Biologia 69/5: 696—704, 2014
Section Zoology
DOI: 10.2478/s11756-014-0347-y
Age-related differences in prey-handling efficiency and feeding
habitat utilization of Squalius carolitertii (Cyprinidae)
according to prey trait analysis
Javier Sánchez-Hernández
Department of Zoology and Physical Anthropology, Faculty of Biology. University of Santiago de Compostela. Campus Sur
s/n, 15782 Santiago de Compostela, Spain
Station of Hydrobiology “Encoro do Con”, Castroagudín s/n, 36617 Vilagarcía de Arousa, Pontevedra, Spain; e-mail:
[email protected]
Abstract: Multivariate prey trait analysis is a functional approach to understand predator-prey relationships. Here, seven
macroinvertebrate ecological traits have been used for the analysis of trophic ecology of co-occurring age classes of Northern
Iberian chub Squalius carolitertii, a cyprinid fish species. The present study identified several key factors in the handling
efficiency and habitat utilization for feeding of S. carolitertii that may have a wider application, particularly for other
cyprinid species. The results revealed a remarkable similarity in the feeding behaviour among age classes, suggesting a
foraging behaviour convergence among them in both prey-handling efficiency and feeding habitat utilization. Nevertheless,
some age classes showed clear preferences for particular categories of ecological trait; for example, age 1 showed a clear
ability to feed on flattened prey items, whereas ages 2 and 3 were able to feed on preys with different body shape due to
their general distribution in the fuzzy principal component analysis (FPCA). Finally, this study shows how multivariate
approaches can complement traditional diet analyses, and the method has wide applicability across life-stages of cyprinid
species.
Key words: diet; multivariate approaches; Iberian Peninsula; Cyprinidae; chub
Introduction
A knowledge of the foraging ecology of fishes is fundamental to understanding the processes that function at
the individual, population and community levels since
the factors that influence the acquisition and assimilation of food can have significant consequences for the
condition, growth, survival and recruitment of fishes
(Nunn et al. 2012). In this context, the knowledge on
how prey-handling efficiency and feeding habitat utilization are shared among individuals of the same population is critical for understanding the fish ecological
requirements and its functioning.
The Northern Iberian chub, Squalius carolitertii
(Doadrio, 1988), is a small endemic cyprinid inhabiting the rivers of the Iberian Peninsula across a large
area, including the Douro, Mondego, Lima, Minho, and
Lérez basins (Doadrio 1988, 2001; Carmona & Doadrio 2000). Recently, Perea et al. (2011) reported this
species for the first time from the upper reaches of
the Alberche River (a tributary of the Tagus basin in
central Spain) and in the Oitavén River (a tributary
of the Verdugo River in northwestern Spain). Except
for the populations in the Tagus basin, this species is
listed as vulnerable (VU) in the Spanish Red Data Book
(Doadrio 2001) and was recently upgraded as endanc 2014 Institute of Zoology, Slovak Academy of Sciences
gered (EN) (Doadrio et al. 2011), but is in contrast
recorded as least concern (LC) in both the IUCN Red
List of Threatened Species (Crivelli 2006) and the European Red List of Freshwater Fishes (Freyhof & Brooks
2011). Fortunately, papers published on this fish species
in recent years have provided knowledge about some aspects of its biology such as habitat requirements (Carmona & Doadrio 2000; Santos et al. 2004; Maia et al.
2006), population parameters, growth and reproduction
(Maia et al. 2006), genetics, morphology and phylogeny
(Coelho et al. 1995; Zardoya & Doadrio 1998; Gómez
& Lunt 2007; Cunha et al. 2009) and feeding behaviour
(Sánchez-Hernández & Cobo 2011, 2012).
