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Taxonomic confusion and market mislabelling of threatened skates important consequences for their conservation status.

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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
Published online 19 November 2009 in Wiley InterScience
(www.interscience.wiley.com). DOI: 10.1002/aqc.1083
Taxonomic confusion and market mislabelling of threatened skates:
important consequences for their conservation status
SAMUEL P. IGLÉSIAS, LUCILE TOULHOAT and DANIEL Y. SELLOS
Muse´um national d’Histoire naturelle, De´partement Milieux et Peuplements Aquatiques, USM 0405, Station de Biologie Marine de
Concarneau and UMR 7208 CNRS/MNHN/IRD/UPMC, Biologie des Organismes et Ecosyste`mes Aquatiques, France
ABSTRACT
1. The iconic European common skate (Dipturus batis) has been described as the first clear case of a fish species
brought to the brink of extinction by commercial fishing. Its listing was upgraded to Critically Endangered on the
2006 IUCN Red List of Threatened Species. According to FAO fishery statistics, France is responsible for 60.2%
of the 502 tonnes reported as ‘D. batis’ in the 2005 world landings.
2. Noticeable phenotypic differences within the species and inconsistencies in published data on its sexual
maturation required careful re-examination of its taxonomy. Morphology, genetics, and life history reveal that
two distinct species have been erroneously confused since the 1920s under the single scientific name D. batis. Here
it is argued that they should be resurrected as two valid species. The common skate D. batis species-complex is
split into two nominal species, the blue skate (provisionally called D. cf. flossada) and the flapper skate (D. cf.
intermedia) with maximum lengths of 143.2 cm and 228.8 cm respectively.
3. This taxonomic confusion puts into question all previously accumulated data based on D. batis. Its
endangered status highlights the need for an extensive reassessment of population collapses with accurately
identified species. In 2006/2007 an extensive survey (4110 skates, 14.081 tonnes by weight) was conducted in the
main French ports of the D. batis species-complex and relatives (D. oxyrinchus, D. nidarosiensis and Rostroraja
alba) that are mixed together in landings under the names ‘D. batis’ and ‘D. oxyrinchus’.
4. The survey reveals that official fishery statistics mask species-specific declines, due to the mislabelling of five
species under only two landing names. Trends in landings since the 1960s and the life history of these species
suggest a dramatic decline and collapse of the spawning stock, preventing the recovery of relict populations.
5. The risk of extinction of these depleted species may be higher than previously assessed and might be
unavoidable without immediate and incisive conservation action.
Copyright r 2009 John Wiley & Sons, Ltd.
Received 8 April 2009; Revised 31 July 2009; Accepted 7 September 2009
KEY WORDS:
Rajids; Dipturus batis; mislabelling; taxonomic confusion; species resurrection; Critically Endangered; IUCN Red
List; marketplace; overfishing
INTRODUCTION
Marine biodiversity is suffering from accelerating loss of
populations and species by overfishing (Pauly et al., 2002;
Worm et al., 2006). Large predators, including many
chondrichthyans, are among the worst affected (Stevens
et al., 2000; Baum et al., 2003; Myers and Worm, 2003;
Myers et al., 2007) and large skates are particularly vulnerable
to depletion (Brander, 1981; Casey and Myers, 1998; Dulvy
et al., 2000; Dulvy and Reynolds, 2002). Life history
characteristics which render these species highly vulnerable
to exploitation, particularly to bottom trawling, include: large
body size, slow growth rate, late maturity, low fecundity and
large offspring size (Du Buit, 1968; Brander, 1981; Dulvy et al.,
2000; Dulvy and Reynolds, 2002).
The common skate (Dipturus batis) is considered the world’s
largest rajid (Muus et al., 2005; Froese and Pauly, 2009). It has
been described as the first clear case of a fish species brought to
the brink of extinction by commercial fishing (Brander, 1981).
The common skate, as the name implies, was historically one of
*Correspondence to: Samuel P. Iglésias, Station de Biologie Marine de Concarneau, BP 225, Place de la Croix, 29182 Concarneau cedex, France.
E-mail: iglesias@mnhn.fr
Copyright r 2009 John Wiley & Sons, Ltd.
320
S. P. IGLÉSIAS ET AL.
the most abundant species of skate in the North-eastern
Atlantic, and it is now considered locally extinct over most of
its geographic range (Dulvy et al., 2000; Dulvy and Reynolds,
2002). Skates historically landed under the name of ‘D. batis’
were formerly abundant on the shelf and upper slope of the
North-eastern Atlantic and the Mediterranean. Fishery data
indicate that since the early 20th century these populations
have undergone severe declines to the point that they are now
considered virtually absent from much of their range and have
been extirpated from most inshore areas (Brander, 1981;
Walker and Hislop, 1998; Dulvy et al., 2000, 2006; Dulvy
and Reynolds, 2002; Daan et al., 2005). In the Irish Sea and
Bristol Channel between 1959 and 1997 the relative abundance
of D. batis in total landed skates decreased ten-fold and only six
individuals were captured in government surveys of the Irish
Sea between 1988 and 1997 (Dulvy et al., 2000). This species
remains rare in the Irish Sea, with only occasional individuals
recorded from isolated sites (J.R. Ellis, pers. commun.). In the
North Sea; single individuals are only rarely caught in trawl
surveys (Walker and Hislop, 1998; Daan et al., 2005; ICES,
2006, 2008). Finally, it appears that heavily depleted
populations remain only in waters off western Scotland,
western Ireland, and in the Celtic Sea where they are
exploited mostly by French trawlers. In the French port of
Concarneau, the landings under the name of ‘D. batis’, fished
from these areas, fell by 91% (from 922 tonnes to 85 tonnes)
(Brander, 1981), between 1969 and 1979. The fishing mortality
of immature and mature individuals is likely to be similar
because they are vulnerable to capture from birth by the same
gear (Brander, 1981). Furthermore, as these skates are caught
as bycatch in commercial fisheries targeting more valuable
species, the population decline is likely to continue (Brander,
1981; Dulvy and Reynolds, 2002).
The World Conservation Union — IUCN (www.
iucnredlist.org) assess the conservation status of species to
identify and document taxa most in need of conservation
attention. Of the 75 skate species assessed by IUCN on the
2008 Red List of Threatened Species, 17 are considered
threatened (Critically Endangered, Endangered or Vulnerable)
(IUCN, 2009). Four large skates (4140 cm) are described in
European waters, all of which are affected by overfishing:
the common skate (Dipturus batis) assessed by IUCN as
‘Endangered’ in 2000 and upgraded to ‘Critically Endangered’
in 2006 (Dulvy et al., 2006), suggesting this taxon ‘is facing an
extremely high risk of extinction in the wild’; the longnosed
skate (D. oxyrinchus) assessed as ‘Near Threatened’ in 2007
(Dulvy et al., 2000; Dulvy and Reynolds, 2002); the deep-sea
Norwegian skate (D. nidarosiensis) not yet evaluated by IUCN
but commercially exploited in deep-sea fisheries; and the white
skate (Rostroraja alba) listed as ‘Endangered’ by IUCN in 2006.
