Terrestrial isopods (Oniscidea) are crustaceans that thrive in terrestrial environments. This study provides an overview of the major topics in terrestrial isopod research during the last 70 years in order to provide an example of publication practices in invertebrate zoology and to examine how basic research in this area is transferred to its applications. Co-citation analysis and bibliographic coupling based on citation data from the Web of Science Core Collection was used. Findings show that while research on terrestrial isopods expanded in applicative research prioritised by research policies, basic research continues to flourish. The most productive countries in the field include the major developed economies and several smaller nations. In the smaller countries, as well as in France and Italy, the bulk of woodlouse research is performed at a few institutions with traditions in this field. Some of the most influential works have been published in periodicals or monographs that are not indexed in Web of Science or Scopus and lack impact factors. Conference proceedings represent some of the most influential publications in the field. Our findings indicate that smaller and developing economies make significant contributions in invertebrate zoology if their research organisations can achieve continuity of research on a topic. Another conclusion is that journal metrics may be a misleading descriptor of the impact of studies and researchers in this field. Ultimately, these results identify several examples of how basic research in invertebrate zoology leads to applications with considerable socio-economic impact.

Citation analysis, crustacean, invertebrate zoology, Oniscidea, scientometrics

Invertebrate zoology, as a scientific field, studies the greater part of all living animals, as invertebrates represent the majority of animal biodiversity. Basic research in this field forms the foundation for applicative studies that may extend to other scientific fields and is essential to conservation efforts. Nevertheless, basic research of invertebrates other than model organisms receives relatively little funding and little attention in educational curricula (Leather 2009; Martin 2011). This puts invertebrate zoology in a paradoxical position: although we might expect it to be an extremely important field in the broader scope of the life sciences, it is perceived by the public as almost completely irrelevant. For this reason, it is important to understand how knowledge is shared in the community of researchers in this field and how it is ultimately transferred to its applications.

Terrestrial isopods or woodlice (Oniscidea) are a group of crustaceans that has successfully adapted to the terrestrial environment (Fig. 1). The most recent published account of their diversity lists more than 3700 recognised species, a number that has certainly grown since, making woodlice the most diverse group of isopod crustaceans (Sfenthourakis and Taiti 2015). As litter decomposers, these animals have a profound ecological impact (David and Handa 2010). Woodlice display various degrees of terrestrialisation, making them particularly interesting to the study of evolutionary transition to land (Hornung 2011). In addition to the studies of their diversity and ecology, research interest in terrestrial isopods is very broad, ranging from biogeography to ethology and biochemistry (Schmalfuss 2018).

Figure 1. 

The three most extensively studied woodlouse species (Schmalfuss 2003) A Armadillidium vulgare B Oniscus asellus C Porcellio scaber. Photographs by Ana Sterle (A) and Miloš Vittori (B, C).

A comprehensive list of literature on terrestrial isopods published prior to 2000 was assembled by Schmalfuss and Wolf-Schwenninger (2002). The list covers scientific publications dealing specifically with the biology of terrestrial isopods. Schmalfuss (2018) also provided a historic overview of prominent researchers working on terrestrial isopods, from Aristotle to currently active research groups. His survey focused predominantly on research in the field of isopod systematics and the lives and work of some of the giants of woodlouse systematics in the 20^th century. It also presented the work of prominent researchers working on other aspects of terrestrial isopod biology. An account of major topics in terrestrial isopod biology was also given in the most recent review of the state of knowledge on these crustaceans, published by Hornung (2011).

In the present contribution, we use bibliometric methods to obtain an overview of the main topics and trends in research dealing with terrestrial isopods, including fields of research that use woodlice as experimental organisms and do not necessarily focus on the biology of this taxonomic group as such. Our aim is to use terrestrial isopod research as a case study of how invertebrate zoology functions in the modern scientific environment and to outline how basic research on invertebrates is linked to its applications. We quantitatively describe the development of this field during the second half of the 20^th century and the first two decades of the new millennium and identify the studies that influenced the development of various research directions in the field, including an account of what types of publications they were published in.

