Trends and New Developments in Artemia Research

Simple Summary Artemia is an important crustacean group, especially for aquaculture live food and as a model organism for toxicity assessment. The present study aimed to identify the current trends, research gaps, and literature development in the study of Artemia around the world. This primitive Arthropod has undergone significant evolution in terms of its application in various industries as well as relevant literature patterns in terms of scientometric analyses. Abstract An increasing number of scientists since 1970 has examined Artemia as an important species in aquaculture-related fields. However, a global scientometric review of Artemia literature is still lacking, which is the objective of this research. Using a CiteSpace analysis, the distribution of core authors and institutions, highly cited keywords and papers, author and journal contributions, and hot topics in the literature, as well as a co-citation analysis, particularly regarding authors, journals, documents, and clusters, were determined. Hence, 8741 relevant publications were generated from the Web of Science Core Collection database. The results revealed that the most significant contributions in Artemia research primarily originated from the USA, Brazil, Spain, India, China, and Belgium. Moreover, Artemia research focused mainly on top keywords such as brine shrimp and antimicrobial activity. Emerging trends related to Artemia research were Atlantic halibut, elongation factor, Artemia salina, lean protein, inert diet, alpha-crystallin protein, and Artemia embryo. At the same time, the study generated a vast total of 45 co-citation clusters. The present study provides the existing body of knowledge on Artemia research by sharing a visual knowledge map. This study offers a valuable perspective and profound understanding for researchers, farmers, and consortia interested in promoting Artemia as a sustainable live food in the global aquaculture industry.


Introduction
Artemia, or brine shrimp, is a primitive group of Arthropods with sizes between 8 and 12 mm. They are endemic to Asia, Europe, Africa, and Australia. They are sexually reproducing or bisexual species; few are parthenogenetically reproducing populations [1]. Historically, Artemia was considered a potential economic commodity species as early as the 1930s, and it was commercially marketed around the 1950s. Naturally, the Great Salt Lake in the USA was the first available natural habitat for the Artemia. However, because of their increasing demand for marine fish and crustacean larviculture [2], many inland salt lakes have emerged, such as in Bohai Bay, China, southern Siberia, Kazakhstan, and seasonal

Survey Methods
The details of the research framework used in this study are shown in Figure 1. The survey methods include a description of the metadata search and a scientometrics-based analysis. To conduct our scientometric analysis, we followed the protocol outlined by Chen [15].

Data Sources
The database from Web of Science (WOS) is used to administer a manuscript search for a scientometric review. We concentrated on the navigation of the entire citation network of the WOSCC database of subscription materials, which is regarded as one of the top databases of scholarly journals, books, and proceedings in the sciences, social sciences, and arts as well as humanities in the world. Major bibliographic sources, such as WOS, routinely include cited references, whereas other sources, such as PubMed and China National Knowledge Infrastructure (CNKI), do not include cited references [15]. Additionally, for these reasons and because of its wide coverage of different disciplines, as stated above, we focused on using WOS to retrieve scientific literature.

Article Search
The "subject" (TS) field served as the basis for the WOS article searches, which included article titles, keywords, abstracts, and "KeyWords Plus". The keyword "Plus" is a generated term pulled automatically from the titles of cited articles in the WOS database. Artemia species' common names and available scientific names were based on the Food and Agriculture Organization of the United Nations (FAO) catalog published on their respective website or referred to on their "Cultured Aquatic Species Information Programme" for the Artemia group [1]. We used two tags in WOS: the Boolean function (OR) and asterisk symbols (*). The asterisk symbols were applied to identify variations in the keywords

Data Sources
The database from Web of Science (WOS) is used to administer a manuscript search for the scientometric review. We concentrated on the navigation for the entire citation network of the Core Collection of subscription materials, which is regarded as one of the top scholarly journals, books, and proceedings in the sciences, social sciences, and arts and

Eligibility Criteria
Several eligibility criteria are required for conducting the scientometric review, especially during the scientific literature search. Firstly, the research articles are original research papers written in English. In addition, we exclude studies in the form of conference papers, chapters in a book, review papers, letters, editorials, and abstracts. Such articles were excluded because they might complicate the analytical process, since they might add any tangible value to the analyzed results. However, our results may include books and chapters within a book because the co-citation analysis automatically includes books/chapters when they are cited by original research articles.

