Revista de Biología Marina y Oceanografía

Online ISSN: 0718-1957

RBMO Vol. 57, N° especial: 122-131, 2022

<https://doi.org/10.22370/rbmo.2022.57.Especial.3338> Article

Research on chimaera with a thematic focus for life history:

A scientometric analysis
Investigación sobre peces quimera con un enfoque de su historia de vida: Un análisis
cienciométrico
Cicero Diogo Oliveira 1*
, Lucia Vanessa Santos 1
and Carlos Yure Oliveira 2

1
Instituto de Ciências Biológicas e da Saúde, Universidade Federal de Alagoas, Lourival Melo Mota s/n, Tabuleiro do Martins, zip code 57072-970, Alagoas, Brazil
2
Departamento de Pesca e Aquicultura, Universidade Federal Rural de Pernambuco (UFRPE), Dom Manoel de Medeiros s/n, Dois Irmãos, zip code 52171-900,
Pernambuco, Brazil
*Corresponding author: [email protected]

Resumen.- Los peces quimera, representados por 52 especies existentes, son animales de aguas profundas por lo cual de difícil accesibilidad
para su estudio; además, son vulnerables a la pesca debido a sus características k-estratégicas. A pesar de ser vulnerables, sobre su historia de
vida hay pocos estudios, lo que dificulta comprender el estado de la población de las especies. Los parámetros de historia de vida son esenciales
en la ecología de poblaciones para evaluar la situación y tendencias de las poblaciones. En este estudio se propuso evaluar la tendencia de las
publicaciones sobre estos peces y las lagunas en el conocimiento, analizando qué temática y especies son más frecuentemente estudiadas. Para
ello se utilizó el método de la cienciométrica, con búsqueda de artículos, utilizando un grupo de palabras dirigidas a quimera en bases de datos de
referencias bibliográficas (Scopus® y Web of ScienceTM). Los artículos se clasificaron por año de publicación, ubicación de los autores (a nivel de
país), especie de interés y tema. El número de artículos por año muestra una tendencia de crecimiento exponencial, lo que indica que se están
investigando cada vez más los peces quimera. Entre los países de autores, se destacan Estados Unidos de América y Reino Unido. Las especies
más estudiadas fueron Hydrolagus colliei, Callorhinchus milii y Chimaera monstrosa. Los temas principales de los artículos fueron la anatomía,
morfología y fisiología, seguidos de la sistemática y evolución. Los temas de investigación más disminuidos fueron la pesca y el crecimiento,
para todas las especies. Por lo tanto, incluso con la tendencia de crecimiento, aún se requiere mayor esfuerzo y refuerzo en la investigación de
estos peces, principalmente en los aspectos de la pesca, crecimiento y la reproducción.

Palabras clave: Holocephali, quimeras, historia de vida, bibliometría, tendencia de las publicaciones

Abstract.- Chimaera, represented by 52 species, are deep-sea animals, therefore difficult to access for study; moreover, they are vulnerable to
fishing due to their k-strategic characteristics. Despite being vulnerable, there are few studies on its life history, which makes it difficult to understand
the population status of the species. Life-history parameters are essential in population ecology to assess the status and trends of population. In
this study, it was proposed to evaluate the publication trends on Chimaera and the gaps in knowledge, analyzing which subject and species are
most frequently studied. For this, the scientometric method was used, based on search of articles using a group of words directed to Chimaera in
databases of bibliographic references (Scopus® and Web of ScienceTM). The articles were classified by year of publication, authors’ location (at
the country level), focus species and subject matter. The number of articles per year showed an exponential growth trend, indicating that studies
on chimaera have been increased. Among the authors’countries, such as the United States of America and the United Kingdom, are prominent.
The most studied species were: Hydrolagus colliei, Callorhinchus milii and Chimaera monstrosa. The main themes of the articles were anatomy,
morphology and physiology, followed by systematics and evolution. The most diminished research topics were fishing and growth, for almost all
species. Therefore, even with the growth trend, more effort and reinforcement is still required in the research of these fish, mainly in the aspects
on fishery, growth, and reproduction themes.

