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Introduction
At the national and international level, the regions or countries where cactus pear, Opuntia spp (Caryophyllales: Cactaceae), particularly O. ficus-indica (L.) Mill. is used or cultivated for human and animal diets, or for the incipient industry; it presents a critical phytosanitary situation because of the recent invasion of Dactylopius opuntiae (Hemiptera: Dactylopiidae). This insect is considered the main pest of cactus pear due to its reproductive capacity, the severity of its damage in cladodes and fruits, and its socioeconomic impact (Vanegas-Rico et al. 2010; 2016; Mazzeo et al. 2019). In Mexico, one of the centers of origin of O. ficus-indica (Griffith 2004), and its plant feeders, is distributed in more than 20 states, where it infests 15 species of cacti (Chávez-Moreno et al. 2011); worldwide, it has been found in more than 29 countries (Méndez-Gallegos and Bravo-Vinaja 2022), and has caused devastating damages from its recent expansion in the basin of the Mediterranean, mainly in northern Africa and the Middle East (Bouharroud et al. 2016; Moussa et al 2017; Bader and Abu-Alloush 2019; Mazzeo et al 2019; Ülgentürk and Hocaali 2019; Bufaur and Bohamdan 2020; El Bouhissi et al. 2022), as well as from its potential expansion to new areas in northeastern Brazil (Torres and Giorgi 2018).
Because of the damages caused by D. opuntiae on Opuntia spp., particularly in Brazil and more recently in northern Africa and the Middle East, the scientific production about the methods to combat this pest has increased during the last 15 years. In a recent study, Méndez-Gallegos and Bravo-Vinaja (2022) found out that during the last decade more than 50 % of the scientific production related to D. opuntiae was focused on the application of tactics for its control, this was considered important to identify the types of control tactics that have been carried out to date to focus future lines of research.
The bibliometric approach allows for the analysis of large volumes of scientific documents, identifies the evolutionary changes of a specific field, and provides information on emerging research trends (Donthu et al. 2021). Likewise, bibliometrics, defined by Pritchard (1969), represent an essential tool to evaluate scientific production (Moral-Muñoz et al. 2020). This study has the objectives of identifying growth, control tactics, co-authorship networks, and emerging trends in scientific research related to control strategies of Dactylopius opuntiae Cockerell (Hemiptera: Dactylopiidae) using four bibliometric indicators to facilitate decision-making regarding the integrated management strategy of this pest to minimize the damage it causes.
Materials and methods
Sources of information and databases
In order to identify the trends in scientific production related to the strategies used in the control of D. opuntiae, the following databases were consulted: Cab Abstracts, Crossref, Google Scholar, Dimensions, Science Citation Index Expanded (SCIE) and Scopus.
Search strategy, refining process and adaptation of bibliographic records
The descriptor used for the extraction of published documents was «Dactylopius opuntiae». This was performed in the search fields of title, abstract and keywords to ensure that it had as its main theme the topics of interest. With the search words applied, 1 121 documents were recovered and sent to a database in Zotero software; then, these were subjected to a refining process to eliminate duplicated documents or those that did not address the theme. The final database used in the analysis had 99 documents published and indexed until March 2022.
So that this describes the type of control tactic used in the analyzed research, some keywords were added to each bibliographic record in the tags field: 1) Biological control; 2) Conventional chemical control; 3) non-conventional chemical control (plant oils, extracts, essential oils, fatty acids and detergents, among others); 4) Plant resistance; and 5) Others (where legal control, physical control, mechanical control, cultural control and ethological control were included).
Bibliometric analysis and scientific mapping
The documents were processed through four bibliometric indicators. According to Donthu et al. (2021), Growth and behavior of scientific production and Control strategies or tactics classification were classified as performance techniques, and both were obtained using Zotero and Excel. Instead, Co-authorship networks and validity through time were valued as scientific mapping techniques (Noyons 2005); in addition, the first one was recovered from the Co-authorship analysis procedure in VOSviewer software (van Eck and Waltman 2011); Research themes through time (1884-2022) was mapped using the co-occurrence of words methodology (van Raan 1993; van Eck and Waltman 2007) through authors or database keywords in VOSviewer. A database of bibliographic records was created in Zotero, and it was imported into VOSviewer in RIS format, which allowed creating and visualizing maps.
