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Agradecimientos
7
No caben aquí todas las personas a las que querría dar gracias por haber sido amistad,
compañía, apoyo y ánimo durante estos maravillosos años.
A la asociación de amigos de la Universidad de Navarra y a la Fundación La Caixa, por
su apoyo económico para la realización de esta tesis.
A Rafa y Arturo, gracias por haberme acompañado desde el primer momento. Para lo
académico y lo que no. Por ser ejemplo y modelo, como profesores, como investigadores y
como personas. A Monni, por ser un ejemplo de investigación pasional y vivida. Ojalá que el
futuro me permita seguir trabajando junto a vosotros y compartiendo proyectos. Y gracias
a todas las personas que, desinteresadamente y muchas veces sin conocerme, me han
ayudado en los distintos proyectos de la tesis.
A Tom y David, ladrones de datos y manzanas. Por las miradas cómplices y el apoyo
cada vez que os he necesitado. Al resto de compañeros que ya acabasteis este camino, o que
lo haréis pronto: Amaia, María, Rubén, Nora, Mónica, gracias por las comidas, el café y la
ayuda desinteresada. A todo el departamento de Biología Ambiental, por haber hecho de
estos años no un trabajo sino un disfrute constante.
A mis compañeros de la carrera, de bata y de bota, por escucharme las turras y
apoyarme en todo momento. Por los años que hemos pasado juntos y por seguir
apuntándoos a mis planes y estar ahí a pesar de los años y la distancia.
A mi grupo scout, especialmente a los chavales con los que he tenido la suerte de
compartir esta etapa de mi vida, gracias por enseñarme a ver la realidad a través de los ojos
de un niño, a creer que un mundo mejor siempre es posible. Y a mis compañeros del kraal,
gracias por ser únicos. Gracias por tantos años de campamentos, travesías, findes, cenas y
aventuras, en vosotros he descubierto a personas maravillosas que nunca voy a olvidar.
A Assen, Marcaida y Tibe, sois la clase de amigos que todo el mundo querría tener.
Muchas gracias por haber sido un apoyo fundamental durante tantos años, por la amistad y
los abrazos sinceros. Por estar disponibles en todo momento, siempre dispuestos a escuchar
y compartir los momentos buenos y malos.
A mi familia, a mis padres y a mi hermana, muchas gracias por haberme acompañado
desde que tengo memoria. Por haber soportado mis frustraciones, malas caras y agobios
con grandes dosis de paciencia. Por enseñarme a ser como soy. Por el cariño. Porque por
muy lejos que estéis, siempre os llevo cerca.
A todos vosotros, gracias por acompañarme en esta maravillosa aventura que es vivir.
Agradecimientos
8
“I wish it need not have happened in my time,” said Frodo.
“So do I,” said Gandalf, “and so do all who live to see such times. But that is not for them to
decide. All we have to decide is what to do with the time that is given us.”
TABLE OF CONTENTS
GENERAL ABSTRACT .................................................................................... 11
AIMS AND STRUCTURE ................................................................................ 17
CHAPTER 1: CONCERNING FISHES ........................................................... 23
Aquatic biodiversity: threats .................................................................................................................... 25
Aiming at Target 11: Protected Areas and aquatic ecosystems ................................................. 27
Aiming at target 12: Species conservation status and extinction risk in aquatic
ecosystems. ...................................................................................................................................................... 28
Fishes and their conservation .................................................................................................................. 31
References ........................................................................................................................................................ 32
CHAPTER 2: ASSESSMENT GAPS AND BIASES IN KNOWLEDGE OF
CONSERVATION STATUS OF FISHES ........................................................ 39
Chapter preface .............................................................................................................................................. 41
Introduction ..................................................................................................................................................... 43
Methods ............................................................................................................................................................. 45
Results ................................................................................................................................................................ 48
Discussion ......................................................................................................................................................... 54
Recommendations ......................................................................................................................................... 58
Chapter Transparency ................................................................................................................................. 60
References ........................................................................................................................................................ 60
CHAPTER 3: CONSERVATION STATUS GAPS FOR TOP FISHED
MARINE COMMERCIAL SPECIES ................................................................ 69
Chapter preface .............................................................................................................................................. 71
Introduction ..................................................................................................................................................... 73
Methods ............................................................................................................................................................. 74
Results ................................................................................................................................................................ 76
Discussion ......................................................................................................................................................... 81
Chapter Transparency ................................................................................................................................. 85
References ........................................................................................................................................................ 85
CHAPTER 4: TRENDS AND PERSPECTIVES IN THE KNOWLEDGE OF
CONSERVATION STATUS OF FISHES ........................................................ 91
Chapter preface .............................................................................................................................................. 93
Introduction ..................................................................................................................................................... 95
Methods ............................................................................................................................................................. 97
Results ................................................................................................................................................................ 98
Discussion ...................................................................................................................................................... 105
Chapter Transparency .............................................................................................................................. 107
References ..................................................................................................................................................... 107
CHAPTER 5: SPATIAL PRIORITIES FOR FRESHWATER FISH
CONSERVATION IN RELATION TO PROTECTED AREAS ................. 113
Chapter preface ........................................................................................................................................... 114
Introduction .................................................................................................................................................. 116
Methods .......................................................................................................................................................... 118
Results ............................................................................................................................................................. 121
Discussion ...................................................................................................................................................... 125
Chapter Transparency .............................................................................................................................. 128
References ..................................................................................................................................................... 128
CHAPTER 6: EFFECTIVE REASSESSMENTS OF FRESHWATER FISH
SPECIES: A CASE STUDY IN THE MEDITERRANEAN ........................ 136
Chapter preface ........................................................................................................................................... 138
Introduction .................................................................................................................................................. 140
Methods .......................................................................................................................................................... 142
Results ............................................................................................................................................................. 144
Discussion ...................................................................................................................................................... 147
Chapter Transparency .............................................................................................................................. 149
References ..................................................................................................................................................... 149
CHAPTER 7: GENERAL DISCUSSION ...................................................... 155
References ..................................................................................................................................................... 162
CHAPTER 8: GENERAL CONCLUSIONS .................................................. 167
APPENDICES ................................................................................................. 171
General Abstract
Resumen General
General Abstract
13
Aquatic biodiversity is severely jeopardized by human actions. Among all vertebrates
that live in aquatic environments, fish species are the most diverse and essential for the role
they play in aquatic ecosystems. Fish conservation status had been partially and
increasingly assessed by the IUCN Red List, but they still remain much less assessed than
any other vertebrate group. Thus, further studies are required to understand fish
conservation and propose new solutions to improve their assessments and subsequently
their conservation status and future viability.
In this work, we started by evaluating the completeness of the IUCN Red List fish
assessment itself. Finding a 50% gap in the list of assessed species, we explored species
traits underlying the assessment status of fish species, distinguishing freshwater and
marine species, and identifying several geographical, life history and social drives
underpinning the assessment selection. We also analysed the assessment gap on the top
commercial fish species, which featured prominently in the results of the first analysis. We
evaluated their conservation status concerning the data available about reported and
reconstructed landing trends, and the implications on the sustainability of fisheries.
We expanded the evaluation of IUCN Red List assessments to include the trends in the
last decades for fish. We analysed assessments and evaluated the role of each country in fish
conservation linking it with its economic capacity and proposing guidelines for future IUCN
assessment and reassessment efforts. Following the results of the trend analysis, we
explored the situation of freshwater fish assessments in the Iberian Peninsula, as an
example of a region with a high proportion of endangered species with out of date
assessments. We proposed recommendations based on the use of molecular techniques to
increase the information available and improve future reassessments of Iberian freshwater
ichthyofauna.
As protected areas have been deemed as critical conservation tools, we further
explored the coverage that such areas offer to freshwater fish diversity. To do so, we
identified the most irreplaceable rivers through freshwater fish distribution and compared
them to the current network of protected areas, which was found to grant little protection
to irreplaceable rivers. Moreover, we compared irreplaceable protected areas for
freshwater fish with those identified as irreplaceable for terrestrial vertebrates, finding a
general discordance that suggested a need for reevaluating future design and management
of protected areas.
We conclude with a discussion on the implications that our results suggest for the
future of fish conservation, listing several recommendations and action lines which we
find essential to guide fish conservation in the upcoming years.
14
General Abstract
15
Las acciones humanas amenazan gravemente la biodiversidad acuática. De entre
todos los vertebrados que viven en los ambientes acuáticos, los peces son los más diversos
y esenciales por el papel que juegan en los ecosistemas acuáticos. Anteriormente, el estado
de conservación de los peces ha sido evaluado gradualmente por la Lista Roja de la IUCN,
pero aún están peor evaluados que otros vertebrados. Por ello, se necesitan más estudios
para entender la conservación de los peces y proponer nuevas soluciones que mejoren sus
evaluaciones y su estado de conservación y viabilidad.
En este trabajo, comenzamos por evaluar la completitud de las evaluaciones de los
peces en la Lista Roja de la IUCN. Al encontrar un 50% de especies sin evaluar, analizamos
los rasgos de las especies de peces para explicar cuáles están influyendo en su evaluación,
distinguiendo entre especies dulceacuícolas y marinas e identificando varias razones
biogeográficas, biológicas y sociales. También analizamos el sesgo de evaluación en los
peces de mayor importancia comercial, que resaltaron en el primer análisis. Evaluamos su
estado de conservación con relación a los datos disponibles sobre capturas declaradas y
reconstruidas, y sus implicaciones en la sostenibilidad de las pesquerías.
Expandimos el estudio de las evaluaciones de la Lista Roja de la IUCN para incluir las
tendencias de evaluación de peces en las últimas décadas. Analizamos las evaluaciones y
evaluamos el papel de cada país en la conservación de los peces relacionándolo con la
capacidad económica de los países y proponiendo líneas de acción para futuras
evaluaciones y reevaluaciones de la Lista Roja de la IUCN. Siguiendo los resultados
obtenidos, exploramos la situación de las evaluaciones de peces dulceacuícolas en la
península Ibérica, como ejemplo de región con una gran proporción de peces amenazados
con evaluaciones desfasadas. Propusimos recomendaciones basadas en el uso de técnicas
moleculares para aumentar la información disponible mejorar futuras reevaluaciones de la
ictiofauna ibérica de agua dulce.
Como las áreas protegidas críticas son herramientas críticas de conservación,
exploramos la cobertura que éstas ofrecen a las especies de peces. Para ello, identificamos
los ríos más irremplazables utilizando mapas de distribución de peces dulceacuícolas, y los
comparamos con la red actual de áreas protegidas, que resultó ofrecer una baja protección
a los ríos irremplazables. Además, comparamos las áreas protegidas irremplazables para
peces de agua dulce con aquellas que se han identificado como irremplazables para los
vertebrados terrestres, encontrando discordancias que sugirieron la necesidad de
reevaluar el diseño y gestión de áreas protegidas.
Finalizamos esta tesis discutiendo los resultados y concluyendo con varias
recomendaciones y líneas de acción para guiar la conservación de peces en los próximos
años.
16
Aims and structure
Objetivos y estructura
18
Aims and structure
19
We chose our topic because aquatic species, and especially fishes, are under serious
threats and its conservation perspectives are compromised unless we take urgent action to
preserve species and prevent extinctions. The need for this action should, however, be
informed by Science, and this thesis, therefore, aims to evaluate the progress in the
knowledge of the conservation status of fishes, identify priority areas for their conservation
and propose new conservation perspectives for the upcoming years. To do so, we have
analysed global databases on conservation and biogeography of fish species and detected
biases and trends in the conservation status of fishes. Furthermore, we have produced
indices and statistical outcomes to support our findings. Data were current at the time of
analysis, and may naturally evolve (e.g. proportion of fish assessed in IUCN Red List). Thus,
the results obtained in this project are based on the data available and should be considered
as provisional as new data will update the databases used. Nevertheless, our study reflects
a generally improving trend in the coverage of biodiversity databases and that will be
further discussed in the last chapter.
The thesis starts with a general introduction to the topic of fish assessments (Chapter
1), and proceeds to develop the five major research questions related to fish assessment
that we aimed to answer:
- What gaps and biases could be identified in the world’s authoritative IUCN Red
List for fishes (Chapter 2);
- The consequences that such degree of completeness in assessments could have
for the main commercial species and their conservation (Chapter 3);
- How those assessments changed over time and whether they were related to
socioeconomic parameters and conservation commitments in the countries
undertaking them (Chapter 4);
- What role those conservations commitments (e.g. protected areas) could have in
the protection of threatened species and irreplaceable habitats (Chapter 5);
- How the above findings could be applied to one case study, the Iberian Peninsula
(Chapter 6).
We end with a general discussion (Chapter 7) and the thesis’ Conclusions.
As the five topics are well delimited and correspond to five compact subprojects
within the overall research topic with varying methodologies, each chapter carries its
own Introduction, Methods, Results, and References subsections.
20
The methodological approaches and main findings of the research will be summarized
below.
