Palmistichus elaeisis (Hymenoptera: Eulophidae) rearing in Tenebrio molitor (Coleoptera: Tenebrionidae) submitted to different diets*

Palmistichus elaeisis (Hymenoptera: Eulophidae) criado em Tenebrio molitor (Coleoptera: Tenebrionidae) submetido a diferentes dietas

ABSTRACT

The ecological, physiological and behavioral processes of insects are linked to their nutrition. The diet of host insects can modify the development of natural enemies and affect their reproductive performance. The objective of this work was to evaluate the development and reproduction of Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) parasitizing pupae of Tenebrio molitor Linnaeus, 1785 (Coleoptera: Tenebrionidae) rearing in different diets. Pupae of T. molitor generated in six different diets (wheat bran, cornmeal, pelleted feed for rabbits, and bran, pelleted or crushed feed for laying hens) were individually placed in plastic pots and exposed to parasitism by six females of P. elaeisis during 72 h. The biological variables of P. elaeisis were observed and bromatological analyses were performed with pupae of T. molitor and the diets used. The percentage of parasitism and emergency was 100% in all treatments. There was no difference in the life cycle, the offspring number and longevity of the parasitoid. Pupae of T. molitor obtained from larvae fed with cornmeal were smaller and generated P. elaeisis offspring with low sex ratio and shorter length of the tibia. The T. molitor diet based on cornmeal was not suitable for the reproduction of P. elaeisis in the laboratory.

KEYWORDS
alternative host; biological control; parasitism

RESUMO

Parte dos processos ecológicos, fisiológicos e comportamentais dos insetos está ligada à sua nutrição. O tipo de dieta pode influenciar o desenvolvimento do inimigo natural e afetar seu desempenho reprodutivo. Objetivou-se neste trabalho avaliar o desenvolvimento e reprodução de Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) parasitando pupas de Tenebrio molitor Linnaeus, 1785 (Coleoptera: Tenebrionidae) criadas em diferentes dietas. Pupas de T. molitor geradas em seis diferentes dietas (farelo de trigo, fubá de milho, ração peletizada para coelhos, ração para aves poedeiras: farelada, peletizada e triturada) foram individualizadas em potes plásticos e expostas ao parasitismo por seis fêmeas de P. elaeisis durante 72 h. Foram observadas as variáveis biológicas de P. elaeisis e realizadas análises bromatológicas com pupas de T. molitor e as dietas utilizadas. A porcentagem de parasitismo e emergência de P. elaeisis foi de 100% em todos os tratamentos. Não houve diferença no ciclo de vida, número da prole e longevidade do parasitoide. Pupas de T. molitor formadas com fubá de milho foram menores e geraram prole de P. elaeisis com menor razão sexual e menor comprimento da tíbia. A dieta para T. molitor à base de fubá de milho não foi adequada para a reprodução de P. elaeisis em laboratório.

PALAVRAS-CHAVE
hospedeiro alternativo; controle bioló- gico; parasitismo

INTRODUCTION

Parasitoids can control populations of insect pests and stand out as one of the main groups of natural enemies. Several species of parasitoids are efficient and have been studied to be used in applied biological control programs (CRUZ et al., 2017; MARTINS et al., 2019).

Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) is a promising natural enemy, parasitizing pupae of several defoliating caterpillars. It is a species of gregarious and generalist endoparasitoid with an important role in insect control in the forest sector (PEREIRA et al., 2008; 2010; CAMILO et al., 2016).

Palmistichus elaeisis can parasitize pupae from several alternative hosts (BITTENCOURT; BERTI FILHO, 1999; 2004; PEREIRA et al., 2009; ZANUNCIO et al., 2008; 2015; RODRÍGUEZ-DIMATÉ et al., 2016; MARTINS et al., 2019). The development of research to maximize its production in the laboratory and allow the development of applied biological control programs is important, but it is necessary to establish low-cost and easy-to-maintain methods that provide adequate nutrition to this species (PEREIRA et al., 2010).

Part of the ecological, physiological, and behavioral processes of insects is linked to their nutrition (VIEIRA et al., 2018). The diet of host insects can modify the development of natural enemies and affect their reproductive performance (LEMOS et al., 2003). Nutritional aspects can be qualitative and quantitative, when it comes to the nutrients that organisms need or when considering the proportion of food eaten, digested, and assimilated (PARRA, 2009).

Size, age, nutritional quality, mechanical resistance and immunological response to natural enemies’ aspects must be considered when selecting the alternative host (BRODEUR; BOIVIN, 2004; MARTINS et al., 2019).

Tenebrio molitor Linnaeus, 1785 (Coleoptera: Tenebrionidae) infests stored grains, especially flours. Its immature stages provide a practical, economical and nutritious way to feed various species in rearings, such as fish, reptiles, birds and small mammals (MYERS et al., 1999). Also, their larvae and pupae are commonly used in the laboratory as alternative prey/hosts for rearing natural enemies (OTUKA et al., 2006), including P. elaeisis (ZANUNCIO et al., 2008). The host T. molitor can be easily multiplied on a large scale and at low cost (OTUKA et al., 2006; PEREIRA et al., 2009).

