Populacional structure of Apistogramma agassizii (Steindachner, 1875) (Perciformes: Cichlidae) in aquatic environments of the Amana Sustainable Development Reserve (Amazonas - Brazil)

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Ichthyological Research (2024) 71:208–211
https://doi.org/10.1007/s10228-023-00925-1
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NEWS ANDCOMMENTS
A rare case ofabnormal hyperpigmentation inafreshwater sardine,
Triportheus auritus (Characiformes, Triportheidae) fromtheAmazon
basin, Brazil
AkemiShibuya1 · WalliceP.Duncan1· JansenZuanon2
Received: 29 May 2023 / Revised: 17 July 2023 / Accepted: 18 July 2023 / Published online: 10 August 2023
© The Author(s) under exclusive licence to The Ichthyological Society of Japan 2023
Skin color abnormalities have been described in many fish
species, especially regarding cases of total or partial absence
of skin pigmentation (hypomelanosis), such as albinism or
piebaldism (Sazima and Pombal 1986; Sampaio etal. 2015;
Finucci 2020; Shipley etal. 2022). Another type of color
abnormality is the hyperpigmentation (or hypermelanosis),
which is characterized by excessive pigmentation present in
the skin or other tissues and has also been reported in fishes
(e.g., Jawad and Ibrahim 2017; Nakhawa etal. 2021). How-
ever, melanism can result from different causes, such as skin
injuries, parasitism, genetic inheritance, climate change or
environmental-related stressor (Akyol and Sen 2012; Roulin
2014; Smith etal. 2020). Melanism in fish refers to par-
tial or complete hyperpigmentation of skin that affects both
natural and farmed specimens or populations (Jawad and
Ibrahim 2017). This abnormality has been frequently found
and reported in flatfishes (order Pleuronectiformes), show-
ing the presence of dark spots or abnormal pigmentation on
the blind side of the body (Bolker and Hill 2000; Akyol and
Sen 2012). Cases of partial pigmentation have also been
observed in other fishes, such as carangids (Jawad and Ibra-
him 2017), the perciform Cephalopholis fulva (Simon etal.
2009), the gasterosteiform Gasterosteus aculeatus (Smith
etal. 2020) and the gadiform Bregmacerus mcclellandi
(Nakhawa etal. 2021). As far as we know, hypermelano-
sis has not yet been documented in Amazonian freshwater
fishes, which may have resulted from a purported rarity in
natural populations or just from a lack of formal records in
scientific literature.
Here, the first report of a hypermelanic Triportheus
auritus is presented. Triportheidae is a characiform family
that comprises 22 valid species distributed in five genera
(Mariguela etal. 2016). Triportheus auritus is a school-
ing species commonly known as freshwater sardine (or
“sardinha comprida”, in Portuguese), that occurs in Ama-
zonas, Araguaia, Tocantins and Orinoco rivers (Malabarba
2004). The species presents an overall ground color silver to
yellowish brown and can reach 25.5 cm of standard length
(SL) (Cella-Ribeiro etal. 2015). Triportheus auritus has
a relatively high importance for artisanal and commercial
fishery in the Amazon basin, representing in average nearly
3.5% of the total landed production, but reaching up to 14%
in low-water periods, being one of the most consumed fishes
from Amazon River (Santos etal. 2006).
