RETRACTED: Crayfish Research: A Global Scientometric Analysis Using CiteSpace

Abstract

Simple Summary

Here, we strive to summarize the current literature on crayfish research. Using scientometric analysis, we identified the top contributing researchers, the top-cited research articles, the most popular journals, top areas in the field, most influential articles and most keywords used, etc. The most common themes among these top research articles were related to invasive crayfish species as well as the neurochemistry of crayfish.

Abstract

A scientometric analysis was conducted to investigate the trends and development of crayfish research in terms of literature published, author, affiliation, and countries’ collaborative networks, as well as the co-citation dataset (e.g., author, article, and keywords). The study analyzed 12,039 bibliographic datasets from the Web of Science, using CiteSpace as a tool for the co-citation analysis. The study revealed extraordinary increases in publication trends, with a total of 21,329 authors involved in approximately 80% of countries around the world (163/195) having conducted crayfish research. Unsurprisingly, countries such as the USA and China, followed by European countries, were among the top countries that have published crayfish-related studies. The findings also indicated that “invasive crayfish” was the world’s top keyword for crayfish research. Crayfish species are important for both environmental sustainability (invasiveness and species composition) and social wellbeing (aquaculture), which provides directions for research, philanthropic, academic, government, and non-government organizations regarding how to invest limited resources into policies, programs, and research towards the future management of this species. Our study concluded that strategic collaboration among authors, institutions, and countries would be vital to tackle the issue of invasive crayfish species around the world.

1. Introduction

Freshwater ecosystems are the most important for crayfish. Crayfish are aquatic crustaceans typically found in freshwater environments such as rivers, streams, and wetlands [1]. They play a vital role in these ecosystems as they have a wide range of ecological roles, including acting as key functional species, keystone species, and ecosystem engineers [2]. Crayfish are also important food sources for many aquatic animals, and their presence can have a significant impact on biodiversity in freshwater ecosystems [3].

Crayfish can be found on all continents except Antarctica and continental Africa [4]. They have a wide range of habitat usage and food source preferences. Some species of crayfish are restricted to rivers, streams, and small lakes, while others are characteristic of wetlands outside main drainages. Some burrowing crayfish live essentially terrestrially, and their ecological roles relate to terrestrial ecosystems [5]. Crayfish are known to affect biodiversity differently in various compartments of the aquatic ecosystem [6]. Furthermore, crayfish are opportunistic feeders, eating whatever is available to them in their habitat, including plants, insects, and other aquatic animals [7].

Crayfish have the potential to become an invasive species when introduced to new ecosystems. The pet trade is a major source of introduction of new non-indigenous crayfish species [8,9,10], and has led to the introduction of several species in European countries and other places worldwide. These introductions have the potential to negatively impact native species and disrupt the balance of the ecosystem.

The pet trade and crayfish aquaculture have led to the distribution of several species worldwide. The trade in crayfish has been systematically examined in several countries, with an estimated 130 crayfish species reported as available for sale as pets [4,11]. Most of these species originate in North America and Australasia. However, many species are sold under incorrect names, which could lead to confusion in identifying them. Additionally, many of these species have been introduced to new ecosystems through the pet trade, and this has led to the establishment of non-indigenous populations in several countries. This could have a negative impact on the ecosystems they were introduced to [12,13].

Despite their high importance in crustacean aquaculture development and their substantial contribution to the loss of aquatic biodiversity [12,14], systematic scientometric studies on crayfish are still scarce. Bibliometric quantitative analyses, such as scientometric analyses, are deemed useful for investigating the development of selected scientific disciplines and research programs over time [15,16]. Such studies are crucial for academics, researchers, and companies or consortiums that are working on crayfish-related studies to unravel the potential research gaps and available opportunities for future research and development plans, aquaculture business investments, and policymaking [17,18].

CiteSpace is a software package known to be a visual analytical tool for identifying the landscape, pattern, and emerging trends in a field of research or any knowledge domain on the basis of selected literature databases, e.g., Web of Science (WoS) and Scopus [19]. Citespace and VOSviewer are common software packages used to analyze bibliometric results for the process of mapping science based on different algorithms [20,21,22]. The scientometric analysis is considered a type of scientific review that objectively maps the current scientific knowledge area and can identify research themes as well as challenges or gaps in the literature [23]. In this scientometric analysis, the descriptive and co-citation datasets were generated to explain the current knowledge of the selected research themes. Notably, the topics focused on crayfish in the published reviews ranged from the aquacultural potential of crayfish [4,24], environmental and culturing practices [25,26], records of their introduction in the European and African regions [27,28], and crayfish-related diseases [26,29,30,31,32] to ecological interactions and biodiversity [33,34,35,36].

In addition, despite the growing numbers of review articles and original research, studies conducted on bibliometric assessments of the research literature on crayfish are lacking. This type of study is predicted to contribute to better coordination of sustainable management practices and further implementation processes in the future.