Results and discussion
Growth and behavior of scientific production
According to the search strategy, 99 publications were identified and extracted. Scientific production about Dactylopius opuntiae control tactics and their regularity increased in a progressive and sustained manner during the last seven years since publications quadrupled; this reflects the growing scientific interest in the theme (Fig. 1). This could be associated with the recent invasion of D. opuntiae in Brazil in 2001 (Torres and Giorgi 2018), and successively in northern Africa, the Middle East and other countries that exploit Opuntia spp. commercially. Israel and Lebanon stood out at the end of 2013 (Spodek et al. 2014), and Morocco in 2015 (Bouharroud et al 2016).
Source: Prepared by the authors, 2023.
Figure 1 Behavior and evolution of scientific production, regarding control tactics used for Dactylopius opuntiae. 1848-2022.
From 1848 to 2000, only 12 documents were found, most of them published in the last two decades. This trend coincides with the importance that Opuntia spp. acquired at the international level, driven by different international agencies during the last 30 years (Méndez-Gallegos and Bravo-Vinaja 2022), as a strategy to combat poverty, food safety and the reduction of desertification; likewise, the discovery of new properties and applications of cactus pear and its byproducts, which motivated the expansion of its cultivation and exploitation (Castellano et al. 2021; da Silva et al. 2021). The value of the coefficient of determination (R2) indicates, in this case, a moderate growth of scientific production throughout the period studied but in 2016-2022, the growth was higher.
Control strategies or tactics classification
Regarding the thematic areas of research addressed by the scientific publications, almost all the control tactics were mentioned in the 99 publications (20 of them were grouped into two research fields). However, there was an emphasis on the application of less invasive tactics, which could be more sustainable than conventional chemical control (Fig. 2). The most outstanding areas were focused, primarily, on biological control through predators and entomopathogens (48 %), with the following references: Vanegas-Rico et al. (2010; 2016); Bouharroud et al. (2018); El Aalaoui et al. (2019; 2022); Ramírez-Sánchez et al. (2019); Mendel et al. (2020); and more. On the other hand, non-conventional chemical control used various products such as oils, plant extracts, soaps, and detergents, which represented 21 % (Pérez-Ramírez et al. 2014; El Aalaoui et al. 2021; López-Rodríguez et al. 2021; Ramdani et al. 2021, among others). An important number of documents (14 %) corresponded to organo-synthetic insecticides, derived from the urgency of reducing the impact of damage immediately (Pretorius and van Ark 1992; Hernández-Pérez et al. 2019; Zeitoun et al. 2020).
Source: Prepared by the authors, 2023.
Figure 2 Control strategies of Dactylopius opuntiae addressed by scientific publications from 1848 to 2022.
After the tactics reported as most frequent, studies about plant resistance also stood out, with 13 % (Palacios-Mendoza et al. 2004; Vigueras et al. 2009; Passos da Silva et al. 2009; Sbaghi et al. 2019; Akroud et al. 2021; da Silva et al. 2021) . It is important to highlight that some essential tactics, such as legal control, ethological control, and mechanical control, were also common practices in many areas (Moran and Hoffmann 1987; Macêdo et al. 2014; da Silva et al. 2010; and El Aalaoui and Sbaghi 2021).