Key words: Holocephali, chimaera, life-history; bibliometrics, publication trend

Introduction et al. 2012); they are classified into three families and six

T
genera (Didier 1995, Didier et al. 2012). Currently this group
he holocephalan, popularly known as chimaera, belong
has 52 species in existence; the genus Hydrolagus presents
to the chondrichthyans class, one of the oldest groups of
the greatest diversity of species (21 species). Among these
vertebrates which emerged in the Devonian period (Castro
existing species, have a low proportion of threatened (8%)
1987, Grogan & Lund 2004). Chimeras are characterized
and NT (8%) species, but still exhibit some data deficiency
by having a holosthetic mandible in which the palate-
(15%) (Finucci et al. 2021).
square merges with the neurocranium and inhabit a marine
environment, mainly deep waters (Suárez et al. 2004, Didier

122

©The author(s). This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-
Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use,
distribution, and reproduction in any medium, provided the original work is properly cited.
 Despite the high ecological importance of the group Materials and methods

S
(Didier et al. 2012, Finucci et al. 2021), information on the
cientific articles were obtained from only two top-level
life history and reproductive biology of these fish, especially
bibliographic reference databases such as Scopus® and
of the deeper water species, is very scarce (Sion et al. 2004,
Web of ScienceTM on their respective web platforms. The
Shiffman et al. 2020). This low amount of information results
search words were: Holocephalan* OR Callorhinchidae OR
from the low commercial value of the species, which are
Rhinochimaeridae OR Chimaeriformes OR Holocephali*
generally discarded (Blasdale & Newton 1998, Moura et
OR “Chimaera” OR Chimaeridae OR spookfish OR “rabbit
al. 2004, Cotton & Grubbs 2015) and the lack of sampling
fish” OR “ghost shark” OR “chimaeroid fish*” OR “elephant
due to them being in inaccessible locations, or are naturally
shark” OR Elephantfish OR Ghostshark OR Ratfish; present
uncommon or rare (Holt et al. 2013, Finucci et al. 2021).
in the title, abstract or keywords, limiting the time until July
Life history parameters (e.g., growth, reproduction) are 2020. The database with the largest number of articles was
essential to provide baseline information on population chosen, and regression between the number of articles and
dynamics and to assess a species’ susceptibility to extinction year of publication was performed to understand the trend
(Cortés 2007, Dulvy et al. 2008, Rigby & Simpfendorfer on the publications. Then, network analysis of the countries
2015, Olivera et al. 2021). In general, the information for and keywords, present in the base, was performed using
this subclass is relatively low; however, some studies have VOSviewer version 1.6. (CWTS, Centre for Science and
reported that these species are more vulnerable to extinction Technology Studies, Leiden University, The Netherlands),
(Barnett et al. 2009, Didier et al. 2012, Chierichetti et al. 2017, software tool for constructing and visualizing bibliometric
Finucci et al. 2017, Francis & Maolagáin 2019). Chimaeras networks.
are characterized by low productivity, and have slow growth
In addition, a new search was conducted, following the
rates, late sexual maturity and low number of offsprings per
same keywords and time limitation, however using only the
reproductive cycle (Didier et al. 2012). Additionally, they
keywords present in the title. This was done to select only the
are less able to offset increased mortality, either by fishing
articles with focus on chimeras’ fish. In this new database,
or environmental changes. Therefore, life history studies of
the focus species were selected and then quantified for the
these species are necessary for their conservation.
absolute frequency of publication by species. In addition to
Scientometric analyses have become fundamental tools the title and abstract, these articles were classified by their
for analyzing current trends within scientific literature and respective theme (Table 1). They were all sorted by the
to indicate knowledge gaps (Seppelt et al. 2011, Zhang et al. same person to reduce the change of inter-encoder reliability
2016, Oliveira et al. 2020, Santos et al. 2021). Assessing the problems.
research attention distributed by taxa and in which scientific
A generalized model analysis (GLM) was performed to
research degree it is conducted have also proved to be a
understand the publication patter by species using variable
frontier for new researchers (Shiffman et al. 2020). These gaps
response to the number of publications and four predictive
can be used to assist in chondrichthyan conservation efforts,
variables: (1) area of distribution, (2) depth, (3) year of species
as well as stimulate new scientific research (Zhang et al. 2016,
description and (4) threat status. All these predictive variables
Shiffman et al. 2020). Therefore, scientific publications on the
were extracted from the International Union for Conservation
life-history, vulnerability, and fishing traits of chimera species
of Nature and Natural Resources platform (IUCN 2020).
have been highly important for understanding and determining
For variable distribution, the species distribution shapefile
the population status, and for making management and
available in the IUCN platform was used and calculated by
conservation decisions.
the area polygons with the aid of the “gArea” function of the
In view of this, the goal of this study was to identify Rstudio raster package (Hijmans et al. 2020); for depth, the
patterns in the number of publications per species of chimaera, mean of maximum and minimum depth was used (IUCN
related to life-history traits and degree of population threat. 2020); the status of threats (Data Deficient - DD; Least
To assess that, the following guiding questions were used: Concern - LC; Near Threat - NT; Vulnerable - VU) were
(1) Is there an increasing trend in chimera publications? (2) converted to numeric values following Dulvy et al. (2014),
Which are the main countries that contribute to the knowledge where species categorized as VU and NT were converted to
and which topics are discussed on subclass? (3) What are the value 1 and LC to 0. The MuMIn package in the R software
main species on this group? (4) Is there a correlation between was used for the GLM (Bartoń 2020).
the number of publications by species and their occurrence
and threat status? To answer these questions, the distribution,
description and threat status data available on the IUCN
platform have been used to perform a scientometric analysis.