The diet offered to T. molitor can influence its development (MORALES-RAMOS et al., 2011) and, possibly, the performance of parasitoids that develop in this species. The wheat bran-based diet is the most widely used for rearing T. molitor, but some bird breeders have used alternative diets, such as poultry feed (MENEZES et al., 2014).

The objective of this work was to evaluate the development and reproduction of P. elaeisis in pupae of T. molitor rearing in different diets.

MATERIAL AND METHODS

The study has been conducted in the Biological Control Laboratory (Laboratório de Controle Biológico, LCB) of the Universidade Federal dos Vales do Jequitinhonha e Mucuri, in Diamantina, Minas Gerais, Brazil, in an air-conditioned room, with temperature ranging between 24 and 26 °C, a relative humidity of 60 and 80% and photoperiod of 12 h. The parasitoid P. elaeisis was obtained from the rearing of LCB, where it was kept in 500 mL plastic pots with newly formed T. molitor pupae as an alternative host and honey droplets for adult feeding.

Tenebrio molitor eggs were transferred to six plastic trays (42 × 26 × 7 cm) containing different diets, constituting the following treatments: T1: wheat bran, T2: cornmeal, T3 pelleted feed for rabbits; and T4: bran, T5: pelleted or T6: crushed feed for laying hens. A slice of sugarcane stalk was added to the trays (Saccharum spp. L.), changed weekly to provide moisture to the larvae.

The experimental design was completely randomized, with six treatments and ten replicates. Each replicate consisted of a pupa of T. molitor from different diets. These pupae were individualized in 250 ml plastic pots and exposed to parasitism for 72 h by six females of P. elaeisis, without previous experience of oviposition and fed with a drop of honey. Percentages of parasitism and emergence, number of emerged individuals, life cycle and sex ratio were observed. The sex ratio was calculated using the formula: SR = (nº♀/nº♂ + nº♀).

A couple from each replicate was used, placed in a 14 × 2.2 cm test tube, capped with a cotton ball, and fed with a drop of honey to assess longevity. After death, individuals were submitted to the analysis of morphometric variables. The size of the head capsule was measured at the median height of the eyes. The body size was measured from the midline of the insect’s back, from the head to the abdominal end. Additionally, the length of the posterior tibia was obtained. A camera Optika OPTIKAM B5 attached to a stereoscope microscope with the software Optika Vision Lite 2.1 was used for these measurements.

Bromatological analyzes were carried out on the pupae of T. molitor from the different treatments, as well as on the diets used to feed the larvae. The moisture content was determined by the kiln drying method in air circulation (AOAC, 1997). The protein value was calculated from the total nitrogen content (JONES, 1941). Total lipids were determined by the Soxhlet extraction method, the fiber content by the enzymatic-gravimetric method, and the ash content by muffle incineration (AOAC, 1997). The carbohydrate content was calculated by the difference between 100 and the sum of the percentages of water, protein, total lipids, fiber and ash.

The data were subjected to the homoscedasticity and normality tests of the residues. If these assumptions were not met, data were transformed according to the distribution trend. Longevity data underwent logarithmic transformation (Log x) and data referring to the morphology of the male body by $$1/\sqrt{\left(x\right)}$$. Analysis of Variance (ANOVA) was performed and in the case of normality, the means were compared by the Tukey’s test (p ≤ 0.05). When the data were transformed and still did not meet the assumptions, the Kruskal-Wallis test (p ≤ 0.05) was used. In this case, comparisons were made between treatments, one-tailed and two-tailed. All tests were conducted with the R software, 0.99.903 version, package ExpDes.pt and Pgirmess (R CORE TEAM, 2016).

RESULTS AND DISCUSSION

The pupae biomass of the alternative host T. molitor, from the cornmeal-based diet, differed from the other treatments (p < 0.01; F = 6.348; df = 5) with the average of 89.31 ± 2.41 mg (Table 1). Once parasitized, the host becomes the only source of food and shelter for the endoparasitoid, and its size can influence the development, as well as the progeny of the natural enemy (VINSON; BARBOSA, 1987). In general, larger hosts contain more resources and can be considered to be of superior quality, as they can influence survival and size in the adult stage of the parasitoid (WANG et al., 2014).

Table 1
Body biomass of T. molitor pupae formed by different diets.

Treatments	Body biomass
Wheat bran	110.92 ± 4.99a
Cornmeal	89.31 ± 2.41b
Pelleted feed for rabbits	114.59 ± 5.24a
Bran feed for laying hens	118.40 ± 3.47a
Pelleted feed for laying hens	112.62 ± 6.96a
Crushed feed for laying hens	126.75 ± 4.22a

• * The means followed by the same letter in the column do not differ from each other by the Tukey’s test (p < 0.05).

Chemical composition information of diets provided to insects is indispensable for studies of nutrition. It is important to know the essential components to choose a diet. Although carbohydrates, proteins and fats are nonessential, the insect must ingest at least one of these compounds, for energy production and use in metabolic processes (BECK; REESE, 1976).

