Latin

404 American Journal of Aquatic Research, 49(3): 404-417, 2021

Latin American Journal of Aquatic Research
DOI: 10.3856/vol49-issue3-fulltext-2654

Research Article

Otoliths morphology and age-record in Bagre panamensis

(Siluriformes: Ariidae) inhabiting at the southeast of Gulf of California

Juan Antonio Maldonado-Coyac1 , Rebeca Sánchez-Cárdenas2 , Jorge Saúl Ramírez-Pérez2

Luis Antonio Salcido Guevara2 , Karla Paola Valdez-Núñez3
Armando Pérez-Centeno4 & Maria de los Angeles Maldonado-Amparo2
1
Ph.D. student, Posgrado en Ciencias en Recursos Acuáticos
Universidad Autónoma de Sinaloa, Mazatlán, Sinaloa, México
2
Facultad de Ciencias del Mar, Universidad Autónoma de Sinaloa, Mazatlán, Sinaloa, México
3
Universidad Politécnica de Sinaloa, Mazatlán, Sinaloa, México
4
Departamento de Física, Centro Universitario de Ciencias Exactas e Ingenierías
Universidad de Guadalajara, Guadalajara, Jalisco, México
Corresponding author: Rebeca Sánchez-Cárdenas (rsanchez@uas.edu.mx)

ABSTRACT. Among Bagre genera, there is a high variation in the estimation of age, a concern due to
overexploitation risk in fisheries because of age underestimation. Bagre panamensis is an important fishery
resource of the Mexican Pacific and the Gulf of California. Its age is known from otoliths, but its accuracy needs
to be confirmed, and the periodicity of the otoliths record validated. The external morphology, some
microstructure attributes, and age record of B. panamensis' otoliths were described from 371 specimens collected
southeast of the Gulf of California. The lapilli otoliths were larger than the sagittae and asterisci otoliths. The
lapilli otoliths present aragonite crystals with a prismatic shape, and their growth is radial, from the core to the
otolith edge. The lapilli otoliths form an annual growth ring, defined by the slowdown in the growth that occurs
during April to July, during the breeding season. The ages of the individuals ranged from 1 to 15 years, and the
applied method is considered adequate and accurate for its estimation (otolith cross-sectioning and red-neutral
staining).
Keywords: Bagre panamensis; sea catfish; lapillus otolith; growth rings; aragonite crystals; accurate age
method; otolith staining

INTRODUCTION et al. 1996, Pracheil et al. 2019, Thomas & Swearer

2019). These can be located in membranous chambers
Otoliths are structures used for balance and hearing in (saccule, utricle, and lagena) connected by semicircular
all teleost fish (Campana 1999). They are composed of canals in the inner ear of fish (Campana 1999, Schulz-
inorganic material (>90% calcium carbonate; Campana Mirbach et al. 2018). In most fish species, sagitta
1999) and ≤10% of organic material (glycoproteins, otolith is the largest and it is the most frequently used
proteoglycans, and collagens; Lundberg et al. 2015), in estimating age (Panfili et al. 2002). However, in the
which grows throughout the life of fish (Schulz- superorder Ostariophysi including the sea catfishes
Mirbach et al. 2018). Fish have three different pairs of (Siluriformes: Ariidae), the lapilli otoliths tend to be
otoliths (sagitta, lapillus, and asteriscus) that can be larger and more robust (Assis 2005, Diogo 2005) and
developed by any combination of the three most they are the most suitable structures for fish age studies
common forms (calcite, aragonite, or valerite) in which (Maciel et al. 2018), by the method of cutting, polishing
calcium carbonate crystallizes (Gauldie 1993, Oliveira and defining the periodicity deposition of material (Reis