Multivariate approaches like prey trait analysis
have been proposed as a functional approach to evaluate the potential vulnerability of invertebrates to fish
predation (de Crespin de Billy 2001; de Crespin de
Billy & Usseglio-Polatera 2002). Advantages and disadvantages of prey traits analysis and its application in
different freshwater species to study feeding behaviour
have been addressed elsewhere (Sánchez-Hernández et
al. 2011b), suggesting that this methodology provides
highly valuable ecological information on the mechanisms involved in predator–prey relationships, and
thus constitutes a useful complement to traditional diet
analysis (de Crespin de Billy & Usseglio-Polatera 2002;
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Ontogenetic dietary shifts in a cyprinid fish species
Sánchez-Hernández & Cobo 2011; Sánchez-Hernández
et al. 2011b, 2012). However, although diet, food selection and ontogenetic dietary shifts of S. carolitertii
have been described previously in the Iberian Peninsula
(Sánchez-Hernández & Cobo 2011, 2012), differences in
the prey-handling efficiency and habitat utilization for
feeding among age classes are unknown. Hence, a better knowledge on this subject would provide important
information on the feeding behaviour of S. carolitertii, helping to understand ontogenetic variation in the
resource partitioning. For this reason, the aim of to
the present study was to explore potential ontogenetic
shifts in the handling efficiency and habitat utilization
for feeding of S. carolitertii in an Iberian river during
summer.
Material and methods
Study area
The study site (altitude 1051 m a.s.l.) is located in the
Tormes River (Ávila, central Spain; UTM: 30T 288707
4466342), a tributary of the Duero River (897 km total
length) (Fig. 1). The Tormes River has a catchment area
of 7096 km2 and a total length of 284 km. Geologically,
the Tormes basin is located in a great batholith with relatively uniform mineralogical granite composition (AlonsoGonzález et al. 2008). The basin includes a mixture of agricultural and relatively undisturbed areas, with small rural areas interspersed. The vegetation structure comprises
a series of extended grazing lands with Scots pine (Pinus
sylvestris) and rebollo oak (Quercus pyrenaica) forests. The
climate is typically continental, with high differences between extreme temperatures in summer and winter. The
studied site does not have any significant flow regulation
structure, and the flow regime shows a great variability
(Alonso-González et al. 2008).
At the time of the field survey, the average water temperature was 18 ◦C and conductivity and pH was
28.8 µS cm−1 and 6.4, respectively. Dissolved oxygen levels
were high (91.5% and 8.7 mg L−1 ). Deciduous riparian vegetation was principally composed of alder (Alnus glutinosa),
ash (Fraxinus angustifolia) and willow (Salix spp.), and the
bottom substrate of the river section consisted of boulders,
gravel and sand. Additional information about both macrobenthos and fish community of the study area can be
found in Sánchez-Hernández (2011) and Sánchez-Hernández
& Cobo (2011), respectively.
Fish collection
The study was conducted in a wadeable riffle section of the
river, and samples were collected in August 2010. Fish were
collected using pulsed direct-current backpack electrofishing
equipment (Hans Grassl GmbH, ELT60II). For the purpose
of the study, 57 S. carolitertii were captured and immediately killed by an overdose of anaesthetics (benzocaine),
and thereafter transported in coolboxes (approx. 4 ◦C) to the
laboratory, where they were frozen at –30 ◦C until processed.
Fork length of S. carolitertii ranged from 4.4 to 14 cm (mean
fork length ± standard error = 6.5 cm ± 0.28). The age of
fishes was determined by scale reading and by length frequency analyses (LFA) with the Petersen’s method. The
sample included specimens from one to five years: nage1 =
35, nage2 = 13, nage3 = 7 and nage5 = 2. No S. carolitertii of
age 4 were collected and fishes of age 5 were not included in
the diet analysis due to only two specimens were captured.
697
Diet analysis
In the laboratory the fish were dissected and their gastrointestinal tracts removed. No empty gastrointestinal tracts
were observed. Prey items were allocated to main diet categories as follows: aquatic invertebrates, terrestrial invertebrates, and other prey items. Animal prey items were subsequently identified to the lowest taxonomic level possible.
The abundance of detritus was not quantified because it was
impossible to count individual items, but the number of gastrointestinal tracts in which it was found, it was noted. To
describe the diet, the data are presented as relative abundance (Ai = (ΣSi /ΣSt ) × 100, where Si is the stomach content (number) composed by prey i, and St the total stomach
content of all stomachs in the entire sample) and frequency
of occurrence of prey (Fi = (Ni /N ) × 100, where Ni is the
number of fishes with prey i in their stomach and N is the
total number of fishes with stomach contents of any kind)
(Amundsen et al. 1996).
