Background: In the bestseller book “Why Zebras Don’t Get Ulcers”, Robert Sapolsky argues that animals do not suffer from stress-related diseases like humans because for them, stress is episodic, while humans in contrast suffer from chronic psychological stress. In particular, the idea that fish cannot experience psychological stress is still prevalent, partly due to the lack of a homologous brain area to the neocortex. However, emerging evidence suggests that teleosts can undergo psychological stress, defined as a subjective and perceptual experience of the stressor, and in recent years, the underlying mechanisms started to be unveiled. Summary: The occurrence of cognitive appraisal in the assessment of stressors has been demonstrated in fish, indicating that the subjective evaluation of stimulus valence and salience, rather than absolute intrinsic characteristics of the stimulus itself, play a key role in the activation of the stress response. Moreover, individual biases (i.e., cognitive bias) in the cognitive appraisal of stimuli have also been described in fish, with some individuals consistently evaluating ambiguous stimuli as positive (aka optimists) whereas other individuals (aka pessimists) appraise them as negative. As a result, optimists and pessimists show consistent differences in stress reactivity and susceptibility/resilience to disease. Finally, social context has also been shown to modulate the response to aversive stimuli with the behavior of conspecifics either buffering or enhancing the response (i.e., social buffering vs. social contagion). Key Messages: Cognitive appraisal of stressors occurs in fish, implying that the stress response is modulated by a subjective and perceptual experience of the stressor. Moreover, interindividual consistent cognitive biases in the appraisal of stressors are also present in fish making some individuals more susceptible to stress-related diseases. Therefore, psychological stress has a health toll in fish, and psychologically stressed fish can potentially have ulcers.

1.
Sapolsky
RM
.
Why zebras don’t get ulcers: a guide to stress, stress related diseases, and coping
;
1994
.
2.
Selye
H
.
Stress and the general adaptation syndrome
.
Br Med J
.
1950
;
1
(
4667
):
1383
92
.
3.
Del Giudice
M
,
Buck
CL
,
Chaby
LE
,
Gormally
BM
,
Taff
CC
,
Thawley
CJ
, et al
.
What is stress? A systems perspective
.
Integr Comp Biol
.
2018
;
58
(
6
):
1019
32
.
4.
Romero
LM
,
Dickens
MJ
,
Cyr
NE
.
The reactive scope model - a new model integrating homeostasis, allostasis, and stress
.
Horm Behav
.
2009
;
55
(
3
):
375
89
.
5.
Ellis
BJ
,
Del Giudice
M
.
Beyond allostatic load: rethinking the role of stress in regulating human development
.
Dev Psychopathol
.
2014
;
26
(
1
):
1
20
.
6.
Del Giudice
M
,
Ellis
BJ
,
Shirtcliff
EA
.
The adaptive calibration model of stress responsivity
.
Neurosci Biobehav Rev
.
2011
;
35
(
7
):
1562
92
.
7.
Ursin
H
,
Eriksen
H
.
Cognitive activation theory of stress, sensitization, and common health complaints
.
Ann N Y Acad Sci
.
2007
;
1113
:
304
10
.
8.
Ursin
H
,
Eriksen
HR
.
The cognitive activation theory of stress
.
Psychoneuroendocrinology
.
2004
;
29
(
5
):
567
92
.
9.
Moors
A
,
Ellsworth
PC
,
Scherer
KR
,
Frijda
NH
.
Appraisal theories of emotion: state of the art and future development
.
2013
;
5
(
2
):
119
24
.
10.
Smith
CA
,
Kirby
LD
.
Putting appraisal in context: toward a relational model of appraisal and emotion
.
Cogn Emot
.
2009
;
23
(
7
):
1352
72
.
11.
Roseman
IJ
,
Smith
CA
.
Appraisal theory: overview, assumptions, varieties, controversies
. In:
Scherer
KR
,
Schorr
A
,
Johnstone
T
, editors.
Appraisal processes in emotion: theory, methods, research
.
Oxford University Press
;
2001
. p.
3
19
.
12.
Scherer
KR
.
The dynamic architecture of emotion: evidence for the component process model
.
Cogn Emot
.
2009
;
23
(
7
):
1307
51
.
