CHAPTER 21

Grey Mullet as Possible Indicator of

Coastal Environmental Changes:
the MUGIL Project
Jacques Panfili,1,a,* Catherine Aliaume,1,b
Aikaterini Anastasopoulou,2 Patrick Berrebi,3 Claude Casellas,4
Chih-Wei Chang,5 Papa Samba Diouf,6
Jean-Dominique Durand,1,c Domingo Flores Hernandez,7,e
Francisco J. García de León,8 Philippe Lalèyè,9
Beatriz Morales-Nin,10 Julia Ramos Miranda,7,f
Jaime Rendon von Osten,7,g Kang-Ning Shen,11,h Javier Tomas,1,d
Wann-Nian Tzeng,12 Vassiliki Vassilopoulou,13 Chia-Hui Wang11,i
and Alan K. Whitfield14

Introduction—General Overview of the MUGIL Project

The position of estuaries, deltas and lagoons in coastal areas at the interface of marine and riverine
influences, results in highly variable environmental and ecological conditions that shift over both space
and time. In addition, the effects of global change also have a tremendous impact on these ecosystems.
The health and conservation of these environments is one of the biggest challenges facing humanity and,
in order to achieve integrated management, scientists, ecologists and managers need to select relevant
indicators which could be used as tracers for the state of coastal areas. These indicators are generally
chosen from living species or physico-chemical parameters or a combination of both. Among the fish
species living in estuaries, very few occupy these ecosystems in more than one oceanic region, but there
is one particular species among the mullets, the flathead mullet Mugil cephalus which is found worldwide
in almost all tropical, subtropical and warm temperate coastal zones. This fish is able to live in widely
different habitats, but the mechanisms which drive the life cycle of M. cephalus are poorly known or have
been studied separately in each area.
The aim of the MUGIL Project (Main Uses of the Grey mullet as an Indicator of Littoral environmental
changes), financed by the European Commission between 2006 and 2009 (INCO-CT-2006-026180), was to

Authors’ affiliations given at the end of the chapter.

© 2016 by Taylor & Francis Group, LLC

 Grey Mullet as Possible Indicator of Coastal Environmental Changes: the MUGIL Project 515

build a collaborative network to coordinate research across the world using Mugil cephalus as an indicator
of the state of coastal environments and to standardize methodologies for further studies. Since the flathead
mullet is distributed worldwide, from tropical to temperate seas, and is of great commercial importance
to fisheries in certain developing countries, it represented a good candidate for an indicator species. The
project covered four global areas (Europe, Africa, Asia, and America) and involved collaborators from
southern Europe (Spain, France, and Greece) and sub-tropical and tropical countries (Mexico, Senegal,
Benin, South Africa, and Taiwan). The project was structured around two seminars and six workshops
dealing with specific topics (life history traits, migration, genetics, biomarkers, databases). Each of these
meetings involved mullet specialists and produced a report with a synthesis of the presentations, discussions
and recommendations, available at http://www.mugil.univ-montp2.fr/.

Life History Trait Studies

Only a few studies have been carried out on the life history traits of Mugil cephalus on a global
scale (Whitfield 1990). Studies on growth and/or reproduction around the world have rarely used the
same methods or protocols, making international comparisons difficult. In addition, growth data on
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M. cephalus in the primary literature is scarce and even in studies focusing on age validation, growth rate
data are not given (Smith and Deguara 2003). A few studies involving growth assessment of M. cephalus
have highlighted the very variable growth rates and appear dependent on the environment (Ibáñez-Aguirre
et al. 1999), but no global comparisons have been undertaken.
The reproductive behaviour of M. cephalus is seasonal, usually occurring when water temperature is
appropriate for reproduction, but even this appears to be very variable from one area to another (Whitfield
et al. 2012). More integrated studies on the reproductive cycle of M. cephalus throughout the world could
highlight the relationship between reproductive season, environmental physico-chemical parameters and
phylogenetic structure. Similarly, studies need to be undertaken on the possible effects of the environment
on reproductive traits such as fecundity, size at first maturation, oocyte size, etc.
As no standardized methods for age and reproduction of M. cephalus are available in the literature,
the MUGIL Project focused on their standardization. For age estimations, it recommended that otoliths and
not scales be used. Comparisons were undertaken on otolith samples collected from different parts of the
world (Mauritania, Senegal, Spain, Benin, South Africa, Greece and Taiwan). The shapes of the otoliths
from the different areas were generally the same and measurements along the otolith axis were similar,
thus reinforcing the idea that the species is cosmopolitan. For age estimation, the MUGIL consortium
recommended the use of growth rings on transverse otolith sections of 300 μm thickness, preferably
observed under transmitted light in order to reveal thin bands (Panfili et al. 2007). Nevertheless, a validation
stage (i.e., verification of the timing of band deposition) should be obligatory in each study. The MUGIL
consortium also defined a common maturation scale for gonad examination, which could be used when
working on reproduction (Panfili et al. 2007).