In this study, we reviewed the trends and developments in the crayfish literature to better understand the progress and constitution of various collaborative and emerging fields. Specifically, the major component of this study was to analyze the descriptive data and visual networks of crayfish research through (i) selected descriptive datasets on the topic of interest; (ii) time series networks in order to track the underlying landscape of the crayfish literature; (iii) the evolution of crayfish research in terms of a cluster analysis over time, as well as the distribution of their citations; and (iv) the growth potential of crayfish research.

2. Survey Methodology

In this section, we describe our methods for analyzing the scientific patterns, trends, and developments in crayfish research, as summarized in Figure 1. We categorized the data we used throughout our descriptive and scientometric analyses, and we outlined the two approaches used to assess both types of metadata. The descriptive dataset was analyzed using traditional techniques in Microsoft Excel 2019 spreadsheet software, as well as through the web-based Google Docs editors and Google Sheets. On the other hand, the advanced techniques of CiteSpace software version 6.1.R2 for 64-bit Windows were used to conduct panoramic and knowledge graph analyses (i.e., scientometric-based analyses). The WoS Core Collection was the only database used for the present study, as it is considered the biggest accessible database for bibliometric analyses based on the scientometric technique [37]. The downloaded data were generated for publications from 1971 to 2021.

Figure 1.

The research flow chart for the analysis of crayfish research around the world.

2.1. Descriptive Analysis

The metadata of a publication used for the descriptive analysis included the total number of publications, the list of authors, the primary and secondary sources, the institution or university, and the country or region actively involved in the research. This type of metadata helped us answer our first objective, which was to identify the selected descriptive dataset on the topic of interest. All sources of terms, including the title, abstract, author keywords, and additional keywords, were chosen for text processing (*.txt).

2.2. Scientometric Analysis

Typically, the cited references, as well as the list of important keywords in the article (e.g., research or review article), are important for scientometric-based analyses. The scientometric techniques of CiteSpace provide a few indicators based on these data, which include a dual map overlay, a burstiness view, clustering, labeling, and a timeline view [38,39]. These types of indicators allowed us to track: (i) the underlying landscape of the crayfish literature through the dominant knowledge carriers; (ii) the evolution of crayfish research in terms of a cluster analysis over time; and (iii) the great potential for the growth of research, based on the impactful publications and keywords.

The main keywords “crayfish” and “crawfish” captured all the literature in the selected database, and the addition of the species’ names was only for the supporting keywords. The following search code was used based on a previous review and factsheets on crayfish in the world created by Gherardi (2010) and FAO (2020): (“crayfish*”) OR (“crawfish”) OR (“cray-fish”) OR (“Cherax sp.”) OR (“Cherax destructor”) OR (“Cherax quadricarinatus”) OR (“Cherax cainii”) OR (“Procambarus sp.”) OR (“Procambarus clarkii“) OR (“Procambarus virginalis“) OR (“Procambarus fallax”) OR (“Orconectes sp.”) OR (“Orconectes immunis”) OR (“Orconectes rusticus”) OR (“Orconectes virilis”) OR (“Orconectes limosus”) OR (“Astacus sp.”) OR (“Astacus leptodactylus”) OR (“Astacus astacus”) OR (“Pacifastacus leniusculus”) OR (“Faxonius sp.”) OR (“Faxonius virillis”) OR (“Faxonius rusticus”) OR (“Faxonius limosus”) OR (“Faxonius immunis”) OR (“Faxonius hylas”) OR (“Faxonius barrenensis”) OR (“Faxonius wagneri”) OR (“Faxonius quadruncus”) OR (“Faxonius forceps”) OR (“Faxonius macrus”) OR (“Faxonius roberti”) OR (“Faxonius obscurus”).

2.3. Glossary (Concepts and Metrics)

Some important terms are used in scientometric studies that should be explained for a better understanding. The most commonly used ones are described below.

2.3.1. Betweenness Centrality

The betweenness centrality is defined for each node in a network. It measures how likely the arbitrary shortest path in the network will go through the node. A node with a high betweenness centrality is likely to sit in the middle of two large communities or subnetworks, hence the term betweenness. In CiteSpace, a node with high betweenness centrality is shown with a purple ring. The thickness of the purple ring depicts the value of the betweenness centrality. The use of betweenness centrality in CiteSpace is guided by structural hole theory. The theory was originally developed for social networks. An insightful observation is that connectivity, or the lack of it, can guide us to find the most valuable nodes in a network. CiteSpace builds on these theories to detect the boundary-spanning potential and novel brokerage connections in scholarly publications.

2.3.2. Citation Burst

A burst refers to a surge in the frequency of a particular type of event, for example, a surge in citations of a Nobel Prize-winning publication. For instance, CiteSpace supports burst detection for several types of events, including single- or multi-word phrases from the title, abstract, or other parts of a publication; the number of citation counts for the cited references over time; the frequencies of keywords appearing over time; and the number of publications by an author, an institution, or a country.

