| |

Received: 13 May 2019    Revised: 24 September 2019    Accepted: 15 October 2019

DOI: 10.1002/jnr.24550

REVIEW

Emotional behavior in aquatic organisms? Lessons

from crayfish and zebrafish

Murilo S. de Abreu1,2  | Caio Maximino2,3  | Filipe Banha4 |

Pedro M. Anastácio4  | Konstantin A. Demin5,6 |
Allan V. Kalueff7,8  | Marta C. Soares9

1
Bioscience Institute, University of Passo
Fundo (UPF), Passo Fundo, Brazil Abstract
2
The International Zebrafish Neuroscience Experimental animal models are a valuable tool to study the neurobiology of emo‐
Research Consortium (ZNRC), Slidell, LA,
tional behavior and mechanisms underlying human affective disorders. Mounting
USA
3
Institute of Health and Biological
evidence suggests that various aquatic organisms, including both vertebrate (e.g.,
Studies, Federal University of Southern and zebrafish) and invertebrate (e.g., crayfish) species, may be relevant to study animal
Southeastern Pará, Unidade III, Marabá,
Brazil
emotional response and its deficits. Ideally, model organisms of disease should pos‐
4
Department of Landscape, Environment sess considerable genetic and physiological homology to mammals, display robust
and Planning, MARE – Marine and behavioral and physiological responses to stress, and should be sensitive to a wide
Environmental Sciences Centre, University
of Évora, Évora, Portugal range of drugs known to modulate stress and affective behaviors. Here, we sum‐
5
Institute of Experimental marize recent findings in the field of zebrafish‐ and crayfish‐based tests of stress,
Medicine, Almazov National Medical
anxiety, aggressiveness and social preference, and discuss further perspectives of
Research Center, Ministry of Healthcare of
Russian Federation, St. Petersburg, Russia using these novel model organisms in translational biological psychiatry. Outlining
6
Institute of Translational Biomedicine, St. the remaining questions in this field, we also emphasize the need in further develop‐
Petersburg State University, St. Petersburg,
Russia ment and a wider use of crayfish and zebrafish models to study the pathogenesis of
7
School of Pharmacy, Southwest University, affective disorders.
Chongqing, China
8
Ural Federal University, Ekaterinburg, KEYWORDS
Russia aggressiveness, anxiety, crayfish, social preference, translational research, zebrafish
9
CIBIO, Research Centre in Biodiversity
and Genetic Resources, University of Porto,
Porto, Portugal

Correspondence
Allan V. Kalueff, PhD., School of Pharmacy,
Southwest University, Chongqing, China.
Email: avkalueff@gmail.com

Marta C. Soares, CIBIO, Research Centre

in Biodiversity and Genetic Resources,
University of Porto, Porto, Portugal.
Email: marta.soares@cibio.up.pt

Murilo S. de Abreu and Caio Maximino shared first authorship.

Edited by Michael Hendricks. Reviewed by Trevor Hamilton and David Baracchi.

The peer review history for this article is available at https​://publo​ns.com/publo​n/

10.1002/jnr.24550​.

J Neuro Res. 2019;00:1–16. © 2019 Wiley Periodicals, Inc. |  1

wileyonlinelibrary.com/journal/jnr  
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2       DE ABREU et al.

1 |  I NTRO D U C TI O N
Significance
Proper responses of animals to stress are critical for their survival, Mounting recent evidence suggests that aquatic organisms,
however maladaptive responses may also become pathological, re‐ including both vertebrate (e.g., zebrafish) and invertebrate
sulting in social and affective disorders (Campos, Fogaca, Aguiar, & (e.g., crayfish) species, may be relevant to studying emotional
Guimaraes, 2013; Nuss, 2015). Animal experimentation has been behavior and its deficits. These model organisms possess
an indispensable tool for understanding the neurobiological bases considerable genetic and physiological homology to mam‐
of stress and how it connects with emotional responses (Belzung mals, display robust behavioral and physiological responses
& Lemoine, 2011; van der Staay, 2006). An emotional response has to stress, and are sensitive to various drugs known to mod‐
subjective, behavioral, and physiological components and, while the ulate stress and affective behaviors. Here, we summarize
former is fundamental for human experience, the latter two can be recent findings in the field of zebrafish‐ and crayfish‐based
studied in animals (Oatley & Johnson‐Laird, 2014), including both modeling of stress, anxiety, aggressiveness and social prefer‐
vertebrate and invertebrate species (Baracchi, Lihoreau, & Giurfa, ence, and discuss further perspectives of using these novel
2017). Considering that shifts in emotional response are a crucial model organisms in translational biological psychiatry.
component of many mental disorders and that the translatability of
current studies is still limited, additional and more focused studies
are needed to ultimately contribute to understanding these disor‐ zebrafish stress‐related behaviors, we also critically evaluate their
ders, including  widening the spectrum of species used in the cen‐ utility for probing neural underpinnings of anxiety, aggression and
tral nervous system (CNS) disease modeling (de Mooij‐van Malsen, social preference.
Vinkers, Peterse, Olivier, & Kas, 2011; Kas et al., 2011; Maximino et
al., 2015; Stewart et al., 2015; van der Staay, Nordquist, & Arndt,
2017). Clearly, the choice of model organisms from other taxa be‐ 2 | B E H AV I O R A L ECO LO G Y O F C R AY FI S H
yond mammals is a challenging task driven by numerous considera‐ A N D ZE B R A FI S H
tions (Maximino et al., 2015). To increase the translatability of such
tests, their ethological, ecological and evolutionary aspects must be Crayfish include >540 Decapoda species belonging to three fami‐
considered to ensure construct validity (Kas et al., 2011; Maximino, lies (Crandall & Buhay, 2008)—Astacidae (native to Western North
de Brito, Dias, Gouveia, & Morato, 2010; Maximino & van der Staay, America and Europe), Parastacidae (native to the Southern hemi‐
2019). sphere), and Cambaridae (inhabiting the East of the Americas) (Shen,
A broader knowledge of behavioral biology of model organisms 2008). Found in freshwater environments (e.g., lakes, reservoirs
is critical, and must consider the natural habitat, movement prefer‐ and streams), crayfish tend to burrow or hide under rocks or other
ences and the overall distribution of organisms in ecological contexts shelters to avoid their natural predators (Rhoades, 1962), such as
(Benvenuto, Gherardi, & Ilheu, 2008; Brown, Laundré, & Gurung, fish, birds and mammals (Delibes & Adrián, 1987; Holdich, 1988).
1999; Ferrari, Sih, & Chivers, 2009; Laundré, Hernández, & Ripple, Generally, crayfish are social animals and form  overt social domi‐
2010). In rodents, this approach has already been widely used to sup‐ nance (Figler, Finkelstein, Twum, & Peeke, 1995; Issa, Adamson, &
port the choice of specific behavioral models and tests (Blanchard & Edwards, 1999). Mostly nocturnal and crepuscular species (Holdich,
Blanchard, 1988; Hånell & Marklund, 2014). Complementing rodent 2001), their locomotion is characterized by short peaks of intense
models, some aquatic vertebrate (e.g., zebrafish, Danio rerio), and in‐ crawling alternated with periods of low mobility (Anastácio et al.,
vertebrate (e.g., crayfish) models have recently emerged to improve 2015; Aquiloni, Ilhéu, & Gherardi, 2005; Francesca Gherardi &
our understanding of emotional‐like states under normal and patho‐ Barbaresi, 2000; Gherardi, Barbaresi, & Salvi, 2000). In particu‐
logical conditions (Fossat, Bacqué‐Cazenave, De Deurwaerdère, lar, crayfish (Procambarus clarkii) is an omnivore species that feeds
Cattaert, & Delbecque, 2015; Maximino et al., 2015). Studies focus‐ on plant and animal detritus, macrophytes and small live animals
ing on these models reveal some comparative relevance to humans (e.g., molluscs, insects, annelids, nematodes, platyhelminthes, tad‐
(Fossat et al., 2015; Fossat, Bacqué‐Cazenave, De Deurwaerdère, poles and fingerlings) (Loureiro, Anastácio, Araujo, Souty‐Grosset,
Delbecque, & Cattaert, 2014; Gerlai, 2014; Stewart, Braubach, & Almerão, 2015). The genome of this species contains nearly 137
Spitsbergen, Gerlai, & Kalueff, 2014), with the advantages of hav‐ thousand genes and 152 thousand predicted exons, ranging from
ing a shorter generational time that potentially enhances the de‐ 150 to 12,807 bp in length (Shi, Yi, & Li, 2018).
tection of developmental (e.g., drug/toxin) and transgenerational Zebrafish is a small teleost fish species, native to Southeast Asia,
(e.g., genetic and epigenetic) effects (Imeh‐Nathaniel, Orfanakos, that typically inhabits shallow slow‐moving streams, small rivers
Wormack, Huber, & Nathaniel, 2019; Lakstygal, de Abreu, & and especially still pools formed during the monsoons (Engeszer,
Kalueff, 2018; Scholtz et al., 2003; Spence, Gerlach, Lawrence, & Patterson, Rao, & Parichy, 2007; Parichy, 2015). Their most common
Smith, 2008). Here, we call for a wider use of aquatic organisms, predators include other fishes (e.g., snakeheads [Channa spp.], Indian
such as zebrafish and crayfish, for modeling stress, anxiety, aggres‐ Leaf fish [Nandus nandus] or freshwater garfish [Xenentodon cancila]
siveness and social preference deficits. As we discuss crayfish and [Bass & Gerlai, 2008; Engeszer, Patterson, et al., 2007]), birds, and
DE ABREU et al. |
      3

