Anais da Academia Brasileira de Ciências (2019) 91(Suppl.

3): e20190260
(Annals of the Brazilian Academy of Sciences)
Printed version ISSN 0001-3765 / Online version ISSN 1678-2690
http://dx.doi.org/10.1590/0001-3765201920190260
www.scielo.br/aabc | www.fb.com/aabcjournal

Fishes of the Amazon: diversity and beyond

ADALBERTO LUIS VAL

Instituto Nacional de Pesquisas da Amazônia – INPA/MCTIC, Laboratory of Ecophysiology and

Molecular Evolution, Ave. Andre Araujo, 2936, 69080-971 Manaus, AM, Brazil

Manuscript received on March 5, 2019; accepted for publication on March 23, 2019

How to cite: VAL AL. 2019. Fishes of the Amazon: diversity and beyond. An Acad Bras Cienc 91: e20190260. DOI
10.1590/0001-3765201920190260.

Abstract: The Amazon basin houses a particular group of freshwater organisms, whose study tells the
geological history of the region, how biological diversity was shaped, how it is maintained, and what it
hides. The fish of the Amazon is represented by more than 3,000 known species distributed from the basal
groups up to the more specialized ones. This species richness hides a diversity of adaptations that are
dispersed at all levels of the biological organization. In this summary of the conference delivered at the
Brazil-France Bilateral Symposium, held in Manaus in 2018, we describe two aspects of the hidden world
of adaptive diversity: adaptations to changes in dissolved oxygen and the abilities of the Rio Negro fish to
face acidic and ion-poor waters of their habitats. Also, we present the vulnerability of Amazonian fish to
ongoing climate changes. Then, very briefly, we call attention to the many hidden biological processes that
allow these fish species to survive their environments, much of which is unknown. Indeed, however, they
are intricately related to men, either by responding to environmental disturbances that we have caused, or
by containing information that contributes to improving the quality of the environment in which we live.
Key words: Amazonia, biodiversity, adaptations, hypoxia, dissolved organic carbon, climate changes.

INTRODUCTION science, production of robust information about the

region must be considerably expanded. It means a
Extending across all countries in the north of South
treasure for all the Amazonian countries and should
America, the Amazon biome includes unmeasurable
occupy a prominent position in a sound science and
qualities. The biome is better described by its
immeasurableness and by its unknowns than by its technology agenda. However, none of the Amazon
known conditions. This statement does not mean a countries, including Brazil, has a robust science and
lack of information about the region; on the contrary, technology agenda to explore the hidden potential
the volume of existing knowledge is significant. of any small portion of the region.
However, given the unparalleled diversity of natural The Amazon biome has an area of 7.76 million
resources, dynamic environments that vary in space square kilometers, of which more than five million
and time, and a biological diversity that hides a are in the Brazilian territory. Comparatively, the
vast number of organisms yet to be described by Amazon area in Brazil is larger than the sum of the
areas of all European countries. It is in this region
E-mail: [email protected] that the longest and most abundant river on the
ORCid: https://orcid.org/0000-0002-3823-3868 planet runs: The Amazon River, 6,992 km long,

Biological Sciences An Acad Bras Cienc (2019) 91(Suppl. 3)

