# Survival Analysis of the Green Lacewing, Chrysoperla externa (Hagen) Exposed to Neem-Based Products

^{1}

^{2}

^{*}

## Abstract

**:**

^{®}: 0 (control treatment with distilled water), 12, 24, 36, 48, 60, 72, 84, 96, and 108 mg a.i. L

^{−1}; Organic neem

^{®}: 0, 3.3, 6.6, 9.9, 13.2, 16.5, 19.8, 23.1, and 26.4 mg a.i. L

^{−1}; Natuneem

^{®}: 0, 3.8, 7.5, 10.5, 15.0, 18.8, 22.5, 26.3, 30.0, and 33.8 mg a.i. L

^{−1}), using a parametric approach. Predator larvae were exposed to neem-based insecticides and evaluated for 20 days. Survival curves estimated by the models—Log-logistic for Azamax

^{®}, Weibull for Organic neem

^{®}, and Log-normal for Natuneem

^{®}—demonstrated an inverse relationship between increasing doses and survival time. These concluded that the application dose should be less than 84 mg a.i. L

^{−1}for Azamax

^{®}, 19.8 mg a.i. L

^{−1}for Organic neem

^{®}, and 26.3 mg a.i. L

^{−1}for Natuneem

^{®}to keep 50% of the green lacewings alive for 13 days, which is the average time for the larval cycle of C. externa.

## 1. Introduction

^{−1}of azadirachtin prevented the development of mines [23]. Neem seed extract has a systemic and translaminar effect that permeates the leaves, stops leaf miner development, drastically reduces pupation, and prevents adult emergence [23]. Plants treated with neem products are expected to have a lower coffee leaf miner infestation, either because treated plants repel egg-laying females or because coffee leaf miner development is adversely affected by neem. Azadirachtin concentrations above 0.065 g L

^{−1}reduced the population growth rate of O. ilicis [23]. Despite these advantages, some natural enemies can be negatively affected by neem, and the effect will depend on the formulation and concentration used [23,24].

## 2. Materials and Methods

#### 2.1. Chrysoperla Externa Rearing and Neem-Based Products

^{−1}) (UPL do Brasil Indústria e Comércio de Insumos Agropecuários S.A., Ituverava, São Paulo, Brazil), Organic neem (emulsifiable concentrate formulation 3.3 g Azadirachtin A and B L

^{−1}) (Dalquim Industria e Comércio, Itajaí, Santa Catarina, Brazil), and Natuneem (emulsifiable concentrate formulation 1.5 g Azadirachtin A and B L

^{−1}) (Natural Rural Industria e Comercio de Produtos Orgânicos e Biológicos Ltd.a, Araraquara, São Paulo, Brazil).

#### 2.2. Bioassays

^{−2}with a volume of 2.5 mL with different concentrations of the three commercial neem-based products. After drying, a newly emerged larva of C. externa was transferred to each disc. The larvae were kept on the discs for six days until the beginning of the deterioration of the leaf discs. Subsequently, they were transferred to glass tubes (2.5 × 8.5 cm) and kept until adult emergence in an acclimatized room (temperature: 25 ± 2 °C, relative humidity: 70 ± 10%, and photophase of 14 h). During the larval period, they were fed an ample supply of eggs of the flour moth Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) [27]. The experimental design was completely randomized, with ten replications for each tested concentration; the experimental unit consisted of one larva.

**a**) Azamax

^{®}: 0 mg a.i. L

^{−1}(control treatment with distilled water), 12 mg a.i. L

^{−1}, 24 mg a.i. L

^{−1}, 36 mg a.i. L

^{−1}, 48 mg a.i. L

^{−1}, 60 mg a.i. L

^{−1}, 72 mg a.i. L

^{−1}, 84 mg a.i. L

^{−1}, 96 mg a.i. L

^{−1}, and 108 mg a.i. L

^{−1}; (

**b**) Organic neem

^{®}: 0 mg a.i. L

^{−1}, 3.3 mg a.i. L

^{−1}, 6.6 mg a.i. L

^{−1}, 9.9 mg a.i. L

^{−1}, 13.2 mg a.i. L

^{−1}, 16.5 mg a.i. L

^{−1}, 19.8 mg a.i. L

^{−1}, 23.1 mg a.i. L

^{−1}, and 26.4 mg a.i. L

^{−1}; and (

**c**) Natuneem

^{®}: 0 mg a.i. L

^{−1}, 3.8 mg a.i. L

^{−1}, 7.5 mg a.i. L

^{−1}, 10.5 mg a.i. L

^{−1}, 15.0 mg a.i. L

^{−1}, 18.8 mg a.i. L

^{−1}, 22.5 mg a.i. L

^{−1}, 26.3 mg a.i. L

^{−1}, 30.0 mg a.i. L

^{−1}, and 33.8 mg a.i. L

^{−1}.