To evaluate the potential vulnerability of invertebrates
to fish predation, de Crespin de Billy & Usseglio-Polatera
(2002) created a total of 71 different categories for 17 invertebrate traits (see trait categories used in this study in
Table 1). Information was structured using a ‘fuzzy coding’
procedure (Chevenet et al. 1994). A score was assigned to
every taxon describing its affinity for each trait category,
with ‘0’ indicating ‘no affinity’ to ‘5’ indicating ‘high affinity’ (de Crespin de Billy & Usseglio-Polatera 2002). The
taxonomic resolution (order, family or genus) used in the
classification process corresponded to the lowest possible
level of determination of taxa in fish gut contents. When
the identification to genus was not possible or in the case
of missing information for a certain genus, the value assigned for a trait was the family level, using the average
profile of all other genera of the same family, as recommended by de Crespin de Billy & Usseglio-Polatera (2002)
and Rodrígues-Capítulo et al. (2009). The same prey trait
database as de Crespin de Billy (2001) and de Crespin de
Billy & Usseglio-Polatera (2002) was used to make prey trait
analyses. Indeed, the complete list of taxa and scores used
in the prey trait analysis are provided as online supplementary material (Appendix A). Thus, in the present study,
Copepoda, Leptoceridae and Arachnida were not included
in the analysis because trait values are still not available. In
total, seven macroinvertebrate ecological traits were chosen
for the study of handling efficiency (‘agility’, ‘body flexibility’, ‘body shape’ and ‘concealment’ traits) and feeding
habitat utilization (‘macrohabitat’, ‘current velocity’ and
‘substratum’ traits) of S. carolitertii (see trait categories in
Table 1).
Prey trait analyses were conducted using the free software R (version 2.11.1). A fuzzy principal component analysis (FPCA) was used to analyse prey-handling efficiency
and feeding habitat utilization according to the specific prey
items consumed by the fish. This multivariate approach
(FPCA) is a robust method that diminishes the influence of
outliers and it has been widely used by scientist in different
topics (e.g. Cundari et al. 2002; Sârbu & Pop 2005). Affinity scores were rescaled as proportions (sum = 1) for each
taxon, thus, representing the probability that any taxon
belonged to a particular category. For example, if a given
taxon at a specific trait with three categories has an assigned affinity code of 0.25/0.15/0.60 based on information
from the primary literature, it becomes 25%/15%/60% for
the analysis. Then, to describe both prey-handling efficiency
and feeding habitat utilization of S. carolitertii in terms of
trait relative abundance, the proportion of each category
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J. Sánchez-Hernández
Table 1. Traits, categories and codes used in analyses and graphics. Based on de Crespin de Billy & Usseglio-Polatera (2002).
Trait
Categories
Code
Trait (continued)
(1) Macrohabitat
Hyporheic ‘burrower’
hypo.b (4) Agility
Hyporheic ‘interstitial’ hypo.i
Epibenthic depositional epi.d
Epibenthic erosional
epi.e
Water column
water (5) Concealment
Categories
Code
None (sluggish)
Weak
High
none
weak
high
Fixed accessory (nets, retreats)
net
Movable accessory (cases/tubes) case
Solidly coloured
sold.c
Variable
var.c
(2) Current velocity (cm/s) Still (0–5)
Slow (5–25)
Moderate (25–75)
Fast (>75)
0.5
5.25
25.75
>75
(3) Substratum (mm)
mud
silt
sand
gravel
cobble
bloc
(7) Body flexibility
None (<10◦ )
bryo (including cases/tubes) Weak (10–45◦ )
bryo-o
High (>45◦ )
root
detr
Mud
Silt (0.001–0.2)
Sand (0.2–2)
Fine gravel (2–8)
Gravel-Cobble (8–256)
Blocks (>256)
Bryophytes
Other macrophytes
Roots
Litter, organic detritus
(6) Body shape
Patterned
(including cases/tubes) Cylindrical
Spherical
Conical
Flattened
Streamlined
patt.c
cyl
sph
con
flat
strl
none
weak
high
Table 2. Diet composition in age groups of Squalius carolitertii from the Tormes River, central Spain. Abundance (Ai %) and frequency
of occurrence (Fi %).
Age 1
Aquatic invertebrates
Hydracarina
Copepoda
Baetis spp.
Epeorus spp.
Habrophlebia sp.