_________________
Corresponding editor: Alejandra Volpedo
 Otoliths morphology and age-record in Bagre panamensis 405

1986, Cheraghi-Shevi et al. 2015, Maciel et al. 2018, There is a high variation in age estimation among sea
Flinn et al. 2019; Table 1). catfishes in the Ariidae family and even in Bagre
The knowledge of fishes age is necessary for growth genera, with maximum ages from 3.5 to 36 years. Even
rate, mortality rate, and productivity estimates (Cailliet different studies have gotten maximum ages differing
et al. 2001, Campana 2001, Piddocke et al. 2015), by more than 50% in the same species. In Bagre
particularly for biomass yield estimation and monitoring marinus, the maximum ages of 10, 24, and 25 years
fisheries and aquaculture for sustainable management have been defined, considering very close maximum
purposes. In Mexico, 25 sea catfishes species have been sizes (55.7 cm in total length, 57.7 cm in furcal length,
registered to inhabit the Pacific Ocean and the Gulf of and 55 cm in total length, respectively) (Table 1).
California and 30 species in the Atlantic Ocean and the In this context, it is not always appropriate to use a
Caribbean waters (Marceniuk & Ferraris 2003, unique method to estimate the age (Beamish &
Robertson & Allen 2015). Some of them are currently McFarlane 1983, Maciel et al. 2018). It is
fished mainly by Mexican small-scale fisheries (DOF recommended to re-estimate the age using improved or
2012, 2018). Bagre panamensis (Gill, 1863) (Siluri- better methods. The cross-sectioning and neutral-red
formes: Ariidae) has been one of the most intensively staining methods have been widely used to improve the
exploited species (Arreguín-Sánchez & Arcos-Huitrón contrast of growth rings and to estimate the age in
2011) and also it is part of bycatch of the industrial sagittae otoliths of several marine fish species (Richter
shrimp fishery (Amezcua et al. 2006, López-Martínez & Mcdermott 1990, Arneri et al. 1998, 2001, Franks et
et al. 2010, Muro-Torres & Amezcua 2011). It is worth al. 2001, Peltonen et al. 2002, Easey & Millner 2008),
mentioning that nowadays, there is a growing interest and therefore to reduce the interpretation error (Easey
in their conservation and responsible use in fisheries & Millner 2008). While scanning electron microscopy
and aquaculture (Maldonado-Coyac et al. 2018), but (SEM) is a powerful tool that provides useful
their management is still incipient. information about the structure and composition of fish
The sea catfish B. panamensis is a benthopelagic otoliths, even if daily resolution is required (Panfili et
fish widely distributed from southern California, USA, al. 2009). In this sense and using these mentioned
the Gulf of California to northern Peru (Robertson & techniques, the age-record in lapillus otolith of B.
Allen 2015). Previous studies of B. panamensis from panamensis and some morphological attributes of the
the southeastern Gulf of California have defined age by external shape and microstructure of inorganic crystals
counting growth rings in whole lapilli otoliths without of otoliths were described.
any treatment (Table 1). The age definition from whole
otoliths could be easy and accurate in young individuals MATERIALS AND METHODS
(Khan et al. 2016). But it is impossible to visualize all
growth rings in older individuals (i.e. age >10; A monthly sample of 10 to 49 specimens (371 total
VanderKooy 2009). Since the growth rings are more sample) of Bagre panamensis was collected from
overlapping near the edge of older otoliths, and usually, Mazatlán, Sinaloa, from September 2014 to November
the age could be underestimated (Panfili et al. 2002, 2015 and January 2015, with the support of small-scale
Easey & Millner 2008, Volpedo & Vaz-dos-Santos fishery. The total length (TL), eviscerated body weight
2015, Khan et al. 2016). Therefore, there is a greater (We), and sex of each organism were recorded, and
interpretation error (Campana 2001). While, in the lapilli otoliths were extracted, washed with water,
youngest individuals could be difficult to identify the marked, and stored to estimate age. Also, gonads
first annual growth ring (i.e. Brachyplatystoma weights were registered (Gw).
rousseauxii) due to the presence of false rings (Hauser The three pairs of otoliths (lapillus, sagitta, and
et al. 2018). Unfortunately, the process of estimating asteriscus) from 10 individuals were extracted,
fish age based on any bony structure incorporates error photographed, and identified in order to describe their
due to subjectivity which originates with the prepa- external morphology according to Martínez &
ration and interpretation of the periodic features in the Monasterio de Gonzo (1991), Volpedo & Echeverría
calcified structures, and even in the same structure as (2000), Acero & Betancur (2007), Chen et al. (2011),
the otolith, results in age estimates can differ among Aguilera et al. (2013), Santificetur et al. (2017) and
researchers (Campana 2001). In fisheries, particularly, Volpedo et al. (2017). Also, these lapilli otoliths were
this is a concern due to an aging error that can prepared to observe their microstructure using a Tescan
contribute to overexploitation of a population or MIRA 3 LMU scanning electron microscope; this
species, often because age underestimation (rather than procedure consisted of embedding the lapillus otolith in
overestimation) results in overly optimistic estimates resin and cutting them transversely across the core with
growth and mortality rate (review by Campana 2001). a circular diamond-tipped blade. Right away, the cut
406 Latin American Journal of Aquatic Research

