Biocompatibility of fungi and essential oils or vegetable extracts: a bibliometric review

Duponchelia fovealis is an agricultural pest that causes great losses in strawberry plantations. As an alternative to traditional chemical insecticides, entomopathogenic fungi (EPF) are used to control this pest. One way to increase the effectiveness of these EPF is by combining them with plant extracts or essential oils (EOs). We carried out a literature review in the Web of Science database using Bibliometrix (version 4.0.0. – R free software tool). Our purpose was to analyze data on the use of EOs or plant extracts with microorganisms to control pests, and observe research trends on this topic. Between 1994 and 2020, 112 articles were published, with the Egyptian Journal of Biological Pest Control as the most outstanding journal. The country with the greatest number of publications on the topic in the analyzed period was Brazil (n=38), followed by India (n=26) and the United States (n=20).


Introduction
The strawberry is a fruit with high added value. Nonetheless, strawberry crops are susceptible to attack by several pests, such as the crown caterpillar Duponchelia fovealis Zeller (Lepidoptera: Crambidae) (Zawadneak et al., 2017). In an attempt to control this pest, pesticides have been used indiscriminately, resulting in an accumulation of these substances in the fruit (EWG, 2019). Biocontrol agents represent an ecological alternative to chemical insecticides (Xu & Hu, 2020). In this regard, the use of entomopathogenic fungi (EPF) is a viable strategy for integrated pest management (IPM) (Gonzalez et al., 2016), with proven efficacy in the control of D. fovealis Amatuzzi, Poitevin, Poltronieri, Zawadneak & Pimentel, 2018;Poitevin, Porsani, Poltronieri, Zawadneak & Pimentel, 2018).
However, another promising management strategy is the use of essential oils (EOs) or plant extracts (Isman, 2000).
An EO is defined as the product obtained through hydrodistillation, steam distillation, or dry distillation of a crude vegetable source (ISO, 2013), whereas the vegetable extract is described as the product acquired by treating a natural raw material with one or more solvents (ISO, 2013).
The study of joint action between EPF and EOs or vegetable extracts can help pest control (Diniz et al., 2020) by increasing the efficiency of control and decreasing the amount of chemical pesticides used (Halder, Rai & Kodandaram, 2013).
Accordingly, the present review aimed to analyze the body of literature published between 1941 and 2020 that focused on the combined action of EOs or plant extracts and fungi to combat pests.

Methodology
The bibliometric tool Bibliometrix, version 4.0.0. (R free software tool) was used to analyze the papers published on this topic since they promote a quantifying analysis of literature data (Zupic & Čater, 2015). For this review, we chose the Web of Science database as it is the most traditional and oldest indexing database (Vieira & Gomes, 2009). Therefore, on January 19, 2021, a search was carried out using the keywords TS=(compatibility AND (essential oil OR extract) AND fungi), in which the defined period was 1941 until the research date (01/19/2021).
We found a total of 112 results. After reading the abstracts of all the documents, 91 publications were excluded. The exclusion criteria were: (i) not an original article document; (ii) not addressing the combination of EOs or extracts with fungi to combat pests. Consequently, 21 articles were selected for full reading.

Results
The bibliographical analysis showed that 112 articles were published between 1994 and 2020 ( Figure 1). The journal Egyptian Journal of Biological Pest Control stood out the most (Figure 2). Number of annual publications on biocompatibility between essential oils or plant extracts and fungi between 1994 and 2020, with data obtained by bibliometrics.
Here, it is noticeable the growing number of documents on this subject published since 2015, approximately. With this data, we can affirm that the field of combined action between fungi and essential oils or plant extracts is ascending in the academic community.  With this figure, we can observe that the keywords that stood out the most were "compatibility," "entomopathogenic fungi," "Beauveria bassiana," "biological control," "Azadirachta indica," "silver nanoparticles," "entomopathogenic fungus," "Metarhizium anisopliae," "neem," and "biocompatibility". The figure presented above shows that the use of "compatibility" as a keyword is descending, however, the use of "biocompatibility" is ascending. This suggests that the two words are not synonyms and that the use of one is preferred in comparison to the other.
In addition, the five countries that published the greatest number of articles are Brazil (n=38), followed by India (n=26), the United States (n=20), China (n=19), and Pakistan (n=14).