The diet used for T. molitor based on cornmeal has a lower protein content (p < 0.01; F = 24.766; df = 5) (6.77 ± 0.47%) and lipids (p < 0.01; F = 5.2782; df = 5) (13.63 ± 0.67%) and higher carbohydrate content (p < 0.01; F = 28.507; df = 5) (59.21 ± 0.82%) compared to other diets (Table 2).

Table 2
Percentage of centesimal composition of diets offered to T. molitor larvae.

Parameters	Treatments
	Wheat bran	Cornmeal	Pelleted feed for rabbits	Feed for laying hens
				Bran	Pelleted	Crushed
Humidity (%)	7.36 ± 0.37b	9.17 ± 0.37a	7.76 ± 0.03b	8.22 ± 0.19ab	2.90 ± 0.30c	7.70 ± 0.05b
Fiber (%)	12.92 ± 0.59de	10.43 ± 0.43e	17.68 ± 1.41bc	15.14 ± 1.59cd	21.47 ± 0.43b	27.93 ± 0.25a
Ashes (%)	4.25 ± 0.26cd	0.79 ± 0.08d	9.67 ± 0.51abc	8.66 ± 0.09bc	15.20 ± 2.78a	10.26 ± 0.85ab
Proteins (%)	13.32 ± 0.48a	6.77 ± 0.47b	13.83 ± 0.87a	13.39 ± 0.62a	12.86 ± 0.31a	13.81±0,36a
Lipids (%)	18.46 ± 2.51ab	13.63 ± 0.67b	22.37 ± 1.32ab	25.00 ± 3.13a	19.46 ± 3.37ab	28.09 ± 0.41a
Carbohydrate (%)	43.69 ± 2.53b	59.21 ± 0.82a	28.69 ± 3.06c	29.58 ± 2.89bc	28.11 ± 5.27c	12.21 ± 1.27d
Energy (Kcal/100 g)	394.14 ± 12.39a	386.57 ± 5.56ab	371.38 ± 4.98ab	396.94 ± 20.59a	338.99 ± 11.13b	356.91 ± 0.89ab

• * The means followed by the same letter in the column do not differ from each other by the Tukey’s test (p < 0.05).

The nutrient content in the T. molitor diets, such as casein, glucose, cholesterol, yeast, carbohydrates and proteins, is important for the insect’s development (URREJOLA et al., 2011). The lack of one or more of these nutrients can limit the growth and reproductive capacity of insects (BECK; REESE, 1976). The lower amount of protein present in cornmeal could have generated pupae with less biomass. However, even though carbohydrates are involved in energy-producing reaction cycles and are found in greater quantities in cornmeal, once it has not been assimilated (measured by the conversion efficiency of the ingested and digested food), it may not be nutritionally acceptable for the insect (LIPKE; FRAENKEL, 1956).

The nutritional analysis of T. molitor pupae showed no differences in moisture and carbohydrate levels (Table 3). Pupae formed with pelleted feed for laying hens showed a higher amount of fiber (p = 0.011; F = 4.99627; df = 5) (8.10 ± 0.15%), and those formed by pelleted feed for rabbits had a lower protein content (p < 0.01; F = 6.007; df = 5) (15.07 ± 0.58%) and greater amount of lipids (p = 0.020; F = 4.1393; df = 5) (11.83 ± 0.57%). The amount of energy supplied by T. molitor pupae varied from 149.47 ± 5.34 to 184.78 ± 8.77% (p = 0.017; F= 4.3792; df = 5).

Table 3
Percentage of the centesimal composition of pupae of T. molitor formed by the different diets.

Parameters	Treatments
	Wheat bran	Cornmeal	Pelleted feed for rabbits	Feed for laying hens
				Bran	Pelleted	Crushed
Humidity (%)	63.71 ± 0.32a	60.41 ± 1.46a	60.93 ± 0.44a	62.63 ± 0.84a	61.37 ± 0.74a	61.72 ± 0.53a
Fiber (%)	4.97 ± 0.92b	5.11 ± 0.50ab	7.47 ± 0.77ab	7.66 ± 0.79ab	8.10 ± 0.15a	7.72 ± 0.28ab
Ashes (%)	1.16 ± 0.02bc	1.21 ± 0.08abc	1.21 ± 0.07abc	1.14 ± 0.1c	1.47 ± 0.04ab	1.53 ± 0.07a
Proteins (%)	16.65 ± 0.55ab	18.41 ± 0.28a	15.07 ± 0.58b	17.34 ± 0.39a	16.74 ± 0.4ab	17.25 ± 0.42a
Lipids (%)	7.14 ± 0.61b	10.34 ± 0.56ab	11,83 ± 0.57a	7.04 ± 1.02b	7.69 ± 1.71ab	9.46 ± 0.73ab
Carbohydrate (%)	6.37 ± 0.58a	4.51 ± 1.17a	3.50 ± 0.39a	4.19 ± 1.35a	4.63 ± 1.53a	2.32 ± 0.48a
Energy (Kcal/100 g)	156.33 ± 4.92ab	184.78 ± 8.77a	180.75 ± 3.96ab	149.47 ± 5.34b	154.66 ± 10.27ab	163.43±6.41ab

• * The means followed by the same letter in the column do not differ from each other by the Tukey’s test (p < 0.05).

