The Invasive Red Swamp Crayfish (Procambarus clarkii) in the Scientific Literature Using a Text Mining and Topic Modelling Approach

Abstract

The red swamp crayfish (Procambarus clarkii) is the most widely introduced crayfish species worldwide. Its spread causes massive environmental impacts on native species and ecosystems. Owing to its commercial value and impacts in introduced countries, the literature on P. clarkii has increased exponentially, making necessary studies for synthesising the collected information. In this study, a text mining and topic modelling approach was used to analyse the scientific literature on P. clarkii as an invasive species, to identify the interests and trends of research lines through time and space. A keyword-based search of research databases was performed, and the abstracts of 519 articles were analysed to identify the most characterising terms. These included both descriptive terms of the species and terms related to its invasiveness and impacts. The analysis of the scientific literature allowed us to identify 14 research topics focusing on the ecological impacts of P. clarkii and its geographical distribution, with a growing interest in invasion mechanisms and dispersal pathways. On the contrary, management studies are less abundant, despite their scientific value is highlighted by their increasing number of citations. This reflects the fact that most management-related studies are found in the grey literature and are therefore underrepresented in the scientific literature. The limited accessibility to data and the complexity of control strategies are obstacles to the effective management of this species. Improvement in information sharing through the creation of digital platforms that support distribution data suitable for modelling species spread, and the integration of knowledge from non-academic sources may help fill current knowledge gaps and provide new perspectives for the management of P. clarkii.

1. Introduction

Invasive alien species (IAS) are one of the major causes of biodiversity loss [1], and their introduction rate shows no signs of saturation over time [2]. The pressure exerted by IAS is predicted to increase in the future due to trade expansion, habitat disturbance, and climate change, which will affect the geographical distribution of IAS [1,3,4]. Their introduction causes many ecosystem impacts. For example, IAS could contribute to the decrease in the abundance and richness of native species, the modification of community structures, the alteration of genetic diversity [1,5], and also producing impacts on the economy [6] and human health [7].

Research on biological invasions is a growing topic [8], particularly research that focuses on the impacts of IAS, providing better knowledge on the mechanisms underlying the impacts, and developing theoretical basis and conceptual frameworks [1,9]. However, the analysis of the scientific literature between 1980 and 2006 indicates that only a part of the species has been studied in detail. It is assumed that the more invasive a species is, the more likely it will become the subject of scientific studies. Therefore, it has been hypothesised that the impact of a species, together with other factors such as geographic context, taxonomy, and the perceived charisma of the species, may contribute to the probability of some species receiving more scientific attention than others [8,10].

The red swamp crayfish (Procambarus clarkii) is one of the IAS of greatest scientific interest [8] and the most globally widespread crayfish species [11]. Among the crayfishes introduced outside their native range, P. clarkii represents 40% of the introduction cases [12]. This species is native to northeastern Mexico and the southern part of the United States but currently occurs in 40 countries on five continents, excluding Australia and Antarctica, and has the potential for further expansion [11,13,14]. The impacts of P. clarkii have been widely studied [15,16,17]. Among the species introduced in Europe for aquaculture purposes and related activities, P. clarkii shows the widest range of impacts [1,17]. The species is considered one of the 100 worst IAS in the world [18]. It can replace native crayfishes through competitive exclusion and the transmission of the crayfish plague caused by the oomycetes Aphanomyces astaci [19,20,21]. Moreover, P. clarkii negatively affects aquatic ecosystems through a combination of behavioural traits and species characteristics [17]. Its intense burrowing activity can cause river and canal banks erosion [22], modify geomorphology, and increase the costs of managing water systems [23]. Together with foraging, these activities alter the physiochemical parameters of water, reducing dissolved oxygen, increasing turbidity and suspended solids, and sometimes promoting the proliferation of toxic cyanobacteria [23]. Feeding habits lead to the decline of macrophytes [24], amphibians [25], molluscs [26], and macroinvertebrates [27], with indirect effects that destabilise food webs [17]. Overall, these impacts compromise several ecosystem services, including provisioning services (e.g., reduction in the quality and availability of native edible resources), regulating services (e.g., bank erosion and alterations in water quality), but also supporting services (e.g., structure and functioning of food webs), and cultural services linked to native crayfish [23].