The first objective of this thesis was to analyse the biases present in the IUCN Red List
for fish species. We compared species present in FishBase (global database of fish) and IUCN
Red List and analysed species traits to find the reasons underlying the assessment gap of
fish species. Assessments were found to be biased towards developed regions, early
description rates and specific IUCN specialist groups. Our results highlighted the low
assessment rates of south American freshwater species. Moreover, fish species commercial
importance did not influence assessment status.
Following the previous findings, we focused our analyses on the conservation status
of top fished commercial fish species. We analysed data on reported catches from FAO and
reconstructed catches from Sea Around Us project. No difference was found in the
assessment rates of top-fished species and fish species of commercial interest in general.
Furthermore, FishBase Vulnerability index was not related to IUCN Red List population
trends or fishing threat. Finally, reconstructed catches showed an increase in landings of
many species with declining population trends, even after IUCN Red List evaluations. We
considered that urgent action between stakeholders to improve species knowledge related
to conservation is essential to ensure future fisheries sustainability.
We then explored fish assessment trends by IUCN Red List in the last decades. In this
study, we analysed species description rates and assessments between 1996-2019 and
evaluated the role of countries in fish conservation according to their economic capacity.
Our results showed an increase in the number and quality of assessments in the last years.
Furthermore, we also found higher proportions of threat and data deficiency for recently
described species. Higher-income countries should pay more attention to reassessing out of
date species, whereas countries with lower levels of assessment were also the ones where
more species have been described in the following years. We found essential to
strengthening evaluations in the upcoming years to develop the role of National Red List
and its integration in the global IUCN Red List.
Considering the need for protection for freshwater fish, we analysed the role played
by protected areas in their conservation. To that end, we applied an irreplaceability index
to identify those rivers in the world with higher irreplaceability value based on their
freshwater fish fauna. Then, we examined whether these irreplaceable rivers fall within the
current network of PAs and the concordance with identified irreplaceable PAs for terrestrial
vertebrates. PAs offer low protection to irreplaceable rivers for freshwater fish, continuing
a traditional trend of miss protection of freshwaters within PAs. Moreover, terrestrial and
Aims and structure
21
freshwater irreplaceable PAs do not generally agree, potentially under considering
freshwater fish necessities in PAs management and design. A paradigm shift is needed to
incorporate freshwaters in future conservation perspectives and ensure the protection of
freshwater ecosystems and the biodiversity they host.
Finally, we applied the previous findings in a case study of a region which hosts high
numbers of endemic and endangered freshwater fish species, high assessment rates and
many outdated assessments, the Iberian Peninsula. Our study found that the rate of
threatened species differed between National and global Red Lists. Considering the high
number of out of date assessments, we identify priority areas inhabited by fish species in
need of reassessments. To ease the reassessment process, we propose the use of eDNA, for
which the coverage for Iberian freshwater fish is high. In the future, the regular update and
maintenance of National Red Lists are essential to ensure effective protection of freshwater
fish.
We conclude with a general discussion of the results and the main conclusions of this
thesis.
CHAPTER 1:
Concerning fishes
Capítulo 1:
Acerca de los peces
Chapter 1
25
Water is widely recognised as the most essential of human resources, on which our
life-support system depends (Dudgeon et al. 2006; Vörösmarty et al. 2010, 2013). Aquatic
ecosystems (rivers, lakes, groundwater, coastal waters or seas) support the delivery of
crucial ecosystem services. Among them, we can mention services as food (fish production
and water for drinking), industry, flood and erosion protection, carbon sequestration and
recreation, most of which can be directly appreciated by people (Grizzetti et al. 2016).
Moreover, aquatic ecosystems harbour outstanding biodiversity. Since the first living
organisms millions of years ago, life has evolved in the aquatic environments and currently,
330,000 species live in the oceans (www.marinespecies.org) and at least 126,000 in the
freshwater ecosystems, and many more may remain yet undiscovered (Mora et al. 2011).
In this chapter, we introduce the topic of the research. We analyse the threats of
aquatic ecosystems and how they are considered within the global conservation objectives.
We focus on fish as study taxa for this project, analysing their conservation challenges and
addressing them in the different chapters of the thesis.
Aquatic biodiversity: threats
In a rapidly changing world, aquatic ecosystems and their biodiversity are threatened
by a wide suite of anthropogenic stressors. Concerning the marine environment, main
threats emerge from overfishing, pollutant, sediment and nutrient input (Halpern et al.
2007, 2008), habitat loss (Dulvy et al. 2003) and invasive alien species (Bax et al. 2003).
These anthropogenic processes are causing a strong impact on critical ecosystem services
such as fisheries or nutrient cycling (Selig et al. 2014). Furthermore, climate change is very
likely to be a driver of marine fish species turnover, local extinction and invasion in the
upcoming years (Cheung et al. 2009). Biodiversity loss in the oceans will increase resource
collapses and decrease stability and recovery potential (Worm et al. 2006). In the
freshwater environment, human activities have globally increased in the last century,
overexploiting natural resources (Garcia-Moreno et al. 2014). Freshwater ecosystems are
potentially the most endangered ecosystems in the world (Dudgeon et al. 2006). Nowadays,
freshwaters receive impacts from habitat loss and fragmentation, water pollution, extensive
wetland drainage, groundwater depletion, the establishment of introduced alien species,
and overfishing of native ones (Dudgeon et al. 2006; Strayer & Dudgeon 2010; Vörösmarty
et al. 2010). Climate change is also challenging freshwater ecosystems function (Woodward
et al. 2010) and the physiology, distribution, and survival of freshwater species, such as
fishes (Poesch et al. 2016). Immersed in the Anthropocene, we are undergoing the “sixth
mass extinction” (Barnosky et al. 2011), not only causing direct extinctions but also
26
populations extirpations and declines in species abundance (Dirzo et al. 2014; McCauley et
al. 2015) (Figure 1.1).
Figure 1.1: Terrestrial and marine anthropogenic stressors driving defaunation processes. From
McCauley et al. (2015).
In the early 2000s, world countries committed through the Convention on Biological
Diversity (CBD) “to achieve by 2010 a significant reduction of the current rate of
biodiversity loss”. Indicators developed to evaluate this target showed increased pressures
towards biodiversity and the rate of biodiversity loss in the first decade of the millennia did
not slow down (Butchart et al. 2010). To overcome this failure, the CBD created in 2010 the
Aichi Biodiversity Targets for the 2011-2020 period “to take effective and urgent action to
halt the loss of biodiversity to ensure that by 2020 ecosystems are resilient and continue to
provide essential services, thereby securing the planet's variety of life, and contributing to
human well-being, and poverty eradication (SCBD 2010). This plan relates directly to the
UN’s Sustainable Development Goals (SDGs), particularly, to the 2 goals focused on the
protection of terrestrial and marine life (Green et al. 2019). Among these targets, two of
them address biodiversity loss and their conservation: Targets number 11 and 12. Target
number 11 states that “by 2020, at least 17 per cent of terrestrial and inland water, and 10
per cent of coastal and marine areas, especially areas of particular importance for
biodiversity and ecosystem services, are conserved through effectively and equitably
managed, ecologically representative and well-connected systems of protected areas and
other effective area-based conservation measures, and integrated into the wider landscapes
and seascapes”. Target 12 proposes that “by 2020 the extinction of known threatened
species has been prevented and their conservation status, particularly of those most in
decline, has been improved and sustained”.
Chapter 1
27
Aiming at Target 11: Protected Areas and aquatic ecosystems
Over the last 20 years, the number and extent of protected areas established globally
have increased dramatically, with more than 240,000 Protected Areas (PAs) covering over
46,000,000 km2 in both land and sea (https://www.protectedplanet.net/). This progress
represents the growing recognition of their value as a way to safeguard nature and cultural
resources and mitigate human impacts on biodiversity (UNEP-WCMC and IUCN 2016),
contributing to human wellbeing and sustainable development. According to the last
Protected Planet report, PAs cover now 15.2 % of the earth land’s surface and 7.4% of the
world’s oceans, and CBD target 11 was expected to be achieved by 2020 (UNEP-WCMC et
al. 2018), though we consider this hypothesis optimistic (Figure 1.2).
Nevertheless, PAs designation does not necessarily imply direct protection to
biodiversity and ecosystems. Traditionally, PAs designation has been biased towards
remote areas (Venter et al. 2014) and still favours low-cost lands. This low-cost trend has
intensified through time (Venter et al. 2018) and does not take into consideration species
or ecosystems necessities. Given the current targets established for conservation and
development, the key role of PAs in many social and environmental agendas, and the
reduced political commitment in some countries (Watson et al. 2014), we need some
changes in the way how PAs are established and managed.
28
Figure 1.2: Evolution in protected area coverage on land and ocean EEZ (Exclusive Economic Zones)
and ABNJ (Areas Beyond National Jurisdiction) between 1990 and 2018 and projected growth to
2020 according to commitments from countries and territories. From UNEP-WCMC et al. (2018)
Countries are underperforming in locating PAs such that they contribute to
representing threatened species and reach the goal of stopping their decline (Venter et al.
2018). Furthermore, PAs tend to be allocated according to terrestrial necessities, lagging
behind effective freshwater protection (Juffe-Bignoli et al. 2016). These under
consideration of freshwater necessities in PAs design has been widely discussed in the past
(Abell et al. 2007, 2011) and many suggestions have been done on how to effectively
allocate PAs to protect freshwater biodiversity (Hermoso et al. 2016, 2017; Juffe-Bignoli et
al. 2016). The objective of 17% of inland water protection must go together with realistic
conservation objectives, owing to the extreme level of threat that freshwater biodiversity
suffers (Collen et al. 2014).
In the marine realm, there are high differences in protection between PAs in
countries’ Exclusive Economic Zone (EEZ) and in Areas Beyond National Jurisdiction
(ABNJ), where almost no protection is offered for biodiversity (UNEP-WCMC et al. 2018).
With the exponential growth of Marine Protected Areas (MPAs) in the last years, there is a
growing concern about how these areas can be managed or the industrial fishing that is
sometimes developed within them (Sala et al. 2018).
Aiming at target 12: Species conservation status and extinction risk in
aquatic ecosystems.
Human activities have driven hundreds of species to extinction (Barnosky et al. 2011).
Aware of this problem, several initiatives and institutions have emerged to protect nature
and achieve a sustainable future. Among them, we could cite the World Wildlife Fund
(WWF), the above-mentioned Convention on Biological Diversity, or the Intergovernmental
Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES). Nevertheless, in
this project, we will focus on one of the most important institutions for the direct
implication that it has on the establishment of conservation priorities (Rodrigues et al.
2006), the International Union for the Conservation of Nature Red List (IUCN Red List).
In 1948, the International Union for the Conservation of Nature (IUCN) was founded,
bringing together governments and civil society with a common goal, to protect nature. The
IUCN aimed to encourage international cooperation and provide scientific knowledge and
tools to guide conservation action. In 1964, IUCN created the IUCN Red List of Threatened
Species, which made available to public access the first comprehensive list of threatened
Chapter 1
29
mammals and birds, compiling information from evaluations in previous years. More and
more species have been added every year since its establishment, and full assessments for
several groups have been completed.
IUCN Red List classifies species into several extinction risk categories, according to a
range of quantitative criteria. These categories and criteria have changed over time, since
their first release in 1991. Over the following 10 years, two more versions and a series of
updates of the versions were published. Finally, in 2001, Version 3.1 was adopted by the
IUCN Council (IUCN 2012). All new assessments from January 2001 use this latest version.
Nevertheless, species previously assessed which have not been reassessed may have older
categories (especially from the 2.3 version of 1994).
As mentioned before, IUCN Red List categories describe a chance of becoming extinct.
A higher extinction risk implies a higher chance of extinction in the absence of effective
conservation action. From lower to higher extinction risk, IUCN Red List categories (and
their acronyms) are Least Concern (LC), Near Threatened (NT), Vulnerable (VU),
Endangered (EN), Critically Endangered (CR), Extinct in the Wild (EW) and Extinct (EX)
(Figure 1.3). Together, species under categories VU, EN, and CR are described as threatened
species. Moreover, species may be classified as Data Deficient (DD), when information is not
adequate to assess its extinction risk. Dealing with DD species is complicated and several
studies have been performed with these species (Morais et al. 2013; Böhm et al. 2013; Bland
et al. 2015, 2017; Bland & Böhm 2016), dealing with the issue of whether to consider these
species as threatened or no and the chance of using new methodologies to address their
conservation status.
Nevertheless, the IUCN Red List is not only a classification scheme. Species
evaluations offer detailed information on species taxonomy, geographic range, population
trends, habitat and ecology, threats, and conservation action. Several of these fields are used
as criteria to establish species extinction risk. Criteria used by IUCN Red List categories are
a series of quantitative values associated with risk factors of organisms and their life
histories. Used for classifying species as VU, EN, or CR, meeting any one of these criteria
qualifies a taxon for hierarchically classifying at that level of threat (e.g. meeting a single
criterion for a higher level places the species at that level even though most criteria could
be met for a lower level). These criteria refer to reductions in population size, reduced
geographic range, small population size (mature individuals), and quantitative analyses of
extinction in the wild. Further details on those criteria can be found in the IUCN Red List
Categories and Criteria Version 3.1 (IUCN 2012).