Inadequate nutrition of the host T. molitor causes limited use of resources by parasitoids. Parasitoids in inadequate hosts have a series of morphofunctional adaptations that regulate various physiological processes, such as longer development times and less body biomass. However, immature parasitoids can maximize the acquisition and use of nutrients inside the host and, thus, survive (PENNACCHIO; STRAND, 2006).

Parasitism and the emergence of P. elaeisis in pupae of T. molitor formed by different diets was 100% in all treatments (Table 4). The occurrence of host parasitism shows that the females of P. elaeisis evaluated the host as an adequate food source for feeding their offspring (VINSON; BARBOSA, 1987). Thus, the diet provided to the host did not interfere with these parameters. However, the host’s nutritional status can influence the size, sex ratio and survival of the parasitoid (VINSON; BARBOSA, 1987). For parasitism and emergence of pupae of T. molitor by P. elaeisis, rates of 100 and 90.76% have already been found (ZANUNCIO et al., 2008). For another parasitoid Trichospilus diatraeae Cherian & Margabandhu, 1942 (Hymenoptera: Eulophidae), 80% of parasitism was found in the same host exposed to parasitism by 20 females from 24 to 72 h (FAVERO et al., 2013). These data indicate that this host does not present nutritional or physiological barriers to the development of more than one species of endoparasitoid.

Table 4
Parasitism (%), emergence (%), μ ± standard error (EP) of the development cycle, offspring sex ratio (♀/♀+♂), female longevity and male longevity of progeny (in days) of P. elaeisis.

Parameters	Treatments
	Wheat bran	Cornmeal	Pelleted feed for rabbits	Feed for laying hens
				Bran	Pelleted	Crushed
Parasitism (%)	100	100	100	100	100	100
Emergence (%)	100	100	100	100	100	100
Cycle (days)1	25.90 ± 0.59a	26.20 ± 0.55a	28.00 ±0.45a	27.30 ± 0.91a	28.00 ± 0.61a	27.7 ± 0.75a
Offspring	66.00 ± 7.83a	61.56 ± 10.02a	49.70 ± 6.78a	56.10 ±7.31a	45.10 ± 4.21a	58.40 ± 10.51a
Sex Ratio2	0.94 ± 0.01a	0.81 ± 0.01b	0.91 ± 0.02a	0.92 ± 0.01a	0.89 ± 0.01ab	0.89 ± 0.03ab
Longevity ♂1	40.50 ± 2.65a	37.40 ± 3.76a	35.70 ± 3.24a	35.30 ± 3.79a	32.70 ± 3.87a	34.40 ± 3.72a
Longevity♀1	44.90 ± 3.45a	41.30 ± 4.48a	39.60 ± 3.71a	32.20 ± 3.45a	37.80 ± 2.53a	35.20 ± 3.08a

• * The means followed by the same letter in the line do not differ from each other by the Tukey’s test (p <0.05). * The means followed by the same letter in the line do not differ from each other by the Kruskal-Wallis test (p < 0.05).

The duration of the life cycle of P. elaeisis in pupae of T. molitor in the six treatments did not present significant differences, ranging from 26 to 28 days (p = 0.1105; F = 1.8962; df = 5) (Table 4). The duration of the immature stages of this parasitoid in pupae of Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae), Diatraea saccharalis (Fabricius, 1794), (Lepidoptera: Crambidae), Heliothis virescens (Fabricius, 1781), Spodoptera frugiperda (J.E. Smith, 1797) (both Lepidoptera: Noctuidae), Thyrinteina arnobia (Stoll, 1782) (Lepidoptera: Geometridae) was 18,9; 19,5; 22; 19,7 and 20,2 days, respectively (BITTENCOURT; BERTI FILHO, 2004). These results demonstrate that the host species can influence the period of development of P. elaeisis.

The density of parasitoids can also affect the development cycle of P. elaeisis (PASTORI et al., 2008; MARTINS et al., 2019). A shorter cycle was reported for this parasitoid in pupae of T. molitor (23.42 ± 0,18 days) with the parasitoid/host density 4:1 (ZANUNCIO et al., 2008). There is a negative correlation between the increase in the number of parasitoid females per host and the length of the life cycle of P. elaeisis, since the immature competition for nutrients reduces the development time (PASTORI et al., 2012; MARTINS et al., 2019). This was also observed by exposing five densities of Melittobia digitata Dahms, 1984 (Hymenoptera: Eulophidae) per pupa of Neobellieria bullata (Parker, 1916) (Diptera: Sarcophagidae) (SILVA-TORRES; MATTHEWS, 2003). However, the reduction in the life cycle period was not observed in this study, with densities of 6:1 parasitoids/hosts showed a longer life cycle than in densities 4:1 (ZANUNCIO et al., 2008).

The number of parasitoids that emerged in the six treatments did not differ (p = 0.4820; F = 0.9095; df = 5) (Table 4). For P. elaeisis, 511 and 110 individuals emerged from pupae of Bombyx mori (Linnaeus, 1758) (Lepidoptera: Bombycidae) and A. gemmatalis, respectively (PEREIRA et al., 2009). These values were higher than those found in this study. The lower number of offspring of this parasitoid in pupae of T. molitor may be due to the higher biomass of pupae of B. mori and A. gemmatalis when compared to those of T. molitor. In the mass rearing of parasitoids, this can be offset by the low cost and effort required to produce pupae from the alternative host.