With more than 150 extant species, skates of the family
Rajidae (excluding Arhynchobatidae and Anacanthobatidae
(Last and Stevens, 2009)) are among the largest families of
cartilaginous fishes (Chondrichthyes). Rajids are unique among
chondrichthyans for their high species diversity but very high
morphological and ecological conservatism (McEachran and
Miyake, 1990; McEachran and Dunn, 1998). As a consequence
the taxonomy of this group appears arduous and numerous
synonym species have been erroneously described in the past.
Nowadays many new species are regularly described (Last and
Stevens, 2009) and taxonomic uncertainties still exist for some
species. The morphological conservatism within the group
Copyright r 2009 John Wiley & Sons, Ltd.
combined with high morphologic and morphometric
modifications during species growth (called ontogeny) makes the
identification of many species difficult even for specialists. As a
consequence published results on biology and life history based on
erroneously identified species or mixed species are not uncommon.
Nowadays the common skate (D. batis) is considered in literature
as a valid species. However from the mid-19th century up to the
1920s it was frequently described in the literature as two different
species (the blue skate, provisionally called Dipturus cf. flossada,
and the flapper skate, provisionally called D. cf. intermedia in the
present paper, but more often called by other scientific names in
the literature (see discussion)). In the absence of fully documented
original descriptions, including morphological variations with
respect to size, the taxonomy of these species was widely confused.
In his influential 1926 revision of European rajids, Clark (1926)
recognized only D. batis as valid. Most work following Clark’s
revision only deals with D. batis and the other scientific names
were considered as junior synonyms without documented
demonstration. In his review, Clark (1926) stated for the species
D. batis: ‘I have noted frequently the occurrence of mature males
with large claspers, and other equally large males with the claspers
quite undeveloped. So far I have not given any special study to
this phenomenon’. Later, the only author to document results on
sexual maturation of the common skate based on clasper growth
(Du Buit, 1968), similarly questioned the atypical and complex
maturation of that species and stated: ‘We distinguish two groups
of individuals, some reaching the first sexual maturity at 130 cm
and the others at 180 cm. In the interval, the classes 150 and
160 cm only comprise immature individuals. Do two forms or two
local races exist for D. batis, distinguished by their size at first
sexual maturity?’ The inconsistencies noticed by different authors
regarding the sexual maturation of that species as well as
noticeable morphological differences regarding the original
description of the species synonymized with D. batis raise
questions about the validity of that species and suggest possible
mixing of species under a single scientific name.
The first aim of the present study was to test the hypothesis
that under the scientific name D. batis two valid species,
provisionally called D. cf. flossada and D. cf. intermedia in
the present paper, have been erroneously confused since the
1920s. To test this hypothesis, morphological characters,
measurements and data on sexual maturation were recorded
on a large sample of specimens; otherwise molecular phylogenetics were also inferred for the European Dipturus and
relatives. The threat of extinction for European Dipturus
together with mislabelling in fishery statistics highlight the
need for a huge reassessment of populations for the different
Dipturus species in European waters. The second aim of the
study was to estimate the proportion of the different species
potentially confused and landed under the two landing names
‘D. batis’ and ‘D. oxyrinchus’ as used in the French fishmarkets
and reported in official fishery statistics through an extensive
survey of landings on a corrected species-specific basis in the
main French ports between July 2006 and October 2007.
METHODS
Morphometrics
In total, 17 morphometric measurements were recorded (for
D. cf. flossada/D. cf. intermedia): (M1) Total length, (M2) Disc
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
length (n 5 76/87), (M3) Horizontal length from snout tip to
pelvic fin tips (n 5 75/79), (M4) Length from tail origin to first
dorsal fin insertion (n 5 76/84), (M5) Preorbital length (n 5 76/
85), (M6) Disc width (n 5 76/85), (M7) Orbit length (n 5 76/
86), (M8) Horizontal length from orbit anterior end to spiracle
posterior end (n 5 76/86), (M9) Interorbital width (n 5 76/86),
(M10) Length between spiracles (n 5 62/74), (M11) Interdorsal
space (n 5 241/264), (M12) First dorsal fin base length (n 5 62/
75), (M13) Internarial width (n 5 76/86), (M14) Nasal flap
shortest width (n 5 76/86), (M15) Horizontal distance from
snout tip to nostrils (n 5 76/86), (M16) Snout length (n 5 222/
241), (M17) Clasper inner length (n 5 596/571). Measurements
were performed in the fishmarkets and obtained on specimens
ranging from 382 to 1432 mm total length for D. cf. flossada
and from 314 to 2288 mm total length for D. cf. intermedia.
Results and discussions on measurements and morphological
characteristics will be related in detail in a future paper focused
on resurrection of the two species names confused under the
single name D. batis.
Taxonomic sampling for molecular analysis
Muscle samples for DNA analyses were obtained from
specimens collected in the North-eastern Atlantic (Iglésias,
2006), except for the specimen of D. gigas, which came from
Taiwan. Tissue samples are preserved in the ‘Station de
Biologie Marine de Concarneau’ under collection numbers
that appear in front of terminal branches in Figure 4.
European voucher-specimens are preserved in the ‘Muséum
National d’Histoire Naturelle’ of Paris. The tissue samples/
voucher-specimens are preserved under the following
collection numbers: Rostroraja alba BPS-0228/MNHN 20040817; Malacoraja kreffti BPS-0223/MNHN 2003-2019; Raja
brachyura BPS-0298/MNHN 2004-1543; R. microocellata
BPS-0230/MNHN 2004-0816; Dipturus gigas BPS-0357/
unpreserved; D. nidarosiensis BPS-0226/MNHN 2004-0814,
BPS-0547/TFMCBM VP-1622, BPS-0587/uncatalogued; D. cf.
flossada BPS-0054/MNHN 2003-0536, BPS-0569/MNHN
2004-1545, BPS-0574/MNHN 2004-1546, BPS-0583/MNHN
2004-1547, BPS-0584/MNHN 2004-1548; D. oxyrinchus BPS0258/MNHN 2004-1515, BPS-0259/MNHN 2004-1516; D. cf.
intermedia BPS-0213/MNHN 2004-0828, BPS-0570/MNHN
2004-1549, BPS-0573/MNHN 2004-1550, BPS-0575/MNHN
2004-1551, BPS-0586/MNHN 2004-1552.
DNA extraction, amplification and sequencing
Muscle tissue was taken from fresh specimens and stored
frozen in 80% ethanol. DNA was extracted following the
modified CTAB method (Winnepenninckx et al., 1993).
Approximately 2630 bp of the mitochondrial genome
including partial tRNA-Phe, complete 12S rRNA, complete
tRNA-Val and partial 16S rRNA genes were amplified by Long
Polymerase Chain Reaction (Long-PCR) using the
TripleMasters PCR System (Eppendorf AG, 22331
Hamburg, Germany). The thermo-cycles were: predenaturation 941C/0.5 min.; 45 cycles: denaturation 941C/
0.5 min., annealing 56–601C (depending on the primers)/
0.5 min., extension 721C/4 min. Two overlapping fragments
were obtained with the PCR primer pairs Chon-Mito-S005
(Iglésias et al., 2005)/R035 and S032/R039. PCR products were
purified using the QIAquick Gel Extraction Kit (Quiagen SA,
Copyright r 2009 John Wiley & Sons, Ltd.