The bibliometric analysis of scientific literature showed that two control tactics used for D. opuntiae could be the most sustainable: 1) the selection and improvement of resistant varieties represent the most important tactic for management proposals of D. opuntiae in the world (Akroud et al. 2021), although the reproduction and replanting of these varieties are still a problem, particularly in northern Africa; on the other hand, the process of selection and improvement of varieties that are not destined to fodder, as in Brazil, northern Africa and most of the Middle East, can be longer and more complicated, as in the case of Mexico, with the selection for consumption of fresh vegetable or fruit cultivars with particular characteristics; and 2) classical biological control in Israel (Mendel et al. 2020) or conservation in Mexico (Vanegas-Rico et al. 2010; 2015; 2016; Cruz-Rodríguez et al. 2016; Barreto-García et al. 2020) represent the best alternatives. The use of chemical control, particularly non-conventional, is one of the complementary tactics with the highest impact in the strategy of integrated management, together with legal and mechanical control, which should not be dismissed.
Co-authorship networks and their validity through time
The co-authorship patterns of the researchers indicated how these are related and participate in processes of research and publication (Fig. 3). For practical purposes, the scientific production was concentrated in three countries, primarily Brazil, Morocco, and Mexico. This could be associated with the fact that they are the countries where damage from D. opuntiae on Opuntia spp. caused the greatest socioeconomic impact in the last 15 years. In Brazil, the presence of four important research groups of authors: 1) Antonio Felix da Costa, Patricia Vieira Thiago, Luciana Gonçalves de Oliveira; 2) Djalma Cordeiro dos Santos, H. Marinho Falcao, Cavalcanti Vanildo Leal Bezerr; 3) Cesar Auguste Badji, Edcleyton José de Lima, and Keila Aparecida Moreira; 4) Jacinto de Luna Batista, Ivanildo Cavalcanti de Alburquerque, Carlos Henrique de Brito and Edson Lopez Batista. These authors mainly belong to Empresa Pernambucana de Pesquisa Agropecuaria (IPA), Universidade Federal de Pernambuco, the Agronomical Institute of Pernambuco, and Universidade Federal do Agreste de Pernambuco. Likewise, this country also stood out for having the highest number of participating researchers who have published constantly since 2010.
Source: Prepared by the authors, 2023.
Figure3. Co-authorship networks, and their distribution throughou time, which addressed the Dactylopius opuntiae control tactics, 1848-2022.
In Mexico, research involves mainly four institutions: Colegio de Postgraduados, Universidad Autónoma Chapingo, Universidad de Guadalajara and Instituto de Investigaciones Agrícolas y Pecuarias (INIFAP). It is also important to highlight that one of the active work groups is represented by Rodríguez-Leyva, and Lomelí-Flores, from Colegio de Postgraduados, which maintains close collaboration with other authors, such as Vanegas-Rico, Méndez-Gallegos, Mena-Covarrubias, and Portillo.
In addition, they are the researchers that have established, together with Dr. Zvi Mendel and Colegio de Postgraduados, the first international program of classical biological control of D. opuntiae in Israel (Mendel et al. 2020); this program seems to evidence success that should be corroborated and disseminated among the rest of the countries of the Mediterranean and the Middle East.
In Morocco, the collaboration pattern is constituted by the network of authors of more recent appearance (mainly Bourrahoud, Sbaghi and El Aalaoui) concentrated particularly in two institutions: Institut National de la Recherche Agronomique (INRA) and the International Center for Agricultural Research in the Dry Areas (ICARDA) (Fig. 3). The research groups from Brazil and Mexico have remained in force for a longer period, perhaps due to the severity of the damage caused by D. opuntiae in those countries and the economic and social importance of Opuntia spp.
Although there is a collaboration pattern of working groups between education and research institutions at the national level -which established networks to address this problem and take better advantage of its capacities and infrastructure, particularly in Brazil and Mexico- it was observed that there is a reduced rate of international collaboration and publication in high-impact journals. The most recent example of international collaboration, and apparently the most successful, is the program for classical biological control of D. opuntiae between Mexico and Israel (Mendel et al. 2020).
Research topics through time (1848-2022)
The analysis of the co-occurrence of words in the publications allowed establishing a complete outlook on D. opuntiae control tactics as well as a relationship with the descriptors. To ease the understanding of Figure 4, the terms recorded with the highest frequency are shown in the largest circles; in the same way, the closeness between words determines the degree of association, and the lines connecting the words indicate that the terms are related regardless of their closeness or distance. For their part, darker or lighter colors indicate closeness in terms of the time these documents were published. From the 400 terms obtained, 55 appeared at least 5 times during the period 1848-2022 (Fig. 4).