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 The MASS package in the R software (Ripley et al. 2020) Results

S
was used to calculate the value of the Akaike Information
earches on the search platforms resulted in 757 articles on
Criterion for small samples (AICc) for each model, then
the Web of ScienceTM and 1,242 on the Scopus® (Suppl.
performed the ΔAICc, which is based on the subtraction of the
material: Table S1). According to the platform data, the first
AICc from the model and the value of the smaller AICc. The
article published was in 1847, however the topic became
calculated AICc weight (AICc-Wt), which considers ΔAICc,
more frequent from 1980 onwards. Annually, the publications
was also done to choose the best model (Akaike 1973).
show an exponential growth [Y= 0.8821*exp(0.0579*X);
r2= 0.8979] (Fig. 1), with a peak of 55 publications in 2011.

Table 1. Descriptions of the themes used to classify scientific articles / Descripciones de las temáticas utilizadas para clasificar los artículos científicos

Figure 1. Trend in the number of publications on Holocephali fish in worldwide based on the Scopus® platform /
Tendencia en el número de publicaciones sobre peces Holocéfalos en el mundo basado en la plataforma Scopus®

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 Among the countries with the largest number of The main keywords in the articles were: Chondrichthyes
publications, the United States of America (385), the United (present in 58 documents); holocephali (55); chimaera (46);
Kingdom (214), Canada (98) and Japan (98) stand out. and evolution (40). In addition, it is observed that words
Countries such as Portugal (27), Brazil (11 documents) and related to genetics (gene duplication; gene loss) have the
Iran (6), became more present after 2015 (Fig. 2). frequency increased after 2015 (Fig. 3).

Figure 2. Network of countries that publish scientific articles on Holocephali, based on Scopus® platform / Red de interacción de
países que publican artículos científicos sobre Holocéfalos, basada en la plataforma Scopus®

Figure 3. Keyword network of scientific publications on Holocephali, based on Scopus® platform / Red de interacción de palabras
clave de publicaciones científicas sobre Holocéfalos, basada en la plataforma Scopus®

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 The second research focused on species resulted in 367 The main themes of the articles are “Anatomy, Morphology
articles (30% of the first research), in which 37 existing and Physiology” (45.0%), followed by “Systematics and
species were mentioned (Suppl. material: Table S2). Among Evolution” (20.5%). However, in the last decade (2010s) the
them Hydrolagus colliei (77), Callorhinchus milii (60) and percentage of these two themes has declined, and the theme
Chimaera monstrosa (54) were the more frequent (Fig. 4). “Distribution and Occurrence” has increased (Fig. 5).
Other species have less than 17 articles, and the majorities
have less than five articles (27 species).

Figure 4. Representation of the number of publications related to species of Holocephali fish, based on Scopus® platform /
Representación del número de publicaciones relacionadas con las especies de peces Holocephali, basado en la plataforma Scopus®

Figure 5. Thematic trend of Holocephali fish publications by decade, based on Scopus® platform / Tendencia temática de las publicaciones de peces
Holocephali por década, basada en la plataforma Scopus®

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 The relationship between species by fundamental themes The GLM that best represented the quantity of publications
for management and conservation shows that only 22 species per species was the interaction between the variables area
are present in publications containing one of the themes (Table of distribution and time of description (Table 3). When
2); the other 30 species do not present any articles on these each of these variables is observed individually, there is a
themes. The scarcest topics are fishery and growth, present positive correlation between the number of publications with
in only two and three species, respectively. distribution area and time of description of the species. The
IUCN status and mean depth does not show a significant
correlation (P-valor < 0.05) (Fig. 6).