30
Figure 1.3: IUCN Red List categories according to IUCN Red List Categories and Criteria Version 3.1.
Adapted from IUCN (2012).
Unfortunately, along the years that the IUCN Red List has been recording species data,
a total of 882 species went extinct (IUCN 2020) and 77 more species were extinct in the wild
(but survive in captive populations). But the problem is not only a matter of species loss but
also of declines in populations and local abundances which have led to local extinctions
(Ceballos et al. 2017). Vertebrate populations are declining both in terrestrial and marine
ecosystems, in a defaunation process of uncertain future (Dirzo et al. 2014; McCauley et al.
2015). Reports published in the last decade state a dramatic decline in vertebrate
populations, no matter the taxa, using metrics such as the Living Planet Index (LPI), a
measure of the state of global biological diversity based on population trends of vertebrate
species from around the world (McRae et al. 2017).
Figure 1.4: Population declines in the Living Planet Index (LPI) for a) all vertebrates, b) freshwater
vertebrates and c) marine fishes. Adapted from WWF (2015, 2020).
Local and global LPI declines of populations have been reported worldwide (Figure
1.4), with an overall decline of 68% in the population sizes of vertebrates between 1970 and
Chapter 1
31
2014 (WWF 2020), increasing up to 84% for freshwater vertebrates. Among the freshwater
vertebrates species, fishes have suffered the greatest declines (WWF 2020) and marine
fishes have also declined by 50 % (WWF 2015), calling conservation efforts in the upcoming
years in order to revert such trends.
Fishes and their conservation
Fish are doubtlessly the most speciose group of vertebrates, with more than 36,000
species described so far (Fricke et al. 2020) and current description rates suggest that many
more species remain undiscovered (Pelayo-Villamil et al. 2018). Diverse in morphology,
physiology, behaviour, and habitats that they occupy, they are adapted to almost all aquatic
environments on earth (Nelson et al. 2016). They occur in rivers, lakes, and oceans
throughout the world. Some species, the diadromous species, can live for part of their life in
freshwaters systems and part in marine environments. But many other species live in
estuarine habitats or, belonging to one environment, may have populations that live in the
other one. In both freshwaters and oceans, a higher diversity is found in the tropics. Higher
rates of freshwater fish diversity are found in central Africa, the Amazonian basin in South
America, and South-Eastern Asia (Abell et al. 2008). For marine species, fish diversity is
concentrated in continental shelves, and among them, in tropical coral reefs (Snelgrove et
al. 2017)
Fishes are important species in terms of food supply, but also as recreational value
for naturalists, recreational fishing (Hughes 2014; Winfield 2016), and aquarists (Maceda-
Veiga et al. 2013, 2016). We must recognize the value of and our dependency upon fishes
and other organisms, but our threats to the integrity of the environment also pose a serious
threat to fish species (Nelson et al. 2016). Both changes in distribution patterns of many fish
species and the extinction of some native fish have been directly linked to human
intervention. As an example, the mean freshwater fish extinction rates during the last 110
years in Europe and North American is a hundred-fold that of the calculated natural rate
(Dias et al. 2017). Furthermore, fishes are described at incredibly high rates (Nelson et al.
2016; Fricke et al. 2020), and many species are likely left to be discovered in most diverse
regions (Reis 2013).
The importance of fish diversity and its conservation has resulted in a set of databases
where fish information is stored and made accessible to stakeholders, such as
ichthyologists, conservationists, and even the general public. Among them, we could cite
two outstanding databases in terms of both species coverage and information they provide.
First, Eschmeyer’s Catalog of Fishes stores the most up to date records of fish species, with
a strongly taxonomic and systematic point of view and currently comprising 35,613 valid
32
fish species (Fricke et al. 2020). Secondly, FishBase, a reference tool for fish study which
includes a wider range of data such as geographic range, description, life traits, and
reproduction for 34,300 fish species (Froese & Pauly 2019). Nevertheless, none of these
databases provides us with direct metrics or estimations of species conservation status,
which is a task carried out by the IUCN Red List.
Up to date, almost 21,000 fish species have been evaluated in the IUCN Red List (IUCN
2020), with more species evaluated in the marine systems than in the freshwater ones. As
we will analyse in chapters 2 and 5, this number has significantly increased in the last years
and plans to evaluate all freshwater fish species are being developed all over the world.
Several IUCN groups have contributed with their effort to increase global coverage of fish
assessments, such as IUCN's Freshwater Biodiversity Unit
(www.iucn.org/theme/species/our-work/freshwater-biodiversity), the IUCN Freshwater
Fish Specialist Group (www.iucnffsg.org/), IUCN Shark Specialist Group SSG
(www.iucnssg.org) or the Global Marine Species Assessment GMSA
(http://sci.odu.edu/gmsa/) (Arthington et al. 2016). Nevertheless, fish assessments (all
together with reptiles) remain far from the assessment rates common for other vertebrates
(Meiri & Chapple 2016) and further efforts are required to evaluate all fish species and
ensure their conservation and protection in the future.
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CHAPTER 2:
Assessment gaps and biases in knowledge of conservation status of
fishes
Capítulo 2:
Lagunas de evaluación y sesgos en el estado de conservación de peces
This chapter is based on the following journal article:
Miqueleiz, I., Bohm, M., Ariño, A.H., Miranda, R. (2020)
Aquatic Conservation: Marine and Freshwater Ecosystems
Assessment gaps of fishes
41
Chapter preface
Fish species are important for both humans and ecosystems. According to FishBase
database records, currently, more than 33,500 fish species inhabit marine and freshwater
environments, and many more remain yet undiscovered. As we have seen in the General
Introduction, many of these species are threatened with extinction, and conservation
measures are needed to protect them. The International Union for the Conservation of
Nature (IUCN) Red List has assessed the conservation status of approximately half of
current known fish species, the lowest percentage in any vertebrate group. Furthermore,
many fish species remain assessed as Data Deficient, misrepresenting extinction risk levels
for them. To improve further assessment strategies, we first need to know about assessment
biases that could push conservation decisions, and therefore help focus evaluation efforts
towards those taxa and regions that are in the greatest need of assessments.
In order to identify the variables that may underlie this assessment gap, we examined
several species traits related to distribution, life-history, taxonomy, conservation, and the
economic relevance of species according to their IUCN Red List assessment status. We
explored IUCN Red List assessment patterns and included separate statistical analyses for
freshwater and marine species.
Our results showed that several traits analysed were under the assessment bias for
fish species. IUCN Red List assessments were biased towards economically developed
regions, species with early description dates and species covered by current IUCN
taxonomic specialist groups. Species living in remote areas or habitats were more likely to
be unassessed by IUCN Red List. In particular, South America had low assessment levels for
freshwater fish species. Other traits such as commercial importance did not influence the
assessment status of fish species, an issue that will be addressed in the following chapter of
the thesis. Fish species low assessment rates combined with an increase in species
discovery resulted in a large proportion of recently discovered species not being evaluated
by IUCN Red List. Altogether with other conservation initiatives, we encourage assessment
in poorly assessed areas and taxonomic subgroups to prompt timely conservation action to
prevent species extinctions. Further implications on how IUCN Red List assessments have
been carried out will be discussed in chapter 4 of this work.
Assessment gaps of fishes
43
Introduction
Throughout the earth’s history, aquatic ecosystems have formed both a mosaic and a
continuum of habitats ranging from the freshwater springs, rivers, lakes, and wetlands of
continents and islands to estuaries, shallow coastal habitats, reefs, and the seas (Arthington
et al. 2016). Fishes are one of the world’s most important natural resources, as they provide
humans with various ecosystem services (Olden et al. 2007). Fish regulate food web
dynamics and nutrient balances (Holmlund & Hammer 1999)and also contribute to health,
well-being, cultural identity, and economies of societies (Hughes 2014). With more than
33,500 species currently described, fishes constitute an important part of the biomass of
aquatic ecosystems (Jennings et al. 2008), with slightly more fish species in freshwater than
marine ecosystems (Carrete Vega & Wiens 2012; Fricke et al. 2020). However, population
declines, mainly caused by habitat loss and degradation, invasive species, overexploitation,
pollution, and climate change (Dudgeon et al. 2006), are increasing the risk of global or local
extinctions of species (Darwall & Freyhof, 2016). Over the current century, marine and
freshwater organisms will face a suite of environmental conditions that have no analogue
in human history (Harnik et al. 2012; Garcia-Moreno et al. 2014).
Fish continue being described at very high rates, with about 3,900 new species
described between 2005-2014 (Nelson et al. 2016). The most comprehensive database on
fish species is FishBase (Froese & Pauly 2016), which provides information about species
distributions, taxonomy, and biological traits and indices for species, However, this
database does not provide an estimation of species’ extinction risk (Miranda 2017). To
evaluate a species’ extinction risk, and assess its current, past, and future threats, we need
to access the reference guide on extinction risk over the last 50 years (Rodrigues et al.
2006), the IUCN Red List of Threatened Species (IUCN 2017). Having failed to reduce the
rate of biodiversity loss by 2010 (Butchart et al. 2010), the Convention on Biological
Diversity determined that during the past decade there was insufficient policy-specific
scientific information to aid the decision-making process (Costelloe et al. 2016). Given the
global threat to a large proportion of species (Pimm et al. 2014), the IUCN Red List and the
Red List Index (Butchart et al. 2004) are essential indicators to track progress towards
meeting Aichi Biodiversity Target 12: that “by 2020 the extinction of known threatened
species has been prevented and their conservation status, particularly of those most in
decline, has been improved and sustained” (SCBD 2010). Besides, the IUCN Red List directly
inputs in several conservation and policy instruments, such as the development of Key
Biodiversity Areas (KBAs; Langhammer et al., 2007), the Convention on International Trade
in Endangered Species of Wild Fauna and Flora (CITES) (Rodrigues et al. 2006) and
Chapter 2
44
dissemination of biodiversity and threat information to researchers, conservation planners
and business as an environmental impact tool.
Several specialist groups and assessment projects exist under the umbrella of the
IUCN’s Species Survival Commission (SSC), such as the Marine’s Biodiversity Unit’s Global
Marine Species Assessment (GMSA), several marine fish Specialist Groups, and the
Freshwater Fish Specialist Group (FFSG), which have so far assessed the extinction risk of
half of all known fish species (IUCN 2017). This is much lower than assessment levels in
other vertebrate groups (e.g. almost 99% in mammals and birds) (Meiri & Chapple 2016),
although fish are far richer (e.g. six times the number of mammal species and three times
the number of birds). Knowledge of aquatic biodiversity is also lower than that of terrestrial
groups due to bias in conservation research toward charismatic terrestrial species (Darwall,
Holland, et al., 2011). Assessment processes are currently struggling to catch up with fish
discovery rates, resulting in incomplete knowledge of fish biogeography, population
density, and threats (Arthington et al. 2016).
In addition, many fish species have cryptic or remote distributions, such as tropical
freshwater fishes (Alofs et al. 2014), thus lacking sufficient information to assess their
extinction risk. An additional consequence of this knowledge gap is the high number of
species assessed as Data Deficient (DD). Data deficiency may be caused by a lack of
information on population status and trends, outdated information, or because a species is
known only from the type specimen (Bland & Böhm 2016). With over 20% of fish species
on the IUCN Red List currently classified as DD, there is a dangerous misrepresentation of
risk levels in this group and overlooking many species in conservation efforts (Morais et al.
2013) even though they may require them. In a context of limited resources and funding for
species assessments (with half of it coming from philanthropic sources) (Juffe-Bignoli et al.
2016), many species remain unassessed by IUCN. However, the affordability of assessments
when considered at a global scale has been demonstrated (Turak et al. 2016; Juffe-Bignoli
et al. 2016) and constitutes a best-value knowledge product into which money should be
invested.
Considering that only half of all fish species are assessed, how representative of the
broader fish fauna is this subset of assessed species? Complex reasons may account for
certain species being systematically overlooked while others are more likely to be assessed.
Species presumed to be at high risk of extinction may be assessed first, such as species with
small range size, which is one of the main criteria used by IUCN to establish a risk category
for a species (Meiri & Chapple 2016). Other traits like short generation times and small body
size associated with fast life histories, should enable species to increase their resilience from
Assessment gaps of fishes
45
the effects of human activities, thereby reducing their extinction risk according to ecological
theory (Olden et al. 2007) and becoming less prone to assessments. However, assessment
exercises are often driven by funding availability and are often first applied to better-known
regions or specific taxa (Bland et al. 2017; Tapley et al. 2018). This will leave some areas or
species unevaluated and introduce potential geographical and taxonomic biases. Olden et
al. (2007) reported that as larger marine species face higher rates of extinction, they might
be likely better evaluated than smaller ones. Knowledge about these biases in assessed
species traits may steer conservation and funding decisions, and therefore help focus efforts
towards the taxa and regions that are in the greatest need of investigation and
determination of their conservation status (Meiri & Chapple 2016).