Data and Scientometric Analysis
CiteSpace was used to analyze the metadata for the present study, which will support the data mining from WOS through the visual summarization features of Artemia research. The present study used CiteSpace V version 6.1.R2, Basic (built 6/20/2022; expires 31 December 2022) for 64-bit Windows along with Microsoft Office Professional Plus 2019, the Excel spreadsheet software (i.e., apps). A co-citation instance occurs when two sources are cited in a single work, and a co-citation analysis of journals, authors, and articles was determined to acquire a cluster of co-citing factors [16][17][18]. A variable's quality was apprised using degree, centrality, and sigma [15].

Productive Authors
There were a vast number of authors involved in the Artemia research, 23,632 authors, from a total of 51 years of publications. The average number of authors is 463 authors per year. The author with the highest publication is known as "Father of Artemia", Patrick Sorgeloos, from Ghent University, Belgium, with 190 related publications, followed by his colleague, Peter Bossier with his international collaborators, Thomas H. MacRae from Dalhousie University, Canada at the third most published author in Artemia related research in the world, based on the WOS Core Collection database (Table 1).

Productive Authors
There was a vast number of authors involved in Artemia research: 23,632 authors, from a total of 51 years of publications. The average number of authors is 463 authors per year. The author with the highest number of publications is known as the "Father of Artemia", Patrick Sorgeloos, from Ghent University, Belgium, with 190 related publications, followed by his colleague, Peter Bossier, with his international collaborators, and Thomas H. MacRae, Animals 2022, 12, 2321 5 of 18 from Dalhousie University, Canada, as the third most published author in Artemia-related research in the world, based on the WOS Core Collection database (Table 1).

Productive Journal
We detected eligible papers from 1554 journals in total. Of these, Aquaculture had the most publications (628 publications), almost triple that being published by Aquaculture Research (239 publications), followed by Hydrobiologia (119 publications) ( Figure 4). During the 51 years of publication, most journals released an average of 5.6 articles (1970-2021).

Most Cited Article
This subsection indicates the most cited article in Artemia research in the world, based on the WOSCC database ( Table 2). The results indicated that the article entitled "A review of toxicity testing protocols and endpoints with Artemia spp." received the highest total number of citations, which was published in the peer-reviewed journal Ecological Indicators [19]. The book published by McLaughlin [20] is the second most cited scientific publication on Artemia research, followed by the study by Rajabi et al. [6] on the ability to use Artemia as a model organism for toxicity assessments. This result was based on the cluster analysis, which was automatically generated from the CiteSpace software. 3.1.6. Regional Distribution Fifty-one different countries had relevant publications on Artemia research ( Figure 5). The USA, Brazil, Spain, India, China, Belgium, Japan, Pakistan, Italy, and Germany contributed the most published articles in Artemia research (> 300 publications), with these top 10 countries accounting for 68.24% of the total publications. Our findings also revealed that less than a quarter of the world's countries (51/195) are actively researching Artemia.

Co-Citation Analysis
Co-citation analysis creates a science map with connections, nodes, and density values to depict the main structure of a variable's development status and changes over time.
The results of the co-citation analysis are shown below for author, journal, country/region, institution, and article document.

Author Co-Citation Analysis
Author from Purdue University, USA, Brian N. Meyer is the most influential author in the field, with the highest 400.34 sigma score compared to the next most influential author, Ulrich K. Laemmli, previously from the Medical Research Council (MRC) Laboratory of Molecular Biology, and currently affiliated with Université de Genève, Geneva, Switzerland, with the 164.77. The third most influential author based on the sigma score is Oliver H. Lowry from Washington University, USA (Table 3). However, based on Figure 6, the most cited author is Patrick Sorgeloos, from Ghent University, Belgium.