Table 1. Some age studies realized using lapilli otoliths of sea catfishes of Ariidae family, Siluriformes. NS: not specified,
TL: total length, FL: fork length.

Maximum
Species and aging method Sex Age Length Country Reference
(yr) (cm)
Whole otolith and whole operculum
Plicofollis tenuispinis (Day, 1877) Both 3.5 41 TL India Dan (1981)
Whole otolith
Bagre bagre (Linnaeus, 1766) Both 6 42 TL Brazil Costa & Juras (1981, 1982)
Ariopsis guatemalensis (Günther, 1864) Both 6 43.4 FL Mexico Warburton (1978)
Occidentarius platypogon (Günther, 1864) Both 8 52.5 TL Mexico Muro-Torres (2011)
Bagre panamensis Both 8 50.5 TL Mexico Muro-Torres (2011)
Sectioned otolith
Netuma thalassina (Rüppell, 1837) Both 11 NS India Dmitrenko (1975)
Netuma thalassina Both 19 NS Kuwait Bawazeer (1987)
Plicofollis dussumieri (Valenciennes, 1840) Both 12 76.7 FL Iran Cheraghi-Shevi et al. (2015)
Galeichthys feliceps (Valenciennes, 1840) Male 16 37.9 FL South Africa Tilney (1990)
Galeichthys feliceps Female 18 37.9 FL South Africa Tilney (1990)
Galeichthys ater (Castelnau, 1861) Male 15 31.9 FL South Africa Tilney (1990)
Galeichthys ater Female 15 31.9 FL South Africa Tilney (1990)
Genidens barbus (Lacépède, 1803) Female 36 98 TL Brazil Reis (1986b)
Genidens genidens (Cuvier, 1829) Male 11.5 38 TL Brazil Maciel et al. (2018)
Genidens genidens Female 11.5 47 TL Brazil Maciel et al. (2018)
Ariopsis felis (Linnaeus, 1766) Male 20 34 TL USA Armstrong et al. (1996)
Ariopsis felis Female 23 43.9 FL USA Armstrong et al. (1996)
Ariopsis felis Both 24 49.2 TL USA Flinn et al. (2019)
Bagre marinus (Mitchill, 1815) Male 18 49.5 FL USA Armstrong et al. (1996)
Bagre marinus Female 24 57.7 FL USA Armstrong et al. (1996)
Bagre marinus Both 10 55.7 TL USA Flinn et al. (2019)
Bagre marinus Male 14 50 TL USA Miguez (2019)
Bagre marinus Female 25 55 TL USA Miguez (2019)