ADALBERTO LUIS VAL FISHES OF THE AMAZON: DIVERSITY AND BEYOND

is rivaled only by the Nile River, 6,671 km. It is parallels (Val and Almeida-Val 1995). There are
along its route, from the Nevado Mismi in Peru to about 3,000 species of fish distributed from the
its mouth in the Atlantic Ocean, that the Amazon basal groups to the more specialized ones, such
River collects water from the different tributaries as the Cichliformes until recently included among
in the North and South to discharge more than the Perciformes. Among these fish are small fish
250,000 m3 of water per second in the ocean, which species such as the cardinal, weighting few grams,
represents approximately 20% of all freshwater up to the giants pirarucu and piraíba, weighing
flowing into all world’s oceans. Even its tributaries more than 250 kilograms. Many of these species
have big numbers: The Negro river, for example, emerged millions of years ago and have evolved
discharges 28,000m3 of water per second in the in challenging environments. Amazonian fish have
Amazon River. Therefore, it is a unique space. always confronted scientists who have visited
Also, the basin is neither homogeneous nor the region as soon as the first expeditions were
monotonous. Each small space is unique and organized aiming the unknown world. Indeed, to
undergoes dynamic changes over a single day. maintain this diversity of fish, other equally diverse
There are three types of water: white, black and aquatic organisms must be present. The myriad
clear water, each with specific characteristics. For
of organisms composing the biota, including that
example, while the Amazon river has a pH close
of nearby “terra firme”, is indeed biologically
to neutral, the waters of the Rio Negro are acidic
interdependent. Many species are endemic and
and poor in ions (Sioli 1984, Val and Almeida-Val
occur only in the Amazon, some of which occur
1995). There is no physical barrier between the
just in specific sub-regions. For example, in the
different types of water, i.e., the aquatic biota can
Duke biological reserve, the average richness is
freely move among the different types of water.
similar in the different sampling sites; however, the
On the other hand, river water levels vary
composition is tightly related to the chemical and
significantly throughout the year, with pulses of
physical characteristics of the streams, leading to
flood and ebb (Junk et al. 1989, Schöngart and Junk
a differentiated distribution in small spaces within
2007). During flood periods, significant portions of
the 100ha reserve (Mendonça et al. 2005), pointing
the land forest are flooded making transient new
habitats available to the aquatic biota; during ebb to the existence of many species to be described.
periods, these habitats do not exist. At the same On the other hand, the presence of long-distance
time, several water characteristics vary throughout migratory species needs to be pointed out, not only the
the day, both during periods of high water and giant catfish that migrate thousands of miles across
during drought, being oxygen availability the most the basin but also several species of Characiformes,
relevant aspect from the physiological point of such as the jaraqui and matrinchã, that migrate from
view. The water in many places varies from anoxic the headwaters of several tributaries to the main
to hyperoxic, as observed in floodplain regions (Val central river channel. Many are the factors that have
and Almeida-Val 1995). Geographical variations in contributed to the diversification of fish species in
the availability of dissolved oxygen in water can the Amazon. These factors include: the formation
also be striking, such as those observed for the of the basin, which begins with the Andes uplift;
Trombetas and Purus rivers (Rocha-Silva et al. its unparalleled size; the dynamics of the basin;
2011). the pulses of flood and ebb; its open character with
It is in this diverse and dynamic environment connections with the North and with the South; the
that one finds a rich ichthyofauna, almost without paucity of some part of the Central Amazon; and the

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ADALBERTO LUIS VAL FISHES OF THE AMAZON: DIVERSITY AND BEYOND

continuing evolution and adjustments of genetic and water of the river are regularly normoxic, while in
physiological features. the flooded forest the oxygen levels may reach zero
at night. These lateral migrations are associated with
A DIVERSITY OF BIOLOGICAL STRATEGIES several biological processes, including breeding
TO SURVIVE LOW OXYGEN WATERS
(Cox-Fernandes 1997). Several questions arise from
Amazonian fish have developed a wide array of this observation and are related to geo-positioning
adaptations throughout the evolutionary process and oxygen sensing. For long-migratory fish, there
to optimize oxygen transfer processes to meet are already studies relating physiological processes
metabolic demands. Hypoxia has been an ever- and geo-positioning (Krylov et al. 2014, Putman
present challenge for fish in the region (Val et et al. 2014), but information for lateral migrations
al. 1998). Many species can breathe air, some of involving relatively reduced distances is not yet
available. Aquatic surface respiration (ASR) involves
which do so continuously and are called obligatory
repositioning the animal near the surface of the
air-breathing species, that is, they breathe air
water column so that the animal can pump through
independently of the amount of dissolved oxygen;
the gills the thin surface layer of the water column
others are called facultative air-breathing species,
that is richer in oxygen. Aquatic surface respiration
that is, they only breathe air when there is insufficient
is an essential alternative to aerial respiration and
dissolved oxygen to meet their metabolic demands.
is present in a significant number of species; the
These fish use different structures to uptake oxygen:
oxygen threshold that triggers positioning near
Lepidosiren, the South American lungfish, uses
the surface of the water column, however, varies
a real lung, while Arapaima, also an obligatory
between species (Kramer and McClure 1982). For
air-breather, uses a modified swim-bladder that
air-breathing species and those that can breathe on
resembles a lung. Among the facultative air-
the aquatic surface, many other challenges need to
breathing fish, the oxygen is taken up through
be studied. Among them, the risk of aerial predation
the skin, the vascularized region of the stomach that may have important ecological implications,
and intestine, diverticula of the mouth, gills, and but is unknown (Shingles et al. 2005, Abdallah et al.
pharynx, as well as through a partially vascularized 2015), and exposure to ultraviolet radiation (Groff
swim-bladder (Table I). For facultative air-breathing et al. 2010). Several questions arise regarding the
fish, the gills are functional and therefore, during processes that control ASR.
aerial respiration, there occur gill adjustments to A fascinating example of breathing on
secure carbon dioxide excretion and to avoid loss the aquatic surface is provided by tambaqui,
of oxygen to the external hypoxic environment. Colossoma macropomum, an emblematic species
Among the species of gill respiration, unable for the Amazon. When exposed to low oxygen
to capture oxygen directly from the air, adaptations availability, specimens of this species can expand
occur at all levels of the biological organization, the lower lips that are used to efficiently capture
from the behavioral to the molecular level (Figure 1). the thin surface layer of the water column (Braum
At the behavioral level, there are several strategies, 1983, Saint-Paul 1984, Val 1995). Below 10%
but two with a relatively high occurrence, namely water saturation, all specimens have lips and skim
lateral migration and respiration at the aquatic the water surface. In the same way that the lips
surface. Many species of fish migrate laterally from appear when there is low availability of oxygen,
the river to the flooded forest during the day and they regress when normoxia is reestablished.
back to the river before nightfall since in the running However, what is the physiological mechanism