Discussion
The bibliographic analysis allowed us to select 21 articles for full reading. After this step, an additional five articles were excluded as they did not describe the combination of fungi and EOs or plant extracts to combat pests. Therefore, the main points of the 16 selected documents are presented below. Rehman et al. (2020) analyzed the compatibility of neem (Azadirachta indica), eucalyptus (Eucalyptus globulus), and tobacco (Nicotidiana tabacum) extracts with B. bassiana in combating the caterpillar stage of the beetle Tribolium castaneum.
The authors found that higher caterpillar mortality was achieved with the combined treatment between B. bassiana and the extracts. For example, 71% mortality was achieved with combined treatment between B. bassiana and 5% neem extract. Sosa et al. (2020) studied the compatibility between EOs of oregano (Origanum vulgare) and anise (Pimpinella anisium) with Purpureocillium lilacinum (nematophagous fungus) on combating the nematoid Nacobbus aberrans. The most expressive mortality (86%) was reached after the application of anise EO (0.02%) with P. lilacinum.
Farooq, Atta, Gogi, Arif e Arain (2020) evaluated the mortality of the caterpillar of the pink bollworm Pectinophora gossypiella after the application of neem extract (A. indica) with three EPF (B. bassiana, M. anisopliae, and Verticillium lecanii). The highest mortality (74.67%) was found with the combined application of the three EPF and neem extract at 5%. Diniz et al. (2020) studied the effects of Fusarium caatingaense with tobacco (N. tabacum) and brazilwood (Paubrasilia enchinata) extracts against the cochineal Dactylopius opuntiae. The highest pest mortality (98.7%) was achieved by applying F. caatingaense URM 6779 variant and 10% aqueous neem extract. Velez et al. (2019) verified the potential mortality achieved through joint treatment of Fusarium incarnatum-equiseti, Chenopodium embrosioides (mastruz) and Enterolobium contortisiliquum (monkfish) extracts in combating D. opuntiae. Their study showed no significant increase in mortality of D. opuntiae when treatment was performed using fungus with extracts, compared to treatment using fungus alone. According to the authors, two treatments should be carried out in the field (URM6777 with aqueous extract of E. contortisiliquum 5% and URM6779 with aqueous extract of E. contortisiliquum 5%) since they caused relatively high mortality to the pest in their experiments (70.34% and 73.64%, respectively). According to the authors, some concentrations of neem (above 5%) were not compatible with the fungus, but compatibility was achieved with neem at 1%, and there was an increase in mortality (88.25%) with a conidial solution at 1x108 conidia/ml.
Observing the data presented above, Brazil was the country that published the most on biocompatibility between EOs or plant extracts and fungi between 1994 and 2020. Corroborating this result, 25% of the articles (four) were published by Brazilian correspondents among the 16 selected for full reading (Diniz et al., 2020;Velez et al., 2019;De Oliveira, 2016 andSousa et al., 2011). On the other hand, only one article was published with a correspondent from India (Halder, Rai & Kodandaram, 2013), diverging from the bibliometric results. None of the 16 documents had a US correspondent, also diverging from the data shown. Only one article had a correspondent from China (Islam, Olleka & Ren, 2010), which also differs from the data. Finally, three articles had Pakistani counterparts (Rehman et al., 2020;Farooq, Atta, Gogi, Arif &Arain, 2020 andAli et al., 2018), also contrasting with the results obtained. Figure 1 shows that work on biocompatibility between EOs or plant extracts and fungi has increased since 1994. In line with this result, all 16 articles selected were published between 2010 and 2020 (Diniz et al., 2020;Halder, Rai & Kodandaram, 2013;Rehman et al., 2020;Sosa et al., 2020;Velez et al., 2019;Ali et al., 2018;Jaber, Araj & Qasem, 2018;Vásquez, Velandia, Jiménez & Velastegui, 2018;Nana, Ekesi, Nchu & Maniania, 2016;Santos, Oliveira, Da Costa, Tiago & De Oliveira, 2016;Zibaee, Bandani & Sendi, 2013;Nana et al., 2012;Vergel, Bustos, Rodríguez & Cantor, 2011;Sousa et al., 2011And Islam, Olleka & Ren, 2010, showing that this subject is gaining ground in the scientific community. Furthermore, the journal that stood out between 1994 and 2020 was the Egyptian Journal of Biological Pest Control  3 depicts "compatibility" as the most used keyword, and "biocompatibility" as the least used. However, according to Figure 4, the use of "compatibility" as a keyword has decreased, while "biocompatibility" has increased in the same period. Among the 16 studies analyzed, two had "compatibility" as a keyword (Vergel, Bustos, Rodríguez & Cantor, 2011) and (Islam, Olleka & Ren, 2010), and none had "biocompatibility." Although this data is not in agreement with the results shown in Figure 4, it is in line with Figure 3.
We can also affirm that the use of the keyword "EPF" increased in the observed period   (Figure 4).
The same figure shows that the use of "neem" as a keyword as well as its use in the analyzed works increased in the period studied . Of the 16 articles, five used "EO" or "plant extract of neem" (Halder, Rai & Kodandaram, 2013;Rehman et al., 2020;Farooq, Atta, Gogi, Arif & Arain, 2020;Ali et al., 2018 andIslam, Olleka &Ren, 2010), three of which were published as of 2018 (Rehman et al., 2020;Farooq, Atta, Gogi, Arif & Arain, 2020) and (Ali et al., 2018), indicating the increased use of this keyword. Furthermore, Figure 4 shows that the use of "biological control" as a keyword increased between 1994 and 2020, but only one article among the 16 had this term as a keyword (Farooq, Atta, Gogi, Arif & Arain, 2020), although all documents read in full-except for one (Sousa et al., 2011)-were about combating an agricultural pest.

Conclusion
Bibliometric methods allowed us to carry out a comprehensive analysis and identify that biological control is one of the expanding lines of research in the scientific community. In recent years, the attention of researchers has focused on the use of fungi, predator agents, and parasites that can control D. fovealis.
However, there is a lack of studies on the applicability of these agents with EOs or plant extracts to combat this pest.
Therefore, we suggested that this subject be explored in future studies, as it represents a sustainable and safe strategy in controlling the European pepper moth from an environmental perspective.