Bibliometrics are becoming an integral part of research evaluation due to the greater availability of article and citation data, as well as the development of new analysis software (Ellegaard and Wallin 2015). Compared to traditional review techniques, they offer several advantages. Firstly, they are a quantitative way of measuring research impact, meaning that they are objective. Secondly, they are transparent and the results can be replicated using the same method. Thirdly, they are scalable, which means that they can be applied on an individual, institutional, national, or international level. Finally, they allow for the analysis of publication performance, as well as the structure and dynamics of the research field under study.

Our bibliometric analysis relies on citations, which provide an objective measure of a paper’s impact in a field of knowledge (Garfield 1979). We use two methods, namely co-citation analysis and bibliographic coupling (Kessler 1963; Small 1978). Each uses citation relationships between publications in its own way, thus complementing each other. Co-citation analysis clusters publications that are often cited together. This property allowed us to identify important publications not included in our database due to being published in non-indexed journals or books as well as works published earlier than the publications in the database. In contrast to co-citation, bibliographic coupling clusters publications with overlapping bibliographies and is thus an adequate technique for the detection of the current state of research, as well as the identification of future trends.

To obtain a relevant dataset of publications on terrestrial isopods, we used the Web of Science Core Collection, which contains publication and citation data. We obtained our dataset by searching for the scientific and trivial names of the taxon Oniscidea, as well as several of the most studied genera of terrestrial isopods that we were able to identify in the World catalogue of terrestrial isopods (Schmalfuss 2003) and the literature overview by Schmalfuss and Wolf-Schwenninger (2002). Our search was limited to the period between 1950 and 2020. While it is possible to search WoS for works published as far back as 1900, few works published before 1950 are indexed in WoS and including this period would not be representative. Earlier relevant publications were therefore identified using co-citation analysis. Upon inspection of the obtained database, we refined the search by excluding keywords most frequently shared by publications that were not relevant to the study.

To obtain our dataset we applied the following search using the appropriate Boolean operators (AND, OR, and NOT):

1. - TS=”terrestrial isopod*” OR TS=”oniscoid*” OR TS=”woodlice” OR TS=”oniscid*” OR TS=”pill bug” OR TS=”sow bug” OR TS=”sea slater” OR TS=”roly-poly” OR TS=”potato bug” OR TS=”armadillidium” OR TS=”porcellio*” OR TS=”philoscia” OR TS=”oniscus” OR TS=”ligia” OR TS=”hemilepistus” OR TS=”platyarthrus” OR TS=”woodlouse”
2. - TI=”crab” OR TI=”crayfish” OR TI=”decapod” OR TI=”daphnia” OR TI=”aquatic” OR TI=”amphipod*” OR TI=”lobster” OR TI=”prawn” OR TI=”shrimp” OR TI=”gastropod*” OR TI=”snail” OR TI=”marine isopod” NOT (TI=”terrestrial” OR TI=”littoral”)
3. - TS=”mitochondrial” OR TS=”androgenic gland” NOT (TS=”terrestrial isopod*” OR TS=”oniscoid*” OR TS=”woodlice” OR TS=”oniscid*” OR TS=”pill bug” OR TS=”sow bug” OR TS=”sea slater” OR TS=”roly-poly” OR TS=”potato bug” OR TS=”armadillidium” OR TS=”porcellio*” OR TS=”philoscia” OR TS=”oniscus” OR TS=”ligia” OR TS=”hemilepistus” OR TS=”platyarthrus” OR TS=”woodlouse”)
4. - TS=”random walk” OR TS=”navigation” OR TS=”path integration”
5. - #1 NOT (#2 OR #3 OR #4)

To visualise bibliometric networks, we used VOSviewer (van Eck and Waltman 2010) and CitNetExplorer (van Eck and Waltman 2014a). VOSviewer can visualise networks of keywords, individual publications, authors, journals, or even countries based on citation, bibliographic coupling, co-citation, and co-authorship relations. To structure a bibliometric map, VOSviewer first uses a co-occurrence matrix to obtain a similarity matrix. Moreover, it constructs a map by locating items close to each other by minimising the weighted sum of the squared Euclidean distances between all pairs of items. Finally, it uses translation, rotation, and reflection to obtain consistent results (Dominko and Verbič 2019). An individual item is assigned to only one cluster and colours are used to distinguish between different clusters. The size of the circle indicates citation strength or occurrence strength in the case of keywords. A more detailed account of the VOSviewer software package can be found in van Eck and Waltman (2010, 2014b). We complemented VOSviewer with CitNetExplorer, which allowed the visualisation of publications on a map where closeness between publications is highlighted on the horizontal axis and the year of publication on the vertical axis. As such, it is an ideal tool for the analysis of the development of a research field. A detailed explanation of CitNetExplorer is available in van Eck and Waltman (2014a).