Here we assess whether distributional, ecological, life history, or taxonomic biases
exist in IUCN assessments of marine and freshwater fishes. We hypothesise that higher
assessment rates will be found for (1) species inhabiting developed regions with high levels
of research activity (i.e. Europe, North America, Mediterranean region); (2) larger species
in the marine environment because of higher perceived extinction risk (Olden et al. 2007);
and (3) species that are easier to study (e.g., large, long-lived), have commercial importance,
are considered more vulnerable to threats, and have been long known (i.e. described
earlier). The results should serve as a guide to research efforts, conservation planning, and
funding to improve the knowledge of species and areas that are in the highest need for
research and assessment of their conservation status.
Methods
In this study, the 2016 version of FishBase was analysed (Froese & Pauly 2016). This
database, a reference tool for fish study, includes information about the extinction risk of
the species on the IUCN Red List. The status of the species was updated, where possible,
according to the IUCN Red List classification (IUCN 2017). Old Red List categories were
translated into current categories following the latest IUCN standards (IUCN 2012):
therefore, LR/nt was renamed as Near Threatened, NT; LR/lc as Least Concern, LC; and
LR/cd was merged into NT. Analyses were performed on the five classes of fishes
(Actinopterygii, Chondrichthyes, Myxini, Petromyzontida, and Sarcopterygii) as recognised
by FishBase.
Data on fish traits and other species information were collected from FishBase and
grouped into the following five categories: 1) distributional traits, 2) life-history traits, 3)
vulnerability index, 4) taxonomic traits, and 5) commercial importance. In terms of
distributional traits, the presence of species in each FAO Major Fishing Area (henceforth
FAO area) was collected. Preferred habitat for each species was recorded as assigned in
Chapter 2
46
FishBase (bathydemersal, bathypelagic, benthopelagic, demersal, pelagic, pelagic-oceanic,
pelagic-neritic, and reef-associated). For life-history traits, there were considered:
maximum length (in mm) of the longest individual recorded for the species; maximum
weight (in g) recorded for the species; longevity (oldest age recorded for the species); and
generation time (time from birth to the average age of reproduction for the species). The
vulnerability index (Cheung et al. 2005), originally developed for marine fishes but now
applied to all species in FishBase, is used to establish the vulnerability of a species to fishing
pressure. Three relevant taxonomic traits were considered: The phylogenetic index (Faith
et al. 2004), that uses phylogenetic patterns of evolutionary diversification to predict
feature diversity of sets of species, is calculated as a sum of phylogenetic differences present
in an assemblage (Tucker et al. 2016) and takes values ranging from 0.5 (low uniqueness of
the species) to 2.0 (high uniqueness) (Froese & Pauly 2016) to check whether the
phylogenetic uniqueness of a species could be a trait driving IUCN Red Lists assessments.
Secondly, fish order according to FishBase to see if there were certain orders which could
be potentially over or under-represented in Red List assessments. Finally, in the case of the
year of description (based on species authorship), it was assumed that more-recently
described species were less susceptible to being assessed than previously described
species. FishBase commercial importance reflects whether the species is regularly targeted
by fisheries or regularly found in aquaculture activities.
FishBase did not contain data on all of the above traits for all species (Table 2.1).
Rather than inferring data from similar species, species without direct data for a specific
trait were classed as non-available (NA) for this trait. Our data were analysed across three
groups of species: 1) all species present in FishBase (including species both assessed and
non-assessed by IUCN, hereafter referred to as the full dataset), 2) species assessed by the
IUCN and included in the IUCN Red List, and 3) species assessed by the IUCN excluding those
classified as Data Deficient (DD). Analyses were performed separately for freshwater and
marine fish.
Assessment gaps of fishes
47
Table 2.1: Number of fish species evaluated for each trait in each group. Only FAO (Food and
Agriculture Organisation) Area, order, and year of description were available for all species.
Population refers to the full dataset of all species present in FishBase. Assessed refers to those species
assessed by IUCN Red List. Assessed non-DD refers to those species assessed by IUCN Red List
excluding those classified as Data Deficient.
We firstly did multiple logistic regression models (generalized linear model (GLM)
with binomial errors) where the status of IUCN Red List assessment (“no” or “yes”) was the
response variable. Sample sizes for different variables were very unequal (Table 2.1). Only
those variables for which data were available for >85% of species were used as predictors:
Habitat, length, Vulnerability Index, Phylogenetic Index, description year, and order. In
these analyses, there were not considered body mass, tightly correlated to length (Froese et
al. 2011), longevity, and generation time (due to the insufficient percentage of species
having data for these traits).
Then differences in the assessment were tested (assessed vs. non-assessed) between
the three groups through chi-square tests for analyses of frequencies (e.g. the number of
assessed species in the FAO areas, commercial or non-commercial species and orders) and
Wilcoxon rank-sum test with continuity correction (due to non-normal distributions of the
variables) for the numeric data (e.g. length, weight, description year), with log
transformations for length and weight. All statistical analyses were performed with R
Trait
Population
Assessed
Assessed non-DD
Distribution
FAO Area
32568
15029
11931
Life History
Length
27967
13579
11092
Weight
1737
1104
990
Longevity
1264
865
825
Generation time
25490
12413
10095
Conservation
Vulnerability Index
32541
14990
11892
Taxonomy
Phylogenetic Index
32338
14977
11881
Order
32568
15029
11931
Year of description
32568
15029
11931
Commercial
Commercial
importance
7362
4376
3735
Chapter 2
48
software version 3.3.3 (R Development Core Team 2019). Each trait was analysed twice to
identify biases: full dataset vs. assessed species (comparison 1) and assessed vs. assessed
non-DD species (comparison 2).
As assessment levels vary across vertebrate groups, with fish potentially being among
the least assessed (Hermoso et al. 2017), it was tested whether there was a decline in
assessment level over time. The year of species description for fish was contrasted with that
from other vertebrate groups (Amphibians, Reptiles, Birds and Mammals) obtained from
Catalogue of Life (http://www.catalogueoflife.org/), distinguishing between non-assessed,
assessed-DD and non-DD by year to analyse how IUCN evaluations changed with time.
Results
The IUCN Red List 2017.1 has assessed 15,029 fish species (7,984 freshwater and
7,457 marine), which is 46% of the species listed in FishBase. Different FAO areas had
varying proportions of species assessed, both when comparing all evaluated species and
when excluding species assessed as DD (Table 2.2). South America (19% of species
assessed) and Antarctic Ocean (12%-24 % depending on the FAO Area) had the lowest level
of assessment, followed by the Arctic and the Pacific Ocean, (Figure. 2.1, Supplementary
Data 2.1). The Atlantic Ocean (including the Mediterranean and the Black Sea) was the best-
assessed area in the marine realm, while Africa and Europe had the highest levels of
assessment among inland areas; however, Africa had a higher proportion of DD-species
than Europe. Both the Indian and Pacific Oceans remained relatively poorly assessed (24%-
40% and 12%-62% respectively). The proportion of species assessed differed significantly
among habitats, in both comparisons (Table 2.2). Bathydemersal and bathypelagic habitats
were least assessed, while reef associated-habitats were the best-evaluated habitats and
with a relatively low proportion of DD-species. In contrast, in bathydemersal habitats, the
proportion of species assessed was reduced from 32% to 18% assessment if DD-species
were excluded (Supplementary Data 2.2).
Assessment gaps of fishes
49
Table 2.2: Chi-square results for the comparisons between global and assessed species included on
the IUCN Red List (Total vs RL) and excluding Data Deficient species (RL vs RL non-DD) for each FAO
area, preferred habitat, the number of species assessed in each taxonomic order in all the
environments, and commercial categories. Original data can be found in Supplementary Data 2.1, 2.2
and 2.4.
Total vs RL
RL vs RL non-DD
χ2
df
p
χ2
df
p
FAO areas
16894.4
25
< 0.001
801.0
25
< 0.001
Habitats
9521.4
7
< 0.001
706.7
7
< 0.001
Orders
10319.0
61
< 0.001
782.4
61
< 0.001
Orders (Freshwater
species)
4476.4
61
< 0.001
393.8
61
< 0.001
Orders (Marine species)
6011.6
61
< 0.001
407.3
61
< 0.001
Commercial importance
1214.8
5
< 0.001
100.2
5
< 0.001
Commercial importance differed in both comparisons (Table 2.2): commercial
species were not the best-assessed ones, despite having the biggest number of assessed
species. Even excluding DD species, species of minor commercial interest were better
assessed than other species (56% vs 52%) (Supplementary Data 2.3).
Regarding biological traits, assessed species tended to be larger than the average of
the full dataset (Table 2.3). Heavier species were better assessed in marine habitats when
analysing total and assessed species, but not in the assessed vs non-DD comparison; weight
was a non-significant factor for freshwater fish. Assessed species had shorter lifespans
when compared to the full species set (marine and freshwater combined), but this
difference was not observed when analysing freshwater and marine species separately.
Assessed species had longer generation times (Table 2.3), but this could not be seen in the
comparison between assessed and non-DD species in the freshwater environments.
Chapter 2
50
Figure 2.1: Total number of fish species included on FishBase 2013 (outer black circles), and relative number of assessed species (dark grey circles) and assessed
and non-Data Deficient species (light grey circles) in the IUCN Red List, by FAO Major Fishing Area. Grey sectors: Proportion of species described in the Fishing
Area after 1994. Full data in Supplementary Data 2.1. Figure by R. Miranda.
Table 2.3: Values and biases of life-history traits in the three groups: Total, assessed species included on Red List (RL), and assessed excluding data deficient species
(RL non-DD) were compared. All values are reported as the median and interquartile range in brackets. Wilcoxon rank-sum test with continuity correction statistic
(W) and associated probability (p assoc.) are shown.
Trait
Length
(log cm)
Weight
(log g)
Longevity
Generation Time
Vulnerability Index
Phylogenetic Index
Year of description
Overall
Total median
1.1 (0.8-1.5)
3.6 (3.0-4.1)
10.0 (5.0-18.0)
1.8 (1.1-3.1)
21 (10-34)
0.5 (0.5-0.5)
1928
RL median
1.2 (0.9-1.5)
3.7 (3.1-4.3)
8.0 (4.0-15.0)
1.8 (1.2-3.1)
23 (12-36)
0.5 (0.5-0.5)
1917
RL not DD median
1.2 (0.9-1.5)
3.6 (3.1-4.3)
8.0 (4.0-15.0)
1.8 (1.2-3.1)
23 (12-35)
0.5 (0.5-0.5)
1911
Total vs RL
177330000
887440
591610
154800000
228120000
245890000
268090000
p assoc.
< 0.001
0.001
0.001
0.001
< 0.001
0.001
< 0.001
RL vs RL not DD
74322000
554770
360770
62998000
88381000
88220000
94615000
p assoc.
0.076
0.548
0.693
0.479
0.233
0.138
< 0.001
Freshwater
Total median
1.0 (0.8-1.3)
3.5 (2.8-4.0)
7.0 (4.0-12.0)
1.5 (0.9-2.6)
15 (10-27)
0.5 (0.5-0.5)
1935
RL median
1.0 (0.8-1.3)
3.5 (3.0-4.1)
6.0 (4.0-11.0)
1.6 (1.1-2.7)
17 (10-30)
0.5 (0.5-0.5)
1927
RL not DD median
1.1 (0.8-1.4)
3.5 (2.9-4.1)
6.0 (4.0-11.0)
1.6 (1.1-2.7)
18 (11-31)
0.5 (0.5-0.5)
1921
Total vs RL
48165000
175230
169280
37545000
57670000
64586000
70037000
p assoc.
< 0.001
0.272
0.371
< 0.001
< 0.001
0.004
< 0.001
RL vs RL not DD
20605000
108340
134060
17632000
24065000
24640000
26409000
p assoc.
< 0.001
0.788
0.927
0.182
< 0.001
0.222
< 0.001
Marine
Total median
1.3 (1.0-1.6)
3.7 (3.2-4.2)
12.0 (7.0-25.0)
2.2 (1.3-3.5)
26 (14-39)
0.5 (0.5-0.5)
1918
RL median
1.4 (1.0-1.7)
3.8 (3.2-4.4)
12.0 (7.0-22.5)
2.2 (1.3-3.7)
27 (15-42)
0.5 (0.5-0.5)
1904
RL not DD median
1.4 (1.0-1.7)
3.8 (3.2-4.4)
12.0 (7.0-22.0)
2.1 (1.3-3.5)
27 (15-41)
0.5 (0.5-0.5)
1897
Total vs RL
43493000
380090
174280
42631000
59736000
63703000
71410000
p assoc.
< 0.001
0.002
0.197
0.042
< 0.001
0.286
< 0.001
RL vs RL not DD
18896000
238810
88981
15984000
22672000
22037000
23622000
p assoc.
0.094
0.714
0.848
0.017
0.049
0.402
< 0.001
Chapter 2
52
Assessed species had higher vulnerability indices in both freshwater and marine
environments (Table 2.3), with no difference in vulnerability indices when comparing
assessed and non-DD species. In terms of taxonomic traits, phylogenetic index values of all
fish ranged from 0.5 (low) to 2 (high), although most species had low values (0.5). The only
significant difference in this comparison was that assessed species had higher phylogenetic
indices compared to the full dataset, in both the full comparison and for freshwater fish only.