From 1924 to 2019, the number of published articles on P. clarkii increased to 5442 [11]. At the beginning of the invasion process (1942–1960), studies mainly focused on crayfish physiology, using it as a model species. Scientific interest on P. clarkii has increased over the years, particularly between the early 1970s and the mid-1980s, a period in which the number of aquaculture and fishing studies increased, probably in relation to the growing commercial exploitation of P. clarkii. These research topics constantly increased in the number of publications since the mid-1980s. More recently, from the 2000s, an increase in the number of studies dealing with the role of P. clarkii as an IAS was recorded, reaching approximately 25% of the total scientific studies in the decade 2000–2010 [11].

The scientific literature is growing exponentially, making synthesis an increasingly difficult task. However, the adoption of computational approaches to the scientific literature allows a straightforward identification of the publications and the extraction of information from the documents [28]. Text mining techniques are data exploration methods that use word indexing approaches [29] to summarise trends and provide insights from large amounts of textual data [30,31]. Text mining also allows the identification of changes in research priorities, such as a lack of interest in certain topics [32]. Although this technique is particularly used in information technology and informatics, few studies have been performed in the fields of biology and ecology [28,31].

In this study, a text mining approach was adopted to identify the main trends in the scientific research on P. clarkii as an invasive alien species (IAS). Text mining was combined with a topic modelling technique based on the Latent Dirichlet Allocation (LDA) algorithm. This approach was used to systematically analyse the content of the scientific literature, identifying the most recurring and relevant terms. Through topic modelling, the main research themes related to P. clarkii were identified, for investigating their temporal evolution and scientific impact with the aim of providing a detailed overview of the most discussed topics within the scientific community and the evolution of research priorities.

2. Materials and Methods

2.1. Data Collection and Analysis

Data collection was carried out using the following search string: (“introduced species” OR “invasive species” OR “invasive alien species” OR “IAS” OR “alien” OR “non-native” OR “non-indigenous” OR “pest” OR “feral” OR “exotic”) AND (“Procambarus clarkii” OR “Red swamp crayfish” OR “Louisiana crawfish”). These terms were searched in the title, abstract, and keywords of scientific publications using Scopus, Web of Science, and PubMed databases. The search was performed on the 30th of June 2023 and focused on English-language scientific literature. Using the information provided by Scopus, the macro and subject areas of the selected publications were identified, and the number of citations were recorded. Moreover, for each publication, the geographical location was estimated based on the study area or, if this was not available (i.e., in reviews), the affiliation of the first author.

Selected documents were analysed by publication year and country to describe their trend, and their geographical distribution was visualised using the rworldmap package of R software (v. 4.2.3) [33].

Except for data collection, all analyses including text mining, topic modelling, and the assessment of temporal changes and geographical distribution of research topics were performed with R software [33] and are described in detail in the following sections.

2.2. Text Mining

Text mining consists of a semi-automatic extraction of information from unstructured text data using word indexing methods [29,30]. To transform textual data into a structured format, a pre-processing phase of the text is requested. Pre-processing was performed on the abstracts of the selected documents using the tm package [34]. The corpus of documents was converted to lowercase and deprived of punctuation, numbers, and stop words because these are textual parts that are unnecessary for semantic understanding [34,35]. Stop words, such as “the”, “is”, “at” and “on”, are common text elements that do not provide additional information to the meaning of text. Furthermore, the terms used in the search string were removed as their presence in most abstract was uninformative [31]. Using the SnowballC package, a stemming process was performed to reduce the words to their root; for example, through stemming, the words “ecology”, “ecological” and “ecologic” are reduced to the root “ecolog” [36]. Through stemming, the complexity of the corpus of documents is reduced without causing information loss [34].

Once the pre-processing phase was completed, the corpus of documents was transformed into a structured format for processing. A document–term matrix (DTM) was created using the tm package; the matrix contains the documents along the rows and the terms along the columns. In the DTM, the bag-of-words principle is used, which means that the order of terms is irrelevant. Each cell of the matrix contains the total frequency (TF) of the terms, i.e., a count on how many times a term appears in the corpus of documents. Since the frequency of a term is not always informative, the weighting of the terms was carried out through the Term Frequency Inverse Document Frequency (TF-IDF), a measure that gives greater importance to discriminatory terms than to terms that commonly occur in documents [32,34]. The most important terms based on the TF-IDF weight were plotted using the ggplot2 package.