Migration Studies
Mugil cephalus is diadromous and often migrates between continental and marine environments during
its life cycle. Juveniles and sub-adults grow in freshwater and/or estuarine habitats, but adults undertake
off-shore migrations for spawning, usually in the form of large schools (Bacheler et al. 2005). Among
the tools available to study fish migration, otolith microchemistry has proved successful in resolving
habitat occupation between freshwater and seawater environments by diadromous fish (e.g., Jessop et al.
2002, Tomás et al. 2005, Arai 2007). Otolith microchemistry has also been successfully applied to the
identification of saline habitats occupied by flathead mullet, but these studies were scarce and confined to
Taiwan (Chang et al. 2004a, Chang et al. 2004b). In the absence of detailed studies on saline habitat use
by M. cephalus in other parts of the world, otolith microchemistry constitutes a very efficient approach to
determine the migration habits of this species.
The MUGIL Project defined the best methods for otolith collection, storage and preparation for
microchemical analysis to study the transhaline migrations of M. cephalus. The guidelines were presented

© 2016 by Taylor & Francis Group, LLC

 516 Biology, Ecology and Culture of Grey Mullet (Mugilidae)

in a specific deliverable (Tomás et al. 2008), which enables all future research on the subject to follow the
same standard protocols for the use of otolith microchemistry, thereby facilitating global comparisons.
The MUGIL consortium recommended chemical analysis of transverse sections of otoliths using Laser
Ablation—Inductively Coupled Plasma Mass Spectrometry along the axis of the otolith with visible and
interpretable growth rings. It is acknowledged that strontium and especially the strontium:calcium ratios
are the best candidate elements to track transhaline fish migrations. The possibility exists however that
other elements may bring additional information to identify dispersal within freshwater environments
by using strontium isotopes, or to identify fidelity to certain coastal areas using Mn, Ni, Zn and Ba. The
MUGIL consortium strongly recommended that validation experiments be conducted under controlled
rearing conditions before applying these microchemistry approaches.