The level of assessment varied significantly across different orders, in both
freshwater and marine habitats, as well as in the global analysis (Table 2.2 and
Supplementary Data 2.4). Among the richest orders, Squaliformes and Rajiformes appeared
to have most species assessed (90% and 92% species assessed respectively), whilst other
orders such as the marine orders Scorpaeniformes (15% assessed) and Gadiformes (21%),
were relatively poorly represented in the IUCN Red List. Among freshwater fish,
Gymnotiformes (11% assessed non-DD), Characiformes (21%) and Siluriformes (26%) had
the lowest assessment levels.
Assessed species had generally been described earlier, both for freshwater and
marine species (Table 2.3). Fish were (together with reptiles) the least assessed vertebrate
taxa, with hundreds of species described in recent years but often not yet included in the
Red List. When examining the proportion of non-DD vertebrate species according to their
description date, it was observed that while all vertebrate groups had a lower proportion of
recently-described species assessed, fish described in the last thirty years have generally
not been assessed yet on the IUCN Red List. The ratio of species assessed to species
described (excluding those years with less than 10 species described) showed that lower
percentages of assessment were associated with higher numbers of discovered species in
reptiles, amphibians, and especially in fish (Figure 2.2). Many fish species discovered since
1996 (2,782 freshwater species) occurred in South America and Asia, two areas with
relatively poor assessment levels (Figure 2.1).
The best model for species assessments among those models for which data on >85%
of species were available included the positive effects of length and Vulnerability Index. On
the other hand, Phylogenetic Index and description year had a negative influence on species
assessment probability, confirming the results obtained in the individual analyses (Tables
2 and 3). Considering fish orders, certain orders were positively associated with the
probability of assessing a species (Carcharhiniformes, Chimaeriformes, Squaliformes,
Rajiformes, and Syngnathiformes) whereas others had a negative association
(Characiformes, Gadiformes, Gymotiformes). The full result of this model is presented in
Supplementary Data 2.5
Assessment gaps of fishes
53
Figure 2.2: Number of species described per year assessed by IUCN as non-DD (blue) and DD
(orange), and Not Evaluated (grey), in main vertebrate groups. From Miqueleiz et al. (2020).
Chapter 2
54
Discussion
Our study highlights certain areas and habitats on Earth where additional assessment
efforts for fish are needed to ensure that levels of threat to fish species are adequately
represented within the IUCN Red List and that fish feature in subsequent conservation and
policy instruments. Longer (but not heavier) species tend to be better assessed, as are short-
lived species - but not those with shorter generations, i.e. those that reproduce earlier.
Assessed species have a higher vulnerability index (VI, the vulnerability of a species to
fishing pressure) than non-assessed ones. Certain fish orders are better assessed, such as
sharks and rays (Dulvy et al. 2014), while others lack sufficient assessment
(Scorpaeniformes, Gymnotiformes). Species assessed had been described earlier than
unassessed ones, resulting in an assessment gap for fish species described during the most
recent decades, comparable to a similar gap observed in reptiles (Meiri & Chapple 2016)
and amphibians (Tapley et al. 2018). Finally, no evidence was found to support the
hypothesis that assessment rates are higher in species with higher commercial interest or
value.
As predicted, fish from developed regions (e.g., Mediterranean, Europe, and the
Atlantic Ocean) had higher rates of assessment. The higher levels of freshwater fish
assessment in Europe are due to a comprehensive European assessment programme that
exists for freshwater fish (Freyhof & Brooks 2011). However, such exhaustive assessments
are not confined to developed regions only: the higher levels of freshwater fish assessment
in Africa compared to other developing regions are the result of an exhaustive assessment
by IUCN in 2011 (Darwall, Smith, et al., 2011). South America and Asia, on the contrary,
require further attention in freshwater fish assessment efforts (Darwall & Freyhof, 2016),
although some Asian regional assessments have focussed on the Western Ghats, and the
Indo-Burman and Eastern Himalayan regions (Allen et al. 2010; Molur et al. 2011). These
regions might be subject to particularly high extinction risk, as they represent hotspots with
high threat status (tropical regions), small species ranges (Albert et al. 2011), and high data
deficiency, especially in South America (Alofs et al. 2014). Around 40% of freshwater fish
species occur in the Neotropical region (Albert et al. 2011); given that only 19% of the more
than 5,000 South American freshwater fish species are assessed on the IUCN Red List, the
definition of key biodiversity areas for freshwaters in South America are likely inadequate
for fish, due to a lack of fish representation. (Collen et al. 2014) showed that there was little
congruence in the patterns of species richness, endemic species richness and threatened
species richness between different groups of freshwater species, so that one freshwater
taxon group is unlikely to be an adequate surrogate for another in analyses of priority areas
Assessment gaps of fishes
55
for conservation. Initiatives like the Alliance for Freshwater Life aim to place freshwater
species and their associated ecosystems on the global agenda as legitimate targets for
conservation action (Darwall et al., 2018).
In the marine realm, it was surprising to see that the Atlantic Ocean was far better
assessed than areas of the Indian and Pacific Oceans that belong to economically developed
regions, such as the Eastern Pacific (Figure 2.1). In this case, we consider that our hypothesis
is not truly valid for oceans, as more factors may be affecting fish assessment rates.
Similarly, species assessment was not equally distributed among habitats. Coral reefs, which
are known to provide several ecosystem services to humans (Moberg & Folke 1999) were
better assessed than other habitats (Table 2.3). Their ease for survey and charismatic image
(Duarte et al. 2008) is combined in this case with a high risk, as reef-associated fish face
habitat-degrading threats originating from land, such as coastal residential and commercial
development (McClenachan et al. 2016) and coral bleaching induced by climate change
(Alvarez-Filip et al. 2009). Assessments of deep water benthic species are lagging behind
that for neritic species, likely due to better information availability for neritic species, and
possibly due to lower perceived threats affecting these species (Halpern et al. 2007).
However, deep-sea habitats are often found in international waters with fewer restrictions
and regulations; areas around hydrothermal vents, for example, are likely targets for deep-
sea mining (Van Dover 2011) and the impacts of such activities are at present vastly
overlooked in conservation planning and policy. Non-assessed marine fish species were
consistently smaller than those assessed by the IUCN, but there was no size bias in
freshwater fish assessments (Table 2.3). Threats affect freshwater species in a complex
manner, not always related to body size (Dudgeon et al. 2006). An assessment bias towards
species of commercial interest was expected, as the most significant threat for marine fishes
is associated with direct mortality from human fishing activities targeting large-bodied
species (Olden et al. 2007), often with slow population growth (Reynolds et al. 2005), and
those species may be prioritised for conservation assessment. No evidence of commercial
fish being better assessed than other species was found (Table 2.2). Species of commercial
interest were expected to be better assessed as a result of the fishing pressure they are
subjects of.
Assessed species generally had higher vulnerability indices (Table 2.3). Previous
studies have compared this index and IUCN Red list categories (Strona 2014; Miranda
2017), and Red List categories were found to be more suitable for conservation purposes
than the VI (Miranda 2017). Both measures are equally valid because they are considering
different threat processes (VI measures the intrinsic extinction vulnerability due to being
Chapter 2
56
fished, based on biological traits of fish species whilst the IUCN Red List evaluates the
extinction risk of species considering a wide range of threat processes that are affecting
species, and including data on symptoms of extinction risk, such as populations declines,
distribution size, population size, etc.). With aquatic systems being affected by several
different threats (Reis et al., 2017), including emerging threats such as climate change and
plastic pollution, the understanding of species vulnerability needs to be expanded to the
wide spectrum of threat processes, e.g. through assessment processes such as climate
change vulnerability assessments (Chin et al. 2010). Vulnerability assessments allow to
highlight those species potentially vulnerable to a specific threat and act on safeguarding
these before the threat may take full effect, i.e. lead to population declines and hence higher
extinction risk. On the contrary, IUCN Red List gives an estimate of the extinction risk at
present, given the threats already affecting or about to affect a species. Furthermore,
previous results of species of commercial interest (more vulnerable to fishing pressure) do
not show similar patterns. Therefore, this incongruity in the results will be subject to study
in further research about the relationship between VI and commercial interest in chapter 3.
As predicted, the assessment of threat status in fish is taxonomically biased (Table
2.2). The presence of several Fish Specialist Groups (https://www.iucn.org/ssc-
groups/fishes) may skew IUCN efforts towards certain groups or species. The IUCN Shark
Specialist Group (http://www.iucnssg.org) published significant work in 2014 (Dulvy et al.
2014) assessing the conservation status of all sharks, rays, and chimaeras, resulting in
higher assessment levels than in other orders. Such levels respond to an increasing concern
over the past decades on shark conservation, with the change in perception, from one of
needing to protect humans from sharks to that of needing to protect sharks from humans
(Simpfendorfer et al. 2011). However, a closer look at these groups showed that there was
a large proportion of DD species (51% in sharks, 44% in rays, and 40% in chimaeras),
slightly improved in the 2017 Red List. Thus, despite it being better to have a DD assessment
than not being assessed, further investigation is required in these and other highly DD
orders to obtain data that will allow scientists to classify their extinction risk (Bland et al.
2012).
Regarding marine orders, Scorpaeniformes (10% assessed non- DD) and Gadiformes
(15%) had the lowest levels of assessment (Supplementary Data 2.4), despite including
many species of commercial importance in certain areas of the world (Winfield 2016). In
the case of Scorpaeniformes, their low growth rate and long generation time make them
especially sensitive to overexploitation, which has resulted in the disappearance of many
stocks in the Atlantic (Ricard et al. 2012). Unfortunately, these results are consistent with
Assessment gaps of fishes
57
data obtained for commercial fishes, suggesting that human consumers may be largely
unaware of the conservation status of the consumed marine fish. Many of these
commercially fished species may also be of importance to subsistence fishermen,
endangering important food stocks and protein availability in areas around the world.
Freshwater tropical species are possibly within the least assessed groups compared
to other Red List assessed fish, requiring in-depth research to evaluate their conservation
status. Characiformes, freshwater-restricted species distributed in tropical Africa and South
America, had a low assessment rate (21% if DD species are excluded). Considering that over
300 of the 2022 characiform species have been described as recently as the 2000-2010
decade (Oliveira et al. 2011), a combination of high description rates and few evaluations
has led to a significant assessment gap in this order. Gymnotiformes (11% non-DD) and
Siluriformes (26%) from South America, Africa, and South-Eastern Asia (only Siluriformes)
(Cordiviola et al. 2009) inhabit extensive and difficult to sample habitats such as deep river
channels and flood-plain floating meadows (Albert 2001), which severely hamper
initiatives for their conservation.
In this study, we have demonstrated that most of the non-evaluated species were only
recently described (Figure 2.2). Since the mid-1990s, IUCN’s capacity to provide assessment
for newly-described species seems to be decreasing as observed in the time-dependent
rates of assessment. As new species are being described in those areas which already have
low assessment rates, such as South America, Asia, or tropical oceans (Figure 2.1; Nelson et
al., 2016) the gap between described and assessed species widens. South America is the sole
FAO Major Fishing Area where more species were described between 1994 and 2013 than
were included in the Red List for that area (Figure 2.1). Current rates of species discovery
and publication suggest there are likely more than 8,000 Neotropical freshwater fishes
(Reis, 2013), urging the need for an exhaustive effort to sample and study South American
inland waters. This is of particular importance given the threats of naturalised species (e.g.
non-native fish; Pelicice, Vitule, Junior, Orsi, & Agostinho, 2014), and damming (Reis et al.,
2017), amongst others, which are likely to impact a large number of freshwater species in
South America. In addition, these threats have the scope to impact the freshwater
community structure, leading to a homogenisation of the fauna, loss of genetic diversity, etc.
and thus impacting wild fish stocks which may play a major part in protein provisioning
along inland waters.
Furthermore, comparing data from fish with other vertebrate groups, fish species
have been suffering from an evaluation decline since the 1980s which, combined with an
increase in species discovery, resulting in a large proportion of recently discovered species
Chapter 2
58
not being evaluated, a trend shared with reptiles (Meiri 2016) and amphibians (Tapley et
al. 2018). In the case of amphibians, for which previously complete global assessments had
been carried out, assessments are now rapidly becoming out-dated with an increasing
proportion of non-evaluated species (Tapley et al. 2018). Previous studies with lizards and
snakes (Meiri & Chapple 2016; Böhm et al. 2017) have found that those species easier to
study (large range sizes, temperate latitudes) are described earlier and are better assessed,
whilst species with small ranges and inhabiting tropical regions remain unassessed or even
undiscovered, with a higher risk of extinction as a result of their rarity (Pimm et al. 2014).
The tropical biodiversity data gap may influence certain indicators established by the
Convention on Biological Diversity more than others (Collen et al. 2008) and, despite recent
efforts led by IUCN (Tognelli et al. 2016), further research and investment in this area is
needed to ensure the effective protection of species dwelling there. Implications of lower
assessment rates for recently described species will be discussed further in chapter 4 of this
thesis.