2.3. Topic Modelling

Topic modelling is a statistical method of latent semantic analysis [35] in which the corpus of documents is distributed into a set of topics, allowing thus the identification of the main themes [31]. Topics are combinations of terms that occur together in a document more likely than others. Each document is a mixture of topics, and a single term could belong to multiple topics [31,35].

Topic modelling allows researchers to perform a probabilistic modelling of term frequency in documents [37]. The Latent Dirichlet Allocation (LDA) is a Bayesian mixed model [38] used in topic modelling to estimate the latent topics and their probabilistic distributions in documents [35]. With LDA, terms are assigned to each topic but not based on the lexicon. This means that despite the presence of many polysemous terms whose meaning changes depending on the context, LDA can model such polysemy using latent variables. The DTM used for the LDA can be reduced by selecting the terms based on their document occurrence or based on the TF-IDF weight. This selection defines the vocabulary to be used; since the input data of the DTM is based on total frequency, the order in which the terms occur is negligible (bag-of-words models) [37]. In this study, a topic modelling analysis was conducted using the LDA model implemented in the topicmodels package [37,39]. Since the appropriate number of topics into which to divide the corpus of documents is not known a priori [37], the ldatuning package was used to select the optimal number of topics [35,40]. The optimal number of topics was identified using the indices of Griffiths 2004 and CaoJuan 2009 [35]. The final LDA model was estimated with Gibbs sampling, using burn-in = 4000, iterations = 2000, thinning = 500, and five random starts with different seeds (2003, 5, 63, 100001, and 765), retaining the best solution; default Dirichlet priors of the topicmodels package were applied. Finally, based on the probabilities of the terms falling into each topic and the assigned documents, the topics were labelled to describe their semantic content [35,39]. Moreover, the top 10 most frequent words of each topic was extracted and represented graphically.

2.4. Temporal Changes and Geographical Distributions of Research Topics

Research topics undergo variation based on scientific interest, determining the presence of hot and cold topics [39]. The subdivision of the corpus of documents into topics permit to analyse their dynamics and temporal changes [31,39]. Furthermore, the assignment of the geographical location to the publications allows us to evaluate the global distribution of research topics [41].

To evaluate the scientific interest, the number of annual publications and the number of annual citations were calculated for each topic. The annual citations of the articles were obtained from Scopus and corrected by the number of annual publications, to then calculate the mean number of annual citations per topic. A linear regression was adopted to analyse the trends of publications and citations over the years. The slope of the regression line and p-values were used to detect hot and cold topics. Finally, the distribution of topics to the different continents was represented using a Sankey diagram with the networkD3 package.

3. Results

3.1. Overview of the Publications of P. clarkii

Data collection allowed us to recover a total of 1261 publications, respectively, from Scopus (n = 553), Web of Science (n = 615) and PubMed (n = 93). The identified publications were manually screened to exclude incorrect findings (n = 1), publications without authors (n = 1), without an abstract (n = 16), and duplicates between databases (n = 526). Furthermore, book chapters and conference materials were excluded (n = 20) as well as publications related to the native range of P. clarkii (n = 14) or concerning only other alien crayfish species (n = 167). After this process, the dataset was reduced to 519 documents. The selected publications were primarily research articles (97%) while reviews accounted for 3% (n = 15). The first publication about P. clarkii as an IAS dates back to 1991, while the first review was published in 2004, corresponding to the period when the number of annual publications about the species started to increase. The publication trend has increased steadily over the years (Figure 1a; linear regression: R² = 0.63, p < 0.001).

The geographical distribution of the publications shows significant global differences. Europe is the continent with the highest number of published articles, thanks to the publication rate of a few countries. Indeed, Italy is the country with the highest number of publications (n = 114), followed by Spain (n = 69) and Portugal (n = 57), and these three countries constitute 67.8% of the overall European publications (Figure 1b). In the number of publications at a global level, Europe is followed by Asia (n = 78; 15.0%) and North America (n = 63; 12.1%), the latter primarily from the USA. Finally, 25 articles were published in Africa (4.8%), 15 in South America (2.9%), and 2 in Oceania (0.4%) (Figure 2).