faces were polished using 1000, 300, and 50 nm diamond-tipped blade. One cut face of each otolith was
alumina powders in order to eliminate possible stained for 30 min in a neutral-red solution prepared
scratches on the surface of the structure. Subsequently, with 100 mL of distilled water, 0.2 g of neutral red, 0.5
the otolith sections were immersed in 1% HCl solution mL of glacial acetic acid, and 1 g of sodium chloride
for 25 s, washed with double distilled water, and dried (Easey & Millner 2008). It was washed with distilled
to reveal the microstructure. Then, the otoliths were water to remove solution excess and photographed. The
mounted on a holder-sample by conductive carbon neutral-red staining decalcified a thin layer of the
film, and the surface was coated with a thin layer of otoliths' cut-face surface to expose the protein matrix to
gold (Au) of about 2 nm to avoid the electron charge be stained by the neutral-red (Arneri et al. 1998, Easey
effect. The images were recorded by utilizing SEM. & Millner 2008). The staining is less intense where
Then, some morphologies and attributes of lapilli there is a lower concentration of proteins and higher
otoliths microstructure were described according to concentration of inorganic material (mainly calcium
Tomás & Geffen (2003), Cermeño et al. (2006), Panfili carbonate crystals), and vice versa (Richter &
et al. (2009), and Green et al. (2009). The micros- McDermott 1990, Arneri et al. 1998, Easey & Millner
tructures were measured from the digital images using 2008).
SigmaScan Pro, version 5.0 (Systat Software Inc.) The photographs of whole and cut-stained otoliths
software. were obtained through a stereomicroscope with reflec-
One lapillus otolith (left) from all collected otoliths ted light. Two independent readers counted the otoliths
pairs was first photographed whole beside a scale (0.01 growth rings on the digital images of cut-stain otolith;
mm precision). It was then embedded in epoxy resin one growth ring was composed of red-light (RL) and
and cut transversely across the core using a circular red-dark (RD) adjacent bands (Fig. 1). It was also recor-
 Otoliths morphology and age-record in Bagre panamensis 407

number of growth rings by sex. The diameters of otolith

were measured from the digital images of the whole
otolith using SigmaScan Pro, version 5.0 (Systat
Software Inc.) software (Fig. 2a).
The ring counting accuracy was evaluated with the
average error rate (APE, Beamish & Fournier 1981)
and the coefficient of variation (CV, Chang 1982). The
monthly relative frequency (%) of the percentage of RL
and RD bands at the otolith edge by sex was explored
throughout the year to define the deposition periodicity
Figure 1. Stain cross-section of right otolith lapillus of
Bagre panamensis, observed under reflected light. of the growth rings (Reis 1986, Fowler 2009, Maciel et
Position of otolith; D: dorsal, V: ventral, Pr: proximal, and al. 2018). Moreover, the frequencies were correlated
Di: distal. Structures; N: nucleus, RL: red-light band, RD: with the gonadosomatic index (GSI = Gw / We × 100;
red-dark band. Green dots indicate the growth rings. Pinheiro et al. 2006) to explore the interaction between
Neutral-red staining. reproductive and growth processes, using the
Spearman's rank correlation coefficient (rs) and a t-test
ded if the otolith had an RL or RD band at the edge. with n-2 degree of freedom and a significance level P
Additionally, particularities and anomalies of the = 0.05 (Zar 2010). Furthermore, the statistical relations
growth rings were identified and described according to of otoliths diameter with TL and the number of growth
Cermeño et al. (2006, 2008), Green et al. (2009), ICES rings were defined using linear and power models,
(2009), Cerna & Plaza (2016), and Hauser et al. (2018), respectively, fitted by the least-squares method (Zar
and their occurrence was explored concerning the 2010). Finally, the age structures of B. panamensis of

Figure 2. Morphological characteristics of the otoliths of the sea catfish Bagre panamensis. Position of otoliths: D: dorsal,
V: ventral, A: anterior, and P: posterior. a) Lapillus: upper dorsal face and lower ventral face. 1) Core, 2) antirostrum,
3) rostrum, 4) growth rings, 5) semipronunciated anterodistal ditch, 6) superficial mesial depression, 7) internal mesial
curve, 8) indistinct acoustic sulcus, 9) gibbus maculae. Red dots indicate the extremes of the otolith's diameter; b) Sagitta:
upper dorsal face and lower ventral face. 1) Ventral wing, 2) dorsal wing, 3) dorsal fissure, 4) ventral fissure, 5) growth
rings; c) Asteriscus: upper dorsal face and lower ventral face. 1) Face, 2) antirostrum, 3) core, 4) growth ring, 5) lobus
major, 6) sulcus "acoustic fossa", 7) canaliculum, 8) excisura "opening".
408 Latin American Journal of Aquatic Research