Recommendations
Since conservation efforts to date have resulted in only 46% of fish species being
formally assessed by the IUCN Red List at the time of the study, completing the assessment
for the remaining ones seems a colossal task, complicated by the rate of new species
discovery. With a cost of US$38 million, having 160,000 species evaluated by 2020 seemed
hardly feasible in the context of funding shortfalls (Juffe-Bignoli et al. 2016). Thus, we
suggest focusing efforts in the following key areas:
1) Develop working groups for under-assessed areas: We strongly recommend the
creation of a working group on Central and South American fish species. Several regional
initiatives have been developed by IUCN in Europe (Abdul Malak et al. 2011; Freyhof &
Brooks 2011; Nieto et al. 2015), Africa (Darwall, Smith, et al., 2011), and Asia (Allen et al.
2010, 2012; Molur et al. 2011). However, only a partial report of North and Central America
Chondrichthyans (Kyne et al. 2012) and an assessment in the Andean region (Tognelli et al.
2016) have been carried out on the continent so far. To fulfil this aim, collaboration with
local organisations and investment in local institutions is essential to develop the
infrastructure and expertise for long-term monitoring (Collen et al. 2008) and study not
only individual species but also species assemblages and interactions. The Global
Freshwater Fish Assessment has been developed by IUCN Freshwater Unit to evaluate all
discovered fish species by 2021, and has already improved assessments in many of the areas
in need of assessment detected in this chapter. Further considerations on the Global
Freshwater Fish Assessment project will be discussed in the next chapters of this work.
Assessment gaps of fishes
59
2) Increase knowledge of fish distribution, ecology, and life history to combat Data
Deficiency: Only 37% of fish species have been assigned an IUCN category, excluding DD
species, which are often known from type specimens or type localities only. More resources
should be directed to research those Data Deficient species (Hoffmann et al. 2008), where
field surveys are likely to bring about an immediate increase in knowledge and hence
expedite a non-DD assessment, i.e. species where a lack of population data or knowledge
about threats are affecting a DD status. The application of environmental DNA (eDNA)
sampling can provide greater probabilities of detection of aquatic species when compared
with the use of traditional sampling procedures (Antognazza et al. 2019). Machine-learning
techniques may also help to classify the most likely extinction risk category for those DD
species that are more difficult to survey (Bland, Collen, Orme, & Bielby 2015). Furthermore,
we cannot underestimate the risk of outdated assessments, that combined with unassessed
areas should drive conservation priorities (Hermoso et al. 2017).
3) Explore the role played by Protected Areas (PAs) and Key Biodiversity Areas
(KBAs) in fish conservation (especially freshwater fish), congruently with Aichi target 11
(SCBD 2010). The establishment of PAs to benefit fish populations relies on improved
knowledge on fish distribution (Hermoso et al. 2016) and knowledge on species extinction
risk, distribution and endemism is vital to inform at least some of the criteria for definition
of a KBA (KBA Standards and Appeals Committee 2019). Up until now, in many regions of
the world fish species have played a limited role in the designation of protected areas or
KBAs. Thus, further studies on both the ability of the current network of PAs to adequately
protect freshwater fish (Abraham & Kelkar 2012) and on gaps within the PA/KBAs network
are urgently needed (Pino-del-Carpio et al. 2011, 2014). This task is even more urgent in
under-assessed areas like the Andean region of South America, where 88% of the species
are not adequately represented in any protected area (Tognelli et al. 2019). This question
will be addressed in chapter 5 of this thesis.
4) Enhance the role played by national Red Lists: IUCN Red List and Criteria are
being increasingly used for regional and national red lists (Rodríguez 2008; Zamin et al.
2010). Several measures are proposed to better link national, regional, and global Red Lists
such as taxonomic uniformity and enhance data transfer between national and the global
Red Lists (Brito et al. 2010). The ability to now also submit IUCN Red List Assessments in
French, Spanish, and Portuguese is likely to improve coverage of assessments for regions
such as South America. In addition, financial investment for national Red List development
should favour those countries with the richest biodiversity but lower GDP (Zamin et al.
2010). Better linkage of global and national Red List processes also increases the pool of
Chapter 2
60
experts available for global IUCN Red List assessments, through increased networking,
collaboration, and capacity building. The possibility of doing national assessments of
endemic species following global Red List standards also increases the value of such
assessments and we should not underestimate their possible contribution to the IUCN Red
List.
5) Finally, this study goes beyond a simple listing of IUCN Red List gaps. In a context
of global threat to fish species, jeopardized by human and climate pressures combined, we
consider that the voice of conservation initiatives like the IUCN Red List should be
extensively heard by other authorities. CBD’s Aichi target #12 referred to in the
introduction is a call to “improve and sustain species conservation status”. The results of
the study fully support this target by pointing out where assessment efforts should be
focused on. FAO could benefit from improved Red List evaluations, too. There is also room
for improved use of IUCN outputs in FAO assessments (especially those subject to intensive
fishing). For example, the 2016 SOFIA (State of World Fisheries and Aquaculture) report by
FAO did not refer to the IUCN Red List (FAO 2016) whilst this collaboration is emerging in
the 2018 report (FAO 2018). With insufficient funds to both expand taxonomic coverage
through new assessments, and keep existing assessments up to date (Rondinini et al. 2014)
a compromise solution should be achieved. This study supports others like Hermoso et al.,
(2017) to help guide assessment efforts and, afterwards, implement conservation actions
for such species. We do not want to devaluate conservation actions, but we consider that
proper assessments provide not only a status, but also valuable information required to
achieve successful conservation programs.
Chapter Transparency
This chapter is based in the following article “Miqueleiz, I., Bohm, M. M., Ariño, A. H. ,
Miranda, R. (2020). Assessment gaps and biases in knowledge of conservation status of
fishes. Aquat. Conserv. Mar. Freshw. Ecosyst. 30, 225–236”, with DOI 10.1002/aqc.3282. I.
Miqueleiz and R. Miranda conceived the present idea. I. Miqueleiz developed the
experiment, carried out the analyses and interpretated the results. R. Miranda contributed
with Figure 1 to the results. I. Miqueleiz wrote the manuscript. M. Böhm, A.H. Ariño and R.
Miranda provided comments to the analysis and the manuscript.
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CHAPTER 3:
Conservation status gaps for top fished marine commercial species
Capítulo 3:
Sesgos en el estado de conservación de las especies comerciales de mayor
importancia pesquera
Miqueleiz, I., Miranda, R., Ariño, A. H., Ojea, E.
Conservation gaps top fished species
71
Chapter preface
Biodiversity loss is a global problem accelerated by human-induced pressures on the
environment. In the marine realm, one of the major threats to species conservation,
together with climate change, is overfishing. The future of many dependent human
communities relies on the sustainability of fisheries. Harvesting marine species above safe
biological boundaries limits species resilience and can contribute to extinction risk, but
often regulatory policies do not effectively control overfishing or even allow it to some
extent. In this context, having information on the conservation status of target commercial
marine fish species becomes crucial for assuring safe standards. However, we showed in the
previous chapter that commercial fish species did not seem to stand out in terms in
assessment among all fishes, despite the obvious interest that assessing commercial stocks
has both from the economic and conservation viewpoints. A handful of commercial species
carry the brunt of commercial fisheries—did they fare better or worse than the rest?
In this study, we combined fisheries statistics from the FAO, the IUCN Red List,
FishBase and Sea Around Us to understand to what extent the top commercial species have
been assessed in terms of their Red List conservation status. We focused the study on a
subset of top commercial fish species which constitute almost half of global fish landings.
We compared IUCN Red List assessments with FishBase Vulnerability Index and FAO and
Sea Around Us landings to find differences among IUCN Red List categories.
Levels of assessment for top fished species were higher than those for general
commercial or highly commercial species. Nevertheless, almost half of the species had
outdated assessments. We found no relation between IUCN Red List traits and FishBase
Vulnerability Index. Reconstructed catches as reported by Sea Around Us were 21.5%
higher than those reported by FAO. Species with declining population trends according to
the IUCN Red List have had their catches increased in recent years, even after evaluation in
the IUCN Red List, and many other species have unknown population trends. Conservation
status cannot be directly inferred from landing trends, and IUCN Red List methodology
cannot easily be applied to fisheries management. Nevertheless, we suggest a closer
cooperation between countries, FAO, and IUCN Red List to guarantee that reliable data are
available to ensure commercial fishes assessment.
Conservation gaps top fished species
73
Introduction
For millennia, mankind has had an especially close bond with the sea as it provides
people with food (Schröder 2013), as well as other ecosystem services (Worm et al. 2006)
that contribute to health, well-being, cultural identity, and to the economy of societies
(Hughes 2014). Billions of the world’s poorest people rely on healthy oceans to provide
“livelihoods, jobs and food and the range of goods and services that flow from coastal and
marine ecosystems” (WWF 2018), and the oceans contribute significantly to the support of
many of the Sustainable Development Goals (SDGs) (FAO 2018; Singh et al. 2018).
Marine fisheries are the main contributors of seafood (referred as finfish and marine
invertebrates) for human consumption (Pauly & Zeller 2016), with almost 6 billion tons of
fish and invertebrates taken from the oceans since the 50s (Pauly et al. 2020) contributing
to 17% of global human protein intake (FAO 2017) and sustaining millions of jobs (FAO
2014). Nevertheless, their importance is closely linked to their long-term sustainability. The
Convention on Biological Diversity (CBD), through the Aichi targets, aims to achieve both
sustainable management of existent fish stocks (target 6) and prevention of the extinction
and improvement of the conservation status of threatened species (target 12) by 2020
(SCBD 2010). In the same line, SDG14 on “Life below water” has the same goal of effectively
regulating overfishing and rebuilding stocks to levels that produce maximum sustainable
yield by 2020 (sub-target 14-4).
Historically, humanity has failed in preventing fish population collapses and has not
taken conservation biology of marine fishes seriously enough (Hutchings & Reynolds 2004),
resulting in declines in species diversity and abundance (Butchart et al. 2010). However,
the number of sustainably harvested stocks is, in fact, increasing. This apparent paradox has
been explained by some studies as those stocks being offset overall by several heavily
exploited fisheries that are unmanaged (Froese et al. 2012, 2013). Food and Agriculture
Organisation (FAO) reports a global fishing decline since the ’90s (Pontecorvo & Schrank
2012), which seems to have stabilized in recent years (2011-2015 period) at around 80
million tonnes annually (FAO 2016, 2017). However, this stability can be affected by an
underestimation of the amount of fish extracted from the sea (Pauly & Zeller 2016, 2017)
as it may be misled by the omission of small-scale (Pauly 2006) and recreational fisheries
(Pauly & Zeller 2016), as well as manipulated or highly questionable statistics that locally
increase catches (Pauly & Zeller 2017).
Beyond this evidence lies a low concern about marine fish species conservation in the
fishing industry (Worm et al. 2009; Fitzgerald et al. 2020) and/or an institutional failure
during the past century (Acheson 2006). Globally, a few fish species dominate catches owing
Chapter 3
74
to several factors such as natural abundances, consumer preference, geography, history and
ease to catch (Sadovy de Mitcheson et al. 2013). Overfishing not only affects these target
species, but it also has a cascade of effects on other species and population assemblages
(Duffy 2003; Springer et al. 2003). For example, the selective extraction of species and
individuals of higher commercial value leads to the disappearance of higher trophic levels
of the marine food webs, implying an increased fishery reliance on organisms at the low
levels of the food webs (Pauly et al. 2002; Szuwalski et al. 2016). Overfishing is also
identified as one of the main threats to marine biodiversity (Jackson et al. 2001; Morato et
al. 2006). Population declines as deep as 90% have been reported for pelagic fish species
(Myers & Worm 2003), which can cause a range of ecological impacts, restructuring
communities with top-down effects (Hutchings 2000; Myers et al. 2007).
The IUCN (International Union for Conservation of Nature) is the institution
responsible for assessing the global conservation status of plants and animals through their
periodically reviewed Red List of Threatened Species (Rodrigues et al. 2006). Overfishing is
considered by the IUCN Red List as a threat to many marine fish species under the “fishing
& harvesting aquatic resources” category, acknowledging that it can lead to population
declines, which is one of the criteria to classify species under the IUCN Red List Categories
(IUCN 2012). Despite this, the status of only a small fraction of described marine animal
species has been evaluated by the IUCN (McCauley et al. 2015). FishBase (Froese & Pauly
2019), the most comprehensive database compiling fish species information, has more than
40% of “commercial” and “highly commercial” species unassessed in the IUCN Red List (see
Chapter 2).
Considering the existing level of overfishing in marine commercial species, together
with the direct extinction risk, and the indirect impacts on communities, we considered
monitoring of the IUCN Red List conservation status of top fished marine commercial
species a priority. The objective of the present study was, therefore, to explore how most
important marine commercial species are categorized within the IUCN Red List and to
understand the degree of knowledge we have on marine commercial species conservation
status.
Methods
We explored fisheries statistics extracted from databases compiled by FAO, IUCN Red
List, FishBase, and Sea Around Us. The datasets had information about fishing trends,
species conservation status, and other traits. We first identified the most fished species
globally from FAO statistics. Then we collected information on IUCN Red List status for these
highly fished species using assessments made between 1996 and 2019. Finally, we explored
Conservation gaps top fished species
75
the trends in landings in the data from Sea Around Us. We then statistically analysed the
relationships between conservation status and landing trends.