Table 2. List of chimaera species vs. fundamental themes for management and conservation actions. 0= absence
of articles; 1= presence of articles / Lista de especies de quimeras vs. temas fundamentales para las acciones de
gestión y conservación. 0= ausencia de artículos; 1= presencia de artículos

Table 3. Coefficients of the Generalized Linear Models related to the variables: distribution area, mean depth,
time of species description and threat status, and the parsimonious values (AIC < 4) / Coeficientes de los Modelos
Lineales Generalizados relacionados con las variables: área de distribución, profundidad media, tiempo de descripción
de la especie y estado de amenaza, y los valores parsimoniosos (AIC < 4)

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 Figure 6. Coefficient estimates (±95% confidence intervals) indicating the magnitude and direction of predictors tested for a model of
scientific production of Holocephali fish. Gray markers represent predictors without significant influence and blue represent positive
effects / Estimaciones de coeficientes (intervalos de confianza de ±95%) que indican la magnitud y dirección de los predictores probados para
un modelo de producción científica de peces Holocephali. Los marcadores grises representan predictores sin influencia significativa y los azules
representan efectos positivos

Discussion trends of the American Elasmobranch Society conference

T
abstracts, these authors observed that the number of studies
he number of publications per year showed an
focused on Holocephali is almost non-existent, and that the
exponential growth trend, however from 2015 the number
most studied species are commonly the most charismatic or
of publications was below the expected value. In 2020, of
easily accessible. According to Cotton & Grubbs (2015), the
the 70 articles expected, only 34 were published (until the
number of articles published is important because in addition
June). The countries which published the most are the most
to biological knowledge, this data is the basis for conservation
developed countries, which consequently have the greatest
management, without which species are unprotected.
financial power to carry out the research (Huveneers et al.
2015). Developing countries tend to have less infrastructure Among the species studied, only five have more than 10
for deep-sea fish research (Shiffman et al. 2020) as such articles. Among these, only one species inhabits environments
research requires high-cost methods and technologically deeper than 750 meters, signifying that logistics (e.g., easy
advanced means (Calis et al. 2005). However, according to access) is also a strong criterion for choosing the focus
the indexed journals in Scopus® from 2013 to 2015, some of species, as diagnosed for elasmobranchs (Huveneers et al.
these countries, such as Argentina and Brazil, have started to 2015, Shiffman et al. 2020). Moreover, these five species
contribute to the knowledge about chimeras. This does not represent 72% of publications. Such a high difference of
mean that before 2013 they had not published about chimeras, some species with many publications and others without,
and there may be publications in journals that are not indexed interferes with scientific progress, especially of little-studied
in the database used. species (Stein et al. 2018). The species with higher mean
depth (>1,000 m), have an average of three articles, in which
Although the number of publications has shown an annual
they practically approach their taxonomy and/or occurrence,
increase when compared to shark groups, there is a clear
resulting in a research gap on life history. Efforts for a better
difference between the groups. According to Ducatez (2019)
understanding of less studied species are necessary, because
study, he counted 9,769 articles on sharks from 1978 to 2014;
as studies which explore marine areas that are little studied
the species with the most articles was Squalus acanthias,
or difficult to access increase, a greater knowledge of the
with 739. This fact may be linked to the diversity of species
biology and the actual number of chondrichthyans species
and consequently their distribution, which is different. This
will be possible (Moral-Flores et al. 2016).
also favors the number of publications, as can be observed
in the study by Shiffman et al. (2020). When analyzing the

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 The present study corroborates with Sion et al. (2004), Acknowledgments
which have pointed out the scarcity of information mainly
We acknowledge the Coordenação de Aperfeiçoamento
on the life history parameters of chimaera, showing that this
de Pessoal de Nível Superior (CAPES) and the Conselho
problem is still recurring, and needs more attention. It was
Nacional de Desenvolvimento Científico e Tecnológico
observed that few species have such well documented data,
(CNPq).
such as Callorhinchus milii, Callorhinchus capensis, and
Chimaera monstrosa. On the other hand, other species which
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Editor: Francisco Concha

Received 28 August 2020
Accepted 05 October 2021

Supplementary material
Table S1. List of articles found on the Scopus® platform / Lista de artículos encontrados en la plataforma Scopus®

See: <https://rbmo.uv.cl/resumenes/v57S1/Oliveira-TablaS1.xlsx>

Table S2. List of articles found on the Scopus® platform for chimera fish species / Lista de artículos encontrados en la plataforma Scopus® para
especies de peces quimera

See: <https://rbmo.uv.cl/resumenes/v57S1/Oliveira-TablaS2.xlsx>

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