Co-Citation Analysis
A co-citation analysis creates a science map with connections, nodes, and density values to depict the main structure of a variable's development status as well as changes over time. The results of the co-citation analysis are shown below for authors, journals, countries/regions, institutions, and article documents.

Author Co-Citation Analysis
An author from Purdue University, USA, Brian N. Meyer, is the most influential author in the field, with the highest sigma score (400.34). The next most influential author, Ulrich K. Laemmli, previously from the Medical Research Council (MRC) Laboratory of Molecular Biology, is currently affiliated with the Université de Genève, Geneva, Switzerland, with a sigma score of 164.77. The third most influential author based on the sigma score was Oliver H. Lowry from Washington University, USA (Table 3). However, based on Figure 6, the most cited author is Patrick Sorgeloos, from Ghent University, Belgium.

Journal Co-Citation Analysis
Only journals with centrality scores greater than 0.1 are shown in the knowledge map of the journal co-citation analysis (Figure 7). High-impact journals, such as Science and Nature, are among the most cited journals in the field, along with Aquaculture and the Journal of Experimental Biology. Two different journals received the highest sigma score in Artemia research (> 90.0), which were the Biochemical Journal and the Archives of Biochemistry and Biophysics (Table 4). With a sigma score of 47.38, the Journal of Agricultural and Food Chemistry (IF: 5.279) was the third most influential journal.

Journal Co-Citation Analysis
Only journals with centrality scores greater than 0.1 are shown in the knowledge map of journal co-citation analysis (Figure 7). High-impact journals, such as Science and Nature, are among the most cited journals in the field, along with the Aquaculture and Journal of Experimental Biology. Two different journals received the highest sigma score in

Document Citation Analysis
The results only included articles with a centrality score greater than 0.1 (Figure 8). Hand and Gnaiger's [27] article was the most influential in this field, with a sigma score of 2.14. Liang and MacRae [28] were the authors of the article with the second highest sigma value (1.96), followed by the study entitled "The American brine shrimp as an exotic invasive species in the western Mediterranean" by Amat et al. [24], with a sigma value of 1.64 (Table 5). The results only included articles with a centrality score greater than 0.1 (Figure 8). Hand and Gnaiger's [27] article was the most influential in this field, with a sigma score of 2.14. Liang and MacRae [28] were the authors of the article with the second highest sigma value (1.96), followed by the study entitled "The American brine shrimp as an exotic invasive species in the western Mediterranean" by Amat et al. [24], with the sigma value 1.64 (Table 5). Figure 8. The network of document co-citation analysis exclusively shows articles with centrality scores greater or more than 0.1. Figure 8. The network of the document co-citation analysis exclusively shows articles with centrality scores greater of more than 0.1. 3.2.5. Document Cluster Analysis Ten significant group clusters were discovered through a document cluster analysis in the CiteSpace software, and each row in Table 6 represents a different research topic. The clusters were numbered and ranked in order of size, with #0 being the largest. Ten different clusters were summarized on a horizontal line, with the cluster label on the right side of the figure (Figure 9). The solid yellow line within each cluster represents the cluster's lifetime. The cluster's size is equal to the number of publications that it has. The top 10 clusters all have more than 134 publications, with cluster #0 having the greatest number of publications, 291 articles.  Figure 9. Summary of identified top 10 document cluster lifetimes (solid lines). Cluster labels were generated from CiteSpace. Figure 9. Summary of the identified top 10 document cluster lifetimes (solid lines). Cluster labels were generated from CiteSpace.

Keywords' Cluster and Burstiness Analysis
The keywords "brine shrimp", "growth", and "survival" were the top three highly cited keywords in Artemia research (Table 7), and the most popular keywords used are shown in Table 8. Typically, keyword analysis has been utilized to uncover developing trends and study hotspots. As shown in Table 9, the red line represents the burstiness period, and the blue line represents the timeline (from 1970 to 2021). We used a burst analysis to identify the most influential or landmark publications and keywords; trends among studies and keywords are described below. The greatest citation burst was "antimicrobial activity", and this was the most vital burstiness keyword in Artemia research.       Artemia franciscana 320 extract 304 Table 9. Top ten keywords with the strongest citation burst.