each sex were presented and described. The monthly RL and RD bands frequencies at the edge of
Kolmogorov-Smirnov two-sample test was performed the otolith show that one growth ring is formed
to compare age structure between females and males, annually because their behavior presented one
with a significance level P = 0.05 (Zar 2010). periodical oscillation per year. The RD bands at the
edge of the otolith (growth slowdown) were less
RESULTS frequent from October to February. Their frequencies
began to increase during March, reaching a maximum
Otoliths frequency during April to July (growth slowdown
The lapilli of the sea catfish Bagre panamensis are season) decreased in August and September. The
behavior of RL bands frequencies was reversed and
large (>12 mm), globose or compressed, thick circle,
presented the higher frequencies during August to
with the rostrum more developed than the antirostrum;
March (fast-growth season) (Fig. 4). The growth
it has growth marks on the dorsal surface, difficult to
slowdown season coincides with the highest values of
identify in old fish because they overlap near the edge
the GSI in both sexes of B. panamensis, supported by a
(Fig. 2a). While the sagitta is elongated (<10 mm), the
anterior margin is more pointed than the posterior positive correlation between RD bands frequencies at
the edges and the GSI (Fig. 4, Table 2).
margin. It has a pair of dorsal and ventral wings that
twist from the middle to the posterior margin of the
Particularities of growth rings
otolith; it is a fragile structure. Some growth rings in
the middle part up to the anterior margin of the otolith Some growth rings of lapilli otoliths in B. panamensis
are difficult to identify (Fig. 2b). On the other hand, the presented different RL and RD bands composition in
asteriscus is a tiny structure (4.5 mm), smaller than the 35% of individuals concerning the previously descri-
lapillus and sagitta. It is very fragile, translucent, and bed. Whereby, three different types of growth rings
rounded, with slightly wavy edges, angular face, while (GR) were identified, characterized by single (S,
the antirostrum is more or less pointed and little normal), double (D), and triple (T) RD bands in their
developed, existing between both a wide excisura; its composition (Fig. 5a). The additional RD bands in D
acoustic fosse has granulations (Fig. 2c). and T growth rings are discontinuous. That is, the bands
do not show continuity around the entire otolith (Fig.
Under the SEM, the low-magnification micro-
5a). The T growth rings were observed in the first to
photography of lapillus otolith's cut face showed dark
fifth rings in males and the first to fourth in the females,
and whitish bands (Figs. 3a-b). Darker areas appeared
from electron absorption associated with the presence but the highest frequency (42%) was observed in the
second ring in both sexes (Fig. 5b). The D growth rings
of insoluble organic material. Dark tonalities are seen
were observed from the first to the ninth rings
throughout the otolith (Fig. 3a), including in whitish
(decreased in the latter) (Fig. 5b), and they were more
bands, indicating that the organic matrix is distributed
frequent (31%) than grow rings T (4%).
throughout the otolith but with greater concentration in
the darker areas. The lapilli otoliths present aragonite Additionally, width alteration of one RL band was
crystals with prismatic shape and long grouped (Figs. detected between the third and sixth growth rings of
3e-f), and the prismatic growth is radial, from the core lapillus otolith in 8.6% of individuals. The width
to the otolith edge (Figs. 3c-d). The surface of aragonite alteration is seen as a widening of the RL band from the
crystals is smooth, and the prismatic form is variable right posterior margin to the middle part of the otolithic
(square, rectangular, pentagonal, hexagonal, or irre- structure (Fig. 6).
gular) (Figs. 3g-h). The width of aragonite crystals is
approximately 3.7 ± 1.3 µm. Rings counting and otolith size relationships
The processing and ring counting of 371 lapilli otoliths
Growth rings periodicity was performed without difficulty. These otoliths have
A total of 371 lapilli otoliths from 176 males and 195 4.6 to 12.1 mm in diameter. The accuracy of the ring
females of B. panamensis were suitably cut, stained, counting between both readers was high (APE = 5.8%
and examined. Lapilli otoliths form growth rings with and CV = 8.1%). The individuals presented 13 to 49.1
an RL band wider and with less fixation of red-neutral cm in total length (TL) and one to 15 years old (age,
dye. An indication of greater calcium crystals AG). The relationships of lapillus otolith diameter
accumulation into the protein matrix due to growth. (OD) as a function of TL and AG showed high
While the RD band of growth rings was the narrower coefficients of determination, demonstrating a clear
and with greater fixation of red-neutral dye, indicating positive proportionality between the increase in OD
a minor accumulation of calcium crystals into the concerning the TL and AG (Fig. 7). The relationship
protein matrix due to growth slowdown (Fig. 1). The between OD and TL was linear in both sexes (r2 = 0.7825
 Otoliths morphology and age-record in Bagre panamensis 409