Tenebrio molitor fed with cornmeal produced a larger number of males of P. elaeisis in relation to those of the other diets (p = 0.05; df = 5). The sex ratio of P. elaeisis in cornmeal was 0,81 ± 0,02 (Table 4) which indicates that 1/5 of the progeny was composed of males. Reports show that the sex ratio values found for P. elaeisis are generally higher in this host (0,94) (ZANUNCIO et al., 2008). High sex ratio values for P. elaeisis are important for maintaining the population dynamics of the parasitoid since females are responsible for parasitism and the production of offspring.

The longevity of males (p = 0.5890; F = 0.7510; df = 5) and females (p = 0.1504; F = 1.7015 df = 5) of P. elaeisis did not change between treatments (Table 4). Male and female individuals had longevity greater than 30 days. Values lower than this (22.65 days for females and 28.3 days for males) were found for P. elaeisis in this same host with a lower density (4:1) of parasitoids per pupae (ZANUNCIO et al., 2008). The parasitoid in this study possibly obtained better nutrition. Adequate nutrition for immatures and adults could generate more long-lived individuals (VINSON; BARBOSA, 1987). This is important in the efficiency of biological control, considering that longer-lived adults have greater chances of mating, reproduction and the ability to parasitize a greater number of hosts in the field (PRATISSOLI et al., 2007).

No differences were found in the body and head size of males and females of P. elaeisis emerged in the six treatments (p = 0.1110; F = 1.8938; df = 5) (p < 0.01; F = 1.0948; df = 5); (p = 0.7162; F = 0.5785; df = 5) (p = 0.7279; F = 0.5641; df = 5) (Fig. 1).

Figure 1
Morphometry of the cephalic capsule, body length and posterior tibia of males and females of P. elaeisis.

The females of P. elaeisis presented body size ranging from 1.84 ± 0.21 to 2.0 ± 0.7 mm and cephalic capsule from 0.46 ± 0.07 to 0.5 ± 0.06 mm. Males, on the other hand, were smaller with body size ranging from 1.3 ± 0.09 to 1.49 ± 0.2 mm and cephalic capsule from 0.33 ± 0.04 to 0.37 ± 0.06 mm, respectively. This parameter was not influenced by the diets provided to the host. Sizes similar to those were found by ZANUNCIO et al. (2008). In Lepidoptera hosts such as A. gemmatalis, D. saccharalis, S. frugiperda, and H. virescens higher values were found for the body size of P. elaeisis females (2.23, 2.25, 2.21, 2.21 mm, respectively) (BITTENCOURT; BERTI FILHO, 1999). This shows that different hosts with different sizes can provide a greater or lesser nutritional source for the larvae of this parasitoid and influence the size of the offspring.

Competition for food and space between immature individuals of P. elaeisis may promote an increase in the number of smaller parasitoids (PEREIRA et al., 2009). Body size has a positive correlation with quality indicators such as longevity, copulation preference, fertility, reproductive longevity, progeny emergence and sex ratio, which can indicate the efficiency of parasitoids (PASTORI et al., 2012).

Males and females of P. elaeisis from pupae of T. molitor fed with cornmeal had tibia sizes of 0.31 ± 0.06 mm and 0.58 ± 0.06 mm, respectively. These values were lower than those found in the other treatments (p < 0.01; F = 3.8278; df = 5) (p < 0.01; F = 3.7955; df = 5). Larger females and males of Anagyrus kamali Moursi, 1948 (Hymenoptera: Encyrtidae) lived longer than smaller ones (SAGARRA et al., 2001). These authors found that females of this species showed no preference for copulation with large or small males. However, fertility was positively correlated with the size of females. In addition, the parasitism capacity, the daily rate of oviposition and the number of progenies of female parasitoids of A. kamali were higher among the larger parasitoids. Male parasitoids from T. molitor fed with cornmeal treatment, due to their smaller size of the tibia, could be less chosen by the females at copulation time (BITTENCOURT; BERTI FILHO, 1999).

The diets with wheat bran, pelleted feed for rabbits and bran, pelleted or crushed feed for laying hens provided to the host T. molitor allowed the proper development and reproduction of the parasitoid P. elaeisis. Cornmeal based diet provides lower body mass of T. molitor and sex ratio and length of the tibia of P. elaeisis not being suitable for the rearing of hosts for this parasitoid.

ACKNOWLEDGEMENTS

Not applicabe.

• FUNDING

  Not applicabe.

• ETHICAL APPROVAL

  Not applicable

• AVAILABILITY OF DATA AND MATERIAL:

  Martins, Daniel (2020), “Palmistichus elaeisis (Hymenoptera: Eulophidae)rearing in Tenebrio molitor (Coleoptera: Tenebrionidae) submitted to different diets Mendeley Data, V1. https://doi.org/10.17632/xwnkkzcjdg.1
• *
  This paper is part of the dissertation thesis of the first author.