321
3av. du Canada, CP809, 91974 Courtaboeuf Cedex, France).
Sequencing reactions were done using a BigDyes Terminator
v3.1 Cycle Sequencing Kit (Applied Biosystems, 850 Lincoln
Centre Drive, Foster City, CA 94404, USA) with the primers:
S003, S005, R008, S009, R010, S014, R017 (Iglésias et al.,
2005), S033, R034, S037, R038, R039, R043, and R044. The
thermo-cycles were: pre-denaturation 961C/2 min.; 45 cycles:
denaturation 961C/0.5 min., annealing 501C/0.5 min., extension
601C/4 min. Long-PCR and sequencing reactions were carried
out on a TGradient thermocycler (Biometra GmbH, RudolfWissell-Str. 30, Postfach 1544, D-37005 Göttingen, Germany).
Sequencing was performed on an ABI PRISMTM 310 Genetic
Analyser (Applied Biosystems). The sequences of the PCR and
sequencing primers are as follows: Chon-Mito-S003: 50 -TCTCTGTGGCAAAAGAGTGG-30 , S005: 50 -AGGCAAGTCGTAACATGGTAAG-30 , R008: 50 -CCACTCTTTTGCCACAGAGA-30 , S009: 50 -CACGAGAGTTTAACTGTCTCT-30 ,
R010: 50 -TAACTTGGTTCATTGATCAGG-30 , S014: 50 -AGTGGGCCTAAAAGCAGCCA-30 , R017: 50 -ATCCAACATCGAGGTCGTAAACC-30 , S032: 50 -AAG(CT)AT(AG)GCACTGAAGATGCTA-30 , S033: 50 -ACTAGGATTAGATACCCTACTATG-30 , R034: 50 -CGCCAAGTCCTTTGGGTTTTAAGC-30 , R035: 50 - (CT)CCGGTCCTTTCGTACTAGG-3’, S037: 50 -TGACCGTGC(AG)AAGGTAGCGTAATC30 , R038: 50 -TCTTC(CT)C(AC)CTCTTTTGC(AC)ACAGAG-30 , R039: 50 -(CT)CCGGTCCTTTCGTACT(AG)GG-30 ,
S043: 50 -AGACGAGAAGACCCTATGGAGCTT-30 , R044:
50 -AAGCTCCATAGGGTCTTCTCGTCT-30 . The sequences
reported in this study have been deposited in GenBank with the
accession numbers EF081261 to EF081280 and alignment is
available upon request from the lead author.
Genetic data analysis
Connecting of sequences and correction of electropherograms
were performed using Sequencher v4.2 (Gene Codes Corporation,
775 Technology Drive, Suite 100A, Ann Arbor, MI 48108, USA).
Sequence alignment was performed by sight using ED of the
package MUST 2000 (Philippe, 1993) with no ambiguity,
resulting in a 2639-bp data set, among which 134 bp were
informative for parsimony. Maximum-parsimony analysis was
performed with PAUP v4.0b10 (Swofford, 1998) using branch
and bound searches. The evolutionary model GTR1I1G
employed in probabilistic methods was estimated initially using
Modelgenerator v0.83 (Keane et al., 2006). Bayesian analyses
were performed using MrBayes v3.1.2 (Ronquist and
Huelsenbeck, 2003). Four Markov chains were run
simultaneously for 2 000 000 Metropolis-coupled generations
(sampled every 100 generations) in two independent runs. Burnin was fixed to 250. The other parameters were used by default.
The total number of trees used to construct the majority-rule
consensus phylograms was 19 750. Maximum likelihood (ML)
analyses were performed using PhyML v2.4.4 (Guindon and
Gascuel, 2003) using the option ‘estimated’ for the following
parameters: base frequency (estimated by ML), Ts/Tv, proportion
of invariable sites, gamma distribution parameter. Substitution
rate was estimated by eight categories. The other parameters were
used by default. Bremer values were calculated with PAUP
v4.0b10. Bootstrap values were obtained with 10 000 replicates for
both MP and ML analyses. Nucleotide diversity (p), and
haplotype diversity (Hd) were calculated with DnaSP v4.10.9
(Rozas et al., 2003). p and Hd are expressed as means7s.d.
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
322
S. P. IGLÉSIAS ET AL.
Sexual maturity
The proportion of mature individuals per length class
was estimated for males and females separately. A logistic
regression (P 5 1/(11exp[–r(L–L50)])) (King, 1995) was fitted
to the data, where P is the proportion of mature individuals for
the length L, r is the slope of the curve and L50 the length at
which 50% of the sample was mature.
Table 1. Weight (A) and number of specimens (B) sampled during the
2006/2007 fishery survey of landings under the names ‘Dipturus batis’
and ‘D. oxyrinchus’ in four French ports
A
Weight sampled in
2006–2007 (wai in Kg)
Landing name (a)
Fishmarket (i)
Fishery survey
From July 2006 to October 2007, 4110 skates (14.081 tonnes
by weight) landed under the names ‘D. batis’ and
‘D. oxyrinchus’ (Table 1) were sampled, equivalent to 3.2%
and 9.0% respectively of the 2005 annual world production
registered under these names (FAO, 2007). In addition, 40
Dipturus individuals (0.196 tonnes by weight) landed as ‘Raja
spp.’, ‘skate wings’, ‘diverse’ or erroneously mixed under
commercial names of other skates were sampled. As the most
recently published data from the FAO for world fishery
statistics and capture production are for the year 2005 (FAO,
2007), the corrected French landings for 2005 were estimated
based on 2006/2007 fishmarket surveys and the registered total
weight landed in 2006 in four ports and provided by the
fishmarket authorities (Table 2), assuming that the relative
proportions of targeted species did not vary significantly
during this time interval. Specimens came from 103 fishing
cruises by 41 different French commercial trawlers and three
Spanish long-liners. They fished over a wide geographical area,
mostly in the Celtic Sea and around western Scotland and
Ireland, at a wide range of depths, from the shelf to 1500 m
depth. Boats were sampled from one to nine times each, with
an average of 2.3 sampling per boat. Fishing boats were
between 15 and 54 m long and fishing cruises were mostly
2 weeks long. The boats sampled were selected for the presence
of Dipturus in their landings. For each landing all specimens
landed under the names ‘D. batis’ and ‘D. oxyrinchus’ were
identified and measured. Dipturus specimens landed under
other landing names were also analysed. The survey was
conducted in four of the main French ports: Concarneau (65
landings), Lorient (13 landings), Loctudy (15 landings) and Le
Guilvinec (10 landings). It is considered that the large number
of boats sampled, the wide area they prospected, the extended
period of sampling and the large number of specimens sampled
limit any possible sampling bias. In France, the marketing
names ‘D. batis’ and ‘D. oxyrinchus’ are used, respectively, in
ten and four fishmarkets. We used quotation marks for
scientific names used as landing names in fishmarkets
(‘D. batis’ and ‘D. oxyrinchus’), suggesting the species landed
under these names are potentially misidentified or the
confusion of several species.