Source: Prepared by the authors, 2023.
Figure 4 Topic network and its distribution throughout time, which addressed Dactylopius opuntiae control tactics, 1848-2022.
The co-occurrence analysis of words created a visualization of the research trends related to the topics of study; this way, it showed that the term that appeared cited most frequently refers precisely to the scientific name of the species: Dactylopius opuntiae. The next term that had a high frequency was 'biological control', primarily predators and entomopathogens, which indicates the importance of this tactic in insect control around the world; in addition, it is a term that has remained current through time. Other outstanding nodes refer to the countries that have focused on the theme and developed high scientific productivity: the USA, Spain and Africa were remarkable initially; continuing with Mexico and Brazil; and then the most recently incorporated countries were Morocco and Israel.
Figure 4 represents the regions within each country where the problem with D. opuntiae is concentrated to a greater degree; for example, Pernambuco in Brazil, Milpa Alta (Mexico City) and Tlalnepantla (Morelos) in Mexico. The following stood out as emerging themes: plant resistance through the selection, improvement, and testing of D. opuntiae clones, as well as biological control and non-conventional chemical control using plant extracts, detergents and plant oils, among others.
Although the terms chemical control, pesticides and commercial insecticides stand out, their use has been applied to indicate the importance of the mentioned tactics, and they represent an alternative to the application of chemical products. Regarding this aspect, there's a need to highlight that a small proportion of the studies addressed conventional chemical control, and that it was focalized at the beginning of the observation period. Deriving from this, the research has been concentrated, at least during the last decade, on the search for more sustainable alternatives, such as biological control and products with a lower environmental impact. Finally, the visualization showed that the highest correlations between these terms were recorded between 2017 and 2019. Derived from this, the strategy for pest control could include some of the tools that are adaptable and replicable in the various regions with this phytosanitary problem.
The research themes with high potential for application could be focalized on the technological development of: new low-toxicity and residual, biodegradable molecules with low risk for health and the environment, as well as a greater selectivity to non-target organisms; identification of secondary metabolites with insecticide activity; selection of entomopathogenic strains and natural enemies, according to each environment in particular where cactus pear is cultivated; and improvement and multiplication of clones with resistance to D. opuntiae, primarily.
Conclusions
The bibliometric study of scientific production on D. opuntiae control tactics was a relevant and appropriate theme of interest for the international community, evident due to the increase in publications in the last 12 years. The countries that showed leadership regarding scientific production were Morocco, Brazil, and Mexico.
The emerging themes were concentrated in the search and evaluation of biological control agents: predators and entomopathogens were the most studied topics; plant resistance also stood out as the tactic that could be most sustainable. After these two, non-conventional chemical control (oils, plant extracts, soaps, and detergents) was the most reported emergent tactic, in agreement with Sabbahi and Hock (2022) for the case of Morocco.
Through the analysis of the scientific information, it was detected that a common control tactic applicable to all the regions suffered from this problem since each region presents diverse conditions and its control agents would not have the expected successful results.
Considering the imminent globalization of knowledge as a priority, promoting collaboration networks with researchers and institutions at the national and international level is an area of opportunity, that facilitates the adoption and validation of management technologies; they could promote and disseminate the scientific development related to D. opuntiae control strategies, which allows taking advantage of synergies, capacities, and resources.
Finally, facing the critical current phytosanitary situation of cactus pear at the international level requires implementing a multidimensional intervention strategy, adaptable and replicable for the management of D. opuntiae that should consider the productive, social and climate conditions of each region.
The creation of clusters or research consortia, through the intervention of various institutions related to the subject, could improve the generation of common control alternatives for D. opuntiae in less time and with greater impact, such as the one established in Brazil.