Leuctra geniculata Stephens, 1836
Aphelocheirus aestivalis (F., 1794)
Elmis sp.
Hydropsyche spp.
Leptoceridae
Allogamus sp.
Chimarra marginata (L., 1761)
Polycentropus sp.
Rhyacophila spp.
Tanypodinae
Simuliidae
Terrestrial invertebrates
Trichoptera
Ephemeroptera
Diptera
Formicidae
Coleoptera
Arachnida
Other prey items
Fish
Detritus
Age 2
Age 3
Ai (%)
Fi (%)
Ai (%)
Fi (%)
Ai (%)
Fi (%)
4.5
0.6
24.4
2.6
1.3
–
1.3
0.6
4.5
–
–
0.6
–
2.6
3.8
42.3
5.7
2.9
42.9
11.4
5.7
–
5.7
2.9
17.1
–
–
2.9
–
11.4
14.3
51.4
33.3
–
20.4
3.7
–
–
–
–
3.7
–
–
–
–
1.9
1.9
25.9
23.1
–
53.8
15.4
–
–
–
–
15.4
–
–
–
–
7.7
7.7
15.4
–
–
79.2
2.6
–
0.6
–
–
–
0.6
3.9
–
1.9
0.6
2.6
3.2
–
–
57.1
42.9
–
14.3
–
–
–
14.3
57.1
–
42.9
14.3
42.9
42.9
1.9
1.3
0.6
5.1
0.6
1.3
8.6
5.7
2.9
17.1
–
5.7
14.3
–
14.3
14.3
14.3
–
–
65.7
7.7
–
–
23.1
–
7.7
–
–
53.8
1.9
–
0.6
0.6
0.6
–
–
–
1.9
–
–
5.6
–
1.9
–
–
–
0.6
–
14.3
28.6
per trait was multiplied by the relative abundances of the
diet for each fish age class (prey items × trait-category matrix). The resulting trait-by-age-class array contained the
relative abundance of each trait category in each age class,
and this new array was used for the multivariate analysis.
Multivariate analysis and graphical outputs were computed
with ADE-4 software (Thioulouse et al. 1997). In order to
explore the statistical significance between-group analysis
(here age classes) a permutation test (Monte-Carlo test) was
used (see Thioulouse et al. 2012 for further details), all tests
were considered statistically significant at P < 0.05.
Results
In general, the diet varied with fish age (Table 2), with
the most abundant prey item differing in each age class:
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Ontogenetic dietary shifts in a cyprinid fish species
699
Fig. 1. Map of Europe and Duero basin (Iberian Peninsula) showing the sampling site in the Tormes River, central Spain.
Table 3. Scores of eigenvalues extracted by fuzzy principal component analysis (FPCA) for each trait.
Trait
Agility
Concealment
Body flexibility
Body shape
Macrohabitat
Current velocity
Substratum
Eigenvalue of axis 1
0.9242
0.5239
0.8086
0.8613
0.6992
0.2482
0.4057
Eigenvalue of axis 2
0.4173
0.3997
0.4059
0.2577
0.2973
0.163
0.112
Simuliidae (42.3%) dominating in age 1, Hydracarina
(33.3%) in age 2, and Baetis spp. (79.2%) in age 3.
Piscivory was observed in only one S. carolitertii (age
3, 10.8 cm fork length, FL), whereas the occurrence of
detritus decreased with the age (67.5%, 53.8% and 28.6
in age 1, age 2 and age 3, respectively).
Diagrams of the prey trait analyses are shown in
Figs 2 and 3. The two first axes were sufficient to illustrate the relationships among faunal groups according
to their combinations of traits (‘eigenvalues’ in Table 3),
and accounted for >65% of the total variability in all
cases (65.1% in ‘concealment’ trait and 100% in ‘agility’
and ‘body flexibility’ traits). The permutations test of
FPCA confirmed that handling efficiency and feeding
habitat utilization traits overlapped greatly among age
classes (P > 0.05 in all the cases), although some important differences were found for the prey utilized by
age classes in some traits like, for example, ‘agility’,
‘concealment’, ‘body shape’ and ‘macrohabitat’ traits.
For the ‘agility’ trait (Fig. 2A), all cohorts showed
a high overlap with ellipses generally displaced to the
right part of the FPCA, and towards ‘none’ category.