FAO data
In the late 40s, the FAO began collecting global fishing statistics (Pauly et al. 2002). In
recent years, FAO has produced several Yearbooks of Fishery Statistics and reports about
the State of World Fisheries and Aquaculture (SOFIA). Based on this work, we used the 2017
FAO Yearbook of Fishery and Aquaculture Statistics (FAO 2019) that identified the top 70
fished species at the global level based on their landings. The subset of data analysed
represents almost half (46.5%) of the global landings in 2017 according to FAO statistics,
considering not only fish sensu stricto but also squids and crustaceans. Most of these species
corresponded to marine species, with only three freshwater-restricted fish. Henceforth, we
will refer to this subset of most important commercial species as “top fished species”.
IUCN Red List and FishBase
For these top fished species, we extracted information from the IUCN Red List (IUCN
2019). The IUCN Red List establishes the extinction risk of species assigning them to a
category according to their conservation status. From lesser to greater risk, these categories
are Least Concern (LC), Near Threatened (NT), Vulnerable (VU), Endangered (EN), Critically
Endangered (CR), Extinct in the Wild (EW), and Extinct (EX). Moreover, there is a category
for those species with insufficient information to assess their conservation status, Data
Deficient (DD). These assessments are regularly updated (IUCN Red List recommends
revaluating species every 10 years) and contain information relevant for species
conservation (population trends, biogeography, threats, or conservation actions). From the
IUCN Red List database, we obtained four variables: 1) Current conservation category; 2)
Assessment date; 3) Population trends (increasing, stable, decreasing or unknown); and 4)
Current threats, focusing on Threat 5.4 “fishing & harvesting aquatic resources” (henceforth
“fishing pressure threat”). We focused only on global scale evaluations and did not consider
regional assessments (e.g. European or Mediterranean) or separate stocks for any given
species.
From FishBase (Froese & Pauly 2019), we obtained the Vulnerability Index of top
fished species, which estimates intrinsic extinction vulnerabilities of marine fishes to fishing
(Cheung et al. 2005) based on species life-history traits, including maximum length, age at
first maturity, longevity, natural mortality rate, fecundity, the strength of spatial behaviour,
and geographic range. This index assigns each species a value between 0 (low vulnerability)
and 100 (high vulnerability). We also obtained from FishBase a list of fish classified as
Chapter 3
76
“commercial” or “highly commercial” interest. For these subsets of species, we obtained
their Vulnerability Index values and their IUCN Red List status.
Sea Around Us
FAO landing data have been suggested to be not completely accurate (Froese et al.
2012; Pauly & Zeller 2017). To avoid this problem, the Sea Around Us project reconstructs
data for major fished species, adding reported FAO data and estimations of unreported
catches. Pauly and Zeller (2016a) suggested that reconstructed data from Sea Around Us
project were overall 53% higher than the reported data. Thus, we collected reported and
unreported data for top fished species in the 1996-2014 period from Sea Around Us at the
global level.
All data used in this study can be found in Supplementary Data 3.
Analysis
We compared the proportion of assessed species from the subset of top fished species
with the assessment rates of FishBase commercial categories (commercial and highly
commercial) through chi-square tests for analyses of frequencies. We also analysed
differences in the Vulnerability Index between the three species subsets (top fished,
commercial, and highly commercial) trough Kruskal-Wallis tests.
Focusing on the subset of top fished species, we examined the proportion of top fished
species within each IUCN Red List category over the last 20 years, the fishing pressure (IUCN
Red List threat 5.4), and also the species population trends. We performed Kruskal-Wallis
tests to assess differences in Vulnerability Index (VI) for the different conservation status,
population trends and IUCN Threat 5.4 for top fished species.
We analysed fishing trends for the top 70 species, from both reported (FAO) and
reconstructed data (Sea Around US). We decided to examine fishing trends grouping them
according to the IUCN Red List categories and population trends. We also examined the
change (increasing or decreasing) in the catches between the most recent assessment date
and 2014.
Results
We compared the top fished species with the larger commercial species groups
(commercial and highly commercial species). No association was found between IUCN Red
List assessment rates and commercial categories trough the chi-square test (p>0.05) (Table
3.1). Vulnerability Index values were also not significantly different among top fished
species and those considered to have a commercial or highly commercial interest (p=0.065).
Conservation gaps top fished species
77
Nevertheless, values for top fished species tend to be lower than in the other categories
(Table 3.1).
Table 3.1: Number and proportion of IUCN Red List assessed and unassessed species for each species
sub-set, and their average vulnerability indices.
Top fished
species
Commercial
species
Highly commercial
species
IUCN Red List assessed
species
49 (70%)
1217 (59.2 %)
126 (56%)
Unassessed species
21 (30%)
839 (40.8 %)
99 (44%)
Vulnerability Index (mean
and SD)
39.8 (±19.5)
42.9 (±18.1)
49.25 (±20.9)
From the 70 top fished species, twenty-one (30%) were not assessed by the IUCN Red
List (IUCN 2019) (Table 3.2), including two of the ten most fished species (Theragra
chalcogramma and Micromesistius poutassou). Within the assessed species, we also found
cases of deficient evaluation, with six of them (five fish and one cephalopod) classified as
data deficient (DD), and two species with dated assessments (from 1996) that do not have
complete information. Most of the assessed species, 35 out of 49 (71.4%), were reported
under fishing pressure (IUCN threat 5.4). Almost all assessed species (47 out of 49) had
information on population trends, but many of them (25, 53.2%) had unknown trends.
Assessment dates ranged between 1996 and 2019, with most species having been assessed
between 2010 and 2011 (Figure 3.1).
No significant differences were found in the Vulnerability Index for different IUCN
categories (χ2=0.49, d.f.=4, p=0.92) , populations trends (χ2=1.13, d.f.=4, p=0.77) or IUCN
Red List fishing pressure threat (χ2=0.24, d.f.=1, p=0.63).
Reconstructed catches for the top fished species tended to be higher than reported
catches for all the cases in our analysis, with an increase of 21.5% in the total amount of fish
extracted for these species in the 1996-2014 interval (Figure 3.2).
Chapter 3
78
Table 3.2: Number and percentage of top fished species assessed in the IUCN Red List, and their
population trends and vulnerability indices. DD: Data Deficient, LC: Least Concern, NT: Near
Threatened, VU: Vulnerable, NE: Not Evaluated.
Conservation
status
DD
LC
NT
VU
NE
Top fished
species
6
(8.6%)
34
(48.6%)
5
(7.1%)
4
(5.7%)
21
(30.0%)
Fishing
pressure
threat
4
(66.7%)
24
(70.6%)
5
(100%)
2
(50%)
Vulnerability
index (VI)
43.4
(+- 25.5)
40.0
(+-20.21)
41.6
(+-20.6)
47.5
(+- 13.4)
33.7
(+- 17.7)
Population
trends
N
VI
N
VI
N
VI
N
VI
Increasing
0
.
3
39.7
0
.
0
.
Stable
0
.
9
38.4
0
.
0
.
Decreasing
0
.
4
55.2
5
41.6
1
50.0
Unknown
6
43.4
18
36.9
0
.
1
65
NA
0
.
0
.
0
.
2
37.5
Figure 3.1: IUCN Red List assessment dates and resulting categories for the top-fished species.
Conservation gaps top fished species
79
Figure 3.2: Catch trends for top fished species (ALL), by IUCN Red List conservation status (LC, NT,
VU and DD, and NE) on the left, and by population trends (Decreasing, Increasing, Not Available,
stable and Unknown) on the right. Black lines for reconstructed data (SAU), grey lines for reported
data (FAO).
The top 70 species suffered significant declining catches in the 1996-2014 period
(Figure 3.2-ALL and Table 3.3). Nevertheless, this trend was not shared for all assessed
groups. Catches of species evaluated as LC declined significantly in both reported and
reconstructed data (Table 3.3), whereas non- evaluated species only had significant
declining trends for reconstructed data. Concerning population trends, significant declining
catches were found for increasing and unknown population trends, whereas catches
significantly increased in stable and decreasing populations (Table 3.3), suggesting a direct
effect of fishing catches/landings on the species population trends.
Chapter 3
80
Table 3.3: Linear models for catch trends in the 1996-2014 period for IUCN Red List categories and
population trends. Results are given for reconstructed and reported data, with black lines for
reconstructed data (SAU), grey lines for reported data (FAO).
Slope
t statistic
P assoc
Adjusted R2
IUCN Red
List
Category
LC
- 332,263
-2.716
0.015
0.262
-251,843
-2.594
0.019
0.241
NT
8,069
2.064
0.055
0.153
2,163
0.561
0.582
-0.04
VU
- 10,349
0.807
0.431
-0.020
6,082
0.561
0.582
-0.04
DD
- 24,882
-1.162
0.261
0.019
-28,032
-1.437
0.169
0.056
NE
- 138,844
-4.088
<0.001
0.466
-26,386
-1.235
0.234
0.029
IUCN Red
List
Population
Trend
Increasing
-38,478
-5.456
<0.001
0.615
-31,374
-4.429
<0.001
0.508
Stable
28,746
2.941
0.009
0.298
38,307
4.289
<0.001
0.492
Decreasing
29,187
3.665
0.002
0.409
27,343
3.806
0.001
0.423
Unknown
-365,110
2.902
0.01
0.292
-308,543
-3.081
0.007
0.321
NA
-13,769
-1.161
0.262
0.019
2,638
0.276
0.786
-0.05
All species
- 498,269
-4.067
<0.001
0.4634
- 298,016
-2.918
<0.001
0.2945
We finally analysed how species catches had varied after having been evaluated in the
1996-2014 period. In other words, we looked at the potential effect of conservation status
listing in landings. We found that all species categorized as having decreasing populations,
according to their IUCN evaluation, had actually increased their catches in the period
comprised between their evaluation and 2014 (Table 3.4).
Conservation gaps top fished species
81
Table 3.4: Species assessed before 2014 and change in catches after evaluation.
Species
Category
Date
Fishing
trend
Change in the assessment
date-2014 period (tonnes)
according to SAU
Clupea harengus
LC
2010
Increasing
-482,541.20
Dosidicus gigas
DD
2010
Unknown
326,834.34
Engraulis ringens
LC
2010
Unknown
-882,668.62
Ethmalosa fimbriata
LC
2010
Unknown
133,432.04
Euthynnus affinis
LC
2011
Unknown
13,534.02
Gadus morhua
VU
1996
NA
-207,420.31
Homarus americanus
LC
2009
Unknown
62,241.58
Illex argentinus
LC
2010
Unknown
433,027.24
Katsuwonus pelamis
LC
2011
Stable
214,342.17
Melanogrammus aeglefinus
VU
1996
NA
-288,299.65
Merluccius productus
LC
2010
Unknown
103,723.46
Oncorhynchus nerka
LC
2011
Stable
26,882.82
Opisthonema libertate
LC
2010
Stable
182,360.40
Rastrelliger brachysoma
DD
2011
Unknown
16,016.82
Rastrelliger kanagurta
DD
2011
Unknown
-158,248.19
Sardinella longiceps
LC
2010
Decreasing
137,119.90
Sardinops sagax
LC
2010
Unknown
-296,688.53
Scomber colias
LC
2011
Unknown
79,004.09
Scomber japonicus
LC
2011
Stable
235,471.27
Scomber scombrus
LC
2011
Decreasing
366,914.44
Scomberomorus
commerson
NT
2011
Decreasing
29,454.15
Tenualosa ilisha
LC
2014
Decreasing
18,570.26
Thunnus alalunga
NT
2011
Decreasing
9,781.26
Thunnus albacares
NT
2011
Decreasing
120,560.38
Thunnus obesus
VU
2011
Decreasing
1,215.94
Thunnus tonggol
DD
2011
Unknown
8,097.14
Todarodes pacificus
LC
2010
Unknown
12,822.69
Trachurus murphyi
DD
2010
Unknown
193,919.08
Discussion
The revision of the conservation status and population trends of the main fish species
of commercial interest is urgent and mandatory. Solutions for restoring marine ecosystems
and the fish species that live in them are still under debate (Worm et al. 2009), but scholars
and international organizations agree in that sustainable management is becoming more
Chapter 3
82
and more urgent for several fish stocks (Froese et al. 2019). With a horizon of human
population increase in the coming years, assessing species conservation status is more
important than ever, and only possible if all players do their part to manage fisheries
sustainably and sustain the oceans and their biodiversity.
We found progress in the higher assessment rates for top fished species, but no
significantly better conservation assessment coverage as compared with the commercial or
highly commercial counterparts (Table 3.2). As stated in chapter 2, one reason could be that
commercial species may not have been given priority in the IUCN Red List conservation
assessment (Miqueleiz et al., 2020). The absence of significant differences in the
Vulnerability Index among IUCN Red List categories had already been noticed by Miranda
(2017), and our results support those findings. We also demonstrated that the
categorisation of a species under fishing threat, or a declining population trend, were
unrelated to a higher Vulnerability Index. In this sense, we consider that the Vulnerability
Index may not be accurately measuring the extinction risk of a species. Biological traits may
not be the most reliable predictor for extinction risk due to fishing pressure as other factors
are also present (Sadovy de Mitcheson et al. 2013). We consider that IUCN Red List
categorisation provides us with more accurate information about species extinction risk.