Genetics Studies
The taxonomic status of Mugil cephalus remains uncertain and no definitive conclusions have been reached
regarding the possible existence of one circumtropical species or, alternatively, a complex of more regional
cryptic species (Briggs 1960, Crosetti et al. 1994). As stated earlier in this book (see Chapter 1—González-
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Castro and Ghasemzadeh 2015 and Chapter 2—Durand 2015), one of the reasons for this may be the lack
of basic information on the phylogeny of Mugilidae. Understanding the origin and evolution of grey mullets
requires general knowledge of the evolutionary background within the family. Furthermore, studies that
investigate the evolutionary history of M. cephalus have usually failed to reach conclusions about species
boundaries due to loose sampling across the geographical range. During the MUGIL Project, specific genetic
methodologies were discussed from four different perspectives: phylogeny, phylogeography, population
genetics and adaptation. The compilation of specific guidelines for genetic studies allows scientists to
follow the same protocol and therefore facilitate comparison of results (Durand et al. 2008).
Allozymes appear inappropriate for phylogenetic studies that involve numerous species from different
parts of the world, due to their low polymorphism and sample handling requirements (i.e., the need for
live tissues preserved at –20ºC). In contrast, DNA sequencing should be the most appropriate method and
numerous genes are available to investigate the molecular phylogeny of Mugilidae. 16S RNA with 12S
RNA have a low mutation rate that should be useful for the inference of deep phylogenetic relationships
(Rossi et al. 2004, Heras et al. 2006, Papasotiropoulos et al. 2007) whereas cytochrome b and cytochrome
oxydase I, with higher mutation rates, are more appropriate to estimate phylogenetic relationships of closely
related and more divergent species (Heras et al. 2006, Blel et al. 2010).
Among different approaches, EPIC and semi-multiplex PCR analysis appear the relevant methods
for species identification of numerous samples within a specific area. These methods are less expensive
than PCR-RFLP and more reliable than D-loop sequences of mitochondrial DNA. If species identification
has to be routinely performed for a large series of samples however, it would be more appropriate to set
up a semi-multiplex PCR analysis.
The phylogeographic approach is particularly suited for studying the origin, dispersal and historical
demography of M. cephalus. Mitochondrial DNA D-loop sequences are likely to be ideal for regional
phylogeographic analyses and could be complemented by the analysis of slower evolving genes to resolve
deeper phylogenetic divergences. D-loop sequence analyses may pose some multiple alignment challenges
at large geographic scales where large sequence divergences have been documented. Lastly, for studying
adaptation and selection, different strategies could be possible in order to find polymorphism under
different selective pressures (e.g., genome scan approach, AFLP or Rad-Seq, link among polymorphisms
of candidate genes and individual fitness, etc.).

Biomarker Studies
The MUGIL Project provided an opportunity to identify interest in developing biomarker studies on Mugil
cephalus from different countries (Casellas et al. 2009). The objectives were to define a standard protocol
for the use of biomarkers. M. cephalus possesses several characteristics required in a sentinel or indicator
species, such as wide salinity and temperature tolerances, which enable them to occupy most coastal waters.

© 2016 by Taylor & Francis Group, LLC

 Grey Mullet as Possible Indicator of Coastal Environmental Changes: the MUGIL Project 517

The use of biomarkers could offer an integrated evaluation of the effects of pollutants on the aquatic biota
and also provide an early warning of potential changes at the ecosystem level.
The MUGIL consortium recommended that field sampling samples for biomarker analyses should
include at least 15 males and 15 females per site. Different equipment would be required for processing
the fish and storing the various sample tissues for later laboratory analysis, depending on the biomarkers
to be used (Table 21.1). Experimental procedures for biomarkers studies in M. cephalus have been
described by Casellas et al. (2009). Biomarkers tested since the turn of the century were listed (Corsi
et al. 2003, Ferreira et al. 2004, Barucca et al. 2006, Ferreira et al. 2006, Neves et al. 2007) and evaluated

Table 21.1. Equipment required for processing the fish and tissues and storing the various samples for later laboratory in the
case of biomarker analysis for mullets. AchE (acetyl cholinesterase).

Sample collection Type of tube Minimum number of tubes Biomarker use

Blood Heparin/Li tubes 1 heparin tube Vitellogenin
for blood sampling + 2 minitubes
Bile Eppendorf 1.5 ml 2 In vitro
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Liver Microtube w/beats 2 EROD

+ biochemical dosages
Brain Eppendorf 1.5 ml 2 AchE
Scales Envelope 1 Age/DNA
Otoliths Eppendorf 0.5 ml 1
Muscle Microtube w/beats 1 AchE

(Casellas et al. 2009). It was also emphasized that future biomarker analyses in different parts of the
world should only proceed once an inter-calibration exercise had been carried out to reference the results.