2.3.3. Co-Citations and Co-Occurrences

Co-citations refer to a situation where two references are cited by a third article. Traditionally, as long as two references are cited anywhere within the third article, they are considered co-cited. If the full text of the third article is available, one can narrow down the scope to sections, paragraphs, or sentences. Citing a reference may serve many purposes and be motivated by various reasons. However, the way a reference has been cited may function similarly to referencing an underlying concept.

2.3.4. Modularity and Silhouette Scores

The modularity of a network gives us an idea about the internal structure of the network. When the structure is highly modularized, it means the network essentially consists of some loosely coupled components (subnetworks), and its modularity is moving to the highest end, namely a score of 1. In contrast, if all the components of the network are tightly coupled, then its modularity is moving towards the low end of the metric, i.e., a score of 0. The silhouette score of a cluster measures the homogeneity of the cluster, which is used to answer the question of whether the cluster’s members are lumped together according to what they have in common in some aspects. In other words, a cluster with a high silhouette score is considered more meaningful than a grouping with a low silhouette score.

2.3.5. Pathfinder Network Scaling

In a given network, its pathfinder network is the combination of all its minimum-spanning trees. Alternatively, a pathfinder is also defined as a network scaling process. The process removes the links in a network that violate the assumption of triangular inequality. The network of the remaining links is the pathfinder network. A pathfinder network can be considered a compromise between a network with an excessive number of links and its potentially arbitrarily chosen minimum spanning tree.

The CiteSpace software allows the users to prune a network, i.e., to reduce the number of links and retain the most salient ones. A network can be pruned to a pathfinder network or a minimum spanning tree, especially when the total number of links in the network is excessive.

2.3.6. Sigma

Sigma highlights a structurally important node showing a rapid growth in its citations (citation burstiness) as a temporal property. Sigma is useful for detecting potentially important works that are evidently receiving attraction. Sigma is a metric of a node in a network of cited references.

3. Results

3.1. Evolution in Publication Trends

This subsection presents the publication trends with regard to the number of published articles and the total number of authors, institutions, and countries involved in the crayfish research. The results also include the top journals involved in the publication of articles on crayfish-related research. Our analysis identified a total of 12,039 published articles (Figure 2) between January 1970 and December 2021. There was a significant increase in the number of publications between 1970 and 2021.

Figure 2.

Production of scientific research on crayfish from 1970 to 2021.

Table 1 presents the top 10 most productive authors in the field of crayfish research in the world. The scientometric analysis showed a remarkable total of 21,329 researchers in this field of study. The author with the highest number of publications was Kenneth Soderhall, from Uppsala University, Sweden, with 149 related publications on crayfish, followed by Antonín Kouba (115 publications) and Josef Dudel (86 publications).

Table 1.

Top 10 authors involved in crayfish research worldwide.

Authors	Record Count	Affiliations
Kenneth Soderhall	149	Uppsala University
Antonín Kouba	115	University of South Bohemia in Ceske Budejovice
Josef Dudel	86	Technical University of Munich
Francesca Gherardi	85	University of Florence
Paul A. Moore	77	Bowling Green State University
Robin L. Cooper	76	University of Kentucky
Amir Sagi	76	Ben-Gurion University of the Negev
Harold L. Atwood	69	University of Toronto
Toshiki Nagayama	69	Yamagata University
Miloš Buřič	63	University of South Bohemia in Ceske Budejovice

The top 10 affiliations with the highest number of publications are listed in Table 2, and crayfish research has seen contributions from 4522 organizations worldwide. With 327 publications, the Centre National De La Recherche Scientifique (CRNS, France) was the leading institution, followed by the University of California (291 publications).

Table 2.

Top 10 affiliations involved in crayfish research.

Affiliations	Number of Publications
Centre National De La Recherche Scientifique (CNRS)	327
University of California	291
Udice French Research Universities	219
United States Department of the Interior	202
Uppsala University	199
Universidad Nacional Autonoma De Mexico	191
Consejo Superior De Investigaciones Científicas CSIC	188
State University System of Florida	186
Hokkaido University	181
University System of Georgia	179

Table 3 lists the journals with the highest number of publications. In total, we identified eligible articles from 1517 journals. Of these, Aquaculture had the highest number of publications (386), followed by the Journal of Experimental Biology (333 publications) and Fish and Shellfish Immunology (287 publications).

Table 3.

Primary or secondary sources (journals) used for the literature search and scientometric analysis.

Titles	Number of Publications
Aquaculture	386
Journal of Experimental Biology	333
Fish and Shellfish Immunology	287
Journal of Crustacean Biology	285
Journal of Neurophysiology	233
Crustacean	208
Comparative Biochemistry and Physiology B: Biochemistry Molecular Biology	167
Freshwater Biology	166
Hydrobiologia	163
Aquaculture Research	142

The top 10 articles were ranked by the number of total citations (Table 4), indicating that Holdich et al. [8] had the highest citation count, with 375 citations, followed by Taylor et al. [40], with 273 citations. Both of these articles were published in peer-reviewed open-access journals related to the topics of management and conservation issues, particularly in freshwater ecosystems. The article with the third-highest number of citations was Gherardi [27], “Crayfish invading Europe: the case study of Procambarus clarkia”, published in Marine and Freshwater Behaviour and Physiology.