REFERENCES

• ASSOCIATION OF OFFICIAL ANALYTICAL CHEMISTS (AOAC). Official Methods of analysis of the Association of Official Analytical Chemists Washington: AOAC, 1997.
• BECK, S.D.; REESE, J.C. Insect-plant interactions: nutrition and metabolism. In: WALLACE, J.W.; MANSELL, R.L. (ed). Biochemical interactions between plants and insects Boston: Springer, 1976. p.41-92. https://doi.org/10.1007/978-1-4684-2646-5_2
  » https://doi.org/10.1007/978-1-4684-2646-5_2
• BITTENCOURT, M.A.L.; BERTI FILHO, E. Preferência de Palmistichus elaeisis por pupas de diferentes lepidópteros pragas. Scientia Agricola, Piracicaba, v.56, n.4, p.1281-1283, 1999. Supplement. https://doi.org/10.1590/S0103-90161999000500033
  » https://doi.org/10.1590/S0103-90161999000500033
• BITTENCOURT, M.A.L.; BERTI FILHO, E. Desenvolvimento dos estágios imaturos de Palmistichus elaeisis Delvare & LaSalle (Hymenoptera, Eulophidae) em pupas de Lepidoptera. Revista Brasileira de Entomologia, São Paulo, v.48, n.1, p.65-68, 2004. https://doi.org/10.1590/S0085-56262004000100012
  » https://doi.org/10.1590/S0085-56262004000100012
• BRODEUR, J.; BOIVIN, G. Functional ecology of immature parasitoids. Annual Review of Entomology, Ithaca, v.49, p.27-49, 2004. https://doi.org/10.1146/annurev.ento.49.061703.153618
  » https://doi.org/10.1146/annurev.ento.49.061703.153618
• CAMILO, S.S.; SOARES, M.A.; LEITE, G.L.D.; SANTOS, J.B.; ASSIS JUNIOR, S.L.; ZANUNCIO, J.C. Do floral resources in Eucalyptus plantations affect fitness parameters of the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae)? Phytoparasitica, Bet Dagan, v.44, n.5, p.651-659, 2016. https://doi.org/10.1007/s12600-016-0549-7
  » https://doi.org/10.1007/s12600-016-0549-7
• CRUZ, R.A.; ZANUNCIO, J.C.; LACERDA, M.C.; WILCKEN, C.F.; FERNANDES, F.L.; TAVARES, W.S.; SOARES, M.A.; SEDIYAMA, C.S. Side-effects of pesticides on the generalist endoparasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Scientific Reports, London, v.7, p.10064, 2017. https://doi.org/10.1038/s41598-017-10462-3
  » https://doi.org/10.1038/s41598-017-10462-3
• FAVERO, K.; PEREIRA, F.F.; KASSAB, S.O.; OLIVEIRA, H.N.; COSTA, D.P.; ZANUNCIO, J.C. Biological characteristics of Trichospilus diatraeae (Hymenoptera: Eulophidae) are influenced by the number of females exposed per pupa of Tenebrio molitor (Coleoptera: Tenebrionidae). Florida Entomologist, Gainesville, v.96, n.2, p.583-589, 2013. https://doi.org/10.1653/024.096.0224
  » https://doi.org/10.1653/024.096.0224
• JONES, D.B. Factors for converting percentages of protein (Circular 183). Washington (DC): USDA, 1941. 22p.
• LEMOS, W.P.; RAMALHO, F.S.; SERRÃO, J.E.; ZANUNCIO, J.C. Effects of diet on development of Podisus nigrispinus (Dallas) (Het., Pentatomidae), a predator of the cotton leafworm. Journal of Applied Entomology, Goettingen, v.127, n.7, p.389-395, 2003. https://doi.org/10.1046/j.1439-0418.2003.00765.x
  » https://doi.org/10.1046/j.1439-0418.2003.00765.x
• LIPKE, H.; FRAENK, G. Insect nutrition. Annual Review of Entomology, Ithaca, v.1, p.17-44, 1956. https://doi.org/10.1146/annurev.en.01.010156.000313
  » https://doi.org/10.1146/annurev.en.01.010156.000313
• MARTINS, D.J.; SANTOS, M.M.; SALES, T.S.; SILVA, I.M.; SOARES, M.A.; ASSIS JUNIOR, S.L. Do parasitoid density and host age affect the parasitism of Palmistichus elaeisis (Hymenoptera: Eulophidae)? Arquivos do Instituto Biológico, São Paulo, v.86, p.e0772017, 2019. https://doi.org/10.1590/1808-1657000772017
  » https://doi.org/10.1590/1808-1657000772017
• MENEZES, C.W.G.; CAMILO, S.S.; FONSECA, A.J.; ASSIS JÚNIOR, S.L.; BISPO, D.F.; SOARES, M.A. A dieta alimentar da presa Tenebrio molitor (Coleoptera: Tenebrionidae), pode afetar o desenvolvimento do predador Podisus nigrispinus (Heteroptera: Pentatomidae)? Arquivos do Instituto Biológico, São Paulo, v.81, n.3, p.250-256, 2014. https://doi.org/10.1590/1808-1657001212012