insects (e.g., dragonfly larvae [Spence et al., 2006]). Zebrafish is a al., 2018; Walsh‐Monteiro et al., 2016), the novel object approach
highly social species whose innate shoaling behavior (Engeszer, Da (Fior et al., 2018; Johnson & Hamilton, 2017), and inhibitory avoid‐
Barbiano, Ryan, & Parichy, 2007; Engeszer, Patterson, et al., 2007) ance tests (Blank, Guerim, Cordeiro, & Vianna, 2009; Gorissen et al.,
involves synchronized, ordered group swimming (Delcourt & Poncin, 2015; Manuel et al., 2014). Zebrafish NTT is based on geotaxis, an
2012) that aims to increase the probability of an individual fish de‐ innate escape ‘diving’ behavior in novel environments, where zebraf‐
tecting/avoiding predators (Pitcher, 1983). ish initially spend more time at the bottom and exhibit more erratic
The overlapping ethological and habitat characteristics of these movements and freezing/immobility (Bencan, Sledge, & Levin, 2009;
two aquatic species may provide an opportunity to use their natural Cachat, Stewart, et al., 2010; Egan et al., 2009). Such natural diving
antipredator and social behaviors (including avoidance, aggression response is generally expected from zebrafish, as in the wild they in‐
and other conspecific interactions) to develop behavioral assays habit shallow pools where their main predators—fish or birds—would
enabling the study of basic aspects of affective behavior, including attack from the side or the top (Parichy, 2015). However, due to ha‐
anxiety, aggression and sociality. Recognizing the growing value of bituation to the NTT apparatus with the lack of overt danger, zebraf‐
widening the spectrum of model organisms in translational affec‐ ish gradually (within minutes) begin to explore the top area (Stewart
tive research (Kalueff, Stewart, & Gerlai, 2014; Stewart, Braubach, et al., 2013; Wong et al., 2010). A typical NTT represents a trans‐
Spitsbergen, Gerlai, & Kalueff, 2014), it is timely to consider using parent narrow rectangular tank virtually divided into two (top and
aquatic models, such as crayfish and zebrafish, to examine emotion‐ bottom) or three areas (bottom, middle, and top) (Egan et al., 2009;
ality‐related traits. On the one hand, such use of invertebrate and Kysil et al., 2017). This test assesses three major phenotypic do‐
anamniote model organisms may help bridge important evolution‐ mains: exploration of novel environments (time spent in the upper/
arily‐based gaps in our understanding of the neural underpinnings bottom zone, latency to enter the top, number of crossings between
of normal and pathological behavior (Fossat et al., 2015; Maximino the zones), fear‐like behavior (e.g., freezing and erratic swimming),
et al., 2015). On the other hand, this approach may also increase the and overall activity/locomotion (e.g., distance traveled and velocity;
overall translatability of neurobehavioral models, given that mech‐ Cachat, Stewart, et al., 2010).
anisms shared between rodents, zebrafish (Gerlai, 2014; Stewart, Like in rodents, zebrafish NTT behaviors can be explained by
Braubach, Spitsbergen, Gerlai, & Kalueff, 2014) and, possibly, cray‐ a classical motivational conflict theory (Montgomery, 1955) based
fish (Fossat et al., 2014, 2015), are likely to represent “core” pathways on a balance between anticipation of potential threats versus ex‐
shared with humans. Thus, this strategy may further support inno‐ ploration (Davis, Walker, & Lee, 1997; Maier, 1993) and also by the
vative cross‐species modeling (Kas et al., 2011), based on both ver‐ avoidance theory viewing animal novelty‐evoked behavior as driven
tebrate and invertebrate species, for studying basic, evolutionarily by avoidance responses (e.g., avoiding potentially dangerous areas)
conserved, aspects and neural underpinnings of affective behaviors. (Gallup, 1974, 1979; Wallnau & Gallup, 1977). Finally, while rodent
studies suggest that neural circuits of fear may differ from those in‐
volved in anxiety (Davis et al., 1997), this distinction remains unclear
3 | M E A S U R I N G A FFEC TI V E‐ LI K E
in fish models. However, as NTT responses are highly sensitive to
B E H AV I O R I N C R AY FI S H A N D ZE B R A FI S H
anti‐anxiety drugs (Stewart, Wu, et al., 2011), this suggests a reason‐
able predictive validity in this assay.
3.1 | Stress/anxiety‐like behavior
The OF is another popular test to assess animal affective‐like be‐
Stress‐related behavior has been studied in the red swamp crayfish havior. In rodents, the OF apparatus typically consists of a circular or
(P. clarkii) (Hobbs, 1972), a native to Mexico and South‐Central USA. rectangular arena (Denenberg, 1969; Harro, 2018) to measure loco‐
Since crayfish naturally explore new environments and (like rodents) motion (e.g., the number of squares crossed or total distance trav‐
prefer the dark (Yamane & Takahata, 2002), their anxiety/avoidance‐ eled) and anxiety‐like center avoidance (e.g., entries or time spent
like behavior can be assessed in the light‐dark plus maze consisting in center vs. periphery). Stressed/anxious animals decrease the ex‐
of two shaded “dark” and two open “light” arms (Figure 1; Bacqué‐ ploration and increase time spent in the periphery of the apparatus
Cazenave, Cattaert, Delbecque, & Fossat, 2017; Fossat et al., 2014, (thigmotaxis) (Denenberg, 1969; Harro, 2018). Similar to rodents,
2015). Stressing crayfish by an electric shock (Fossat et al., 2014, both larvae and adult zebrafish display characteristic patterns of ex‐
2015) or descending their social status (Bacqué‐Cazenave et al., 2017) ploration, with prominent thigmotaxis (Ahmad & Richardson, 2013;
increases preference for the dark arms (Table 1). Their sensitivity to Stewart, Gaikwad, Kyzar, & Kalueff, 2012), suggesting that spatio‐
benzodiazepines (Bacqué‐Cazenave et al., 2017; Fossat et al., 2014) temporal strategies of exploration may be evolutionarily conserved
suggests some predictive validity of the model (e.g., similarity of drug across vertebrate species (Stewart et al., 2012).
effects with clinical treatment in humans) despite major neuroanatom‐ The zebrafish LDT is based on the natural tendency of fish to
ical differences from mammals. display scototaxis, avoiding brightly lit areas and spending more
The three most commonly used anxiety tests in zebrafish are time in the dark to minimize their detection by predators (Maximino,
the novel tank test (or novel tank diving test, NTT), the open field De Brito, de Mattos Dias, Gouveia, & Morato, 2010; Serra, Medalha,
test (OF), and the light‐dark test (LDT) (Figure 1; Kysil et al., 2017). & Mattioli, 1999). The typical LDT apparatus is a rectangular tank
Other anxiety screens include the plus‐maze with ramps (Varga et consisting of two equal vertical portions, black and white (Maximino,
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4      