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ADALBERTO LUIS VAL FISHES OF THE AMAZON: DIVERSITY AND BEYOND

TABLE I
Examples of facultative and obligatory air-breathing fish of the Amazon and organs used aerial respiration.

Air-breathing style Organs used for aerial respiration

Family
Pharyngeal,
(Species) Obligatory (O) Stomach and branchial
Swimbladder Skin
Facultative (F) Intestine and mouth
diverticula
Lepidosirenidae
O *
(Lepidosiren paradoxa)
Arapaimidae
O *
(Arapaima gigas)
Erythrinidae
F * *
(Erythrinus erythrinus)
Doradidae
F *
(Corydoras julii)
Callichthyidae
F *
(Callichthys callichthys)
Loricariidae
(Pterygoplichthys F *
multiradiatus)
Rhamphichthyidae
(Rhamphichthys F *
marmoratus)
Electrophoridae
O *
(Electrophorus electricus)
Synbranchidae
(Synbranchus F *
marmoratus)

that leads to the expansion and regression of the apical crypt surface area (Wood et al. 2009). Again,
tambaqui’s lips? The processes of oxygen sensing the controlling mechanisms of these morphological
are possibly involved, and several authors have reorganization processes are unknown suggesting,
sought to analyze the expression of genes related from what has hitherto been described, that these
to lip formation as well as innervation of the lips of mechanisms are complex.
this species (Sundin et al. 2000, Fagundes 2012). The transfer of oxygen from the environment
Another compelling example of morphological to meet the metabolic demands also depends on
adjustments in animals exposed to hypoxia is the biochemical adjustments. Two sets of adjustments
branchial remodeling exhibited by Astronotus are highlighted here: the multiplicity of hemoglobins
ocellatus. When in hypoxia, the gills of A. ocellatus and the intra-erythrocytic organic phosphates.
present reduced abundance of MRCs (mitochondria Fish commonly present multiple hemoglobins.
rich cell) on the filamentous surface; lack of The different types of hemoglobins have different
visible MRCs on the lamellar epithelium; a more functional properties in several species, and in
straightforward pattern of the PVCs (pavement many species, the proportion between them varies
cell) surface with a smooth central part and a few according to environmental characteristics and
concentric micro-ridges; and significantly reduced physiological demands of the animal (Val et al.

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ADAlBeRTO lUIS VAl FISHeS OF THe AMAZON: DIVeRSITY AND BeYOND

Figure 1 - Behavioral, morphological, physiological and biochemical adjustments aiding oxygen transfer in fish of the Amazon.