Among the assessed species, Gadus morhua (cod) and Melanogrammus aeglefinus
(haddock) have extremely outdated assessments, classified as Vulnerable in 1996 (24 years
ago). After the Atlantic stocks collapsed in the late 1980s and early 1990s (Hutchings &
Myers 1994; Fogarty & Murawski 2008), some recent studies have found that cod stocks
have not yet recovered from the collapse in northwest Atlantic (Neuenhoff et al. 2019) while
IUCN Red List Europe assessment classifies G. morua as LC with increasing populations in
some stocks (Cook et al. 2015). Therefore, we consider that urgent global evaluations of
Atlantic cod and haddock are necessary as conditions may have evolved since 1990s, and
there is a need to combine fisheries and conservation assessments to understand the status
of marine biodiversity.
Apart from these two species assessed in 1996, all remaining assessments dated from
2009 onwards. IUCN estimates that assessments to be outdated after 10 years (Rondinini
et al. 2014), so priority reassessments should be done in the following years for 50% of the
top fished species (most of them classified as LC or DD). Data deficiency not only implies
“inadequate information to make a direct, or indirect, assessment of its risk of extinction
based on its distribution and/or population status” (IUCN 2012) but also affects
conservation priorities, which rely upon threatened species lists (Bland & Böhm 2016). The
Conservation gaps top fished species
83
uncertainty associated with data deficiency affects extinction risk patterns (Bland et al.
2012) and should be solved through a reassessment of DD species.
Not all assessed species were considered to be under fishing pressure (Table 3.2).
Certain species may indeed have abundant populations or be subjects to sustainable fishing
or fishing quotas, but examples of stocks overexploitation are abundant (Mullon et al. 2005)
and several models state that the percentage of overexploited stocks has increased in recent
years (Pauly & Zeller 2017). We should not lower the guard even with those species
classified as LC (not to mention DD), as these species show declining catch trends, that could
hint to declining population trends (Table 3.4). Previous studies have stated the importance
of analysing together IUCN Red List assessments with stock assessments, such as RAM
Legacy Stock Assessment Database, resulting in a high agreement in the conservation of
exploited marine fishes (Davies & Baum 2012).
Almost all species assessed (96%) had information about population trends in the
IUCN Red List, with haddock and cod lacking these data because of their outdated
assessments. Many species had unknown population trends, and as subjects of intensive
fishing, we consider that they should be reassessed in the short term to examine if current
data allow us to establish their trends. Recent IUCN evaluations, such as the one done for G.
morhua in Europe, show detailed information about population trends in the different
stocks (Cook et al. 2015) and can be an example to follow. Nevertheless, the chance of
landings data being underestimated (Pauly & Zeller 2016) may turn them into a non-
reliable source of information to establish stocks viability and population trends. We also
urge to analyse whether those data are reliable and if so, proceed to establish whether those
species are suffering or not from overfishing and take the resulting conservation measures.
FAO’s stable catching trends in recent years have been missed in doubt because
unreported or manufactured data have been detected in previous studies (Pauly & Zeller
2017). Since the 90s, it has been observed a global decline in industrial fishing at an average
rate of 1.2 million tons per year, even excluding those countries which have established
quota management systems (Pauly & Zeller 2016). Reconstructed catches in our study were
in average 21.5% higher than those reported by FAO, far from the 53% stated by Pauly &
Zeller, (2016a). In this sense, FAO data for these top fished species seem to be more
accurate, probably owing to their commercial importance. Furthermore, since the year of
peak catches in 1996, reconstructed catch declined strongly at a mean rate of almost 0.5 mt
per year, whereas FAO showed a less pronounced decline (almost 0.3 mt per year).
Only IUCN Red List categories LC and non-evaluated showed significant catch declines
although the trend for the latter could not be observed in FAO reported data. Assuming that
Chapter 3
84
conservation status cannot be directly inferred from catching trends (Branch et al. 2011),
we consider that this difference for trends for unassessed species highlights the necessity
for this species to be assessed by the IUCN Red List, as reconstructed catches suggest that
they are being more fished than reported ones.
IUCN Red List population trends provided us with relevant information for species
status. Especially surprising was to observe how species with decreasing population trends
according to IUCN Red List (10), had significantly increased their captures in the 1996-2014
period, with higher increase rates for the reconstructed data. Scombridae assessed in 2011
with declining populations had increased their catches after the assessment, even though
this family has shown population declines up to 74% between 1970 and 2010 (WWF 2015).
Examples like Scomber scombrus (Atlantic mackerel) and Thunnus albacares (yellowfin
tuna), whose catches widely increased after their IUCN Red List evaluations should call
attention on how can we know the true status of stocks. Science-based recommendations,
despite their uncertainty, cannot be neglected by the fishing industry, as management of
overfished stocks is essential for their sustainability (Fromentin et al. 2014).
Our study does not intend to infer stock status or collapses from landing data or use
landing data as a direct indicator of species conservation status. Several papers in the last
decade have pointed out the potential flaws of using FAO and Sea Around Us catch statistics
to assess the state of marine ecosystems (Branch et al. 2011). Landings frequently do not
track changes in biomass; thus, collapses estimated on the basis of landing data do not
directly report an actual stock collapse. The IUCN Red List classifies the extinction risk of
species whereas the reference points used in fisheries management relate to the
productivity of a stock. This results in the IUCN assessments mostly addressing rates of
decline in fish populations, while the fisheries assessments address the status relative to
biomass target and/or limit reference points (Millar & Dickey-Collas 2018).
Climate change and global warming affect fish populations viability and compromise
the subsistence of human communities linked to them (Cheung 2018; Morley et al. 2018).
In a context of a global threat to marine species, where human and climate pressures
combine to jeopardize them, we consider that the voice of conservation initiatives, like IUCN
Red List, should be extensively heard by fishing authorities. Despite IUCN Red List
categories and criteria posing problems when evaluating marine fish species (Collen et al.
2016), they have proven to provide evaluations congruent with those done by fishing
authorities (Davies & Baum 2012). Having failed in meeting most CDB Aichi targets
(Tittensor et al. 2014; UNEP-WCMC et al. 2018; Visconti et al. 2019), the sustainability of
one of our main food sources is at stake. If the IUCN approach is incorporated into fisheries
Conservation gaps top fished species
85
management, it is important to recognise that the two approaches have been developed for
different purposes. The two approaches may therefore lead to different outcomes and their
integration may require the adoption of further decision rules (Millar & Dickey-Collas
2018). The last SOFIA report states that collaboration efforts between FAO, CITES, and IUCN
are taking place (FAO 2018), but unless urgent measures are taken, the overexploitation of
our seas can lead again to stock depletion and compromise not only species conservation
but also food security and the way of life in many regions.
Chapter Transparency
I. Miqueleiz conceived the present idea. I. Miqueleiz developed the experiment,
carried out the analyses and interpretated the results. E. Ojea contributed with the structure
of the manuscript to better organize ideas and concepts. I. Miqueleiz wrote the manuscript.
R. Miranda, A.H. Ariño and E. Ojea provided comments to the interpretation of the results
and the manuscript.
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CHAPTER 4:
Trends and perspectives in the knowledge of conservation status of
fishes
Capítulo 4:
Tendencias y perspectivas en el conocimiento del estado de conservación de los
peces
Miqueleiz, I., Miranda, R., Ariño, A. H., Böhm, M.
Trends in the conservation of fishes
93
Chapter preface
As described in the General Introduction of this thesis, freshwater and marine fish
species face numerous anthropogenic threats, causing a worldwide decline in their
populations. Populations of the world’s fish have worsened and their extinction risk has
increased in the last decades. In chapter 2 we studied how IUCN Red List has evaluated fish
species and the underlying biases of the resulting assessments. At the time of this study,
assessed fish species number about 20,000 but they are a far smaller fraction than that of
comparable assessment rates for other vertebrate groups. Furthermore, fish species
description rates remain high and efforts must be prioritised when acknowledging new
assessments.
In this study, we aim to address global trends on IUCN Red List fish assessments and
to evaluate the role of individual countries in fish assessments according to their economic
capacity. We compiled a list of all fish species described until 2019 and analysed their
conservation status. We also extracted subsets of newly discovered species (described
between 1996 and 2019), species with dated assessment (IUCN Red List assessment dating
more than 10 years back), and reassessed species, and analysed the resulting dataset.
Finally, we correlated species richness, assessment rate, out-of-date assessments, and new
species by country with the economic power (GDP power per capita) of the country.
Our results showed an increasing IUCN Red List assessment effort for fish in the past
years, but also higher levels of threat and more data deficiency for the more recently
described species. They also suggest that these new species should be prioritised in further
assessment programs. On the other hand, we found that higher-income countries list a large
proportion of out-of-date assessments, suggesting a redirect towards the reassessment
effort. Finally, several countries of South America, had both a large gap in assessments, and
a high proportion of newly described species, clearly indicating a need to step up the
assessment effort in the region, including the development of retrospective assessments for
those recently assessed species. Globally, in view of those trends we recommend the
development of long-term plans for national Red Lists as an essential tool to ensure the
quality of Red List assessments and enhance the conservation perspectives for fish species.
The role of national Red Lists will be further discussed and examined in chapter 6.
Trends in the conservation of fishes
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Introduction
Fish inhabitants in aquatic environments are numerous, with more than 35,000 valid
species in total (over a half of all vertebrate species) and half of them living in freshwater
habitats (Fricke et al. 2020). They constitute a large fraction of biomass in aquatic
ecosystems (Jennings et al. 2008) and provide us with various ecosystem services (Worm
et al. 2006; Green et al. 2015). Nevertheless, in a rapidly changing world, fishes are facing
several threats that jeopardize their survival. Human activities have globally increased in
the last century, overexploiting natural resources (Garcia-Moreno et al. 2014). Nowadays,
freshwaters receive impacts from habitat loss and fragmentation, water pollution, extensive
wetland drainage, groundwater depletion, the establishment of introduced alien species,
and overfishing of native ones (Dudgeon et al. 2006; Strayer & Dudgeon 2010; Vörösmarty
et al. 2010). Concerning the marine realm, main threats emerge from overfishing, pollutant,
sediment, and nutrient input (Halpern et al. 2007, 2008), habitat loss (Dulvy et al. 2003),
and invasive alien species (Bax et al. 2003)., with a strong impact on critical ecosystem
services such as fisheries or nutrient cycling (Selig et al. 2014). Furthermore, climate change
is very likely to be a driver of freshwater and marine fish physiological changes, species
turnover, local extinction, and invasion (Cheung et al. 2009; Woodward et al. 2010; Poesch
et al. 2016). In the last decades, vertebrate populations have declined worldwide, with
freshwater (84% decline) (WWF 2020) and marine fishes (50%) (WWF 2015) at high risk.
Conservation of the world's freshwater and marine fishes requires management and
restoration strategies, focused on species at the greatest risk of extinction (Arthington et al.
2016). In 2010, the Convention on Biological Diversity (CBD) developed the Strategic Plan
for Biodiversity, which included 20 time-bound, measurable targets to be met by the year
2020. Among them, target 12 was established in 2010 to prevent species extinction and
improve and sustain their conservation status (SCBD 2010). To measure species extinction
risk, the International Union for the Conservation of Nature (IUCN) developed the Red List
of Threatened Species, which has turned into the reference guide to identify threats and
prioritise conservation efforts (Rodrigues et al. 2006; Rondinini et al. 2014). This tool not
only provides a classification of each species into a category of threat (IUCN 2012a) but also
supports it with information on species range size, population trends, habitats,
conservation actions, and past assessments (IUCN 2020). Aiming to be a “Barometer of Life”,
IUCN Red List expects to reach a milestone of 160,000 species assessed by the end of 2020.
Nevertheless, IUCN Red List coverage remains unbalanced among different taxa assessed.
Thus, in the case of vertebrate species, while almost all extant mammal and bird species
have been assessed, the remaining vertebrate groups have lower levels of assessments
Chapter 4
96
(Meiri & Chapple 2016; Tapley et al. 2018). Similar trends have been observed when
assessment rates of terrestrial and freshwater species have been compared (Collen et al.
2014). In the case of fish, recent studies estimate that little more than a half of described the
fish species have been assessed in the IUCN Red List, resulting in the poorest representation
of all vertebrate groups (Miqueleiz et al. 2020).
In this sense, IUCN Red List efforts to address this fish assessment gap and increase
our knowledge of fish conservation status are noticeable. Over the last years, several IUCN
Species Specialist Groups (SSG) have increased fish evaluations focusing on specific groups
(Sadovy de Mitcheson et al. 2013; Dulvy et al. 2014). Furthermore, under the IUCN
Freshwater Biodiversity Unit (FBU), regional assessments have increased knowledge in
eastern Himalaya (Allen et al. 2010), Afri