F I G U R E 1   Selected behavioral tests used to assess anxiety, aggressiveness and social preference in zebrafish and crayfish. The line traces represent increased (orange) or decreased (blue)
respective behaviors in these species
DE ABREU et al.
DE ABREU et al. |
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TA B L E 1   Selected examples of pharmacological modulation of crayfish behavior

Drugs Dose Behavioral effects References

Aggression
5‐Hydroxytryptophan (5‐ 100 mg/kg 5‐HTP, or 100 mg/kg Increased aggression in 5‐HTP versus Dingman, Hurlburt, and
HTP) and fluoxetine 5‐HTP + 0.31 mg/kg fluoxetine 5‐HTP + fluoxetine subordinates Otte (2009)
Crustacean hyperglycemic 0.5 µg per crayfish Increased individual aggression Aquiloni, Panksepp, and
hormone (cHH) Huber (2012)
Anxiety
Chlordiazepoxide 15 µg/g Prevented stress effects of electric shocks, Fossat et al. (2014, 2015)
anxiolytic effect
Serotonin (5‐HT) 5 μg/g Anxiogenic effect Fossat et al. (2015)
a
Mianserin and methysergide 1 nmol/g Reduced anxiogenic effects of 5‐HT Fossat et al. (2015)
d‐amphetamine 1 and 5 mg/kg Increased exploration (e.g., antennal move‐ Alcaro et al. (2011)
ments, rearing, and locomotion)
Social preference
Anisomycin 0.1 ml saline solution Increased agonistic behavior in the dyadic Jiménez‐Morales et al.
test (2018)
Scopolamine 100 ng/g Increased agonistic behavior in the dyadic Jiménez‐Morales et al.
test (2018)
a
Mianserin is a serotonin 5‐HT2 receptor blocker, and methysergide is a 5‐HT1/2 receptor blocker.