Corrected estimations of specific landings
Revised estimates of actual annual French landings of
large skate species were extrapolated from the results of the
surveys of the four ports (Tables 1 and 2). These estimates
take into consideration the relative proportions of the different
species landed in the different fishing ports, which depend
mostly on the fishing areas targeted by the vessels from
each port.
Copyright r 2009 John Wiley & Sons, Ltd.
‘D. batis’
Concarneau
Lorient
Le Guilvinec
Loctudy
7257.18
0
526.49
1903.3
9686.97
Total
‘D. oxyrinchus’
3575.37
819
0
0
4394.37
14081.34
B
Number of specimens sampled
in 2006–2007 (nai)
Landing name (a)
‘D. batis’
Fishmarket (i)
Concarneau 1478
Lorient
0
Le Guilvinec
89
Loctudy
1042
2609
Total
‘D. oxyrinchus’
1259
242
0
0
1501
4110
Table 2. Official 2006 landings under the names ‘Dipturus batis’ and
‘D. oxyrinchus’ in four French ports (data from the fishmarket
authorities)
Landing name (a)
Registered total weight landed in
2006 (Wai in Kg)
‘D. batis’
Fishmarket (i)
Concarneau
Lorient
Le Guilvinec
Loctudy
46772.85
0
30244.34
72984
‘D. oxyrinchus’
7314.25
58802
3852.96
0
The estimate of the total weight landed in 2005 in France of
the species X (D. cf. flossada, D. cf. intermedia, D. oxyrinchus, D.
nidarosiensis or R. alba) under the names a (‘D. batis’ or ‘D.
oxyrinchus’) was calculated using the following formula:
P4
wXai Wai
i¼1
wai
WXa ¼
Wa
P4
W
ai
i¼1
The estimate of the total number of individuals landed in
2005 in France of the species X (D. cf. flossada, D. cf.
intermedia, D. oxyrinchus, D. nidarosiensis or R. alba) under
the names a (‘D. batis’ or ‘D. oxyrinchus’) was calculated using
the following formula:
P4
nXai Wai
i¼1
wai
Wa
NXa ¼
P4
i¼1 Wai
The parameters are defined as follows:
a 5 Landing name used in French fishmarkets (‘D. batis’ or
‘D. oxyrinchus’).
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
323
i 5 Landing fishmarket (Concarneau, Lorient, Le Guilvinec
or Loctudy).
Xa 5 Identified species (D. cf. flossada, D. cf. intermedia,
D. oxyrinchus, D. nidarosiensis, R. alba or other skates) landed
under the name a.
WXa 5 Estimated weight landed in 2005 in France, of the
species X, under the name a.
Wai 5 Registered weight landed in 2006, under the name a, in
the fishmarket i (data from the fishmarket authorities, Table 2).
Wa 5 Registered weight landed in 2005 in France, under the
name a (data from the FAO (2007)).
wai 5 Observed weight landed under the name a, in the
fishmarket i.
wXai 5 Observed weight of the species X, landed under the
name a, in the fishmarket i.
NXa 5 Estimated number of individuals landed in 2005 in
France, of the species X, under the name a.
nai 5 Observed number of individuals landed under the
name a in the fishmarket i.
nXai 5 Observed number of individuals of the species X,
landed under the name a in the fishmarket i.
Standard deviation on estimated landing (weight or number
of individuals) is calculated with a bootstrap test consisting of
a random sub-sample with replacement, with 10 replicates of
the 96 vessels having landed species under the names ‘D. batis’
or ‘D. oxyrinchus’.
RESULTS
Morphology
Of the 17 measurements taken on specimens representative of
sex and size diversity for Dipturus cf. flossada and D. cf.
intermedia, nine present noticeable differences between species
when expressed as point distribution: the preorbital length, the
orbit length, the horizontal length from orbit anterior end to
spiracle posterior end, the length between spiracles, the dorsal
fins interspace (Figure 1(A)), the horizontal distance from
snout tip to nostrils, the snout length (Figure 1(B)), and the
clasper inner length. All of these measurements are allometric
(their proportion evolves greatly with growth of the specimens),
so these specific differences are mostly masked when expressed
as percentage of total length (TL). These measurements are
only significant when compared between specimens of a similar
size. Comparing specimens of the same size of D. cf. flossada
and D. cf. intermedia, revealed that D. cf. intermedia have a
longer preorbital length, larger eyes, a longer length from orbit
anterior end to spiracle posterior end, a smaller distance
between eyes, longer distance between spiracles, a longer dorsal
fins interspace (Figure 1(A)), a longer snout (Figure 1(B)), and
longer claspers. Only the distance between dorsal fins is nearisometric and so it is significantly different between species
when expressed as an average. The dorsal fins interspace is
1.270.4 and 2.470.5% TL (means7s.d.) for blue skate and
flapper skate, respectively (Figure 1(A)).
In the present case, the use of non-morphometric
characteristics will be more powerful for species
identification. Whatever the ontogenic stage, the species can
always be distinguished by the colour of the iris (Figures 2(A),
(A0 )). This characteristic appears to be the best one to
distinguish the two species in fresh condition. The species
can commonly be distinguished by ocelli or blotches on the
Copyright r 2009 John Wiley & Sons, Ltd.
Figure 1. Comparison of measurements between Dipturus cf. flossada
and D. cf. intermedia. (A) Relationship between dorsal fins interspace
and total length, an example of allometric relationship (n 5 222 and
241 for D. cf. flossada and D. cf. intermedia respectively) and (B)
Relationship between snout length and total length, an example of
near-isometric relationship (n 5 241 and 264 for D. cf. flossada and
D. cf. intermedia respectively).
wings (Figure 2(B), (B0 )), and the orientation of the lateral
thorns on the tail (Figures 2(C), (C0 )). As the dorsal fins
interspace is a near isometric measurement it can help to
distinguish species (Figures 2(D), 2(D0 )). Shape of the teeth is
also different between adults of the two species (Figures 2(E),
(E0 )). Dipturus cf. flossada and D. cf. intermedia are easily
distinguishable by the absence of malar thorns in the adult
males of the latter species whereas thorns are present for adult
males of the former species. For both species, ventral side
coloration is highly variable depending on an individual’s size.
Small specimens have dark ventral sides (Figure 3(A)) which
become paler with growth to finish white for the larger
specimens with only the anterior end remaining pale grey
(Figure 3(B)). At a similar size D. cf. intermedia is darker than
D. cf. flossada. The dorsal side is mostly dark olive-green for
D. cf. intermedia (Figure 3(A0 )) with some pale spots and
becoming grey brown in larger specimens (Figure 3(B0 )). The
dorsal side is mostly brownish for D. cf. flossada with paler
blotches. Most specimens of both species present specific ocelli
on wings (Figure 2(B), (B0 )), although these are not present in
some specimens. Lateral thorns on the tail are absent in
smaller specimens of both species and presence and number is
also highly variable within species. Medial thorns on the tail
disappear in the larger specimens of D. cf. intermedia. These
two confused species, as with most rajids, are characterized by
low morphological diversity and noticeable morphological
variations that depend on sex and maturity (Figures 1(B), 2(E),
(E0 ) and 3), making the identification of species difficult.