  » https://doi.org/10.1590/1808-1657001212012
• MORALES-RAMOS, J.A.; ROJAS, M.G.; SHAPIRO-ILAN, D.I.; TEDDERS, W.L. Self-selection of two diet components by Tenebrio molitor (Coleoptera: Tenebrionidae) larvae and its impact on fitness. Environmental Entomology, Hamden, v.40, n.5, p.1285-1294, 2011. https://doi.org/10.1603/EN10239
  » https://doi.org/10.1603/EN10239
• MYERS, P.; ESPINOSA, R.; PARR, C.S.; JONES, T.; HAMMOND, G.S.; DEWEY, T.A. Tenebrio molitor: yellow mealworm. Animal Diversity Web. 1999. Available from: http://animaldiversity.ummz.umich.edu/site/accounts/information/tenebrio_molitor.html Access on: 7 Nov. 2015.
  » http://animaldiversity.ummz.umich.edu/site/accounts/information/tenebrio_molitor.html
• OTUKA, A.K.; VACARI, A.M.; MARTINS, M.I.E.G.; BORTOLI, S.A. Custo de produção de Podisus nigrispinus (Dallas, 1851) (Hemiptera: Pentatomidae) criado com diferentes presas. Biológico, São Paulo, v.68, p.431-434, 2006. Supplement. Available from: http://www.biologico.sp.gov.br/uploads/docs/bio/suplementos/v68_supl/p431-434.pdf Access on: 15 Oct. 2020.
  » http://www.biologico.sp.gov.br/uploads/docs/bio/suplementos/v68_supl/p431-434.pdf
• PARRA, J.R.P. A evolução das dietas artificiais e suas interações em ciência e tecnologia. In: PANIZZI, A.R; PARRA, J.R.P. (ed). Bioecologia e nutrição de insetos: base para o manejo integrado de pragas Brasília: Embrapa Informação Tecnológica. 2009, p.91-174.
• PASTORI, P.L.; MONTEIRO, L.B.; BOTTON, M. Biologia e exigências térmicas de Trichogramma pretiosum Riley (Hymenoptera, Trichogrammatidae) “linhagem bonagota” criado em ovos de Bonagota salubricola (Meyrick) (Lepidoptera, Tortricidae). Revista Brasileira de Entomologia, São Paulo, v.52, n.3, p.472-476, 2008. https://doi.org/10.1590/S0085-56262008000300024
  » https://doi.org/10.1590/S0085-56262008000300024
• PASTORI, P.L.; PEREIRA, F.F.; ZANUNCIO, J.C.; OLIVEIRA, H.N.; CALADO, V.F.R.; SILVA, R.O. Densidade de fêmeas de Palmistichus elaeisis Delvare & LaSalle, 1993 (Hymenoptera: Eulophidae) para sua reprodução em pupas de Anticarsia gemmatalis Hübner, 1818 (Lepidoptera: Noctuidae). Arquivos do Instituto Biológico, São Paulo, v.79, n.4, p.525-532, 2012. https://doi.org/10.1590/S1808-16572012000400009
  » https://doi.org/10.1590/S1808-16572012000400009
• PENNACCHIO, F.; STRAND, M.R. Evolution of developmental strategies in parasitic Hymenoptera. Annual Review of Entomology, Ithaca, v.51, p.233-258, 2006. https://doi.org/10.1146/annurev.ento.51.110104.151029
  » https://doi.org/10.1146/annurev.ento.51.110104.151029
• PEREIRA, F.F.; ZANUNCIO, J.C.; PASTORI, P.L.; PEDROSA, A.R.P.; OLIVEIRA, H.N. Parasitismo de Palmistichus elaeisis (Hymenoptera: Eulophidae) em hospedeiro alternativo sobre plantas de eucalipto em semi-campo. Revista Ciência Agronômica, Fortaleza, v.41, n.4, p.715-720, 2010. https://doi.org/10.1590/S1806-66902010000400028
  » https://doi.org/10.1590/S1806-66902010000400028
• PEREIRA, F.F.; ZANUNCIO, J.C.; SERRÃO, J.E.; PASTORI, P.L.; RAMALHO, F.S. Reproductive performance of Palmistichus elaeisis Delvare and LaSalle (Hymenoptera: Eulophidae) with previously refrigerated pupae of Bombyx mori L. (Lepidoptera: Bombycidae). Brazilian Journal of Biology, São Carlos, v.69, n.3, p.865-869, 2009. https://doi.org/10.1590/S1519-69842009000400014
  » https://doi.org/10.1590/S1519-69842009000400014
• PEREIRA, F.F.; ZANUNCIO, T.V.; ZANUNCIO, J.C.; PRATISSOLI, D.; TAVARES, M.T. Species of Lepidoptera defoliators of Eucalyptus as new host for the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Brazilian Archives of Biology and Technology, Curitiba, v.51, n.2, p.259-262, 2008. https://doi.org/10.1590/S1516-89132008000200004
  » https://doi.org/10.1590/S1516-89132008000200004