De Brito, et al., 2010). In this test, anxiogenic‐like effects include Behavioral endpoints in this test vary from low‐stress (decreased
more time spent in the dark (Maximino, De Brito, et al., 2010), in approaches to a potential opponent) to high‐stress (unrestrained
addition to risk assessment (defined as partial or very fast entries fighting with attempts to remove the chelae or legs of the opponent)
in the white compartment, during which the animal gathers infor‐ (Huber & Delago, 1998). Fighting usually stops when one individual
mation on threat levels), thigmotaxis (swimming near the walls of retreats (using a tail flip) or crawls away from the opponent (Bruski
the tank), freezing (cessation of swimming and most movements), & Dunham, 1987).
and erratic swimming (a  zig‐zagging, fast pattern of swimming in In zebrafish, multiple paradigms have been used to elicit and
which the animal's direction is unpredictable to predators) in the assess aggressive behavior (de Abreu et al., 2019; Zabegalov et
white area (Araujo et al., 2012). Interestingly, the characterization al., 2019). For example, a widely used assay is the mirror test
of anxiety in the LDT paradigm is age‐specific, as for instance, lar‐ (Barbosa, Lima‐Maximino, & Maximino, 2019; Gerlai, Lahav, Guo,
val fish display natural dark avoidance (Steenbergen, Richardson, & & Rosenthal, 2000; Giacomini et al., 2016), where aggressive be‐
Champagne, 2011) that is attenuated by anxiolytic (e.g., diazepam, havior is evoked by presenting fish with a mirror, typically placed
buspirone or ethanol) and increased by anxiogenic (e.g., caffeine) on one side of the tank at an angle (Figure 1). The interaction of
drugs (Steenbergen et al., 2011). Such dark avoidance behaviors the fish with its own image is recorded after a short acclimatiza‐
have also been demonstrated in other fish species, including mos‐ tion period (Norton et al., 2011). To score aggression, the tank can
quitofish (Gambusia holbrooki; Maximino, Marques de Brito, Dias, be virtually divided into equal segments, and time spent near the
Gouveia, & Morato, 2010). The sensitivity of zebrafish models to mirror, as well as time spent in aggressive display, is assessed as
anxiotropic drugs (Maximino, da Silva, et al., 2014) suggests their an index of aggressive motivation (Way, Ruhl, Snekser, Kiesel, &
reasonable predictive value, implicating both crayfish and zebrafish McRobert, 2015). Displays are usually scored as the fish erecting
as potential models for anxiety‐like states and the optimization of its dorsal and anal fins and flaring its body flank toward the oppo‐
CNS drug screening. nent. It is also possible to elicit aggressive displays by showing vid‐
eos of conspecifics, evaluating aggressive behaviors (e.g., bites)
and time spent in the area near the video stimulus (de Abreu et al.,
3.2 | Aggression
2019; Way et al., 2015; Zabegalov et al., 2019). Although both
Aggression has long been studied in aquatic invertebrates (Bovbjerg, models elicit aggressive displays in zebrafish, because the animal
1956; Dingman et al., 2009; Sato & Nagayama, 2012; Tierney, is unable to interact with the opponent, such aggressive behavior
Greenlaw, Dams‐O'Connor, Aig, & Perna, 2004). In crayfish, ag‐ does not follow the usual escalation observed in natural contexts.
gressive and social behaviors are usually assessed during dyadic Thus, interactions with conspecifics (e.g., dyadic fights between
agonistic encounters, often with overt dominance‐subordinated size‐matched males) to elicit the complete aggressive repertoire
relationships (Bovbjerg, 1956; Dingman et al., 2009; Issa et al., from both appetitive (display) to consummatory (fight) compo‐
1999; Moore, 2007; Sato & Nagayama, 2012; Tierney et al., 2004). nents (Dahlbom, Backström, Lundstedt‐Enkel, & Winberg, 2012;
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6       DE ABREU et al.

Oliveira, Silva, & Simões, 2011; Teles & Oliveira, 2016), become and the videos are then analyzed, assessing time spent in proximity
necessary⁠. to the conspecifics (Barba‐Escobedo & Gould, 2012; Giacomini et
In dyadic behavioral assays, same‐sex pairs of fish are typically al., 2016). The shoaling test has also been used to assess sociality in
placed into a tank, isolated by a removable opaque divider. After fish (Miller & Gerlai, 2007, 2011). In this test, animals are analyzed in
an overnight acclimation, the divider is removed, and the fish are groups, assessing inter‐fish distance, nearest and/or farthest neigh‐
left to interact for 30 min, which is usually sufficient to determine bor distance, and/or shoal area (Green et al., 2012; Miller & Gerlai,
a clear winner. Behavioral patterns that can be observed include 2007). However, this test does not strictly measure social preference
displays; circling (fish approach one another in opposite direc‐ per se, and is sensitive to changes in other behavioral domains (e.g.,
tions and with erected fins, and in an antiparallel position circle anxiety‐like behavior), since, for example, anxiety naturally increases
around each other usually ascending in the water column); strikes shoal cohesion in zebrafish (Engeszer et al., 2004; Miller & Gerlai,
(fish swims rapidly toward the opponent but no physical contact 2007).
occurs between them); bites (fish opens and closes its mouth in
contact with the body surface of the opponent); chases (similar
3.4 | Neural mechanisms in stress and
to strike behavior but with an active pursuit by the aggressor); re‐
affective behaviors
treats (fish swims rapidly away from the opponent in response to a
strike or a bite); escapes (continued escape reaction in response to In crayfish, stress‐related behavior has been linked to altered sero‐
a chase); and freezing (fish stays immobile with all fins retracted) tonin signaling (Fossat et al., 2014). For example, stressing crayfish
(de Abreu et al., 2019; Oliveira, Silva, & Simoes, 2011; Zabegalov via electric shocks (Fossat et al., 2014, 2015) or by lowering their
et al., 2019). social status (Bacqué‐Cazenave et al., 2017), seems to increase anxi‐
ety‐like behaviors, an effect that is mimicked by injecting serotonin
into crayfish hemolymph (Fossat et al., 2014; Table 1). Serotonin
3.3 | Sociality
also triggers crayfish aggression (Tierney et al., 2004), possibly by
The social domain has also been studied in aquatic invertebrates reducing the likelihood of retreating and by increasing fight duration
(Bovbjerg, 1956; Dingman et al., 2009; Sato & Nagayama, 2012; (Huber & Delago, 1998), thus, evoking a pro‐aggressive and anxi‐
Tierney et al., 2004). Social interactions in crayfish are usually ogenic profile. Crayfish social status is usually established in dyadic
measured during dyadic agonistic encounters, sometimes dur‐ fights (winner vs. loser) with physically larger animals more likely to
ing the establishment of dominance‐subordinated relationships become winners, however, when injected with serotonin, smaller
(Hayes, 1975;  Huber & Delago, 1998). The mirror test has also crayfish are successfully able to win these confrontations against
been used to evaluate social response, in which an adult cray‐ larger untreated crayfish (Momohara, Kanai, & Nagayama, 2013).
fish is placed inside a glass tank with a mirror,  assessing rearing Moreover, larger crayfish injected with octopamine also lose when
up (climbing the wall), turning, cornering (facing the corner for set against untreated smaller animals, while wining by dominant
>5 s), backward walking, and crossing the midline of the aquarium crayfish is prevented by mianserin, an antagonist of serotonin recep‐
(Drozdz, Viscek, Brudzynski, & Mercier, 2006). Crayfish behavio‐ tors, and reinforced by fluoxetine (Momohara et al., 2013). However,
ral responses seem to depend on prior socialization levels (Drozdz current knowledge of socio‐positive behaviors and their modulation
et al., 2006). Indeed, crayfish that had previously been housed by the serotoninergic system in crayfish is still limited, meriting fur‐
in isolation show no difference in rearing, turning, cornering, or ther studies.
backward walking between the mirror and non‐mirror portions of Analyses of zebrafish anxiety‐like (Egan et al., 2009; Maximino &
the tank (Drozdz et al., 2006). In contrast, crayfish housed in pairs Herculano, 2010), aggressive (Norton & Bally‐Cuif, 2012; Zabegalov
increase all five behaviors in front of the mirrors (vs. in the non‐ et al., 2019) and social behaviors (Soares, Cardoso, Carvalho, &
mirror portions of the tank) and spend more time near the mirror Maximino, 2018) strongly implicate the serotonergic system is mod‐
(Drozdz et al., 2006), similarly to zebrafish, whose social isolation ulating fish affective behaviors (Table 2). This system is particularly
typically decreases shoal cohesion, likely due to the absence of relevant, because albeit not fully conserved in terms of neuroanat‐
social cues (Shams, Amlani, Buske, Chatterjee, & Gerlai, 2018). omy and genetics (Herculano & Maximino, 2014), it is functionally
Together, these findings suggest that crayfish may as well be a associated with emotional domains across vertebrates and inver‐
suitable model organism for further social testing. tebrates (Curran & Chalasani, 2012; Herculano & Maximino, 2014;
Several tests are widely used to assess social/agonistic behav‐ Mohammad et al., 2016). Zebrafish anxiety‐like behavior is usually
ior in zebrafish beyond aggression (Barba‐Escobedo & Gould, 2012; affected by serotonin in a receptor‐dependent manner (Herculano
Engeszer, Ryan, & Parichy, 2004; Gerlai et al., 2000; Muto, Taylor, & Maximino, 2014; Maximino, Lima, Costa, Guedes, & Herculano,
Suzawa, Korenbrot, & Baier, 2013). For example, zebrafish social 2014; Nowicki, Tran, Muraleetharan, Markovic, & Gerlai, 2014;
preference can be tested in a tank positioned between two other Ogawa, Ng, Ramadasan, Nathan, & Parhar, 2012; Ponzoni, Daniela,
tanks, one empty and another containing a single conspecific (Barba‐ & Sala, 2016). For example, serotonergic psychedelics, such as lyser‐
Escobedo & Gould, 2012) or a group of zebrafish (Giacomini et al., gic acid diethylamide (LSD) (Grossman et al., 2010), mescaline (Kyzar
2016). Fish are acclimated to the tank before behavior is recorded, et al., 2012) and 3,4‐methylenedioxymethamphetamine (MDMA;
DE ABREU et al. |
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TA B L E 2   Selected examples of pharmacological modulation of zebrafish behavior