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
324
S. P. IGLÉSIAS ET AL.
because phylogenetic analysis indicates that they are never found
as sister taxa, while D. cf. intermedia and D. oxyrinchus are
always found as sister species. To test the robustness of these
results and to estimate the intra and inter-specific molecular
variability of these sympatric species, five specimens of both D.
cf. flossada and D. cf. intermedia collected in the Celtic Sea and
off western Scotland were used. Both species show low nucleotide
and haplotype diversities (Table 3) suggesting a high genetic
homogeneity among each species. (For D. cf. flossada, nucleotide
diversity, p 5 0.01570.009, haplotype diversity, Hd 5 0.4007
0.237. For D. cf. intermedia, p 5 0.06170.027, Hd 5 0.7007
0.218). Two haplotypes were found for D. cf. flossada and three
for D. cf. intermedia. For the 2600 bp sequence analysed, 20
diagnostic characteristics were found (Table 3), which easily
allow the molecular discrimination of the two species.
Life history
Figure 2. The most significant diagnostic morphological
characteristics to distinguish Dipturus cf. flossada (left) and D. cf.
intermedia (right). (A) Eye with pale yellow iris versus (A0 ) dark greenolive iris. (B) Blotch on wing with ocellus with dark centre surrounded
by pale ring versus (B0 ) blotch of grouped pale spots. (C) Lateral
thorns on the tail perpendicular to body axis versus (C0 ) lateral thorns
directed towards the head. (D) Short interspace between dorsal fins
versus (D0 ) long dorsal fins interspace. (E) Tooth (lower jaw, 5th row
from the symphysis; adult male (left), and female (right)) with a
relatively narrow shape versus (E0 ) tooth with a relatively broad shape.
Scale bars 5 10 mm for figures A to D0 and 1 mm for figures E and E0 .
Phylogenetics
Using mitochondrial DNA (mtDNA), the relative phylogenetic
positions of D. cf. flossada, D. cf. intermedia and their European
relatives were established, with the exception of the sailray
(D. linteus) that is easily distinguished by morphology.
Parsimony, bayesian and likelihood analyses all produce
convergent tree topologies (Figure 4). The results strongly
support D. cf. flossada and D. cf. intermedia as distinct species
Copyright r 2009 John Wiley & Sons, Ltd.
In his review, confusing the two species under the single name
D. batis, Clark (1926) stated: ‘I have noted frequently the
occurrence of mature males with large claspers, and other
equally large males with the claspers quite undeveloped. So far I
have not given any special study to this phenomenon’. Later, the
only author to document results on sexual maturation of the
common skate (Du Buit, 1968) based on clasper growth,
similarly questioned the atypical and complex maturation of
that species and stated: ‘we distinguish two groups of
individuals, some reaching the first sexual maturity at 130 cm
and the others at 180 cm. In the interval, the classes 150 and 160
cm only comprise immature individuals. Do two forms or two
local races exist for D. batis, distinguished by their size at first
sexual maturity?’ The two ‘forms’ suspected by these authors
and confused under the name D. batis match with our data on
the sexual maturation for the two species D. cf. flossada and
D. cf. intermedia (Figure 5(A)). The length at 50% maturity
(L50) is estimated to be 115.0/122.9 cm (males/females) and
185.5/197.5 cm (males/females) for blue skate and flapper skate,
respectively (Figure 5(B)). Using the earlier age at length
relationship determined for the D. batis species-complex (Du
Buit, 1977), the age at 50% maturity is tentatively suggested as
11 years and 19–20 years for blue and flapper skate, respectively.
The maximum lengths and weight (eviscerated) observed in the
present study for blue skate and flapper skate were 143.2 cm,
15.2 kg and 228.8 cm, 78.0 kg respectively, so the LN 5 254 cm
estimated for the D. batis species-complex by Du Buit (1977)
may be based primarily on flapper skate, D. cf. intermedia.
The adult females of D. cf. intermedia are more than 80 cm
longer and more than six times heavier than the adult males of
D. cf. flossada. This suggests that an adult male of D. cf.
flossada would not be large enough to firmly grip with its alar
thorns an adult female of D. cf. intermedia during coitus.
Moreover the size of the claspers of a D. cf. intermedia adult
male appear to be too big to be able to penetrate a D. cf.
flossada adult female. These biological findings, together
with the non-sister relationships inferred from molecular
phylogenetics clearly suggest that no hybridization is possible
between D. cf. flossada and D. cf. intermedia.
Fishery
According to FAO fishery statistics, France is one of the largest
skate-fishing nations (FAO, 2007). Worldwide capture
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TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
325
Figure 3. Morphological differences between small and large specimens of Dipturus cf. intermedia. (A) Juvenile male (66.9 cm TL, 0.95 kg, Coll. No.:
MNHN 2004-1551/BPS-0575) with dark ventral side and long snout (grey bar), (A0 ) dorsal side with long preorbital length and with blotch of
grouped pale spots on wings. (B) Adult male (188.4 cm TL, 41.0 kg eviscerated, Coll. No.: BPS-0769) pale ventral side and short snout length, (B0 )
dorsal side with short preorbital length and without blotch on wings.
Figure 4. Molecular phylogenetic relationships between Dipturus cf. flossada, D. cf. intermedia, and their relatives. (A) Strict consensus of the two
most equally parsimonious cladograms. Tree length 345 steps, consistency index 5 0.72, retention index 5 0.83. Robustness of inferred clades was
estimated with Bremer support indices (number above branches) and bootstrap values (numbers below branches). (B) Bayesian phylogram (the same
tree topology is obtained with a maximum likelihood analysis). Numbers above branches indicate posterior probabilities and numbers below
branches indicate bootstrap values in maximum likelihood analyses. Museum collection numbers appear below the photographed voucherspecimens. NT 5 near threatened, EN 5 endangered, CR 5 critically endangered (following 2009 IUCN red list assessment), 5 under the single
name D. batis. Yellow shading groups the specimens of the species D. cf. flossada and D. cf. intermedia confused under the D. batis species-complex.
Orange shading highlights the D. oxyrinchus species that infers the paraphyly of the D. batis species-complex.
production reported as ‘D. batis’, was 502 tonnes in 2005 (the
most recent published data (FAO, 2007)), of which 60.2% (302
tonnes) was landed by France, and capture production of
Copyright r 2009 John Wiley & Sons, Ltd.
‘D. oxyrinchus’ was reported as 49 tonnes, landed exclusively
by France (FAO, 2007). However, skate landings are not
usually recorded on a species-specific basis by most nations
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326
S. P. IGLÉSIAS ET AL.
Table 3. Polymorphic sites within and between mtDNA (12S-16S rRNA region) of Dipturus cf. flossada and D. cf. intermedia. (n 5 sample size;
5 diagnostic specific-characters)
haplotype
n
Position of polymorphic sites
2
2
D. cf. flossada
D. cf. intermedia
hap-1
hap-2
hap-1
hap-2
hap-3
4
1
3
1
1
6
2
1
8
7
5
2
5
8
4
7
9
0
8
1
1
9
9
1
2
5
0
G
.