Figure 3. Scanning electron micrographs of the sea catfish Bagre panamensis' lapilli otoliths. a-b) Dark (arrows) and
whitish bands on the otolith's cut face, c-d) stretch marks from the core (cr) indicating the radial growth (dotted arrows) of
the aragonite crystals (arrows with solid line), e-f) the long grouped aragonite crystals (arrow and dotted marks), g-h) view
of aragonite crystals that reveal the variable prismatic form (arrows).

Figure 4. Monthly red-light (RL) and red-dark (RD) bands frequencies at the otoliths edge and monthly average of
gonadosomatic index (GSI) of males (a) and females (b) of Bagre panamensis from the southeastern Gulf of California.
Standard error (bars).

males and r2 = 0.8752 females) (Fig. 7a). Meanwhile, suitable fit to the power model in both sexes (r 2 =
the relationship between OD and AG presented a 0.7788 males and r2 = 0.7712 females) (Fig. 7b).
410 Latin American Journal of Aquatic Research

Table 2. Correlations between the monthly red-light (RL) and red-dark (RD) bands frequencies at the otoliths edge and
monthly average of gonadosomatic index (GSI) of males and females of Bagre panamensis of southeastern Gulf of
California. n: data number, r s: Spearman's rank correlation coefficient, t: t-test, P: P-value, asterisk (*) indicates a significant
correlation (P < 0.05).

Correlations n rs t(n-2) P
Males
RD band vs. GSI 14 0.6703 3.1292 0.008704*
RL band vs. GSI 14 -0.6703 -3.1292 0.008704*
Females
RD band vs. GSI 14 0.6828 3.2376 0.007118*
RL band vs. GSI 14 -0.6828 -3.2376 0.007118*

Figure 5. a) Cross-sections of lapillus of the Bagre panamensis with different types of growth rings, S: single, T: triple, D:
double, b) relative frequency of the different type growth rings (single, double, and triple) regarding the total number of
growth rings.

Age structure (Martínez & Monasterio de Gonzo, 1988, 1991) and sea
The age structure of the B. panamensis sample from the catfishes (Volpedo & Echeverría, 2000, Acero &
southeastern Gulf of California was composed of Betancur 2007, Chen et al. 2011, Aguilera et al. 2013,
organisms from one to 14 years in females and one to Santificetur et al. 2017, Volpedo et al. 2017), in which
15 years in males. The five to nine years old individuals the lapilli exceed in size the sagitta and asteriscus. The
were the more frequent (Fig. 8). The age structures lapilli of the Ariidae is larger than the lapilli found in
were similar between females and males (Dmax = the Plotosidae, Horabagrus, and Archariidae catfishes
0.021329; P = 0.10). (Oliveira et al. 2001, Diogo 2005). The large size of the
lapillus is attributed to the fact that this structure
occupies the area corresponding to several bones of the
DISCUSSION cranial otic region (Oliveira et al. 2001, Diogo 2005),
which allows it to expand within the cavity and increase
Otoliths its size. Hence, the lapillus otolith is one of the most
The descriptions made on Bagre panamensis otoliths used structures to estimate the age and growth of the
correspond to that reported for freshwater catfishes catfishes.
 Otoliths morphology and age-record in Bagre panamensis 411

Figure 6. Cross-sections lapillus otolith of Bagre panamensis with width alteration of one red-light (RL) band (black
arrows).