Drugs Dose Behavioral effects References

Aggression
Dizocilpine (MK‐801) 5 μM Reduced aggression Zimmermann, Gaspary, Siebel, and Bonan (2016)
Ethanol 0.25, 10 and 20% Increased aggression Fontana et al. (2016), Sterling, Karatayev, Chang, Algava,
and Leibowitz (2015)
Fluoxetine 50 µg/L Reduced aggression Giacomini et al. (2016)
  5 mg/L Reduced aggression in dominants Theodoridi, Tsalafouta, and Pavlidis (2017)
Anxiety
O‐Acetyl‐L‐carnitine 0.1, 1 and 10 mg/L Anxiolytic effect Pancotto, Mocelin, Marcon, Herrmann, and Piato (2018)
Amitriptyline 50 μg/L Anxiolytic effect Meshalkina et al. (2018)
Fluoxetine 0.1 mg/L Reverted effects of unpredictable Song et al. (2018)
chronic stress (UCS)
LSD 250 μg/L Anxiolytic effect Grossman et al. (2010)
MDMA 40–120 mg/L Anxiolytic effect Stewart, Riehl, et al. (2011)
Mescaline 20 mg/L Anxiolytic effect Kyzar et al. (2012)
N‐acetylcysteine 1 mg/L Reverted effects of UCS Mocelin et al. (2019)
Ibogaine 10 and 20 mg/L Anxiolytic effect Cachat et al. (2013)
Noribogaine 1, 5 and 10 mg/L Anxiolytic effect Kalueff, Kaluyeva, and Maillet (2017)
Scopolamine 120 mg/L Anxiogenic effect Volgin, Yakovlev, Demin, Alekseeva, and Kalueff (2019)
Lithium carbonade 100 mg/L Anxiogenic effect Zanandrea, Abreu, Piato, Barcellos, and Giacomini (2018)
Caffeine 100 mg/L Anxiogenic effect Egan et al. (2009)
Social preference
Alcohol 0.25, 0.75 and 1% Disrupted group cohesion Miller, Greene, Dydinski, and Gerlai (2013)
Diazepam 16 µg/L Decreased social interaction Giacomini et al. (2016)
Fluoxetine 50 µg/L Decreased social interaction Giacomini et al. (2016)
Ibogaine 10 and 20 mg/L Disrupted group cohesion Cachat et al. (2013)
Ketamine 20 and 40 mg/L Disrupted group cohesion Riehl et al. (2011)
LSD 100 µg/L Disrupted group cohesion Green et al. (2012)
MDMA 80 mg/L Disrupted group cohesion Green et al. (2012)
MK‐801 5 µM Lower social interaction Seibt et al. (2011)
Nicotine 4 and 8 mg/L Disrupted group cohesion Miller et al. (2013)
Proline 1.5 mM Disrupted group cohesion Savio, Vuaden, Piato, Bonan, and Wyse (2012)

Abbreviations: LSD, lysergic acid diethylamide; MDMA, 3,4‐methylenedioxymethamphetamine.

Stewart, Riehl, et al., 2011), evoke anxiolytic‐like effects in zebrafish, social behaviors (Dekeyne, Denorme, Monneyron, & Millan, 2000;
increasing top swimming in the NTT and decreasing dark preference Gemmel et al., 2017). For example, like zebrafish (Egan et al., 2009),
in the LDT. Serotonin also lowers aggressive behavior (Barbosa et al., rats chronically treated with fluoxetine display anxiolytic‐like behav‐
2019; Norton et al., 2011) and increases social preference in zebraf‐ ior and reduced behavioral responses to stress (e.g., reverting the
ish (Barba‐Escobedo & Gould, 2012; Ponzoni, Sala, & Braida, 2016). suppression of exploration induced by stress; Zhang et al., 2000).
Importantly, distinct behavioral and molecular effects can be In addition, 5‐HT1A receptor agonists buspirone, ipsapirone and 8‐
triggered by both acute (Abreu et al., 2015; Barbosa et al., 2019; OH‐DPAT reduce aggression (Olivier & Mos, 1992) and a selective
de Abreu et al., 2014; Giacomini et al., 2016) and chronic (Egan serotonin reuptake inhibitor (SSRI) citalopram impairs social inter‐
et al., 2009; Marcon et al., 2016; Petrunich‐Rutherford, 2019; Song action in rodents (Dekeyne et al., 2000).  Therefore, zebrafish and
et al., 2018) exposure to serotonergic drugs, suggesting pro‐social, rodents present rather similar effects of serotoninergic modulation
anti‐aggressive and anxiotropic roles of serotonin in zebrafish. In ro‐ of emotional behaviors.
dents, the serotonergic system also modulates anxiety (Broekkamp, While we mostly focus here on serotonin as a well‐studied brain
Berendsen, Jenck, & Van Delft, 1989; Griebel, 1995; Sánchez & neurotransmitter involved in behavioral modulation in multiple spe‐
Meier, 1997), aggression (Chiavegatto et al., 2001; Ferrari, Palanza, cies, other neurotransmitter systems that regulate affective behaviors
Parmigiani, de Almeida, & Miczek, 2005; Olivier & Mos, 1992) and in various species involve the noradrenergic, dopaminergic and gamma
 |
8       DE ABREU et al.