A
A
A
T
.
C
C
C
A
.
G
G
G
T
.
—
—
—
C
.
G
G
G
T
.
C
C
C
A
.
G
G
G
C
.
T
T
T
1
4
2
0
1
5
0
0
G
.
.
A
.
G
.
T
T
T
1
5
0
5
1
5
1
0
C
.
T
.
T
T
.
C
C
C
C
.
T
T
T
A
.
G
G
G
C
.
T
T
T
G
.
A
A
A
T
.
C
C
C
A
.
G
G
G
A
.
G
G
G
T
.
A
A
A
A
.
C
C
C
1
5
1
4
1
6
7
4
1
6
9
8
1
8
6
4
1
9
0
6
1
9
2
1
1
9
4
1
2
0
0
0
2
0
0
4
2
1
0
2
2
2
4
3
2
4
8
2
2
5
5
8
A
G
.
.
.
T
.
.
.
C
C
.
T
.
T
C
.
T
T
T
The 20 diagnostic specific characteristics enable a clear unambiguous genetic distinction between the two species. (For D. cf. flossada hap-1 is for the
vouchers BPS-569, 574, 583 and 584, hap-2 is for the voucher 054; for D. cf. intermedia hap-1 is for the vouchers BPS-573, 575, 586, hap-2 is for the
voucher 213 and hap-3 is for the voucher 570.)
Figure 5. Comparison of the sexual maturations of Dipturus cf. flossada and D. cf. intermedia. (A) Relationships between clasper length and total
length for D. cf. flossada males (n 5 465 for immature individuals and n 5 131 for mature individuals with calcified claspers) and for D. cf. intermedia
(n 5 566 for immature individuals and n 5 5 for mature individuals). (B) The logistic relationships for D. cf. flossada (blue curves) and D. cf.
intermedia (red curves) between the proportion of mature males/females and total length. (n 5 770 and 981 for males, and n 5 659 and 1022 for
females of D. cf. flossada and D. cf. intermedia, respectively).
Copyright r 2009 John Wiley & Sons, Ltd.
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
(FAO, 2007), and so official species-specific landings data for
skates are greatly underestimated. This is problematic, as stable
catches of species aggregated under a single landing name can
mask the population decline of individual species (Dulvy et al.,
2000). Our extensive fishery survey highlights a significant
discrepancy between official fishery statistics and the ‘true’
landed species (Table 4). The corrected species composition
landed by France in 2005 under the names ‘D. batis’ and
‘D. oxyrinchus’ is estimated (Figure 6). This reveals that the
blue skate and the flapper skate are mostly landed under
the names ‘D. batis’ and ‘D. oxyrinchus’ respectively, whereas
the newly exploited Norwegian skate ‘D. nidarosiensis’ is
similarly landed under these two names. As a consequence,
the decreasing catches of these large skates under the two
landing names have been partially masked in the past 20 years
by the increasing catches of the deeper-dwelling D. nidarosienis.
This is explained by the re-direction of fishing effort to deeper
water following depletion of catches on the continental shelf.
The extensive survey of French landings under the names ‘D.
batis’ and ‘D. oxyrinchus’ allows an estimate of the correct
weight and number of specimens landed on a species-specific
basis to be made (Figure 7, Table 5). It is estimated that the true
2005 French landings mostly comprise D. cf. flossada (about 222
tonnes/94000 individuals). D. cf. intermedia and D. nidarosiensis
are much less abundant in landings (about 76.6 tonnes/23500
individuals and 51.5 tonnes/6400 individuals respectively).
Finally it is estimated that only a small weight and number of
individuals of both D. oxyrinchus and R. alba have been landed
in 2005, much less than the 49 tonnes published for
D. oxyrinchus in the official FAO fishery statistics (FAO, 2007).
A detailed and extensive survey of the skate fishery was
undertaken in French ports in 1964/1965 (Du Buit, 1968),
permitting some comparison with 2006/2007 data. The
population collapse is more evident in the larger skate species
than for other landed skates. The species landed as ‘D. batis’
and ‘D. oxyrinchus’ represented 26.5% of the total skate weight
landed in 1964 in the port of Concarneau (Du Buit, 1968),
whereas it only comprised 12.1% in 2006 (including the
Norwegian skate which had not been landed in 1964).
Between 1964 and 2006, landings under the names ‘D. batis’
and ‘D. oxyrinchus’ decreased by 95.4% in the port of
Concarneau and by 91.7% in the port of Lorient (Figure 8).
Such declines need to be viewed in the context of spatial and
temporal changes in fishing patterns and effort as well as
management actions, therefore it is not possible to estimate
proportional declines in the populations. Between 1964 and
2006 it is estimated that landings of R. alba were reduced by
99.470.5% in the port of Concarneau (9 tonnes in 1964 to
0.05870.046 tonnes in 2006). The use of the latter landing name
is now discontinued in French fishmarkets and it is now only
known by the oldest fishermen and fishmarket workers. In 1964,
the corrected landings of D. oxyrinchus were estimated to be 22
and 50.7 tonnes in the ports of Concarneau and Lorient
respectively, whereas the near-disappearance in landings was
noted by 2006. Despite the high sampling effort only single
individuals of both the longnosed skate (October 2007) and the
white skate (January 2007) were recorded during the current
fishmarket survey, and the only previous observations of landed
longnosed skate and white skate specimens go back to June and
March 2004 respectively (when specimens were sampled for
genetic analysis). In 1964, 58.944 tonnes of R. alba were landed
in the port of Douarnenez, when this species was targeted by a
Copyright r 2009 John Wiley & Sons, Ltd.
327
longline fishery (Du Buit, pers. commun.). When this stock
collapsed over the next few years, so too did the fishery.
Fishing effort tends to reduce the size of fish in an exploited
stock (Pauly et al., 2002) so this generally has a direct effect on
the relative frequency of adults. To evaluate the effect of the
fishing effort on D. cf. flossada and D. cf. intermedia, the size
distribution and the proportion of mature specimens in landings
were observed. As these observations were not carried out at the
beginning of the fishery, it is not possible to observe the effect of
fishing effort over time. D. nidarosiensis is a new commercial fish
which has appeared progressively in landings over the last 20
years with the development of the deep-sea fishery in European
waters. Subsequently, the size distribution and the proportion of
mature individuals in landings of this species could be used as a
near ‘zero-point’ for D. cf. flossada and D. cf. intermedia
(Figure 9). For D. nidarosiensis the average size of landed
individuals corresponds to 57.4% of the maximum size observed
for that species (Figure 9(A)), whereas it is 47.0% for D. cf.