Keywords
Year Artemia franciscana 320 extract 304 Table 9. Top ten keywords with the strongest citation burst.

Keywords
Year Artemia franciscana 320 extract 304 Table 9. Top ten keywords with the strongest citation burst.

Keywords
Year

Discussion
Our research sought a scientometric analysis for global studies on the current trends and advancements in Artemia-related literature. Artemia has become a crucial live food for the early phase of juvenile production in the aquaculture industry, especially in marine fish culture. Additionally, Artemia has become a model organism for toxicity-based assessments for various chemical compositions. Thus, any research on Artemia could attract various early career researchers or consortia to perform or refer to Artemia-related studies. Our study represents the first attempt to analyze Artemia research publications through a scientometric analysis using the CiteSpace software. We discuss our results in detail below.

Evolution of the Publications
Research on Artemia has been published more often over the years, reaching more than 100 manuscripts per year in 1991. The trend intensified when sudden increases were also spotted at the same time between 1990 and 1991. This surge is well-known in the scientometric community because of WOS's "artifact" effects [34]. The artifact has been caused due to the restriction of this database search only for the titles, while the searching strategies for the present studies are stated on "titles, abstracts and keywords". Over the last five decades, a vast number of researchers has been involved in Artemia research, reaching almost 24,000 authors in 2021, and three out of the top ten authors mostly come from the same institution: Ghent University, Belgium. As shown by a previous animal-based scientometric analysis [35], the problems with identifying unique authors cannot be ruled out for comparison with the present study, especially for the number of authors involved in Artemia research. Patrick Sorgeloos was the most productive author, from Ghent University, Belgium. This achievement could be attributed to the early publication of Artemia studies mostly from his works and institution [36], especially on Artemia's potential in the aquaculture industry. There are also many institutions involved in Artemia research (4739 institutions), although the number of countries does not reach 30% of the total countries in the world ( Figure 5). It would also be fascinating to compare these results with other scientometric animal-based research on zebrafish. However, no data are available for the total number of affiliations involved in a relevant study [35]. Even though a total of 500 Artemia sites have been discovered worldwide [23], the total number of papers published based on country remains lower. Here, we strongly advocate that more international scientific research exchanges and collaboration should be conducted in the future.
The top two journals that published Artemia research are based on aquaculture, which are Aquaculture (London, UK; publisher: Elsevier) and Aquaculture Research (Publisher: Wiley-Blackwell Publishing Ltd.), the latter of which is the top journal that has published the highest number of articles related to Artemia research. Both journals support articles related to basic and applied works on the improvement of freshwater, brackish water, or marine aquaculture research and development. This fact is also supported by the aquaculture potential of Artemia as an early live food, mostly for commercially important aquaculture species in the world [37]. Based on the top 10 citation counts of published research manuscripts related to Artemia research, 40% of the articles were toxicity-related studies on Artemia [6,19,20,26], biology-related fields [23][24][25], aquaculture [4,21], and others [22]. The trends showed that most of the highly cited literature was related to Artemia as a model organism in toxicity-related studies.
Interestingly, there are a few prominent authors who published Artemia research but whose work was not captured in the WOSCC database because it was published in book series [38][39][40]. Some authors excluded in this way include John A. Beardmore, Robert A. Brown, Joseph C. Bagshaw, Gonzalo Gajardo, and Theodore Abatzopoulos. All of these researchers are very popular in their field and are editors and/or corresponding authors for most Artemia-related research [38][39][40].