aminobutyric acid (GABA)‐ergic systems. For example, exposure to Lopez‐Guzman, & Nava‐Mesa, 2018). Indeed, crayfish exposure to
chlordiazepoxide, a GABA‐ergic benzodiazepine ligand, reverts anx‐ cocaine, morphine and methamphetamine increases mobility (Imeh‐
iety‐like behavior in crayfish caused by stress (crayfish submitted to Nathaniel et al., 2017), whereas exposure to d‐amphetamine stimu‐
varying electric fields; Fossat et al., 2014) independently of changes in lates exploration (Alcaro et al., 2011). Finally, exposure of crayfish
monoamine levels (Fossat et al., 2015). Crayfish exposed to 434 mM to morphine increases locomotor activity acutely but reduces it  at
ethanol show hyperactivity (Blundon & Bittner, 1992), whereas injec‐ higher and/or chronic doses (Dziopa et al., 2011).
tion of dopamine increases crayfish swimmeret beating (Tierney, Kim, Like crayfish, zebrafish are also highly sensitive to pharmacological
& Abrams, 2003). Furthermore, aggressive behaviors in crustaceans modulation, with significant impact on anxiety‐like behavior. For exam‐
involve motivation to engage in fighting, with winners presenting ple, zebrafish also increase locomotor activity following d‐amphetamine
higher blood levels of dopamine and serotonin than losers (Sneddon, exposure (Irons, MacPhail, Hunter, & Padilla, 2010). They demonstrate
Taylor, Huntingford, & Watson, 2000). anxiolytic effects following a 1‐week ethanol treatment, increasing ex‐
Interestingly, the use of crayfish model systems has also demon‐ ploration and reducing erratic swimming (Egan et al., 2009). In moder‐
strated some promise in the study of the biological mechanisms of ate doses, alcohol enhances aggression and preference for conspecifics,
addiction (Alcaro et al., 2011) which are strongly implicated in be‐ whereas its high concentrations impairs these responses (Gerlai et al.,
havioural deficits and stress (Sinha, 2008; Torres‐Berrio, Cuesta, 2000). Discontinuation of ethanol and morphine evokes anxiogenic‐
like behavior and elevated whole‐body cortisol in zebrafish (Cachat,
Canavello, et al., 2010). Such drug responses may also be influenced
TA B L E 3   Selected open questions relevant to modeling by sex, since cocaine withdrawal‐evoked anxiogenic‐like behavior de‐
affective and social disorders in vertebrates and invertebrates velops earlier in female zebrafish, but is more robust and persistent in
Questions males (Patiño, Yu, Yamamoto, & Zhdanova, 2008).
Exposure to dexmedetomidine, an alpha‐2 adrenergic receptor
How to develop crayfish and zebrafish assays that are most robust
to study emotional disorders? agonist, causes sedation in zebrafish (Ruuskanen, Peitsaro, Kaslin,

Are there individual differences in emotional behavior of both cray‐

Panula, & Scheinin, 2005), as do common GABA‐ergic sedatives diaz‐
fish and zebrafish? epam and barbiturates (Zhdanova, Wang, Leclair, & Danilova, 2001).
How does crayfish and zebrafish ‘personality’ contribute to the In contrast, anxiogenic GABA‐lytic drugs, such as ionophore channel
expression of emotional phenotypes? blockers pentylenetetrazole and picrotoxin (Wong et al., 2010), or an
Do emotional behaviors differ in both zebrafish and crayfish in inverse benzodiazepine agonist FG‐7142 (López‐Patiño, Yu, Cabral, &
strain‐ and sex‐specific manner? Zhdanova, 2008), predictably evoke anxiety‐like behavior in zebrafish,
What is the role of epigenetic modulation of crayfish and zebrafish paralleling their well‐studied behavioral effects in rodents and humans.
emotional deficits? Stress itself further modulates crayfish and zebrafish emotional
Are there structures in the zebrafish and the crayfish nervous sys‐ responses. For example, zebrafish exposed to unpredictable chronic
tems that participate in the development of emotional deficits but
stress (UCS) increase aggressive response, whole‐body cortisol lev‐
do not have close analogues in humans?
els (Rambo et al., 2017) and anxiety‐like behavior (Marcon et al.,
How relevant are the existing behavioral assays in crayfish and
2016; Song et al., 2018). Acute stress elevates  zebrafish aggres‐
zebrafish to mimick human emotional disorders?
sive and anxiety‐like behavior, while decreasing social interaction
Are there significant differences in traditional drugs’ effects be‐
tween crayfish, zebrafish and humans? (Cachat, Stewart, et al., 2010; Giacomini et al., 2016). In crayfish,
acute stress also increases anxiety‐like behaviors (Fossat et al., 2014,
How can we objectively link quantitative characteristics of zebrafish
and crayfish behavior to symptoms of human emotional disorders? 2015). In turn, such evoked anxiety can be rescued by anxiolytic,
Is there any difference in emotional phenotypes presented by antidepressant and antipsychotic drugs (e.g., benzodiazepines, SSRI,
zebrafish and crayfish in natural habitat versus laboratory risperidone) (Fossat et al., 2014; Giacomini et al., 2016; Idalencio et
environment? al., 2015; Marcon et al., 2015, 2016).
How can stress affect (or trigger) emotional phenotypes in crayfish
and zebrafish?
How to develop crayfish and zebrafish models of emotional disor‐ 4 | ECO LO G I C A L I M PLI C ATI O N S O F
ders that display sex differences in pathogenesis similar to those in
C R AY FI S H A N D ZE B R A FI S H M O D E L S :
humans?
FU T U R E D I R EC TI O N S
Can computer technologies (e.g., behavioral visualization software)
lead to automatic recognition and extraction of crayfish and ze‐
brafish emotional behaviors? As a model species, zebrafish is characterized by easy laboratory main‐
Can current genetic tools (e.g., CRISPR) assist in the understanding tenance, short generation times, well‐described genetics (Detrich Iii,
of the mechanisms of emotional disorders in these two aquatic Westerfield, & Zon, 1998) and detailed behavioral ethograms (Kalueff
species? et al., 2013). Zebrafish mature at about 3 months in laboratory condi‐
What is the impact of gut microbiota on models of emotional disor‐ tions (Eaton & Farley, 1974). Females can spawn every 1–6 days and
ders in crayfish and zebrafish?
a single clutch may contain several hundred eggs (Spence & Smith,
DE ABREU et al. |
      9