Mugil cephalus Databases

An important activity during the MUGIL Project comprised exchanges between the participants and the
FishBase consortium (www.fishbase.org) in order to (a) update the information on the Mugil cephalus
webpage on FishBase, (b) build a bibliographic reference and pdf database on this species and (c)
collect original data from different parts of the world to facilitate the building of an individual database
(Aliaume et al. 2007, Aliaume et al. 2008). The information available online in FishBase for M. cephalus
was reviewed in 2008 and some webpages were edited and updated.
A database with bibliographic references on M. cephalus (both peer-reviewed articles and grey
literature), together with pdf copies of these articles, was built and is available to the MUGIL consortium
through its intranet website (www.mugil.univ-montp2.fr). The list included 288 references, classified by
world areas and thematic fields of research and applications.
The structure of a database that includes specific individual biological and ecological data was
developed during the MUGIL Project. This database was built using Microsoft Access software with
several tables (Fig. 21.1). The MUGIL consortium compiled individual data from each geographical area
and more than 2800 individual M. cephalus data sets were gathered, mainly providing information on
length, weight and location. Recorded salinities ranged from 0 to 89, and water temperatures from 19 to
34ºC. A large size range was represented in the dataset, with a peak in composition between 200 and 300
mm fork length. Males predominated in the database (more than 60%), followed by females (20%) and
immature fish (15%). The database has not been updated since 2009.

Conclusions
The MUGIL Project reinforced the idea that the flathead mullet could be used as a bioindicator of coastal
environmental states, and the project also gave guidance for different methods and protocols that could
be used when studying life history traits, genetics, migrations and specific biomarkers for M. cephalus.

© 2016 by Taylor & Francis Group, LLC

 © 2016 by Taylor & Francis Group, LLC

518 Biology, Ecology and Culture of Grey Mullet (Mugilidae)

MAIN
Habitat Species Morphometry_Age
Indiv_code_origin Year Indiv_code_origin
Indiv_code_MUGIL Month Indiv_code_MUGIL
Ecosystem_name Ontogenetic_stage Otolith bulk microchem
Day
Station_ID Lenght_TL_mm Indiv_code_origin
Hour
Habitat Country Length_FL_mm Otolith Indiv_code_MUGIL
Substratum FAO area Length_SL_mm Indiv_code_origin Microchemistry
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Depth Ecosystem_name Weight_total_g Indiv_code_MUGIL Microchem_method

Current_speed Ecosystem_type Weight_gonad_g Otolith_weight_mg Element_concentration
Temperature_surf Station_ID Weight_liver_g Left/Right
Temperature_bottom NS_coordinates Weight_stomach_g Otolith_max-length_mm
Salinity_surf WE_coordinates Weight_eviscerate_g Otolith_post_radius_mm Otolith transect microch...
Salinity_bottom Sampling_method Sex Otolith_ant_radius_mm Indiv_code_origin
pH Indiv_code_origin Maturity_stage Otolith_ventr_radius_mm Indiv_code_MUGIL
Oxygen_dissolved_mg/l Indiv_code_MUGIL Age Otolith_dors_radius_mm Microchemistry
Light_penetration_cm Age_method Microchemistry Microchem_method
Observations Analfin_color
Point-number
Analfin_rays_nb
Distance_from_core_ μm
LL_scale_nb
Ecotoxicology Diet Element_concentration
Genetics Observation
Indiv_code_origin Indiv_code_origin
Indiv_code_origin
Indiv_code_MUGIL Indiv_code_MUGIL
Indiv_code_MUGIL
Ecosystem_name Physiology Fullness
Locus
Ecosystem_type Indiv_code_origin Content_weight
Karyotype
Station_ID Indiv_code_MUGIL Sediment
Heterozygosity
Habitat Oxygen_consumption FoodI
Substratum Na-K-ATPase FoodII
Contaminant_type Osmotic_pressure FoodIII
Ecotox_method Ionocyte_nb Commoness
Analytical_sample Hormone CommonessII
Pollutant_concentration Hormonal_expression Foodgroup
Ecotox_response Enzyme_activity Foodname

Figure 21.1. Diagrammatic representation of the database for individual Mugil cephalus developed during the MUGIL Project. The table ‘Main’ includes general information on each
sample and other tables are specific to other thematic fields (Habitat, Genetics, Ecotoxicology, Physiology, Morphology_Age, Diet, and three tables are dedicated to otolith information). The
Individual_MUGIL code is composed of 10 digits: two letters for the country of capture (according to the internet country code), two figures for the year (e.g., 05 for 2005), two figures for
the month, and four figures for the fish specimen.
 Grey Mullet as Possible Indicator of Coastal Environmental Changes: the MUGIL Project 519

