory success. Larval diets significantly influence ovarian development as oocyte development varies with pupal size from larvae treated with different nutritional diets (2525.Al Baki MA, Lee DW, Jung JK, Kim Y. Insulin signaling mediates previtellogenic development and enhances juvenile hormone-mediated vitellogenesis in a lepidopteran insect, Maruca vitrata. BMC Dev Biol 2019; 19: 1-14. https://doi.org/10.1186/s12861-019-0194-8 ). In this sense, it is noteworthy the high number of eggs laid per female when its larvae fed on A. cocois.

Aleurodicus cocois proved to be appropriate for the development of larval and subsequent stages of C. cornuta, which emphasizes the potential of this predator as a biological control agent of A. cocois. In addition, the whitefly could be used as the main or supplementary diet for mass rearing C. cornuta. Similarly, other neotropical lacewing species such as C. externa and C. everes are promising biological control agents against two exotic mealybugs recently introduced in Brazil, Ferrisia dasylirii (Cockerell) and Pseudococcus jackbeardsleyi (Gimpel & Miller) (Hemiptera: Pseudococcidae) (1414.Tapajós SJ, Lira R, Silva-Torres CSA, Torres JB, Coitinho RLCB. Suitability of two exotic mealybug species as prey to indigenous lacewing species. Biol Control. 2016; 96: 93-100. DOI: 10.1016/j.biocontrol.2016.02.005 ).

The lacewing C. cornuta also proved to be suitable for mass rearing due to its relatively short developmental time, high survival larval and pupal viability, and good reproductive potential when it fed either on E. kuehniella or A. cocois. These traits are important in the production of a biological control agent. In addition, although the sex ratio of C. cornuta feeding on A. cocois indicates a greater number of males, it may favor fertility by increasing the possibility of female encounters with virgin males, which would result in increased egg production in the field or in the laboratory (2626.Medina-Pereyra P, Ordano M, Reguilón C, Salvatore AR, Acosta C, Risso L. El papel de la densidad y la proporción sexual de adultos en la fecundidad de Diatraea saccharalis (Lepidoptera: Crambidae) en jaulas de cría masiva. Revista de la Sociedad Entomológica Argentina 2016; 75(3-4): 165-171.).

CONCLUSION

 

Our results indicate that eggs of E. kuehniella are suitable for the development and reproduction of C. cornuta, which corroborates the widespread use of this alternative prey for the mass rearing of lacewings. Also, different biological stages of the whitefly A. cocois proved to be adequate for the development and reproduction of C. cornuta, indicating its potential as a biological control agent of this pest. This whitefly can also be used either as a main or as a supplementary food source for mass rearing C. cornuta.

ACKNOWLEDGEMENTS

 

We are grateful to Francisco José Sosa Duque from the Universidade Federal Rural da Amazônia (UFRA) for identifying the lacewing species.

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