However, the ellipse of age 2 was slightly displaced to
the upper left quadrant of the FPCA, which reveals a
higher contribution in specific abundance of prey items
with high agility. ‘Concealment’ trait (Fig. 2C) showed
that individuals of age 3 showed the highest prey spec-
Eigenvalue of axis 3
–
0.3491
–
0.1508
0.1902
0.06593
0.0643
Eigenvalue of axis 4
–
0.1452
–
0.04039
0.08108
–
0.039
trum with a clear tendency to feed on prey items with
fixed accessories (nets and retreats), whereas age 1 and
age 2 showed the narrowest distribution of FPCA values with a central position in the diagram, demonstrating that these age classes tended to feed on aquatic prey
with patterned or varied concealment. Also for the morphological trait ‘body shape’ (Fig. 2G), a high overlap
was found among age classes. However, age 1 was displaced to the lower left quadrant of the FPCA, preferring to feed on flattened prey items. No clear differences
were in contrast found in age 2 and age 3, and both age
classes had similar distributions in the FPCA. Age 2
showed the smallest distribution of values in the FPCA
according the ‘macrohabitat’ trait (Fig. 3A). Nevertheless, all age classes were located in a central position of
the FPCA diagram, which reveals a clear tendency to
feed on prey items whose macrohabitat was assigned as
‘hyporheic burrower’ and ‘hyporheic interstitial’.
Discussion
The dietary composition of S. carolitertii has previously been described for populations of central Spain
(Sánchez-Hernández & Cobo 2011, 2012). In contrast to
these previous studies, which studied summer food resource partitioning between four sympatric fish species
(Sánchez-Hernández & Cobo 2011) and the ontogeUnauthenticated
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700
J. Sánchez-Hernández
Fig. 2. Biplots of handling efficiency traits obtained from a fuzzy principal component analysis (FPCA). Position of sampling sites
depending on the prey present in gut contents (A, C, E, G) and axes interpretation (B, D, F, H), including the histogram of eigenvalues.
Ellipses envelop weighted average of prey taxa positions consumed by each age class of Squalius carolitertii: Labels (Age1, Age2 and
Age3) indicate the gravity centre of the ellipses. Filled lines link prey families (represented by a point) to their corresponding predator
locality, but are only 80% of their total length for readability. Dotted lines represent the width and height of ellipses. Details and data
needed for the elaboration of graphics can be found in the “Material and methods” section.
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701
Fig. 3. Biplots of habitat traits analyses obtained from a fuzzy principal component analysis (FPCA). See legend of Fig. 2 for further
explanations.
netic dietary shifts and food selection of S. carolitertii
(Sánchez-Hernández & Cobo 2012), the present study
has conducted prey trait analysis to explore potential
differences in the prey-handling efficiency and feeding
habitat utilization among age classes.
The results of this study confirm that all the age
classes showed a remarkable similarity in their prey
utilisation patterns, and the present study exemplifies the possibility of a foraging convergence of age
classes regarding prey-handling efficiency and feeding
habitat utilization. However, regarding the outcomes
of the FPCA, there are some differences among age
classes. According to optimal foraging theory (OFT),
fishes should select prey items that maximise the ener-
getic gains available in relation to the energetic costs
of capturing, ingesting and digesting the prey (Gerking
1994). In chubs, as in many other fish species, there is
normally a change in the diet composition during the
life of the fish (Blanco-Garrido et al. 2003; SánchezHernández & Cobo 2012). These shifts during fish lifestage transitions may be accompanied by a marked reduction in intra-specific competition in the fish population, facilitating the partitioning of resources (Elliott 1967; Amundsen et al. 2003; Oscoz et al. 2006).
In fact, Sánchez-Hernández & Cobo (2012) have found
that age-related shifts occur at three different levels in
S. carolitertii (diet composition, prey selection and prey
size). Nevertheless, based on the present prey trait analUnauthenticated
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702
ysis, the results of this study reveal a generally similar pattern in the prey-handling efficiency and feeding
habitat utilization among age classes of S. carolitertii.