To interpret the obtained bibliometric networks, items displayed on the maps were looked up in the database, allowing us to identify the topics of the items in question and the journals or proceedings in which they were published.

Our study provides a concise overview of the development of terrestrial isopod research during the last 70 years in terms of how the extensive bibliography on this subject is structured according to publication types and the geographical distribution of publication output.

While the top countries in terms of research output include the leading developed economies with large research expenditures, which can be observed in other scientific fields as well (Holmgren and Schnitzer 2004; Jarić et al. 2012), several smaller and somewhat surprising nations are close to the top, such as Portugal, Slovenia, and Tunisia (Table 2). The high productivity of these smaller countries is linked to a handful of institutions with decades-long traditions in this area of research, as can be deduced if these results are considered alongside data on the most prolific organisations (Table 3) and the historic overview by Schmalfuss (2018). This historic survey is also an excellent source of information for all who are interested in research groups and individuals that made exceptional contributions to the field. Considerable outputs are also produced in BRIC countries: Brazil, Russia, India, and China. France has a prominent position in this field and has been home to some of the most productive researchers and organisations as well as the central journals on the subject in the 20^th century. Nevertheless, the majority of the French output is produced by only a few organisations with long traditions in the field, similar to the situation in smaller nations.

The language bias of international scientific databases may distort the representation publications in languages other than English (Amano et al. 2016). This becomes evident in the case of terrestrial isopod biology if we compare the outcome of our analysis of the WoS dataset with the publications published between the years 1850 and 2000 collected by Schmalfuss and Wolf-Schwenninger (2002). Our search in WoS returned fewer than ten publications in individual languages other than English and French (not shown), yet many more such publications can be found in the collection of Schmalfuss and Wolf-Schwenninger (2002) which includes non-indexed publications in a variety of languages. While this does not invalidate our identification of the group of leading nations in the field during the study period, as most of these nations are in a similar position in this respect, the numbers of publications for several countries and institutions are certainly greater than represented in WoS.

By analysing bibliometric networks, we were able to identify several major topics in terrestrial isopod research, the past and current development, and the relationships between these topics. Keyword analysis, co-citation analysis, and bibliographic coupling have identified roughly the same set of general research topics in research related to terrestrial isopods. These are: (1) ecotoxicology, (2) systematics, (3) microbe-host interactions, (4) ecology, with a great focus on population ecology and life histories, and (5) physiology. In the last field, the dominating topics are digestive physiology, ecophysiology (particularly in relation to evolutionary transition to land), and biomineralisation. Many of these topics, such as ecotoxicology, microbe-host interactions, and life-history ecology, have been identified as major topics in this field by authors who reviewed work on terrestrial isopod biology (Hassall et al. 2005; Hornung 2011; Schmalfuss 2018), whereas some prominent topics, such as ecotoxicology, were not in the scope of those reviews. This is understandable, as these areas of research do not focus on isopod biology but use woodlice as experimental organisms.

Ecotoxicology is an obvious topic on the rise. This is attested by the dominance of this field when it comes to citations and the prominent increase in the number of papers on terrestrial isopods that are published in ecotoxicological journals (Figs 6, 7). The explanation of this success is straightforward, as the field is one of the current priorities of research and development policies, particularly in Europe (European Commission 2020). As we can deduce from the obtained co-citation networks, the initial study influencing this field was the work of Wieser (1968) that deals with the metabolism of metals in the terrestrial environment, largely from the point of view of terrestrialisation in arthropods. The initial research therefore considered how isopods obtain and conserve metals as micronutrients in the terrestrial environment, in which direct uptake from seawater is impossible. This resulted in the use of woodlice as bioindicators of potentially toxic metals, leading to their extended use in ecotoxicology (Hopkin, 1989). While metal toxicity was the major focus of research at the turn of the millennium, emerging contaminants, such as nanomaterials and microplastics, are now gaining importance (summarised in van Gestel 2012 and van Gestel et al. 2018).