#### 2.3. Statistical Analysis

## 3. Results and Discussion

^{®}product, the model chosen was Log-logistic; for Organic neem

^{®}, it was the Weibull model; and for Natuneem

^{®}, it was the Log-normal model. The best model presented the lowest AIC values. However, the actual values of AIC have no meaning.

^{®}is the best model with a ${w}_{i}$ of 0.89, which means that there is an 89.0% chance that it is the model which best approximates the described data. The ${w}_{i}$ values for the Weibull model for Organic neem

^{®}and Log-normal for Natuneem

^{®}were 48.0% and 56%, respectively.

^{®}, Organic neem

^{®}, and Natuneem

^{®}products, respectively. In panel (a), a slight deviation can be seen at the end of the two curves. Klein and Moeschberger [46] reported that departures from the exponential distribution may be partially due to the uncertainty in estimating parameters. This uncertainty is the largest in the right-hand tail of the distribution and for small samples.

^{®}, Weibull for Organic neem

^{®}, and Log-normal for Natuneem

^{®}—demonstrate an inverse relationship between increasing doses and survival time (Figure 2, Figure 3 and Figure 4). For insects without exposure to neem-based products (control treatment), the survival rates were 69.5%, 77.9%, and 90.4% at the 20-day evaluation for Azamax

^{®}, Organic neem

^{®}, and Natuneem

^{®}, respectively, and the survival rates with the maximum dose were 7%, 1.1%, and 5.7% at the end of the 20 days of evaluation for Azamax

^{®}, Organic neem

^{®}and Natuneem

^{®}, respectively. Therefore, it is concluded that azadirachtin harms C. externa and that bioinsecticides should not be exempt from the risk assessment [26,47].

^{®}doses should be lower than 48 mg a.i. L

^{−1}and 84 mg a.i. L

^{−1}, respectively (Figure 2). Additionally, for the survival of 25% of the green lacewings, all tested doses can be used.

^{®}, considering the Weibull model, dosages need to be below 13.2, 19.8, and 26.4 mg a.i. L

^{−1}to achieve 75%, 50%, and 25% survival, respectively (Figure 3). For Natuneem

^{®}and the Log-normal model, the dosages must be less than 15 (or equal), 26.3, and 33.8 mg a.i. L

^{−1}(Figure 4).

^{®}to control L. coffeella and H. hampei in coffee plants can vary from 24–30 mg a.i. L

^{−1}and 72–96 mg a.i. L

^{−1}, according to the level of infestation [52]. According to the adjusted model, if these dosages are applied to control these pests, 84–81% and 55–37% of green lacewings would be alive, considering the average survival time of 13 days, respectively (Figure 2). High concentrations of neem-based products to control the coffee berry borer have negative impacts on C. externa and other natural enemies [26], as well as on some pollinators [29]. Azadirachtin is a broad-spectrum insecticide, which affects the neuroendocrine, reproduction, anti-feeding, cellular, and molecular activity of insects, and its toxicity varies between insect orders [21]. These adverse effects on beneficial insects can be minimized if the formulation and concentration of the product to be applied are carefully chosen based on research data and technical information [23,24].

^{®}and Natuneem

^{®}products, and observed that for 13-day survival, doses below 16.5 mg a.i. L

^{−1}and 18.6 mg a.i. L

^{−1}, respectively, kept 50% of the green lacewings alive. Organic neem

^{®}and Natuneem

^{®}products still need to be registered for any crop in Brazil [52]. However, their uses are common in research, such as side effects on bees [29] and control of mites [51,54,55].

## 4. Conclusions

^{−1}for Azamax

^{®}, 19.8 mg a.i. L−

^{1}for Organic neem

^{®}, and 26.3 mg a.i. L

^{−1}for Natuneem

^{®}.

## Author Contributions

## Funding

## Institutional Review Board Statement

## Data Availability Statement

## Conflicts of Interest

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**Figure 1.**Cox–Snell residuals from the (

**a**) Log-logistic model for Azamax

^{®}, (

**b**) Weibull model for Organic neem

^{®}, and (

**c**) Log-normal model for Natuneem

^{®}.