Studies about the gradual development of food
capturing abilities during the ontogeny have been related to differences in relative foraging abilities (e.g.,
Morrison et al. 1978; Sánchez-Hernández et al. 2013). In
addition, fishes can acquire foraging information from
conspecifics (Reader et al. 2003 and references therein),
and as the predator acquires experience, the development of a search image can improve the ability to detect food, helping to account for the greater foraging
efficiency observed in adults (Ware 1971; Morrison et
al. 1978). Handling ability of fishes is an important
variable that may determine food selection (Cunha &
Planas 1999; de Crespin de Billy & Usseglio-Polatera
2002; Sánchez-Hernández et al. 2011a). In this sense,
Oscoz et al. (2006) stated that prey-handling costs in
Cyprinidae species could be responsible for the observed inter- and intra-specific (size-related) changes
in diet preferences. Moreover, Blanco-Garrido et al.
(2003) found that the mean prey size consumed was
positively correlated with mouth size in Squalius pyrenaicus (Günther 1868). Recently, Sánchez-Hernández &
Cobo (2012) demonstrated that active choice through
prey-size selection appeared to be important for the
food selection of S. carolitertii, and that prey size increased with fish size. As expected, this study shows
that morphological traits of the prey might play an
important role in the feeding behaviour of this fish
species, demonstrating that the utilization of prey with
streamlined body shape was more frequent in younger
individuals (age 1). No clear differences were in contrast found in body flexibility among age classes, being in disagreement with observations of Magalhães
(1993) and Blanco-Garrido et al. (2003); who found
that throughout the ontogeny, S. pyrenaicus shifts from
soft-bodied to hard-shelled prey. Thus, these differences
between the present study and previous studies (Magalhães 1993; Blanco-Garrido et al. 2003) could be probably related with the lack of old specimens (≥ age 4)
in this study.
Camouflage is one of the most common antipredator strategies in the animal kingdom, thus the
use of crypsis or adaptive resemblance to the bottom
substratum is frequent in different taxa of macrobenthos (e.g., Feltmate et al. 1992; Tikkanen et al. 2000).
In this study, age 3 showed a wider prey spectrum according to the ‘concealment’ trait, findings that could
indicate that the effect of anti-predatory strategies of
prey items on the feeding behaviour of S. carolitertii
is different among age classes. Hence, the acquisition
of prey types with well-developed anti-predator strategies (concealment) by older fishes (age 3) could be related to the expectation that fishes may learn to attack
and handle prey items via experience such as have been
reported by other researchers (e.g., Reiriz et al. 1998;
Warburton 2003; Tinker et al. 2009). Moreover, it is
important to note that according to the findings found
in this study in respect to the ‘agility’ trait, chubs pre-
J. Sánchez-Hernández
ferred to feed on several invertebrate taxon with none or
weak agility, findings that are in agreement with OFT,
since taxa with low agility are easier to capture, but
also fishes are able to feed on prey with high agility like
Baetis spp.
In contrast to the scarce information available
about the handling efficiency of Squalius species, the
habitat requirements of cyprinids are well known, and
generally the preference for high velocity and deeper areas increases with fish age (e.g., Simonović et al. 1999;
Kováč et al. 2006; Copp et al. 2010). Previous studies
have demonstrated in various Iberian Squalius species
that adults occupy coarser substrata, faster-flowing areas and deeper areas than young-of-year and juveniles
(Santos & Ferreira 2008; Martínez-Capel et al. 2009).
In this study, opposite with previous studies on Iberian
Squalius species (Santos & Ferreira 2008; MartínezCapel et al. 2009), the results related to the ‘current velocity’, ‘macrohabitat’ and ‘substratum’ traits showed
that the overlap was high among age classes, suggesting no age-related preference for any category of these
traits by the chubs. This confirms that habitat requirements for feeding can be similar among cohorts.
To sum up, the general foraging behaviour convergence among age classes found in this study could be
related with the lack of old fishes (≥ age 4), however
the present study shows that multivariate approaches
like prey trait analysis provide useful information on
feeding behaviour and prey-handling efficiency of fishes.
Therefore, a further application of this research is to encourage its extension using data from different cyprinids
species as more data become available.
Acknowledgements
The author would like to thank Spanish Employment
Agency (INEM) for its funding support. Dr. Per-Arne
Amundsen is acknowledged for valuable comments and corrections on the manuscript. I also appreciate the constructive comments on the manuscript given by two anonymous
referees.
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Accepted January 20, 2014
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