Table 4.

Top 10 published articles and their citation counts related to crayfish research.

Article Title	Citation Count	References
A review of the ever increasing threat to European crayfish from non-indigenous crayfish species	375	[8]
Feature: Endangered species—A reassessment of the conservation status of crayfishes of the United States and Canada after 10+ years of increased awareness	273	[40]
Crayfish invading Europe: The case study of Procambarus clarkia	262	[27]
Continental-wide distribution of crayfish species in Europe: Update and maps	243	[10]
Global diversity of crayfish (Astacidae, Cambaridae, and Parastacidae-Decapoda) in freshwater	193	[41]
Managing invasive crayfish: Is there a hope?	186	[42]
Global introductions of crayfishes: Evaluating the impact of species invasions on ecosystem services	181	[43]
A global meta-analysis of the ecological impacts of non-native crayfish	176	[44]
Multiple drivers of decline in the global status of freshwater crayfish (Decapoda: Astacidea)	165	[45]
An updated classification of the freshwater crayfishes (Decapoda: Astacidea) of the world, with a complete species list	156	[46]

3.2. Countries’ Contribution

The United States of America, China, Japan, Australia, Germany, Canada, England, France, Spain, and Italy contributed the most published articles on crayfish research (Figure 3). Among these countries, the USA (3940 records) and China (1085 records) ranked as the two top countries that published crayfish-related studies. However, the significant contribution of the European continent can be seen by combining the top 10 European countries, i.e., a total of 2626 records. Our results also indicated that more than half of the countries around the world (163/195) are actively conducting research on this delicate crustacean species.

Figure 3.

Total publications per nation for crayfish research. Dark magenta represents the highest number of publications, whereas lighter shades represent fewer publications.

3.3. Scientometric Results

The scientometric results can be divided into three main aspects: (i) the co-citation analysis, which includes co-citation analyses of the authors (Table 5 and Figure 4), journals (Table 6 and Figure 5), and documents (Table 7 and Figure 6); (ii) the document cluster analysis; and (iii) the popular keywords and their burstiness. The results for the co-citation analysis are presented in two ways: first in table format, and second, as figures to indicate the centrality of the analysis (figures) and the Sigma score (tables).

Table 5.

Top 10 most influential authors in the field of crayfish research, based on the Sigma score, with the highest at the top.

Author	Year	Title	Degree	Centrality	Sigma
A. Van Harreveld	1970	Institute of Technology, Pasadena	40	0.27	186779614693867000
C. A. G. Wiersma	1970	California Institute of Technology Pasadena	45	0.16	145950,41
F. Gherardi	2002	Università degli Studi di Firenze	34	0.08	103651.98
D. M. Holdich	1996	Crayfish Consultant, Keyworth	38	0.07	2023.08
J. J. Wine	1970	University of Toronto	36	0.1	1661.72
A. L. Hodgkin	1970	Cambridge University	51	0.1	1486.77
D. C. Sandeman	1974	University of New South Wales	39	0.16	1080.28
Unknown	1970	-	30	0.14	317
R. Keller	1978	Ulm University, Germany.	24	0.08	225.67
A. Takeuchi	1970	Niigata University	32	0.04	123.2

Figure 4.

Author co-citation analysis.

Table 6.

Top 10 journals according to co-citation scores.

Journal	Impact Factor (2021)	Degree	Centrality	Sigma
Plos ONE	3.24	10	0.05	52659249690.9
Brain Research	3.252	26	0.09	1253012086.59
Journal of Comparative Physiology	1.97	27	0.07	507679262.28
Proceedings of the Society for Experimental Biology and Medicine	2.688	33	0.08	457338501.7
Freshwater Biology	3.809	28	0.13	965114.5
The Journal of Physiology	5.182	24	0.03	109212.5
Journal of Neurophysiology	2.714	27	0.04	89066.75
Journal of Cell Biology	10.54	28	0.06	47906.51
Biological Invasions	3.113	12	0.03	3533.46
Cellular and Molecular Life Sciences	9.261	23	0.07	1109.57

Figure 5.

Journal co-citation analysis, where only journals with centrality scores greater than 0.1 are included.

Table 7.

Top 10 publications identified by the co-citation analysis, ranked according to Sigma scores.