A similar success story is the use of terrestrial isopods in studies on biomineralisation. Here, the initial work in the co-citation network (Fig. 5) is the extensive study on the moulting process in P. scaber and O. asellus conducted by Messner (1965). Woodlice were quickly recognised as suitable experimental animals for the study of cuticle synthesis and mineralisation due to having several convenient characteristics. Woodlice preparing to moult are identifiable by the presence of sternal calcium carbonate deposits, they moult frequently throughout their lives, and they are relatively easy to maintain and handle in the laboratory. In addition, the need to conserve calcium ions necessary for the mineralisation of their exoskeletons during the process of moulting makes them particularly interesting for the study of mineral dynamics and ion transport (reviewed in Ziegler et al. 2005).

As can be deduced from the importance of the publications and keywords relating to this subject, microbe-host interactions in terrestrial isopods have been a very influential topic as well. A large part of the success of the topic likely results from work on the association of terrestrial isopods with the feminising bacterium Wolbachia, which is of great importance to evolutionary biology and the ecology of microbe-host interactions. Although these studies were, to a large extent, conducted on A. vulgare, Wolbachia is of wider interest as it is capable of infecting numerous arthropods and manipulating their sex. As this is also true for many insects, Wolbachia can potentially be used in pest management. This organism is, of course, not the only one studied in woodlice; several commensals and pathogens have been identified in these crustaceans, as well as potential symbionts aiding in the digestion of plant material and other physiological processes (reviewed in Bouchon et al. 2016). Ultimately, research on these associations is still very intensive and facilitated by recent methodological advances in the study of microbiomes (Bredon et al. 2018, 2020).

The examples of research on ecotoxicology, biomineralisation and microbe-host interactions in terrestrial isopods show how basic research on the biology of an invertebrate group later led to the establishment of the animals in question as experimental organisms in more general, even applicative, research topics. Naturally, other topics in woodlouse research had a broader impact on human knowledge as well, as we can expect from any well-conducted scientific inquiry, and these two cases were only discussed at length here as the most obvious examples in the bibliographic networks we obtained.

Despite poor funding opportunities in the field of invertebrate systematics (Martin 2011), there is vibrant evolutionary and taxonomical work on terrestrial isopods being conducted globally, which is reflected in the popularity of systematics-related journals in this field and the universal presence of a systematics cluster in the bibliometric networks obtained in this study. Furthermore, there is no apparent negative trend in the output or the impact of such studies (Figs 5, 6, 7). The relatively scarce knowledge of the diversity of woodlice, particularly in the tropics, the importance of this group from the point of view of animal terrestrialisation (Sfenthourakis and Taiti 2015; Taiti 2017), and perhaps the captivating nature of terrestrial isopods may be factors contributing to the vitality of their systematics.

As demonstrated by the co-citation analysis, the central publications in the field of terrestrial isopod biology during the last 50 years were often conference proceedings and articles published in institutional periodicals, many of which are not indexed in WoS or Scopus and lack impact factors. While the importance of scientific meetings is diminishing and conference proceedings resonate only briefly in most scientific fields (Lisée et al. 2008), symposia on terrestrial isopod biology have a large and lasting impact that is reflected in meetings contributing the most influential publications. At this point, it is too early to make any conclusions about whether or not this trend has continued in the last decade, but proceedings papers are evidently still important to the field, as can be deduced from the intensive bibliographic coupling of the journal that publishes them (Fig. 6). The ultimate importance of proceedings papers and articles in local periodicals shows that as far as terrestrial isopod biology goes, journal metrics do not likely reflect the influence that the publications ultimately have. By extension, the impact factors of journals in which invertebrate zoologists publish their work are poor predictors of the impact these researchers have on their field, a fact we fear is insufficiently appreciated.

The findings of this study point out that publishing in invertebrate zoology follows somewhat specific principles, with great importance of in-person meetings and publications not captured by conventional bibliographic metrics. In addition, major contributions in this field are produced in small and developing economies at institutions that can achieve continuity of research on a topic despite changing research trends. Ultimately, the example of terrestrial isopods shows that basic research on the biology of a seemingly marginal group of invertebrates can lead to flourishing applicative research on some of today’s most pressing issues. This is all the more reason not to neglect such research in the future, as the findings of today can help resolve the issues of tomorrow.

This work was financed by the Slovenian Research Agency, Research Programs P1-0184 and P5-0096.