Co-Citation Trending Topic
Previous studies have shown that co-citation datasets have been used to identify collaborative networks. Most focused on the influential research of authors, journals, and documents involved in a selected theme [41]. The author co-citation analysis indicated a huge difference between the top three co-cited authors among the top ten, as listed in Table 3. The top three co-cited authors had the highest sigma scores, all more than 100. This ranking could indicate that most of their article(s) are being referred to, since the co-cited authors were analyzed using sigma scores. Authors should improve the quality of their papers and collaborate with others to increase their sigma scores and gain more citations. Surprisingly, all influential authors are researchers from the 20th (twentieth) century, which could also indicate that recently published papers in the 21st century lack collaborative research. The same is true for the journal co-citation analysis, which indicated that all journals were at their peak in the 20th (twentieth) century. The sigma score is also one of the most vital metrics for determining the most influential journal in the proposed field of research.
A "central" article serves as a mediator in the document co-citation analysis. In Artemia research, no article can be stated as a central article based on Figure 8. The article produced by Hand and Gnaiger [27], Liang and MacRae [28], and Amat et al. [24], according to the sigma scores, are among the top ten most influential scientific publications. Hand and Gnaiger [27] briefly explain the calorimetric test to quantify anaerobic dormancy in Artemia embryos. Meanwhile, the study by Liang and MacRae [28] tested the ability of a small heat shock protein, known as p26, to protect Artemia from thermal stress, and they found that p26 has a key role in Artemia's reproduction process. Furthermore, Amat et al. [24] reviewed the distribution of Artemia populations in the western Mediterranean region and their origin. They also compared the impacts of Artemia invasive species on the available native counterparts in the region. They suggested that the aquaculture industry was introducing invasive species and that the native species in the region can rapidly replace invasive species.
In the document cluster analysis, the top three clusters that emerged in the Artemiarelated research were Atlantic halibut, elongation factor-i, and Artemia salina; the most recent cluster was #2, Artemia salina. This analysis suggested that Artemia salina Leach had been used worldwide in recent years, with the important marine flatfish, Atlantic halibut, being incorporated into Artemia research.
The keyword with the highest count was Artemia salina, suggesting that this species is one of the most used research species in the field. According to experts, the most used Artemia species is actually A. franciscana, suggesting a disconnect between published science and aquaculture practices. Future research could consider the main differences between these species and why they seem to be used for different reasons. Perhaps A. salina is better suited for research purposes, particularly when research is not solely focused on Artemia but instead is secondary to the research question. The most recent keyword in the Artemia research was "antimicrobial activity" (strength = 23.17, 2011-2021), and the same keyword was also categorized as having the strongest citation burst among the other keywords in the field. The following top keywords were "requirement" (strength = 19.58, 1999-2008) and "decapoda" (strength = 18.99, 1997-2008).
Artemia is produced in every continent except for Antarctica [42][43][44][45][46][47]. Moreover, previous studies have also shown some information about the bibliometric knowledge on live feed such as Artemia [47], but did not focus on a detailed explanation of the studies, in contrast to the present study.

Conclusions
Artemia research is wide-ranging and spans many fields, yet the body of Artemia research focuses on two topics: its use as an aquaculture feed in fish/shellfish larviculture, and as a model organism in toxicology assessments [6,19,21,26,31]. The author who most consistently ranked highly in our qualitative and co-citation analyses was Brian N. Meyer, from Purdue University. The most influential and most well-cited author in Artemia research was Patrick Sorgeloos, from Ghent University, Belgium. Our results also suggested that Artemia: Basic and Applied Biology [48] is the most influential reference, based on the sigma score of the cluster analysis.

Limitations and Recommendations
The current study has some limitations, including the fact that it only focused on papers from a WOS database, which could have led to publication bias and the exclusion of important field-specific works (e.g., the FAO Manual [49]). Even though our exclusion criteria should have excluded books, some book chapters were still identified in our results due to the nature of the co-citation analysis. Data downloaded from WOSCC include works that are cited by primary articles, which can help reduce some of the publication bias in our data analysis. However, it can cause some important books to still be excluded. Thus, we suggest the incorporation of additional databases that have detailed article information (e.g., titles, authors, abstracts, citations, co-citations, etc.), such as PubMed, China National Knowledge Infrastructure (CNKI), and Chinese Social Sciences Citation Index (CSSCI) [50]. We also recommend that scientometric analyses be started from early 1991 onwards to avoid any data confusion caused by the "artifact effect", especially when searching in the WOSCC database.