The specimen of T. auritus with hypermelanosis was col-
lected by an artisanal fisherman in September 2021 in Tefé
River (03o33′28′′ S, 64o59′34′′ W, Vila Tuiuca community,
Municipality of Tefé, Brazil), a tributary of the Amazon
River. The specimen was received eviscerated; therefore,
it was not possible to determine its sex. After photo-doc-
umentation and morphological examination, the specimen
was preserved in 10% formalin solution for two weeks and
later transferred to 70% ethanol solution. Triportheus auri-
tus differs from other species of Triportheus from the Ama-
zon basin in having 22–28 gill rakers on the lower limb of
the first branchial arch, 40–46 scales on the lateral line and
24–28 branched anal-fin rays (Malabarba 2004). The present
specimen, identified as T. auritus, has 28 gill rakers, 42 lat-
eral line scales and 21 branched anal-fin rays. Morphometric
data are presented in raw values and as percentage of SL
(Table1). To estimate the proportion of unpigmented areas,
digital images of both sides of the fish body were processed
using ImageJ software (Rasband 1997). Samples of scales
were initially decalcified in 5% formic acid for 24 h, then
* Akemi Shibuya
ashibuya.1@gmail.com
1 Graduate Program inAnimal Science andFishery
Resources, Federal University ofAmazonas, Ave. Rodrigo
Otavio 6200, Coroado I, Manaus, AM69.080-900, Brazil
2 Coordination ofBiodiversity, National Institute
forAmazonian Research, Ave. André Araújo 2936,
Petrópolis, Manaus, AM69067-375, Brazil

209
Abnormal hyperpigmentation in a freshwater sardine
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dehydrated in a graded ethanol solution series, embedded
in methacrylate (Historesin, Leica) and sectioned into 5
µm-thickness slices (transversal sections). The specimen is
cataloged at the Fish Collection of the Instituto Nacional de
Pesquisas da Amazônia (INPA), Manaus, Amazonas, Brazil
(INPA-ICT #060181).
The hypermelanic T. auritus specimen is an adult of 194.0
mm SL, apparently healthy and with no evidences of injuries
or presence of parasites. Compared to the regular coloration
of the species, hypermelanism seems to be expressed over
the scales of the entire body and partially on the epidermis
of the head and the intensity of melanic pigmentation var-
ies minimally throughout the body (see differences between
Fig.1a and b). However, small unpigmented areas (small
patches of scales without melanism) are spread on both sides
of the body and comprise 3.18% of the total area (excluding
head and fins). The asymmetric distribution of the spots of
non-melanic scales on the sides of the body suggests that
they may have resulted from healed injuries covered by
regenerated normally pigmented scales.
The mid-lateral dark stripe, a coloration pattern presented
by preserved specimens of normal-colored T. auritus, cannot
be distinguished due to the intensity of melanin pigmenta-
tion in the abnormal specimen. The histological analysis of
a hypermelanic scale (Fig.1c) showed differences in color
pattern when compared to a sample from normal-colored T.
auritus. In a regularly colored scale, the coloration is homo-
geneous across all layers (Fig.1d). However, pigment cells
(melanophores or melanoblasts) are absent in the epithelial
layer of the hypermelanic scales. The most intense hyper-
pigmentation is observed in both the calcified component
of the episquamal and the collagen matrix of the hypos-
quamal sides as a uniform coloration (Fig.1c). A layer of
the hyposquamal side in the circulus was more intensely
stained, evidencing a distinct pigmentation pattern between
the anterior region and the rest of the scale (Fig.1e), when
compared with normal-colored scale (Fig.1f). In addition,
in the hypermelanic specimen, a high density of melano-
phores (with dispersed melanosomes) is clearly observed in
the center of the scales and practically absent in the edges
of the scales, while in the normal-colored T. auritus the few
melanophores (with most melanosomes aggregated) are con-
centrated in the edges and absent in the center of the scales
(Fig.1a, b).
Color changes in freshwater fishes have been observed in
species that occur in different types of waters. The occur-
rence of melanic males of Gasterosteus aculeatus has been
related to tannin-loaded river waters (Smith etal. 2020).
The hypermelanic specimen of T. auritus was collected
in the blackwater Tefé River, which has a blackish water
color; however, due to the influence of the Amazon River’s
flood pulse, the Tefé River shows an intermediate physi-
cal–chemical composition that places it between white- and
black-water types (Ríos-Villamizar 2012, 2014). Despite the
plausible relation between the occurrence of hypermelanistic
fish and black waters, the rarity of the case reported herein
(only one hypermelanic known specimen for an abundant
and widespread species) suggests that the observed case of
hypermelanosis represents an individual abnormality in the
T. auritus population. However, the survival of the hyper-
melanic T. auritus individual to adulthood may have been
facilitated by the aquatic lighting conditions of the black
water of Tefé River.