The macro and subject areas of the journals on which documents were published are summarised in Table S1. About 40% of the publications fall into the “Ecology” and “Ecology, Evolution, Behaviour and Systematics” sectors. Most of the journals relate to the macro-area “Agricultural and Biological Sciences” (64.5%) and “Environmental Sciences” (22.3%). However, approximately 13% of the remaining publications fall into 11 other different macro-areas that deal, among others, with “Social Sciences”, “Arts and Humanities” and “Engineering”.

3.2. Text Mining and Topic Modelling

After the pre-processing phase, the corpus of the 519 selected documents was subjected to the weighting of the terms through TF-IDF. The most relevant terms (TF-IDF > 3.5) are reported in Figure 3.

Through the ldatuning package, an optimal number of 14 topics was defined. The average topic coherence (UMass) was 0.072, confirming the model’s internal consistency. The results of the LDA topic modelling and labelling are reported together with the 10 most descriptive terms occurring in each topic (Figure 4).

3.3. Temporal and Spatial Variations in the Interest of Research Topics

From the analysis on the number of publications and citations per topic, the interest of the scientific community towards specific themes was detected. The annual trend of published documents showed a difference between the 14 analysed topics, and only four of them (“Drivers and pathways of introduction”, “Distribution and first records”, “Physiological responses to stress factors” and “Population genetics”) showed a significant increase in the annual number of published documents (Figure 5). Furthermore, the analyses on the mean annual number of citations per document showed a general increase in the number of citations among the different topics, except for the topics “Impacts on lower trophic levels” and “Physiological responses to stress factors” (Figure 6).

Finally, the distribution of topics varies among continents. Europe, North America, and Asia contributed to each topic, while Africa, South America and Oceania contributed, respectively, to eight, seven and two topics (Figure S1). The spread of P. clarkii appears to drive research priorities across continents, tailoring research to local needs and stage of invasion.

4. Discussion

In this study, a scientific literature analysis on P. clarkii as an IAS was conducted using an innovative approach based on text mining and topic modelling techniques, to systematically and quantitatively examine the main topics addressed by the scientific community, mapping the most relevant themes and the level of attention devoted to each topic. Through this approach, the most studied thematic areas were identified, as well as knowledge gaps that remained underexplored. These gaps represent significant opportunities for future research, which could enrich the global understanding of the dynamics related to this invasive species and contribute to the development of more effective strategies for its management and impact mitigation.

Through data collection, 1261 publications were identified, of which 519 were selected for analysis. The number of publications analysed is significantly lower than that recorded in the review by Oficialdegui [14]. This discrepancy is attributable to our search string, which specifically focused on P. clarkii as an IAS. As a result, the first selected publication dates back to 1991, a more recent period than the studies on the species physiology and its use in aquaculture, but consistent with the beginning of IAS-related studies [8].

The analysis of the geographic distribution of publications revealed a strong bias. This may partly be related to differences in the availability of financial resources, as suggested by previous studies [42]. In countries with lower GDP, resources for monitoring and managing IAS are often limited, whereas in wealthier countries, greater resources and trade may promote both the introduction of new species and more intensive research efforts [5,8]. However, greater financial capacity can also generate a monitoring bias, leading to an apparently higher distribution and abundance of the species in economically richer regions. In the specific case of P. clarkii, the observed geographic bias may reflect a combination of factors, primarily related to the actual distribution and abundance of the species on a global scale, but also influenced by economic aspects and monitoring intensity.

Europe stands out as the region with the most extensive historical documentation on the introductions of invasive species [5]. Here, P. clarkii experienced a rapid expansion following its initial introduction in the 1970s, driven by secondary introductions and economic interests related to its commercial value [14]. Consequently, Europe accounts for 64.7% of the overall publications, with a predominance of studies from Italy, Spain, Portugal, and France, which are countries with a long history of the species invasion and management. Opposite trends are observed in Africa (4.8% of publications) and South America (2.9%), likely due to the later introduction of P. clarkii and its more limited distribution compared with other territories. In Asia, which accounts for 15% of publications, nearly 45% of studies are from China, which has the highest commercial production of P. clarkii [14]. North America contributes 12% of the overall publications and represents a peculiar case because P. clarkii is native to part of this region. Indeed, this relatively low number of publications is explained by the exclusion of some studies from our analysis as they did not meet the IAS selection criteria, focusing instead on the ecological and physiological aspects of the species in its native range. Lastly, Oceania is strongly underrepresented as the species is not present in this territory, and the two publications that are available derived from international collaborations.