**Figure 2.**Survival curves estimated by Log-logistic model for Chrysoperla externa exposed to different doses (mg a.i. L

^{−1}) in Azamax

^{®}. The times for 75%, 50%, and 25% of the individuals to be alive are also presented.

**Figure 3.**Survival curves estimated by the Weibull model for Chrysoperla externa exposed to different doses (mg a.i. L

^{−1}) in Organic neem

^{®}. The times for 75%, 50%, and 25% of the individuals to be alive are also presented.

**Figure 4.**Survival curves estimated by the Log-normal model for Chrysoperla externa exposed to different doses (mg a.i. L

^{−1}) in Natuneem

^{®}. The times for 75%, 50%, and 25% of the individuals to be alive are also presented.

**Table 1.**The probability density functions and survival functions for the models used in the analysis of Chrysoperla externa exposed to neem-based products.

Models | Probability Density Function ^{1} | Survival Function |
---|---|---|

Exponential | $f\left(t\right)=\lambda \mathit{exp}\left\{-\lambda t\right\}$ | $S\left(t|x\right)=exp\left\{-\frac{t}{\mathrm{exp}\left({\beta}_{0}+{\beta}^{\prime}x\right)}\right\}$ |

Weibull | $f\left(t\right)=\alpha \lambda {t}^{\alpha -1}exp\left\{-{\left(\lambda t\right)}^{\alpha}\right\}$ | $S\left(t|x\right)=\mathit{exp}\left\{-{\left(\frac{t}{\mathrm{exp}\left({\beta}_{0}+{\beta}^{\prime}x\right)}\right)}^{\frac{1}{\sigma}}\right\}$ |

Log-normal | $f\left(t\right)=\frac{1}{t\sigma \sqrt{2\pi}}exp\left\{-\frac{1}{2}{\left(\frac{\mathit{ln}\left(t\right)-\mu}{\sigma}\right)}^{2}\right\}$ | $S\left(t|x\right)=\mathsf{\Phi}\left(\frac{-\mathit{ln}\left(t\right)+{\beta}_{0}+{\beta}^{\prime}x}{\sigma}\right)$ |

Log-logistic | $f\left(t\right)=\frac{\alpha {t}^{\alpha -1}\lambda}{{\left(1+\lambda {t}^{\alpha}\right)}^{2}}$ | $S\left(t|x\right)=\frac{1}{1+{\left(\frac{t}{exp\left({\beta}_{0}+{\beta}^{\prime}x\right)}\right)}^{\frac{1}{\sigma}}}$ |

Logistic | $f\left(y\right)=\frac{exp\left\{\frac{y-\mu}{\sigma}\right\}}{\sigma {\left(1+exp\left\{\frac{y-\mu}{\sigma}\right\}\right)}^{2}}$ | $S\left(t|x\right)=\frac{1}{1+exp\left\{\frac{t-\left({\beta}_{0}+{\beta}^{\prime}x\right)}{\sigma}\right\}}$ |

Gaussian | $f\left(t\right)=\frac{1}{\sigma \sqrt{2\pi}}exp\left\{-\frac{1}{2}{\left(\frac{t-\mu}{\sigma}\right)}^{2}\right\}$ | $S\left(t|x\right)=\mathsf{\Phi}\left(\frac{-t+{\beta}_{0}+{\beta}^{\prime}x}{\sigma}\right)$ |

^{1}ln = natural logarithm; $\mathsf{\Phi}$ = cumulative distribution function of the standard normal distribution; y = ln(t).

**Table 2.**Parameter estimates and standard errors (SE), Akaike information criterion (AIC), and Akaike weights (w

_{i}) for the models used in the analysis of Chrysoperla externa exposed to neem-based products.