1986a, b, Weber et al. 2000, Rutjes et al. 2007). It in Hoplosternum littorale erythrocytes, and IPP
is essential to mention that the existence of multiple (Inositol pentaphosphate) in adult Arapaima
hemoglobins in fish erythrocytes continually gigas (Isaacks et al. 1977, Val 2000). The control
exposed to episodes of hypoxia is adaptively vital mechanisms of the 2,3DPg concentration in
because it limits their precipitation in the cell Hoplosternum erythrocytes appear to be related
since they are less soluble in their deoxygenated to water temperature (Val and Almeida-Val
state. Organic erythrocyte phosphates are negative 1995), while the increase of IPP level during the
modulators of Hb-O2 affinity. ATP and GTP are first year of life of pirarucu appear to be related
the main phosphates found in the erythrocytes of to decreases of ATP and gTP concentration (Val
tropical fish and, in general, the GTP concentrations et al. 1992). Recent studies show a redundancy of
are higher than the ATP concentrations. The levels IPP biosynthesis routes in pirarucu erythrocytes
of these two erythrocytic phosphates are reduced (Ribeiro 2017). In summary, the immense
in fish exposed to environmental and physiological diversity of species hides an equally broad set of
hypoxic conditions (Val et al. 2015), with gTP adaptive mechanisms at all levels of the biological
concentrations being decreased much faster than organization that needs to be studied and described.
ATP concentrations. It is possible that this is related
FISH TACKLING THE ACIDIC AND ION-
to the use of gTP by eIF-1α (Eukaryotic Initiation
POOR WATERS OF RIO NEGRO
Factor) in the processes of protein synthesis that
happen when organisms are required to adjust to The acidic and ion-poor water of black water
the hypoxic environment. In addition to ATP and rivers, such as the Rio Negro, impose additional
gTP, two other phosphates were described in challenges to the fish regarding ion homeostasis.
Amazonian fish: 2,3DPG (2,3 diphosphoglycerate) In general, freshwater fish tend to lose salts to the

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ADALBERTO LUIS VAL FISHES OF THE AMAZON: DIVERSITY AND BEYOND

environment, which can be accentuated in acidic what is the influence of different fractions of
environments and be even more challenging in ion- DOC on ion regulation in fish of the Rio Negro?
poor environments, in particular, in waters deficient Since the chemical characteristics of DOC vary
in calcium. Initial analyses of fish of the Rio Negro seasonally and geographically, how do fish respond
showed that they experience ion disturbances only to these variations? Is there an interaction of DOC
when the water pH is lowered to pH 3. Under pH in paracellular junctions? If so, how does this
3 they face a 3 to 5-fold loss of Na and Cl, which interaction occur?
is, however, much smaller than the losses observed Some species of fish, on the other hand, can
for less tolerant fish species. Also, these initial migrate back and forth and even thrive in the
observations evidenced a high gill affinity for Ca different types of water in the Amazon. Are these
(Gonzalez et al. 1998, Wood et al. 1998). These species able to adjust gene transcription to be in
data served as a stimulus for the organization of an different environments such as the waters of the
expedition to the Rio Negro to expand the analyzes Rio Negro? We analyzed this question using the
for other species. Two basic patterns emerged from Triportheus albus as a model, which co-occurs
that expedition: a) species such as Corydoras julii in black, white and clear waters. Specimens were
and Hemigrammus sp, which present significant sampled in the three different types of water, and
efflux of Na at pH 4 (less tolerant species) (Fig. the differential gene expression was determined.
2); and b) species such as Carnegiella strigata and Thousands of genes are differentially expressed
Apistogramma sp, in which the sodium flux is not between specimens of the Rio Negro and the
affected at pH4 and only moderately stimulated Solimões River (approximately 4,000 genes)
at pH 3.5 (Gonzalez et al. 2002). Simultaneously, and between specimens of the Rio Negro and
this later situation was also showed for tambaqui the Tapajós River (approximately 9,000 genes),
specimens that presented significant disturbances with a reduced number of genes (1,551 genes)
of ion fluxes only when exposed to pH 3 (Wood et commonly regulated. It is interesting, however,
al. 1998). that the primarily regulated genes are related to (a)
Subsequent analysis has sought to elucidate the decrease in cellular permeability, in particular, the
mechanisms and effects of typical characteristics of genes coding for claudin proteins, actn4, itgb3b,
the Rio Negro on the processes of ion regulation DSP, Gap junction protein, and Ca2C-ATPase, and
in fish that live in black waters. In these studies to (b) ionic regulation and acid-base, in particular
it was clearly observed that: a) acclimation of the gene coding for rhcG1, slc9a6a (NHE),
cardinal tetras to DOC + low pH resulted in an ATP6V0A2, NaC/KC-ATPase, slc26a4 (pedrin)
increase of whole body Na by 31% and Ca by and slc4a4b (Araújo et al. 2017).
166% compared to animals acclimated to low pH These studies show that biological diversity in
alone; b) DOC protects cardinal tetra acclimated the Amazon is much higher than we see. Also, these
to soft-acidic water by preventing excessive Na studies confront us with a broad set of questions
losses and by stimulating Ca uptake; and (c) Rio that broadens scientific interest in the Amazonian
Negro DOC provided almost perfect protection biome. Understanding how these organisms are
against ionoregulatory disturbances associated capable of facing the environment in which they
with an acute exposure to low pH (pH 4) in ion- live can serve as a model for the design of actions
poor water in the non-native fish Danio rerio for the conservation of the environment and the
(Matsuo and Val 2007, Duarte et al. 2016). There design of solutions to the challenges that we are
are still many questions to answer. For example, ourselves facing.