Using text mining, the most relevant terms in the corpus of documents were identified based on their TF-IDF weight, highlighting the main areas of scientific interest concerning P. clarkii. The term with the highest weight “predat” indicates that predation is one of the central themes in the literature. This reflects the numerous studies showing how P. clarkii profoundly alters local trophic networks [17,43], preying on a wide range of species, including amphibian eggs and larvae, fish, and macroinvertebrates [25,26,27]. At the same time, P. clarkii itself has been incorporated as a prey into the diets of several fish, bird, and mammal species, becoming a new trophic resource and modifying energy flows within invaded ecosystems [43]. This dual role—as both predator and prey—further highlights its strong influence on ecosystem dynamics. Another term characterised by a high weight is “popul”, a root that encompasses several meanings related to the concept of population, which is widely used in the literature. It may refer to the demographic trends of the species, its dispersal capacity, or its interactions with native populations, all of which are recurrent aspects in ecological studies. Consequently, its weight should not be interpreted as pointing to a specific research theme, but rather as evidence of the overall relevance of population-related aspects in P. clarkii studies. Several terms, such as “lake”, “water”, and “pond”, emphasise the close connection between P. clarkii and the aquatic environments, which represent its primary habitat. These environments are particularly vulnerable to the ecological impacts of this species, including the alteration of plant communities [24], as highlighted by the term “macrophyt”, and changes in the physicochemical characteristics of water [44]. The use of terms such as “nativ”, “prey”, “fish”, “ecosystem”, “impact”, and “diet” further confirm the scientific focus on the multidimensional ecological impacts caused by P. clarkii. In addition to its direct effects on prey species and competitors, this invasive species is responsible for ecosystem-level changes, such as habitat loss for other species and reduced ecological complexity in colonised ecosystems [17].

Another area of interest is represented by terms related to the introduction events [12] and its geographic distribution [10,13], such as “distribut”, “area”, “invas”, “model”, “individu”, and “introduct”. This reflects the effort made by the scientific community to map the global spread of P. clarkii, also using genetic approaches (“genet”) [45]. Finally, the presence of terms such as “leniusculus” and “nonnat” indicates that part of the analysed literature focuses on comparative studies between P. clarkii and other non-native invasive crayfish species, such as Pacifastacus leniusculus [46]. This comparison highlights the ecological and behavioural characteristics that make P. clarkii particularly invasive compared with other species.

From the topic modelling analysis, 14 themes that characterise the scientific literature on P. clarkii as an invasive alien species were identified. Among these, the topic “Drivers and pathways of introduction” appears to be the topic with the most scientific interest. Given its status as an invasive species, it is reasonable that substantial research has focused on its distribution and introduction routes. Furthermore, the positive trend in annual publication and citation rate suggests that the invasion phenomenon is still ongoing. Articles under this topic explore the pathways facilitating the introduction of the species, with a particular attention to the ornamental trade by aquarists, including online trade [47,48]. Since ornamental and online trade represent a new introduction pathway for P. clarkii, a greater involvement of policymakers worldwide is necessary to implement regulations aimed at trade restriction, such as the regulations adopted in the European Union (Regulation (EU) No 1143/2014 and Commission Implementing Regulation (EU) 2016/1141), and the growing scientific interest in this topic may reflect an increasing awareness of this need in response to the expansion of the species.

Another topic that has generated significant scientific interest is “Distribution and first records” (Figure 5 and Figure 6) due to the high invasion potential of P. clarkii in new territories or environments. The species has not only invaded wetlands, marshes, and rice fields but has also been found in brackish waters and caves [49,50]. Similarly, the topic “Population genetics”, which includes studies on genetic diversity across invaded areas and investigations into invasion routes [45], exhibits strong scientific interest (Figure 5 and Figure 6). Overall, the interest in these topics indicates that P. clarkii is still expanding its range and that the invasion process is ongoing, with its distribution which is far from reaching a plateau, as highlighted in other studies [14]. On the contrary, the topic “Distribution models” does not appear to be one of the most developed topics so far. This result does not seem to reflect a lack of interest from the scientific community but appears to be connected to the difficulties in developing distribution models for freshwater crayfish rather than other taxa. This is a consequence of the limited or irregular availability of up-to-date distribution data for freshwater crayfish [11] and the lack of adequate predictive datasets for modelling these species, such as wide-scale data on the characteristics of water basins (e.g., hydro-morphology, hydropeaking) [51].