Title	Degree	Centrality	Sigma	References
The effect of social experience on serotonergic modulation of the escape circuit of crayfish	11	0.36	156.19	[47]
A review of the ever increasing threat to European crayfish from non-indigenous crayfish species	14	0.07	104.17	[8]
Serotonin and aggressive motivation in crustaceans: Altering the decision to retreat	5	0.18	10.02	[48]
Roles of crayfish: Consequences of predation and bioturbation for stream invertebrates	14	0.16	5.82	[49]
Managing invasive crayfish: Is there a hope?	6	0.06	5.03	[42]
Mechanosensory integration in the crayfish abdominal nervous system: Structural and physiological differences between interneurons with single and multiple spike initiating sites	13	0.17	7.8	[50]
Invaders for sale: Trade and determinants of introduction of ornamental freshwater crayfish	16	0.05	3.6	[9]
Invasive crayfish in Europe: The impact of Procambarus clarkii on the littoral community of a Mediterranean lake	9	0.08	4.39	[51]
Loss of diversity and degradation of wetlands as a result of introducing exotic crayfish	16	0.08	3.26	[52]
Continental-wide distribution of crayfish species in Europe: Update and maps	10	0.02	2.99	[10]

Figure 6.

Document citation analysis, showing the overall article availability network (Holdich, D. 2019 [8], Yeh, S.-R. 1996 [47], Huber, R. 1997 [48], Usio, N. [49]).

3.4. Author Co-Citation Analysis

Table 5 lists the top 10 authors in crayfish research, based on the level of the Sigma score, with A. Van Harreveld from the Institute of Technology, Pasadena, California, USA, being the most influential author in this field, with a huge Sigma score compared with the next most influential author in crayfish research, C. A. G. Wiersma. Meanwhile, Figure 4 shows the author co-citation analysis for crayfish research with a centrality score greater or equal to 0.1, with only six important authors (i.e., the most interconnected authors) categorized as authors in the co-citation analysis.

3.5. Journal Co-Citation Analysis

Table 4 summarizes the 10 journals with the greatest influence in terms of journal degree, centrality, and Sigma score. Figure 5 shows that Ecology (online ISSN:1939-9170) and Science (ISSN: 0036-8075, print; 1095-9203, web) are the top two most important journals in the field of crayfish research. PLoS ONE had the highest journal degree score, indicating it was the most influential journal (degree score, 10; centrality score, 0.05; Sigma score, 52659249690.9). Brain Research (degree, 26; centrality, 0.09; Sigma, 1253012086.59) and Journal of Comparative Physiology (degree, 27; centrality, 0.07; sigma, 507679262.28) were the second and third most influential journals publishing crayfish research, respectively.

3.6. Document Co-Citation Analysis

Table 7 displays the top 10 most influential scientific publications according to the Sigma score. There are two articles with Sigma scores of more than 100: Yeh et al. [47] and Holdich et al. [8]. Yeh et al. [47] were the most influential in this area of study, with a Sigma score of 156.19, followed by the most cited article and author in crayfish research, Holdich et al. [8], with the article entitled “A review of the ever increasing threat to European crayfish from non-indigenous crayfish species”. Figure 6 shows the document co-citation analysis, where 17 documents have centrality scores greater than 0.1. According to Figure 6, 4 “central” articles have played a mediating role in our field of interest.

3.7. Document Cluster Analysis

The analysis generated a total of 31 co-citation clusters (Figure 7), of which only the top 10 clusters were summarized in the present study (Table 8). Figure 7 shows a summary of the identified document clusters of crayfish research, and the clusters’ labels were generated by CiteSpace. We used the timeline view and the cluster view to visualize the cluster network’s shape and form [38]. The timeline view shows chronological periods from left to right, whereas the cluster view produces a color-coded spatial network of representations that are automatically labeled. The cluster’s size is equal to the number of publications in each (Figure 7 and Table 8). Cluster assignment is based on citation relationships, where being cited by similar groups indicates a co-citation relationship.

Figure 7.

Summary of document cluster lifetimes (solid lines) from 1970 to 2021. The cluster labels were generated by CiteSpace.

Table 8.

Top 10 cluster IDs generated by CiteSpace.

Cluster ID	Size	Silhouette	Label	Average Year
# 0	314	0.949	Invasive crayfish	2003
# 1	211	0.98	Crayfish escape behavior	1973
# 2	209	0.988	Pathogen Aphanomyces	2014
# 3	147	0.914	Local non-spiking interneuron	1983
# 4	144	0.969	Crayfish neuromuscular junction	1998
# 5	121	0.948	Crayfish muscle (spontaneous transmitter)	1983
# 6	120	0.998	White spot syndrome virus	2003
# 8	104	0.962	Crayfish muscle (saturation kinetics)	1978
# 10	84	0.963	Crayfish photoreceptor	1980
# 11	74	0.96	Trophic dependencies	1973

3.8. Keyword Analysis and Burstiness

Table 9 displays the keywords with the highest citation counts, and the keywords’ burstiness is shown in Table 10. Keyword analysis can detect current patterns, emerging trends, and popular research areas over time. Bursts reflect the emergence of a keyword during a specific period. The blue line in Table 10 represents the timeline (from 1970 to 2021), while the red line represents the burst period. Beginning in 1991 and ending in 2002, the word “neuron” had the highest burst strength (49.42). The top keywords were “lobster” (strength = 38.51, 1991–2004) and “transmitter release” (strength = 36.72, 1991–2003).