Since the end of the project, new technological advances and case studies in genetics have demonstrated
that M. cephalus is a cryptic species complex (Chapter 2—Durand 2015, Shen et al. 2011, Krueck et al.
2013), and migrations have been studied in Mexican waters (Ibáñez et al. 2012).
The project produced several outcomes and among them peer-reviewed publications which provide
additional detailed information on the flathead mullet (Hsu et al. 2007, Hsu et al. 2009, Hsu and Tzeng
2009, Jamandre et al. 2009, Trape et al. 2009a, Trape et al. 2009b, Blel et al. 2010, Jamandre et al. 2010,
Shen et al. 2010, Wang et al. 2010, Shen et al. 2011, Wang et al. 2011, Chang and Lizuka 2012, Durand
et al. 2012a,b, Ibáñez et al. 2012, Whitfield et al. 2012, Durand et al. 2013).

Acknowledgements
The MUGIL Project was financially supported by the European Commission (INCO-CT-2006-026180-
MUGIL) from November 2006 to March 2009.
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1
IRD, UMR 5119 ECOSYM, Université Montpellier 2, CC 093, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France.
a
Email: jacques.panfili@ird.fr
Downloaded by [Donatella Crosetti] at 03:19 07 January 2016

b
Email: catherine.aliaume@univ-montp2.fr
c
Email: jean-dominique.durand@ird.fr
d
Email: javier.tomas@mac.com
2
Hellenic Centre for Marine Research, Agios Kosmas, Helliniko, 16777, Greece.
Email: kanast@hcmr.gr
3
Institut des Sciences de l’Evolution, Université Montpellier 2, CNRS-IRD, CC 065, Place Eugène Bataillon, 34095 Montpellier
cedex 05, France.
Email: patrick.berrebi@univ-montp2.fr
4
Département Sciences de l’Environnement et Santé Publique, Faculté de Pharmacie, Av. Charles Flahault, BP 14493, 34093
Montpellier Cedex 05, France.
Email: casellas@univ-montp2.fr
5
National Museum of Marine Biology and Aquarium, Pingtung 944, Taiwan ROC/Graduate Institute of Marine Biology,
National Dong Hwa University, Pingtung 944, Taiwan ROC.
Email: changcw@nmmba.gov.tw
6
WWF-WAMER, Sacré Cœur III, No 9639, Dakar, Senegal.
Email: psdiouf@gmail.com
7
Instituto EPOMEX, Universidad Autónoma de Campeche, Av. Héroe de Nacozari Núm. 480, C.P. 24029. Campeche, Cam.,
México.
e
Email: doflores@uacam.mx
f
Email: ramosmiran@gmail.com
g
Email: jarendon@uacam.mx
8
Instituto Politécnico Nacional 195, Playa Palo de Santa Rita Sur, La Paz, B.C.S., C.P. 23096, México.
Email: fgarciadl@cibnor.mx
9
Faculté des Sciences Agronomiques de l’Université d’Abomey-Calavi, 01 BP 526, Cotonou, Bénin.
Email: laleyephilippe@gmail.com
10
Institut Mediterrani d’Estudis Avançats (IMEDEA-CSIC/UIB), Miquel Marques 21, 07190 Esporles, Illes Balears, España.
Email: beatriz@imedea.uib-csic.es
11
Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung 20224, Taiwan.
h
Email: knshen@mail.ntou.edu.tw
i
Email: chwang99@mail.ntou.edu.tw
12
Department of Environmental Biology and Fisheries Science, National Taiwan Ocean University, Keelung, Taiwan, ROC/
Institute of Fisheries Science, National Taiwan University, Taipei, Taiwan, ROC.
Email: wnt@ntu.edu.tw
13
Hellenic Centre for Marine Research, Agios Kosmas, Helliniko, 16777, Greece.
Email: celia@hcmr.gr
14
South African Institute for Aquatic Biodiversity (SAIAB), Private Bag 1015, Grahamstown 6140, South Africa.
Email: a.whitfield@saiab.ac.za
* Corresponding author

© 2016 by Taylor & Francis Group, LLC