Overall, the interest in topics related to the distribution of P. clarkii highlights the need for continuous monitoring of its expansion and invasion dynamics. From this perspective, data on species distribution could be made accessible to the scientific community and the public through dedicated digital platforms, favouring a more effective information sharing [11]. Real-time mapping tools could in fact promote the development of models to predict scenarios of current and future distributions, but also the implementation of targeted and timely management strategies [11].

P. clarkii causes a wide range of impacts [17,23], consequently, five specific topics related to its impacts were identified (“Impacts on ecosystem structure and functioning”, “Impacts on lower trophic levels”, “Impacts on higher trophic levels”, “Impacts on amphibians and behavioural responses” and “NICS vector of A. astaci”). Despite the broad study and awareness concerning the impacts of P. clarkii, these topics do not show particular scientific interest when considered individually. This result does not indicate a lack of interest or saturation of the topic but rather reflects the detailed subdivision of P. clarkii impacts imposed by the topic modelling process. Among these, the only topic characterised by intense research efforts is “NICS vector of A. astaci” due to the severe threat posed by NICS to native crayfish species, which suffer from direct competition and the transmission of the crayfish plague [13,15,19,52]. In this thematic area, the number of annual publications has remained constant over time, whereas citation rates have been increasing. Another topic partially dedicated to the impacts is “Control and agricultural impact”. In this case, a limit of the topic modelling process was noted because publications addressing the impact of species are grouped with management-oriented publications, particularly those on control methods.

Purely management-related topics include “Dispersal pathways and containment methods” and “Monitoring and trapping methods” which, like “Control and agricultural impact”, do not appear to be particularly explored. Although these topics are characterised by a relatively low number of publications, compared to other thematic areas, these studies arouse a scientific interest as indicated by the positive trend in the number of annual citations (Figure 6). The low number of publications could be attributed to the inherent management difficulties, such as those arising on large-scale control strategies due to the absence of universally applicable control methods. Furthermore, control efforts require significant resources, not always supported by adequate funding and management policies. However, the low number of publications related to management might be biased by our search criteria, which focused on English scientific literature, and therefore some information might have been overlooked. In fact, technical, governmental and project reports are often not published or written in local languages [53].

Lastly, the topic “Physiological responses to stress factors” shows a positive trend in the number of publications, indicating a constant interest in increasing knowledge about the adaptability and invasion capabilities of P. clarkii [8]. This topic includes articles addressing P. clarkii responses to various factors that can affect its survival and reproductive capabilities, such as responses to insecticides [54], extreme temperatures [55], and salinity [56]. Conversely, the topic “Trophic ecology” appears to be a topic with a limited scientific interest, likely because knowledge on this subject area is well-established. The latter topic includes studies on the diet composition of P. clarkii, its trophic influence on food webs, and assessments of whether the pressures exerted by this species are similar to those exerted by native species [57,58].

Finally, while topic model successfully grouped semantically related terms and correctly identified the most relevant research themes, we acknowledge that some non-informative words may occasionally emerge despite the use of a standard stop-word list and the removal of search terms. This residual effect was limited in the present study.

5. Conclusions

In this study, an approach based on text mining and topic modelling techniques was applied to analyse the scientific literature on P. clarkii as an invasive alien species. The analysis highlighted the main areas of interest within the scientific community, as well as existing research gaps that require further attention. The results systematically identified and mapped key topics related to the biology, ecology, and management of this invasive species. Among the most studied topics are ecological impacts, which reflects the significant effect of the species on invaded ecosystems, and geographic distribution, with a particular focus on introduction routes and global spread, alongside a growing interest in invasion mechanisms and dispersal pathways. To effectively address the challenges posed by the spread of P. clarkii, it is essential to improve the accessibility of distribution data and promote information sharing. While there is clear scientific interest in management-related studies, strengthening research efforts by also integrating knowledge from non-academic sources could help enhance the effectiveness of management strategies.