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ADAlBeRTO lUIS VAl FISHeS OF THe AMAZON: DIVeRSITY AND BeYOND

Figure 2 - Sodium influx ( J inNa ) , efflux Na

( J out ) and net flux ( J net ) of four species of fish from Rio Negro exposed to acidic water. From
gonzalez et al. (2002).

GLOBAL WARMING - NEW CHALLENGES and drastic scenarios in relation to the control,
FOR FISH FROM THE AMAZON compromising about 40% of the larvae with one
or more types of anomalies (lopes et al. 2018). If
The inherent challenges posed by the physical and
this high proportion of skeletal anomalies persists
chemical characteristics of the Amazonian waters,
in the face of ongoing climate change, two aspects
as well as their dynamicity, may be exacerbated
need to be carefully considered: firstly, concerning
by ongoing climate changes. Warmer waters with
the conservation processes of fish species, and
lower pHs and less dissolved oxygen are some of
secondly, concerning food security, because
the consequences of climate change in the Amazon.
tambaqui is an important food source for humans.
To analyze the effects of this new challenges on
For larger, growing animals, higher feed intake is
fish, four environmental rooms were constructed at
expected in warmer environments. In fact, for the
INPA’s main campus: a control room that reproduces
tambaqui in the intermediate and drastic scenarios
real-time the conditions in the forest, and three we observed a higher feed intake; however, this
experimental rooms in which the mild, intermediate increase in feed consumption was not accompanied
and extreme scenarios, as projected by the IPCC by a proportional increase in weight, i.e., the
(Intergovernmental Panel on Climate Change) for animal eats more but does not grow (Oliveira and
the year 2100 (IPCC 2013) are also adjusted in real Val 2017), which represents substantial limitations
time. Several experiments were performed there, for fish farming.
and two of them are described herein. The two The effects of warming on Amazonian waters
were completed with tambaqui. In the first one, we may also have more significant consequences.
observed a marked effect of the intermediate and Throughout the evolutionary process, it is possible
drastic scenarios on the larvae. In a short period of that there has been a trade-off between lifestyle/
two weeks, the proportion of larvae with some type energetic requirements and warming. In studying
of skeletal anomaly (lordosis, kyphosis, scoliosis, fish species from Ducke reserve, we observed a
mandibular malformation, among others) increased correlation between routine and thermal maximum
dramatically in animals exposed to intermediate metabolic rate, and between metabolic rate and

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ADALBERTO LUIS VAL FISHES OF THE AMAZON: DIVERSITY AND BEYOND

activity levels. We observed that specimens of adult and developing zebrafish exposed to hypoxia. J Exp
Biol 218: 1777-1786.
Characidae and Crenuchidae presented reduced
ARAÚJO JD, GHELFI A AND VAL AL. 2017. Triportheus
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It is clear that the observed biological richness hides 2016. Dissolved organic carbon from the upper Rio Negro
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know far exceeds what we know. However, what INPA. (Unpublished).
we know already allows us to design actions for the GONZALEZ R, WOOD C, WILSON R, PATRICK M,
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