2006). Generation time is short, typically 3–4 months, and develop‐ conditions (Huner et al., 1991), making them ideal for laboratory use.
ment is rapid, with larvae displaying food seeking and active avoid‐ However, from the bioenvironmental perspective, some risks include
ance behaviors within five days post fertilization, i.e. 2–3  days after escape and invasion of natural habitats, whose strong impacts have led
hatching (Kimmel, Ballard, Kimmel, Ullmann, & Schilling, 1995). Mean to the inclusion of this species in several restrictive national or inter‐
life span of domesticated zebrafish is about 42 months, with the old‐ national legislations (Capinha, Leung, & Anastácio, 2011; Lodge et al.,
est individual surviving for 66  months (Gerhard et al., 2002). In the 2012; Souty‐Grosset et al., 2016). Another ecological risk is the trans‐
wild, individuals normally only live for one year (Spence, Fatema, Ellis, mission of diseases or parasites to wild animals, even if the species it‐
Ahmed, & Smith, 2007). There are also some key ecological implica‐ self does not escape the laboratory. The red swamp crayfish and other
tions in their behavioral output. For instance, zebrafish habitat in‐ North American crayfish species carry the crayfish plague, a deadly dis‐
cludes shallow, slow‐moving water with mud, sand/gravel, aquatic ease whose transmission to wild populations of crustaceans is a serious
vegetation, and shelters from overhanging vegetation and/or banks concern (Svoboda, Mrugała, Kozubíková‐Balcarová, & Petrusek, 2017).
(Parichy, 2015). The presence of vegetation has been associated with Finally, while other common crayfish species may represent potential
increased aggression in zebrafish in population‐dependent manner candidates for laboratory use, they also pose higher ecological risks
(Bhat, Greulich, & Martins, 2015). For example, differences in feeding than the red‐swamp crayfish. For example, Procambarus fallax, f. virgina‐
after disturbance have been observed between wild‐derived and labo‐ lis is a parthenogenetic (Martin, Dorn, Kawai, van der Heiden, & Scholtz,
ratory‐reared zebrafish populations (Bhat et al., 2015). 2010), highly invasive crayfish (Chucholl, Morawetz, & Groß, 2012).
From the ecological point of view, red‐swamp crayfish has  some
added practical advantages (compared to zebrafish), including higher re‐
sistance to experimental manipulations and handling due to their larger 5 | CO N C LU S I O N
size and hard exoskeleton. However, they also present some husbandry
problems, such as considerable cannibalism in captivity (Stein, 1977) In summary, studying affective behavior in both invertebrate (cray‐
and higher aggression (versus other freshwater crayfish (Gherardi, fish) and vertebrate (zebrafish) aquatic models may provide important
2013; Reynolds, 2011), thereby complicating their manipulation and insights into emotional responses and mechanisms underlying human
laboratory use. Another advantage of using crayfish is the possibility of affective illnesses, also fostering the discovery of novel drugs to treat
longer‐term manipulation out of water, since this species is extremely these disorders (see Table 3). These animal models may also become im‐
resistant (physiologically and behaviorally) to air exposure stress (Banha portant tools in the studies of emotional disorders due to their generally
& Anastácio, 2014; Ramalho & Anastácio, 2015). Although zebrafish conserved genetic homology to mammals (Gutekunst et al., 2018; Howe
are capable of surviving in hypoxic conditions (Rees, Sudradjat, & Love, et al., 2013; Shi et al., 2018). For example, crayfish—due to the underly‐
2001), low environmental oxygen concentrations can produce robust ing mechanisms which are strongly conserved—have recently emerged
behavioral, physiological or biochemical deficits (Jensen, Nikinmaa, & as a promising novel model organism in addiction research, showing sen‐
Weber, 1993; Kramer, 1987; Kramer & Mehegan, 1981). Under ideal sitivity to human drugs of abuse (e.g., cocaine and amphetamine) in the
conditions the time to maturation in red‐swamp‐crayfish is 2 months conditioned place preference paradigm (Huber, Panksepp, Nathaniel,
and its generation time is 4.5 months (Huner, Barr, & Coleman, 1991). Alcaro, & Panksepp, 2011). Likewise, zebrafish have also been used to
In the wild, their life span is up to 1.5 years but, in the laboratory, cray‐ study addiction (Mathur & Guo, 2010; Schneider, 2017). For example,
fish can live for 3–6 years (Huner et al., 1991). Depending on their size, larvae pretreated with morphine prefer water containing morphine in a
females usually lay 100–500 eggs in each clutch and can reproduce self‐immersion test (Bretaud et al., 2007). Another key practical advan‐
more than once a year (Huner et al., 1991). Thus, crayfish arise as an tage of utilizing aquatic models, such as zebrafish and crayfish, is the
important model for experimental studies due to their easy laboratory use of immersion as route of administration, which remarkably facili‐
maintenance and high reproductive capacity. tates low‐invasive treatment, group medication (Treves & Brown, 2000)
Individual identification and labeling in the red‐swamp crayfish and increases the ease of drug dosing (Schroeder & Sneddon, 2017).
is easier than in zebrafish, including subcutaneous injection of color Therefore, zebrafish and crayfish may also represent useful model or‐
dyes (Cheung, Chatterjee, & Gerlai, 2014), acoustic (PIT) tags (Cousin ganisms for bioethical research, utilizing less stressful and non‐invasive
et al., 2012; Delcourt et al., 2018), binary‐coded wire tags (Isely & procedures (de Abreu, Giacomini, Echevarria, & Kalueff, 2019).
Eversole, 1998), enumerated plastic streamers (Meriweather, 1986), In general, to better understand human emotional disorders, we
oil‐based permanent markers (Ramalho, McClain, & Anastácio, 2010) may need to target not only specific individual phenotypes of inter‐
and cauterization applied to exoskeleton (Buřič, Kozák, & Vích, est, but also their neural aspects, such as neurochemistry or circuitry
2008). For a longer‐term marking, implanting alphanumeric tag or (Demin et al., 2019). Because no animal is a perfect replication of the
visible implant elastomers (both applied under transparent ventral human emotional landscape, not all criteria can be met by a single
abdominal cuticle) or internal PIT tags (Buřič et al., 2008) have al‐ model of affective behavior (Demin et al., 2019). Thus, using a combina‐
ready been used, therefore making behavioral research of individual tion of different model organisms (e.g., rodents, zebrafish and crayfish)
characteristic easier in this species. may improve our understanding of each specific emotional condition.
Furthermore, somewhat differing from zebrafish, red‐swamp Despite all the advantages, these two aquatic models also  pres‐
crayfish have a remarkable tolerance to a wide array of ecological ent some limitations. For example, there are some discrepancies in
 |
10       DE ABREU et al.