Table 9.

Top 10 popular keywords in titles, abstracts, and keywords.

Keyword	Count
Procambarus clarkii	1202
Freshwater crayfish	699
Decapoda	610
Pacifastacus leniusculus	463
Growth	420
Population	361
Cherax quadricarinatus	349
Red swamp crayfish	335
Behavior	323
Orconectes rusticus	318

Table 10.

Top 10 keywords with strongest citation bursts for the period from 1970 to 2021. Red sections in the timelines represent the period of the burst.

Keywords	Strength	Begin	End	1970–2021
Neuron	49.42	1991	2002
Lobster	38.51	1991	2004
Transmitter release	36.72	1991	2003
Conservation	31.08	2008	2019
Membrane	30.95	1983	1998
Cell	29.98	1991	2001
Amino acid sequence	29.2	1991	2007
Diversity	27.57	2010	2021
Nervous system	27.24	1990	2003
Neuromuscular junction	26.19	1991	2003

4. Discussion

Our study represents the first attempt to analyze crayfish research using the CiteSpace software. Our discussion focuses on the metadata in this article, which have been divided into two sections: descriptive data and the scientometric review.

4.1. Descriptive Data

The number of published articles increased and even doubled from 120 articles in 1990 to 240 in 1991. Indeed, 1991 was a pivotal year for a number of scientific fields, with many important discoveries and advancements being made. This may have led to an increase in research and publication activity, as well as an increase in the number of citations as researchers built upon and referenced one another’s work. It is also worth noting that, in the 1990s, there was a significant increase in funding for scientific research from both governments and private sectors, which also led to more publications and citations. Additionally, in 1991, the number of scientific journals that were indexed in the Web of Science increased as well; this made it easier for authors to find and submit articles and for other researchers to find articles to cite. However, why did the literature on crayfish boom in 2011? It was challenging to identify the main factor behind the sudden increase in the number of publications related to crayfish research during 2011 (Figure 2). However, the present study suggested this might be attributed to the global introduction of crayfish from 2001 to 2011 [53], which may have augmented intensive research on crayfish.

Over the last 5 decades, 21,329 authors have been involved in crayfish research. Why are so many authors involved in this research? This could be an interesting fact to be elaborated on since our previous scientometric analysis [15,16] showed that the ratio between the number of publications and the author for the selected research theme was lower than in this present study.

Aquaculture (publisher: Elsevier) was the journal that published the highest number of articles related to crayfish research. The journal publishes articles related to the exploration, management, and improvement of all freshwater and marine farming of aquatic organisms for human consumption. This is also supported by the aquacultural potential of crayfish around the world, as they were reported to be the fastest-growing cultured species by the Food and Agriculture Organization of the United Nations (FAO) in 2018 [53]. Furthermore, Fish and Shellfish Immunology is among the top three journals that have published research on crayfish, especially disease-related research. The publications on crayfish in this journal revealed that crayfish are transmitting agents for pathogens [30,31]. In addition, crayfish are also considered one of the most prominent aquaculture species in tropical and subtropical regions [4]. Thus, any studies that are related to aquaculture, diseases, or any related research could attract the attention of journals such as Aquaculture and Fish and Shellfish Immunology.

In terms of the countries with the highest publication output (the USA, China, and European countries), this could be attributed to the fact that there are a higher number of available crayfish species for commercial production in these countries [53]. Additionally, it could be that most of our recent analyses related to scientometric studies also showed that countries such as the USA and China have more authors involved in publication [15,16].

Improving scientific understanding of the distribution and establishment of crayfish species as well as scientific data for effective conservation and management of this species are truly needed. This was supported by our identification of the top two articles with the highest number of citations, which were published in Knowledge and Management of Aquatic Ecosystems (publisher: EDP Sciences, France) [8,10] (Table 4). This journal’s aims and scope include management and conservation issues related to freshwater ecosystems. The taxonomic study by Crandall and de Grave [46] is among the most highly cited articles due to the importance of taxonomic validation for experimental crayfish species. Review articles on crayfish, such as Souty-Grosset et al. [14] and Twardochleb et al. [44], were largely used as references for most crayfish studies; therefore, review articles were more highly cited than original research articles.

4.2. Scientometric Analysis

Crayfish research has become increasingly important for the research fields of neuroscience [54,55]; ecological experiments, such as invasive patterns and prey and predator interactions; behavioral experiments [55,56]; and disease-related studies [32]. This was supported by the present metadata in the scientometric document cluster analysis.

Surprisingly, the most influential authors on crayfish were mainly researchers from the 20th century (90%), and only one researcher was from the 21st century (Table 5). As the Sigma parameters indicate whether an author is in the domain’s center (values > 1), this indicates that the researchers from the 20th century were among the top authors in this domain. This might be because most of their publications have been used as a main reference by later studies that have applied their culture methods. This also might be because they indicate the crayfish’s occurrence in certain areas or their history as well as their distribution (Table 5).