flossada (Figure 9(B)) and only 32.0% for D. cf. intermedia
(Figure 9(C)). This suggests the specimens landed are
comparatively much smaller for D. cf. intermedia than for the
other two species. For chondrichthyans there is a very close
relationship between stock size of mature females and
recruitment (Ellis et al., 2005). It is estimated that adults
represent only 0.6% of the 2005 French landings of the flapper
skate (whereas it is estimated that adults comprise 8.9% and
13.3% for D. cf. flossada and for D. nidarosiensis landings
respectively) (Table 5). This equates to estimates of 140 adult
individuals of flapper skate landed by France in 2005 (compared
with about 8300 and 850 for D. cf. flossada and for
D. nidarosiensis, respectively) (Table 5). These data indicate a
strong collapse of the adult breeding population of flapper
skate, resulting in a decrease of recruitment and acceleration of
the global collapse of the species. The collapse of adults is not
surprising, given the late age at maturity for this species, and
reflects the fact that individuals are more likely to succumb to
fishing mortality than attain sexual maturity. Historic literature
and the polling of old fishery professionals reveal that large
specimens of flapper skate were very abundant in former years,
indicating that the abnormally low proportion of adults in
current catches cannot be explained by an under-capture
of adults for this species. As a conclusion, the gradual
decrease of the average size of landed specimens and the
gradual decrease of the adult proportion when comparing
D. nidarosiensis with D. cf. flossada and D. cf. intermedia are
assumed to reflect various fishing efforts and effects on the three
species populations. For all three species the adults are much
more abundant than large immatures, suggesting that when
maturity is attained their growth rate reduces considerably or
stops. Consequently old adults accumulate in the largest size
classes. Theoretical graphs on skate size distribution have been
produced, based on the above size distribution and maturity
frequency observations for all three skate species and illustrating
different stages in skate stock exploitation. (Figure 10).
DISCUSSION
Nomenclature revision
Three large species of Dipturus (excluding the smaller and
more northern D. linteus (Fries, 1838)) are currently
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
Copyright r 2009 John Wiley & Sons, Ltd.
Total
9686.97
Total
Loctudy
Le Guilvinec
Lorient
1441.01
2380.44
1.25
3420.42
9
5.06
0
0
0
0
0
0
461.59
64
0
0
0
0.9
1877.84
21.1
0
0
0
4.36
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
Concarneau
‘D. batis’
Identified species (X)
Fishmarket (i)
14081.34
4394.37
214.06
2999.31
0
361
0
1
85.5
603.5
0
124
0
6
0
0
0
0
0
0
0
0
0
0
0
0
‘D. oxyrinchus’
wXai
2609
300
736
1
438
1
2
0
0
0
0
0
0
87
1
0
0
0
1
1024
11
0
0
0
7
‘D. batis’
4110
1501
84
1150
0
24
0
1
16
212
0
13
0
1
0
0
0
0
0
0
0
0
0
0
0
0
‘D. oxyrinchus’
nXai
68
10
0
57
0
—
—
—
—
—
—
—
19
0
—
0
—
—
66
0
—
0
—
—
‘D. batis’
2
7
—
3
—
—
3
0
—
2
—
—
—
—
—
—
—
—
—
—
—
—
—
—
‘D. oxyrinchus’
nXai (adults)
Weight (Kg) and number of specimens sampled in 2006–2007 under the landing names ‘D. batis’ and ‘D. oxyrinchus’
Table 4. Detailed species composition as weight (wXai) and number of specimens (nXai) landed under the names ‘Dipturus batis’ and ‘D. oxyrinchus’ observed during the 2006/2007 fishery survey in
French ports, with detailed species composition (number of specimens) for adult specimens (nXai (adults))
328
S. P. IGLÉSIAS ET AL.
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TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
329
Figure 6. Estimation of the corrected species composition (as percentage of total weight and total number of individuals) landed by France in 2005
under the name (A) ‘Dipturus batis’, (B) ‘D. oxyrinchus’ and (C) the sum of ‘D. batis’1‘D. oxyrinchus’ (proportions based on Table 5).
Figure 7. Estimation as (A) total weight and (B) total number of individuals of the corrected species composition landed by France in 2005 under the
name ‘Dipturus batis’ and ‘D. oxyrinchus’ (see Table 5 for accurate data).
recognized in the North-eastern Atlantic ocean: D. batis
(Linnaeus, 1758), D. oxyrinchus (Linnaeus, 1758) and
D. nidarosiensis (Storm, 1881). In contrast, this present study
reveals the existence of four distinct species in the area (named
D. cf. flossada, D. cf. intermedia, D. oxyrinchus and
D. nidarosiensis in the present paper). Re-examination of all
original descriptions of European Dipturus reveals that most
are too brief to permit an accurate identification of the species,
and in all likelihood some have confused several species under
a single name. Moreover, the absence of most type specimens
make the taxonomic revision of the group difficult. Four
nominal species (Raja macrorynchus Rafinesque, 1810;
Raja flossada Risso, 1826; Raia intermedia Parnell, 1837 and
Raia gaimardi Valenciennes, 1851) were up until now
recognized as junior synonyms of D. batis. The brief
description of D. batis by Linnaeus does not permit one to
determine to which of the two species distinguished in the
present paper his description refers. In this case, the
application of the principle of priority of the international
code of zoological nomenclature (International Commission
on Zoological Nomenclature, 1999) for the validity of scientific
Copyright r 2009 John Wiley & Sons, Ltd.
names is not possible. Therefore, we focused on researching
the oldest descriptions for which it is possible to recognize a
species without ambiguity. The description of D. flossada
(Risso, 1826) is the oldest description that fits this category.
Risso (1826) noted his species possessed a ‘whitish iris’ and
attained a size of approximately 120 cm. According to our
results, these characteristics are species-specific. The
description of D. intermedia Parnell (1837) is the oldest
description permitting us to recognize this second species
without ambiguity. Parnell (1837) noted the coloration of his
species as ‘body above, dark olive green’ and ‘it is
distinguished from R. batis (we named it D. cf. flossada) by
the snout being longer and the first dorsal fin being more
remote from the second’. We also noted these characteristics as
specific to this species. The formal revision of the Dipturus
species from the North-eastern Atlantic, with the resurrections
and fully documented redescriptions of both D. cf. flossada
and D. cf. intermedia will be finalized in a specialized journal.