Figure 7. a) Relationship between the otolith diameter-total length, b) otolith diameter-age of males and females of Bagre
panamensis in the southeast of the Gulf of California.

The lapilli otoliths presented aragonite micro- bands) due to neutral-red stain is attributed to a higher
crystals with a prismatic form, the typical shape of concentration of proteins (Richter & McDermott 1990,
these structures (Tomás & Geffen 2003, Panfili et al. Arneri et al. 1998, Easey & Millner 2008). This
2009). In some acid-treated otoliths, the crystals were coherence between the two methods supports that the
degraded partially or almost totally due to exposure narrower bands of rings otoliths (dark bands and RD
with HCl (Cermeño et al. 2006, Green et al. 2009). The bands) of B. panamensis present a higher concentration
electron absorption was different along the otolith, of proteins and a minor accumulation of aragonite
revealing dark and whitish bands similar in width and crystals concerning the wider bands (whitish bands and
shape to the RD and RL bands showed by the neutral- RL bands).
red stain, respectively. Therefore, they are representing
the same areas in the otoliths. The darker zones (dark Growth rings periodicity
bands) due to electron absorption are associated with B. panamensis forms one growth ring annually in lapilli
insoluble organic material (Cermeño et al. 2006) in otoliths. Similar to other species of sea catfishes (Reis
higher concentrations. While a more reddish stain (RD 1986, Tilney 1990, Mehanna et al. 2012, Cheraghi-Shevi
412 Latin American Journal of Aquatic Research

periods of starvation were critical factors that led to the

formation of these otoliths anomalies.
Similarly, D and T growth rings were found in the
sagittae otoliths of adult fish of the American eel
Anguilla rostrata (Lesueur, 1817) and the Swedish eel
A. anguilla (Linnaeus, 1758), attributed to the stress
caused by high-temperature levels and low oxygen
concentrations during the summer, that cause slow-or-
stop growth and the deposition of false bands (ICES
2009). Likewise, D growth rings were found in daily
growth rings of sagittae otoliths in juveniles of
European anchovy Engraulis encrasicolus (Linnaeus,
1758) (Cermeño et al. 2006, 2008) and Peruvian
anchovy E. ringens (Jenyns, 1842) (Cerna & Plaza
Figure 8. The age structure of males and females of the 2016). They contained a large amount of protein matrix
Bagre panamensis sample from the southeastern Gulf of (Cermeño et al. 2006), deposited as evidence of
California. metamorphosis stages and habitat changes (Morales-
Nin & Aldebert 1997, Tomás & Panfili 2000).
The false bands' formation (discontinuous RD
et al. 2015, Maciel et al. 2018, Flinn et al. 2019). The bands) and the width alteration of one RL band in
annual growth pattern of rings presented similar
lapillus otolith could be related to various biological
periodicity to the annual reproductive pattern, so the
process such as habitat change during the juvenile stage
fast-growing season coincided with the time of
(from the ocean to estuarine systems and vice versa;
reproductive rest. In contrast, the slowdown growth
Amezcua et al. 2006, Madrid-Vera et al. 2007), sexual
season was overlapped with the time of reproduction
maturity (35.5 cm LT in Muro-Torres & Amezcua
and oral incubation (eggs and offspring) of B.
2011; 3.8 years in Muro-Torres 2011), reproduction
panamensis in the southeast of the Gulf of California
and oral incubation of offspring (Muro-Torres &
(Muro-Torres 2011, Muro-Torres & Amezcua 2011,
Amezcua 2011), and also with changes in environ-
Zavala-Leal et al. 2019). Similar results have been
mental conditions (Beamish & McFarlane 1983, Reis
reported in the sea catfish Galeichthys feliceps and G.
1986, Velasco & Reis 2004). Those otoliths structure
ater of South Africa coasts (Tilney 1990), Genidens
barbus (Reis 1986), and G. genidens (Maciel et al. alterations are occurring at the time in which such
processes could also be occurring in B. panamensis.
2018) of Brazil coasts. They ensure that reproductive
activity and oral incubation (eggs and offspring) entails Those "alterations" are an abnormal change in the
a high energy expenditure (Rimmer & Merrick 1983, deposition of protein matrix (false bands) and the
Tilney 1990), and this is a critical factor in reducing the inorganic material (width alteration of RL band), and
sea catfish growth rate (Reis 1986, Velasco & Reis this alteration may occur during a short time since it is
2004, Velasco et al. 2007, Maciel et al. 2018). not fully developed around the otolith structure.
Perhaps, those "alterations" are caused by a
Particularities of growth rings circumstantial and abnormal limitation (false bands) or
availability (width alteration of RL band) of food or
The S growth rings were considered normal because energy reserves during the fast growth and slowdown
they are the type of growth ring commonly found and growth seasons, respectively.
counted to assess the age in fishes (Campana 2001,
Green et al. 2009). The additional discontinuous RD Rings counting and otolith size relationships
bands in D and T growth rings were considered false The accuracy of ring counting was high, according to
bands since they were not continuously registered Campana (2001), and the growth rings were distin-
around the otolith. Hauser et al. (2018) recorded similar guishable, even in older individuals. However, the rings
growth patterns and types of rings in lapillus otolith of were closer together but the neutral-red staining
the freshwater catfish Brachyplatystoma rousseauxii provided adequate contrast. It is worth mentioning that
(Castelnau, 1855) from the Orinoco River, as in B. neutral-red staining has been widely used to improve
panamensis. The authors documented that it was the contrast of growth rings and for the age study in
difficult to define age due to D and T growth rings cross-sections of sagittae otoliths of several marine fish
presence. They reported that the stress caused by the species (Richter & Mcdermott 1990, Arneri et al. 1998,
increased salinity in the Orinoco River during August 2001, Franks et al. 2001, Peltonen et al. 2002, Easey &
and September and competition for food, and long Millner 2008).
 Otoliths morphology and age-record in Bagre panamensis 413