The top three most influential journals in crayfish research are PLoS ONE, Brain Research, and the Journal of Comparative Physiology. PLoS ONE is a more diverse journal. It includes research on over 200 subject areas, including science, engineering, medicine, and related social sciences and humanities. This journal publishes multidisciplinary and often interdisciplinary articles, which lays the groundwork for multidisciplinary research and indicates that more authors focusing on this domain are needed. As mentioned previously, various fields have been associated with crayfish research, including neuroscience. This could be why most crayfish research studies have been published in Brain Research and the Journal of Comparative Physiology. Both journals focus on articles about neuroethology, sensory science, neural science, and neuroscience, as stated in their aims and scopes.

In the document co-citation analysis, there are two published crayfish-related studies within the top 10 most influential scientific publications according to the Sigma score. Yeh et al. [47] were the most influential. Holdich et al. [8] were the articles with the secondco-citation scores. According to our results in Table 8, the dominant research topics and directions were invasive crayfish, the escape behavior of crayfish, the pathogen Aphanomyces, local non-spiking interneurons, the neuromuscular junction of crayfish, crayfish muscles (spontaneous transmitter), white spot syndrome viruses, crayfish muscles (saturation kinetics), photoreceptors in crayfish, and trophic dependencies. This indicates that most research has focused on the invasiveness of crayfish species and their related behaviors in the field of neuroscience. It also indicates that the white spot syndrome virus is most associated with crayfish research. The keyword with the highest count was Procambarus clarkii, showing that this species is among the most researched species in the field (Table 9). The document burst analysis showed a typical emergence pattern for new research topics, where previous bursts are gradually replaced by more recent publications. The most recent keywords showing burstiness are “conservation” and “diversity”, which are related to current studies on crayfish-related research and development. This shows that the importance of crayfish diversity related to conservation efforts is the most recent trend in crayfish research in the world, especially in the WoS database.

4.3. Limitations

Our study may have a publication bias as we only obtained papers from the Web of Science (WOS) databases. In addition, the present study excluded the common names of crayfish in languages other than English from the keywords. We focused on research written in English, not to question the impact of research in languages other than English, but to reduce the potential bias from reviewers arising from the potentially limited understanding of other languages. Future research could compare other databases with WoS to map these research areas and possibly identify the missing links.

4.4. Current State of Crayfish Research and Future Directions

Crayfish research has covered a wide range of topics in recent years. One of the most important works in this field is the study by Carvalho et al. [57], which examines how temperature and interspecific competition can alter the impacts of invasive crayfish on key ecosystem processes. Similarly, Veselý et al. [58] investigated the trophic niches of sympatric invasive crayfish of EU concern. They found that temperature and prey density jointly influence trophic and non-trophic interactions in multiple predator communities. Guo et al. [59] also conducted a study that explored the effects of air humidity on the successful egg incubation and early post-embryonic development of the marbled crayfish (Procambarus virginalis). This study provides important insights into the reproductive biology of crayfish and has implications for the management of invasive crayfish populations. Kouba et al. [60] studied the significance of droughts for hyporheic dwellers. They found that droughts had a significant impact on crayfish populations and that more research is needed to understand the effects of droughts on these species. Additionally, Dörr et al. [61] have investigated the salinity tolerance of the invasive red swamp crayfish Procambarus clarkii (Girard, 1852). This work is crucial for understanding the adaptability of invasive crayfish species and could inform management strategies in areas where salinity levels vary.

Regarding crayfish and global changes, it is important to specify that global changes, including climate change and habitat destruction, significantly impact crayfish populations worldwide. A study by Adams and Taylor found that rising temperatures are leading to declines in crayfish abundance and distribution [62]. In their study of 2019, the same authors reported that altered precipitation patterns are also affecting crayfish populations by altering their breeding cycles and reducing the availability of food [63]. Furthermore, they found that habitat destruction is a major threat for crayfish, as it leads to the destruction of wetlands and other aquatic habitats, reducing their available habitat [64]. Another study published by the same authors also reported that global changes such as increased water pollution and changes in water chemistry are making it more difficult for crayfish to find food and reproduce successfully [65]. In addition, another study from 2020 [36,62] reported that the spread of invasive species is also impacting native crayfish populations, leading to declines in abundance, distribution, and genetic diversity. Overall, these studies show that global changes are detrimental to crayfish populations and may lead to their decline or extinction if steps are not taken to address these issues.

Future research on crayfish should continue to focus on a wide range of topics, including conservation, diversity, and the impacts of climate change. Studies have already begun to explore the effects of climate change on crayfish populations, such as the impact of sea level rise and increasing sea surface temperature on crayfish [57,66]. However, there is still a need for more research to fully understand the impacts of climate change on coastal environments and crayfish populations [66].