Parameters | Exponential | Weibull | Log-Normal | Log-Logistic | Logistic | Gaussian | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|

Estimate | SE | Estimate | SE | Estimate | SE | Estimate | SE | Estimate | SE | Estimate | SE | |

Azamax^{®} | ||||||||||||

${\beta}_{0}$ | 4.0726 | 0.2992 | 3.4303 | 0.1288 | 3.2001 | 0.1241 | 3.2202 | 0.1079 | 22.5068 | 1.4292 | 22.2546 | 1.5065 |

${\beta}_{1}$ | −0.0158 | 0.0042 | −0.0089 | 0.0018 | −0.0078 | 0.0019 | −0.0084 | 0.0016 | −0.1143 | 0.0205 | −0.1055 | 0.0227 |

$\sigma $ | 1.0000 | 0.0000 | 0.3853 | 0.0450 | 0.5270 | 0.0564 | 0.2725 | 0.0333 | 3.6114 | 0.4361 | 6.4241 | 0.6961 |

Log L | −212.30 | --- | −190.30 | --- | −190.90 | --- | −187.70 | --- | −196.40 | --- | −196.90 | --- |

AIC | 428.67 | --- | 386.56 | --- | 387.76 | --- | 381.42 | --- | 398.74 | --- | 399.87 | --- |

${w}_{i}$ | 0.00 | --- | 0.07 | --- | 0.04 | --- | 0.89 | --- | 0.00 | --- | 0.00 | --- |

Organic neem^{®} | ||||||||||||

${\beta}_{0}$ | 4.2724 | 0.3264 | 3.6093 | 0.1632 | 3.3696 | 0.1618 | 3.3835 | 0.1441 | 24.1767 | 1.6901 | 23.8370 | 1.7897 |

${\beta}_{1}$ | −0.0788 | 0.0181 | −0.0485 | 0.0090 | −0.0453 | 0.0096 | −0.0459 | 0.0084 | −0.5847 | 0.0967 | −0.5540 | 0.1069 |

$\sigma $ | 1.0000 | 0.0000 | 0.4425 | 0.0548 | 0.6297 | 0.0703 | 0.3320 | 0.0429 | 3.8997 | 0.4950 | 7.0087 | 0.7936 |

Log L | −188.00 | --- | −172.70 | --- | −174.70 | --- | −172.80 | --- | −180.40 | --- | −181.10 | --- |

AIC | 379.98 | --- | 351.45 | --- | 355.50 | --- | 351.54 | --- | 366.73 | --- | 368.23 | --- |

${w}_{i}$ | 0.00 | --- | 0.48 | --- | 0.06 | --- | 0.46 | --- | 0.00 | --- | 0.00 | --- |

Natuneem^{®} | ||||||||||||

${\beta}_{0}$ | 4.9722 | 0.3716 | 4.0718 | 0.2205 | 3.8558 | 0.1939 | 3.7988 | 0.1880 | 28.5799 | 2.0402 | 28.8093 | 2.0433 |

${\beta}_{1}$ | −0.0867 | 0.0148 | −0.0549 | 0.0087 | −0.0563 | 0.0083 | −0.0538 | 0.0081 | −0.6350 | 0.0855 | −0.6355 | 0.0874 |

$\sigma $ | 1.0000 | 0.0000 | 0.5041 | 0.0603 | 0.6591 | 0.0712 | 0.3754 | 0.0453 | 4.1101 | 0.4918 | 7.0062 | 0.7705 |

Log L | −198.00 | --- | −185.70 | --- | −183.80 | --- | −184.30 | --- | −195.40 | --- | −194.40 | --- |

AIC | 399.91 | --- | 377.45 | --- | 373.62 | --- | 374.51 | --- | 396.80 | --- | 394.73 | --- |

${w}_{i}$ | 0.00 | --- | 0.08 | --- | 0.56 | --- | 0.36 | --- | 0.00 | --- | 0.00 | --- |

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## Share and Cite

**MDPI and ACS Style**

Martins Filho, S.; Duarte, M.L.; Venzon, M. Survival Analysis of the Green Lacewing, *Chrysoperla externa* (Hagen) Exposed to Neem-Based Products. *Agriculture* **2023**, *13*, 292.
https://doi.org/10.3390/agriculture13020292

**AMA Style**

Martins Filho S, Duarte ML, Venzon M. Survival Analysis of the Green Lacewing, *Chrysoperla externa* (Hagen) Exposed to Neem-Based Products. *Agriculture*. 2023; 13(2):292.
https://doi.org/10.3390/agriculture13020292

**Chicago/Turabian Style**

Martins Filho, Sebastião, Marciel Lelis Duarte, and Madelaine Venzon. 2023. "Survival Analysis of the Green Lacewing, *Chrysoperla externa* (Hagen) Exposed to Neem-Based Products" *Agriculture* 13, no. 2: 292.
https://doi.org/10.3390/agriculture13020292