The proper contrast of the growth rings and their panamensis, like in other fish species, to reduce the
clear temporal formation pattern in lapilli otoliths, in interpretation error and age underestimation (Campana
addition to the clear positive proportionality in the 2001, Easey & Millner 2008). It is worth noting that B.
relationships of otolith size (OD) as a function of TL panamensis is a fishery resource in Mexico and is
and AG, confirm that lapilli otoliths are adequate considered a species with aquaculture potential. The
structures to estimate the age and growth of B. age data are important for fisheries and aquaculture
panamensis as having been reported for other species management, such as estimating growth and mortality
of sea catfishes (Reis 1986, Tilney 1990, Mehanna et rate in productivity assessment. Moreover, the age
al. 2012, Cheraghi-Shevi et al. 2015) and freshwater underestimation (rather than overestimation) could
catfishes (Hauser et al. 2018). cause overly optimistic productivity estimates that may
contribute to overexploitation of a population in a
Age structure fishery (review by Campana 2001) and inaccurate yield
The age structure of B. panamensis was composed of estimates in aquaculture.
organisms between one to 15 years old. The most
frequent ages in the sampled were five to nine years old, ACKNOWLEDGMENTS
mainly adult organisms since B. panamensis reaches
size and age of sexual maturity at 35 cm of TL and 3.8 We thank the small-scale fishermen from Mazatlán,
years (Muro-Torres 2011, Muro-Torres & Amezcua Sinaloa, for providing us with samples of sea catfish.
2011). JAMC thanks the National Council of Science and
The maximum observed age was 15 years, almost Technology (CONACyT) for a Ph.D. scholarship.
twice the maximum age recorded (8 years) by Muro- Special thanks to Jorge Manuel Elenes Lizarraga for the
Torres & Amezcua (2011). Also, for B. panamensis in English review of the manuscript.
the same sampling area, despite that analyzed
individuals in both studies had similar sizes (13 to 49.1
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Received: October 23, 2020; Accepted: January 4, 2021