The provisional names D. cf. flossada and D. cf. intermedia are
used in this paper instead of D. flossada and D. intermedia,
until the latter are formally resurrected and validated by the
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
330
S. P. IGLÉSIAS ET AL.
Table 5. Corrected estimation of (A) weight, (B) number of specimens and (C) number of adult specimens of each species landed in France in 2005
under the names ‘Dipturus batis’ and ‘D. oxyrinchus’ (weight in kg)
A
Estimated weight landed in 2005 in France under the names ‘D. batis’ and ‘D. oxyrinchus’ (Wxa)
Identified species (X)
‘D. batis’
‘D. oxyrinchus’
‘D. batis’ 1 ‘D. oxyrinchus’
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
21705877020
3991977918
16712
4438379429
117789
5077771
487471681
3666075930
0
714575914
0
3217472
22193278701
76579713848
16712
51528715343
117789
82871243
Total
302000
49000
351000
B
Estimated number of specimens landed in 2005 in France under the names ‘D. batis’ and ‘D. oxyrinchus’ (Nxa)
Identified species (X)
‘D. batis’
‘D. oxyrinchus’
‘D. batis’ 1 ‘D. oxyrinchus’
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
93011735534
1051573347
13710
568371279
13710
68271021
9797343
1302472632
0
7287807
0
55780
93990735877
2353975979
13710
641172086
13710
73771101
Total
109917736605
1478672257
124703745063
C
Estimated number of adults landed in 2005 in France under the names ‘D. batis’ and ‘D. oxyrinchus’ (NXa (adults))
Identified species (X)
‘D. batis’
‘D. oxyrinchus’
‘D. batis’ 1 ‘D. oxyrinchus’
D. cf. flossada
D. cf. intermedia
D. oxyrinchus
D. nidarosiensis
R. alba
other skates
817571265
129731
0
7407188
0
—
163746
1174
0
111797
0
—
833871311
140735
0
8517285
0
—
Figure 8. Comparison between 1964 and 2006 landings under the names ‘Dipturus batis’1‘D. oxyrinchus’ for the French ports of Concarneau and Lorient.
International Commission on Zoological Nomenclature. The
usage of common names in the past has also been highly
confused and in the current paper we use the common names,
‘common skate’ for the ‘D. batis’ species-complex (D. cf. batis
1D. cf. intermedia), ‘blue skate’ for D. cf. flossada and ‘flapper
skate’ for D. cf. intermedia, according to their most frequent
usage in scientific records.
Revisions of incorrect synonymizations (called species
resurrections) are common works for systematists, but in the
present case the resurrection of D. cf. intermedia is of great
Copyright r 2009 John Wiley & Sons, Ltd.
conservation significance. The depletion of this species in the
catch record has been masked by confusion with specimens of
the comparatively less threatened populations of D. cf.
flossada. Molecular genetics has been of great use for
recognition of these threatened species of skate as shown
previously for others species (Avise, 1989; Baker et al., 2003;
Marko et al., 2004). This technique combined with
morphology and life history investigations clearly show that
D. cf. flossada and D. cf. intermedia are distinct and should be
resurrected as valid species. A formal review with fully
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
TAXONOMIC CONFUSION AND MARKET MISLABELLING OF THREATENED SKATES
331
Figure 9. Distribution of skate size observed in the 2006/2007 French landings for (A) the newly exploited species Dipturus nidarosiensis (n 5 321),
(B) The long-term and over-exploited D. cf. flossada (n 5 1384), and (C) the long-term and highly over-exploited D. cf. intermedia (n 5 1968).
A comparison of these size distributions reveals from A to C the relative decrease of larger specimens and adults and the decrease in average size of
landed specimens related to the maximum length of each species.
documented re-descriptions of both species is now required.
Without revision and recognition of its distinct status, D. cf.
intermedia, the world’s largest skate (Muus et al., 2005; Froese
and Pauly, 2009), could become extinct in the near future.
Conservation outcome
It is likely that D. cf. intermedia is more vulnerable to fishing
mortality than D. cf. flossada, because the former is
significantly larger and attains sexual maturity at a later age,
therefore the probability of an individual being captured
before successful reproduction is greater. The catastrophic
decline of the D. batis species-complex in landings and the
collapse of the spawning stock of D. cf. intermedia suggest that
both species (D. cf. flossada and D. cf. intermedia) should
remain listed as Critically Endangered (CR) on the IUCN Red
List. The species-complex D. batis is listed by IUCN with
the criteria ‘A2bcd14bcd’, meaning the reduction of the
population size was Z80% over the last 10 years or three
generations. Taxonomic confusion of the species prevents
verification of these criteria for each species individually;
however, the results of this study lead us to believe that this is
a reasonable assumption for both species. The potential
irreversible decline and local extinction of white skate and
longnosed skate discovered by this survey (with only single
specimens occasionally recorded in the European Atlantic),
Copyright r 2009 John Wiley & Sons, Ltd.
suggests that these species should be upgraded immediately to
Critically Endangered status according to IUCN Red List
criteria. As the Norwegian skate is newly exploited, a decrease
in its populations is not yet apparent, but the status of its
relatives with similar limiting life-history characteristics suggests
that this species will collapse in future years if fishing pressure is
maintained at the current level. Thus, it is proposed that this
species should be considered as Near Threatened.
The ICES Working Group on Elasmobranch Fishes (ICES
WGEF), under the Advisory Committee (ACOM), provides
advice on the status and management of sharks and rays in the
North-east Atlantic Ocean. In 2008, ICES noted that common
skate is depleted in the Celtic and North Seas, Skagerrak and
English Channel and advised no target fishing and that bycatch
should be minimized. They also noted that white skate is
severely depleted in the Celtic Seas and advised zero catch,
prohibition on landing and the highest possible protection
(ICES, 2008). These species (common skate and white skate)
were also recently listed on The Oslo-Paris Convention for the
Protection of the Marine Environment of the North-east
Atlantic (OSPAR), which highlights priority species for further
research and can stimulate regulation through management
bodies by drawing attention to the need for their protection.
Lately the European Union TAC and Quota Regulation for
2009 (European Union, 2009) prohibits retention of common
skate, Norwegian skate and white skate on board and requires
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 319–333 (2010)
332
S. P. IGLÉSIAS ET AL.
Figure 10. Theoretical curves of the distribution of skate size representing the effect of fishing effort on the composition (size and maturity) of skate
populations. (A) Size distribution of a newly exploited species and (B) Size distribution of an over-exploited species.
that catches shall be promptly released unharmed to the extent
practicable in all Community waters. It also encouraged fishers
to develop and use techniques and equipment to facilitate the
rapid and safe release of the species. However, these species are
mostly caught by trawling and discard survival is unknown and,
depending on depth, tow duration and catch levels, could be low
and therefore of no benefit to their conservation. The case of the
dramatic reductions and extirpations of the largest European
skates needs to be better addressed by fisheries managers and
the utility of other management measures (e.g. closed areas)
needs to be evaluated. Furthermore, this unfortunate example
of taxonomic confusion masking the decline of a critically
depleted species highlights the importance of improving
accurate identification and data collection in fisheries and
reminds us of the great significance of systematics as the
foundations on which all other biological sciences are build.
This study concludes that long-term taxonomic confusion of
these species has hindered the effectiveness of conservation
action plans and immediate revision of their conservation status
is imperative. The risk of extinction of these depleted species is
higher than previously assessed and appears unavoidable
without immediate and incisive conservation action.
ACKNOWLEDGEMENTS
For support we thank the ‘Conseil Régional de Bretagne’;
Marie-Henriette Du Buit and Bertrand Richer de Forges (IRD)
Copyright r 2009 John Wiley & Sons, Ltd.
for constructive discussion, Sarah Valenti and Sarah Fowler
(IUCN-SSG), Mathilde van der Merwe (Stellenbosch University),
Esmee van Wijk (CSIRO) and Amélia Curd (MNHN) for
comments and corrections to the manuscript, fishermen and
fishmarket workforce for making the sampling easier.
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