pharmacological effects on emotional behaviors, including anx‐ Abreu, M. S. D., Koakoski, G., Ferreira, D., Oliveira, T. A., Rosa, J. G.
iolytic (Hamilton et al., 2017), anxiogenic‐like (de Abreu, Friend, S. D., Gusso, D., … Barcellos, L. J. G. (2014). Diazepam and fluoxe‐
tine decrease the stress response in zebrafish. PLoS ONE, 9(7), 5.
Amstislavskaya, & Kalueff, 2018) or no effects (Cho, Lee, Choi, Hwang,
https​://doi.org/10.1371/journ​al.pone.0103232
& Lee, 2012) of scopolamine in zebrafish. In contrast, the effects of Ahmad, F., & Richardson, M. K. (2013). Exploratory behaviour in the open
scopolamine on anxiety in crayfish are unknown. Serotonin exerts both field test adapted for larval zebrafish: Impact of environmental com‐
anxiogenic‐ and anxiolytic‐like effect in crayfish (Fossat et al., 2015; plexity. Behavioural Processes, 92, 88–98. https​://doi.org/10.1016/j.
beproc.2012.10.014
Trevor James Hamilton, Kwan, Gallup, & Tresguerres, 2016), while in
Alcaro, A., Panksepp, J., & Huber, R. (2011). D‐amphetamine stimu‐
rodents and zebrafish it has an anxiolytic‐like action (Farhan & Haleem, lates unconditioned exploration/approach behaviors in crayfish:
2016; Giacomini et al., 2016). One possible explanation for these dif‐ Towards a conserved evolutionary function of ancestral drug reward.
ferences may be genetic differences from mammals, including some du‐ Pharmacology Biochemistry and Behavior, 99(1), 75–80. https​://doi.
plicated genes (in zebrafish), so the combination of genetic components org/10.1016/j.pbb.2011.04.004
Anastácio, P. M., Banha, F., Capinha, C., Bernardo, J. M., Costa, A.
and the expression of these genes may result in distinct phenotypic re‐
M., Teixeira, A., & Bruxelas, S. (2015). Indicators of movement
sponses, and may explain some of the varying responses to drugs when and space use for two co‐occurring invasive crayfish species.
compared to humans and rodents (Gutekunst et al., 2018; Kalueff et al., Ecological Indicators, 53, 171–181. https​://doi.org/10.1016/j.ecoli​
2014). Taken together, the evidence discussed here suggests both ze‐ nd.2015.01.019
Aquiloni, L., Giulianini, P. G., Mosco, A., Guarnaccia, C., Ferrero, E., &
brafish and crayfish as promising experimental models of stress‐related
Gherardi, F. (2012). Crustacean hyperglycemic hormone (cHH) as a
conditions, including anxiety, aggression and social deficits. modulator of aggression in crustacean decapods. PLoS ONE, 7(11),
e50047. https​://doi.org/10.1371/journ​al.pone.0050047
Aquiloni, L., Ilhéu, M., & Gherardi, F. (2005). Habitat use and dispersal of
AC K N OW L E D G M E N T S the invasive crayfish Procambarus clarkii in ephemeral water bodies
of Portugal. Marine and Freshwater Behaviour and Physiology, 38(4),
MCS is currently supported by National Funds through FCT ‐ 225–236.
Foundation for Science and Technology. AVK is supported by the Araujo, J., Maximino, C., de Brito, T. M., da Silva, A. W. B., Oliveira, K. R.
Russian Science Foundation grant 19‐15‐00053. KAD is supported M., Batista, E. d. J. O, … Gouveia, A. (2012). Behavioral and pharma‐
cological aspects of anxiety in the light/dark preference test. In Allan
by the Fellowship of the President of Russia and SPSU Rector
V. Kalueff, & Adam Michael Stewart (Eds.), Zebrafish protocols for neu‐
Productivity Fellowship for PhD Students. CM is supported by robehavioral research (pp. 191–202). Totowa, NJ: Springer.
CNPq/Brazil under Edital Universal 2016 (400726/2016‐5). PMA Bacqué‐Cazenave, J., Cattaert, D., Delbecque, J.‐P., & Fossat, P. (2017).
and FB are supported by the strategic plan of MARE ‐ Marine and Social harassment induces anxiety‐like behaviour in crayfish.
Scientific Reports, 7, 39935. https​://doi.org/10.1038/srep3​9935
Environmental Sciences Centre (UID/MAR/04292/2019).
Banha, F., & Anastácio, P. M. (2014). Desiccation survival capacities of
two invasive crayfish species. Knowledge and Management of Aquatic
Ecosystems, 413, 1. https​://doi.org/10.1051/kmae/2013084
C O N FL I C T O F I N T E R E S T Baracchi, D., Lihoreau, M., & Giurfa, M. (2017). Do insects have emotions?
Some insights from bumble bees. Frontiers in Behavioral Neuroscience,
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Barba‐Escobedo, P. A., & Gould, G. G. (2012). Visual social prefer‐
ences of lone zebrafish in a novel environment: Strain and anxio‐
AU T H O R C O N T R I B U T I O N S lytic effects. Genes, Brain and Behavior, 11(3), 366–373. https​://doi.
org/10.1111/j.1601‐183X.2012.00770.x
Conceptualization, M.S.A., M.C.S., C.M. and A.V.K.; Writing — Original Barbosa, H. P., Lima‐Maximino, M. G., & Maximino, C. (2019). Acute
Draft, M.S.A., C.M., F.B., P.M.A., K.A.D., A.V.K. and M.C.S. fluoxetine differently affects aggressive display in zebrafish phe‐
notypes. Aggressive Behavior, 45(1), 62–69. https​://doi.org/10.1002/
ab.21797​
ORCID Bass, S. L. S., & Gerlai, R. (2008). Zebrafish (Danio rerio) responds differ‐
entially to stimulus fish: The effects of sympatric and allopatric pred‐
Murilo S. de Abreu  https://orcid.org/0000-0001-5562-0715 ators and harmless fish. Behavioural Brain Research, 186(1), 107–117.
https​://doi.org/10.1016/j.bbr.2007.07.037
Caio Maximino  https://orcid.org/0000-0002-3261-9196
Belzung, C., & Lemoine, M. (2011). Criteria of validity for animal mod‐
Pedro M. Anastácio  https://orcid.org/0000-0003-1808-3847 els of psychiatric disorders: Focus on anxiety disorders and de‐
pression. Biology of Mood & Anxiety Disorders, 1(1), 9. https​://doi.
Allan V. Kalueff  https://orcid.org/0000-0002-7525-1950
org/10.1186/2045‐5380‐1‐9
Marta C. Soares  https://orcid.org/0000-0002-5213-2377 Bencan, Z., Sledge, D., & Levin, E. D. (2009). Buspirone, chlordiazepoxide
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