Pigmentation plays a role in camouflage and ther-
moregulation, protection against UV radiation and patho-
gens (Akyol and Sen 2012; Roulin 2014; Polo-Cavia and
Gomez-Mestre 2017), and these conditions may be favorably
associated with the color of black water. However, the cost
of being hypermelanic is very high, as melanin synthesis
is slow, requires large amounts of tyrosine (a conditionally
essential amino acid) and high energy expenditure (Moreno-
Rueda 2020). Furthermore, abnormal hyperpigmentation
of the skin can negatively affect color-based sexual selec-
tion (Roulin 2016). These aspects may explain the rarity of
hypermelanic T. auritus.
Melanism in fishes has been associated with the presence
of excess pigmentation on the epidermis (Bolker and Hill
2000; Jawad and Ibrahim 2017) or on the both scales and
epidermis (Simon etal. 2009). A particular case has been
documented to a single specimen of the marine ray Raja
montagui (Rajidae), which presented hypermelanosis in
parts of the cartilaginous skeleton, probably resulting from
some metabolic disturbance (Harper 1932).
The specimen of T. auritus did not present hyperme-
lanic pigmentation on the skin of the body, but only in
scales and on the skin of the head. Melanophores were
Table 1 Morphometrics of the hypermelanic Triportheus auritus
specimen
SL standard length
Character Measure (mm) %SL
Total length 225.0
Standard length 187.0
Head length 42.1 22.51
Snout to anal-fin origin 141.0 75.40
Snout to dorsal-fin origin 123.0 65.77
Snout to pelvic-fin origin 89.8 48.02
Anal-fin base length 33.8 18.07
Caudal-peduncle length 12.1 6.47
Caudal-peduncle height 16.1 8.61
Dorsal-fin base length 18.4 9.83
Dorsal-fin height 15.6 8.34
Pectoral-fin length 61.5 32.88
Pelvic-fin length 26.6 14.22

210 A. Shibuya etal.
1 3
expected to occur in the epithelial layer of the scales; how-
ever, hyperpigmentation in calcified structures is possible,
since the deposit of melanin was observed in the skel-
eton of a specimen of R. montagui (Harper 1932). The
specimen of T. auritus studied herein is the first report of
hypermelanosis in Triportheidae, which points out to a
purported rarity of such kind of color abnormality among
Amazon fishes.
Acknowledgments We are grateful to Mr. Jaime Santos da Silva for
collecting and carefully sending this unique specimen, and Rúbia
Machado for initial assistance in the laboratory. We thank the two
anonymous reviewers and the section editor whose contributions
improved the manuscript. AS received fellowships from Coordenação
de Aperfeiçoamento de Pessoal de Nível Superior-CAPES (PDPG-
FAP #88887.702973/2022-00) and Fundação de Amparo à Pesquisa
do Estado do Amazonas-FAPEAM (FIXAM #062.01520/2018), and
a grant from FAPEAM-PAMEQ (#062.01108/2019). WPD received
grants from FAPEAM-PPP (209/2012), FAPEAM-UNIVERSAL
(389/2012) and Conselho Nacional de Desenvolvimento Científico e
Fig. 1 Hypermelanic Tri-
portheus auritus (a) captured
in Tefé River, Amazonas State,
Brazil, showing the almost
fully hyperpigmented body.
b An individual of the same
species presenting regular
coloration, collected from the
Catalão Lake, municipality
of Iranduba, Brazil. c Details
of scales showing a relatively
uniform pigmentation. Differ-
ences of pigmentation between
hypermelanic (c) and regular
(d) scales in the sagittal sec-
tions after staining by toluidine
blue. The regular scales have
a lighter blue color in both the
epi-(ES) and hyposquamal (HS)
sides. Note the circulus portion
(arrows indicate the serrated
surface) of the hypermelanic
scale (e) presenting a distinct
pigmented layer of the hypos-
quamal side (collagen matrix)
(HPL), when compared with the
normal coloration (f)

211
Abnormal hyperpigmentation in a freshwater sardine
1 3
Tecnológico-CNPq (Universal #484374/2011-7). JZ received a pro-
ductivity grant from CNPq (#313183/2014-7).
Declarations
Conflicts of interest The authors declare no competing interests.
Ethics approval The specimen was caught accidentally by local fisher-
man, during the collection of the target species of the second author.
Thus, it was not killed by any of the authors. Furthermore, the speci-
men was collected with permission of the Instituto Chico Mendes de
Conservação da Biodiversidade-ICMBio (SISBIO license # 32360-
2/2019).
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