• PRATISSOLI, D.; POLANCZYK, R.A.; ANDRADE, G.S.; HOLTZ, A.M.; SILVA, A.F.; PASTORI, P.L. Tabela de vida de fertilidade de cinco linhagens de Trichogramma pretiosum Riley (Hym.: Trichogrammatidae) criadas em ovos de Tuta absoluta (Merick) (Lep.: Gelechiidae), sob temperaturas constantes e alternadas. Ciência Rural, Santa Maria, v.37, n.3, p.618-622, 2007. https://doi.org/10.1590/S0103-84782007000300003
  » https://doi.org/10.1590/S0103-84782007000300003
• R CORE TEAM. R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna: R Foundation for Statistical Computing. 2016. Available from: https://www.R-project.org/ Access on: 15 Oct. 2020.
  » https://www.R-project.org/
• RODRÍGUEZ-DIMATÉ, F.A.; PODEROSO, J.C.M.; RIBEIRO, R.C.; BRÜGGER, B.P.; WILCKEN, C.F.; SERRÃO, J.E.; ZANUNCIO, J.C. Palmistichus elaeisis (Hymenoptera: Eulophidae) Parasitizing pupae of the passion fruit pest Agraulis vanillae vanilla (Lepidoptera: Nymphalidae). Florida Entomologist, Gainesville, v.99, n.1, p.130-132, 2016. https://doi.org/10.1653/024.099.0127
  » https://doi.org/10.1653/024.099.0127
• SAGARRA, L.A.; VICENT, C.; STEWART, R.K. Body size as an indicator of parasitoid quality in male and female Anagyrus kamali (Hymenoptera: Encyrtidae). Bulletin of Entomological Research, Brisbane, v.91, n.5, p.363-367, 2001. https://doi.org/10.1079/BER2001121
  » https://doi.org/10.1079/BER2001121
• SILVA-TORRES, C.S.A.; MATTHEWS, R.W. Development of Melittobia australica Girault and M digitata Dahms (Parker) (Hymenoptera: Eulophidae) parasiting Neobellieria bullata (Parker) (Diptera: Sarcophagidae) puparia. Neotropical Entomology, Londrina, v.32, n.4, p.645-651, 2003. https://doi.org/10.1590/S1519-566X2003000400015
  » https://doi.org/10.1590/S1519-566X2003000400015
• URREJOLA, S.; NESPOLO, R.; LARDIES, M.A. Diet-induced developmental plasticity in life histories and energy metabolism in a beetle. Revista Chilena de História Natural, Santiago, v.84, n.4, p.523-533, 2011. https://doi.org/10.4067/S0716-078X2011000400005
  » https://doi.org/10.4067/S0716-078X2011000400005
• VIEIRA, E.R.D.; SILVA, E.B.; SOARES, M.A.; ASSIS JUNIOR, S.L.; BARROSO, G.A.; LEMES, P.G. Lack of macronutrients in Eucalyptus urophylla S.T. Blake (Myrtaceae) seedlings affects feed and development of Podisus nigrispinus (Hemiptera: Pentatomidae). Bioscience Journal, Uberlândia, v.34, n.1, p.42-48, 2018. https://doi.org/10.14393/BJ-v34n1a2018-34484
  » https://doi.org/10.14393/BJ-v34n1a2018-34484
• VINSON, S.B.; BARBOSA, P. Interrelationships of nutritional ecology of parasitoids. In: SLANSKY, F.; RODRIGUEZ, J.G. (ed). Nutritional ecology of insects, mites, spiders, and related invertebrates New York: John Wiley, 1987. chap.21, p.673-695.
• WANG, Z.Y.; HE, K.L.; ZHANG, F.; LU, X.; BABENDREIER, D. Mass rearing and release of Trichogramma for biological control of insect pests of corn in China. Biological Control, Sophia Antipolis, v.68, p.136-144, 2014. https://doi.org/10.1016/j.biocontrol.2013.06.015
  » https://doi.org/10.1016/j.biocontrol.2013.06.015
• ZANUNCIO, J.C., PEREIRA, F.F.; JACQUES, G.C.; TAVARES, M.T.; SERRÃO, J.E. Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), a new alternative host to rear the pupae parasitoid Palmistichus elaeisis Delvare & Lasalle (Hymenoptera: Eulophidae). The Coleopterists Bulletin, Santa Barbara, v.62, n.1, p.64-66, 2008. https://doi.org/10.1649/1015.1
  » https://doi.org/10.1649/1015.1
• ZANUNCIO, J.C.; VINHA, G.L.; RIBEIRO, R.C.; FERNANDES, B.V.; KASSAB, S.O.; WILCKEN, C.F.; ZANUNCIO, T.V. Psorocampa denticulata (Lepidoptera: Notodontidae) Pupae as an alternative host for Palmistichus elaeisis (Hymenoptera: Eulophidae). Florida Entomologist, Gainesville, v.98, n.3, p.1003-1005, 2015. https://doi.org/10.1653/024.098.0338
  » https://doi.org/10.1653/024.098.0338

Publication Dates

• Publication in this collection
  04 Dec 2020
• Date of issue
  2020

History

• Received
  21 June 2019
• Accepted
  27 Sept 2020