In addition to focusing on climate change, future research should also include a broader range of databases such as SCOPUS, China National Knowledge Infrastructure (CNKI), Chinese Social Sciences Citation Index (CSSCI), Index Copernicus, and PubMed. These databases will allow for a more comprehensive analysis of crayfish research and help identify any gaps in knowledge that need to be filled. It is also recommended to bring in interdisciplinary approaches such as eco-hydrology, biogeochemistry, and eco-toxicology to understand the impacts of invasive crayfish species on ecosystem processes and trophic interactions and to develop effective management strategies.

Overall, there is a wealth of opportunities for future research on crayfish, and the field is expected to continue to grow in the coming years. It is crucial that we continue to invest in research on crayfish in order to fully understand their ecology and management, and to develop effective strategies for conservation and biodiversity.

In summary, previous studies have contributed to a better understanding of the ecology and management of crayfish and have provided important insights that can inform conservation and biodiversity efforts. However, more research is needed to fully understand the impacts of invasive crayfish species and to develop effective management strategies.

5. Conclusions

Crayfish research has received significant attention from the scientific community in recent years, as evidenced by the large number of publications and the numerous authors involved in the studies. In this study, our results showed that one of the most established authors in the field of crayfish research is Francesca Gherardi from the University of Florence, Italy, whose team has published extensively on the subject. According to scientometric analysis, Gherardi and her team are ranked among the top 10 authors involved, the top 10 most influential authors, and the top 10 documents in the co-citation analysis.

In addition, even if crayfish research has made significant strides in recent years, providing new insights into the ecology and management of these species. There are still areas of crayfish research that have not been fully explored. For example, there is a need for more research on the genetic diversity of crayfish populations, both native and invasive. This can provide important information on the potential for adaptation and resilience to environmental changes and could inform conservation and management strategies.

Another area that has received limited attention in the literature is the use of citizen science in crayfish research. Involving the public in monitoring and collecting data on crayfish populations can provide valuable information on distribution and abundance. It can also increase public awareness and engagement in conservation efforts.

Additionally, there is a need for more research on the impacts of crayfish on aquatic plant communities. Crayfish are known to be important consumers of aquatic plants, and their impacts on these communities can have cascading effects on the entire ecosystem. Understanding these impacts is crucial for developing effective management strategies and conserving biodiversity.

In conclusion, there is still much to be learned about crayfish and their ecology. Further research on genetic diversity, citizen science, and the impacts of crayfish on aquatic plant communities could provide important new insights into these fascinating creatures and inform conservation and management efforts. With the increasing importance of crayfish in biodiversity-related studies, it is crucial that we continue to invest in research in this field.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/2076-2615/13/7/1240/s1.

Author Contributions

Conceptualization, M.N.A. and H.A.A.; methodology, M.N.A., L.L.W., Z.A.L. and M.I.M.N.; software, M.A.A. and M.I.M.N.; validation, H.A.A. and W.N.W.A.; formal analysis, M.N.A., Z.A.L. and M.I.M.N.; investigation, L.L.W. and M.F.A.; resources, M.A.A. and F.L.; data curation, M.N.A., M.F.A. and F.P.; writing—original draft preparation, M.N.A., H.A.A. and I.Z.; writing—review and editing, H.A.A. and I.Z.; visualization, W.N.W.A.; supervision, H.A.A., I.Z., W.N.W.A. and F.P.; project administration, F.L. and F.P.; funding acquisition, F.L. and F.P. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

All data generated or analyzed during this study are included in this published article (and its supplementary information files).

Conflicts of Interest

The authors declare that they have no known competing financial interest or personal relationships that could have appeared to influence the work reported in this article.

Funding Statement

The preparation of this scientometric study was supported by the Department of Higher Education, the Ministry of Higher Education, Malaysia, through the internal grant entitled “Temperature increase impacts behavior of freshwater crayfish: Implications for biological invasion under climate change” (Vot. No. 55321). The recent study also supported by the grant from Ministry of Natural Resources, Environment and Climate Change, Malaysia under the National Conservation Trust Fund for Natural Resources (NCTF), entitled "Quantifying Red Claw Crayfish Distribution and Invasiveness in Peninsular Malaysia for Societal Wellbeing and Environmental Sustainability" reference No. (KeTSA.BPP.(S)600-5/9/17(1) with the internal Vote. No. of 53511. Corresponding authors also acknowledged the funding from PYPA Initiative managed by the Universiti Teknologi MARA (UiTM) (PYPA in Malay: Pembiayaan Yuran Penerbitan Artikel) to MIMN and FP. These funders and the related organizations were not involved in the writing of this manuscript or in the design of the project, analysis, or interpretation of data collection. The first author wishes to express his gratitude to the Sustainable Ocean Alliance (SOA) and the Environmental Defense Fund (EDF) of the USA for his inaugural fellowship in Leadership for Climate Resilient Fisheries (LCRF).