13.
Scherer
KR
.
Appraisal considered as a process of multilevel sequential checking
. In:
Scherer
KR
,
Schorr
A
,
Johnstone
T
, editors.
Appraisal processes in emotion: theory, methods, research
.
New York and Oxford
:
Oxford University Press
;
2001
. p.
92
120
.
14.
Lazarus
RS
.
Relational meaning and discrete emotions
. In:
Scherer
KR
,
Schorr
A
,
Johnstone
T
, editors.
Appraisal processes in emotion: theory, methods, research
.
Oxford University Press
;
2001
. p.
37
67
.
15.
Ellsworth
PC
,
Scherer
KR
.
Appraisal processes in emotion
. In:
Davidson
RJ
,
Scherer
KR
,
Goldsmith
HH
, editors.
Handbook of affective sciences
.
Oxford University Press
;
2003
. p.
572
95
.
16.
Wong
K
,
Elegante
M
,
Bartels
B
,
Elkhayat
S
,
Tien
D
,
Roy
S
, et al
.
Analyzing habituation responses to novelty in zebrafish (Danio rerio)
.
Behav Brain Res
.
2010
;
208
(
2
):
450
7
.
17.
Xu
X
,
Scott-Scheiern
T
,
Kempker
L
,
Simons
K
.
Active avoidance conditioning in zebrafish (Danio rerio)
.
Neurobiol Learn Mem
.
2007
;
87
(
1
):
72
7
.
18.
Al-Imari
L
,
Gerlai
R
.
Sight of conspecifics as reward in associative learning in zebrafish (Danio rerio)
.
Behav Brain Res
.
2008
;
189
(
1
):
216
9
.
19.
Millot
S
,
Cerqueira
M
,
Castanheira
M-F
,
Overli
O
,
Oliveira
RF
,
Martins
CIM
.
Behavioural stress responses predict environmental perception in European Sea Bass (Dicentrarchus labrax)
.
PLoS One
.
2014
;
9
(
9
):
108800
.
20.
Millot
S
,
Cerqueira
M
,
Castanheira
MF
,
Øverli
Ø
,
Martins
CIM
,
Oliveira
RF
.
Use of conditioned place preference/avoidance tests to assess affective states in fish
.
Appl Anim Behav Sci
.
2014
;
154
:
104
11
.
21.
Galhardo
L
,
Almeida
O
,
Oliveira
RF
.
Measuring motivation in a cichlid fish: an adaptation of the push-door paradigm
.
Appl Anim Behav Sci
.
2011
;
130
(
1–2
):
60
70
.
22.
Weiss
JM
.
Somatic effects of predictable and unpredictable shock
.
Psychosom Med
.
1970
;
32
(
4
):
397
408
.
23.
Piato
ÂL
,
Capiotti
KM
,
Tamborski
AR
,
Oses
JP
,
Barcellos
LJG
,
Bogo
MR
, et al
.
Unpredictable chronic stress model in zebrafish (Danio rerio): behavioral and physiological responses
.
Prog Neuro-Psychopharmacol Biol Psychiatry
.
2011
;
35
(
2
):
561
7
.
24.
Galhardo
L
,
Vital
J
,
Oliveira
RF
.
The role of predictability in the stress response of a cichlid fish
.
Physiol Behav
.
2011
;
102
(
3–4
):
367
72
.
25.
Weiss
JM
.
Effects of coping responses on stress
.
J Comp Physiol Psychol
.
1968
;
65
(
2
):
251
60
.
26.
Greiveldinger
L
,
Veissier
I
,
Boissy
A
.
Behavioural and physiological responses of lambs to controllable vs. uncontrollable aversive events
.
Psychoneuroendocrinology
.
2009
;
34
(
6
):
805
14
.
27.
Overmier
JB
,
Patterson
J
,
Wielkiewicz
RM
.
Environmental contingencies as sources of stress in animals
.
Coping and health
.
Boston, MA
:
Springer US
;
1980
. p.
1
38
.
28.
Bean
GJ
,
Mason
G
,
Bateson
.
Mason, and Bateson, “contrafreeloading in starlings: testing the information hypothesis,”
.
Behav
.
1999
;
136
(
10–11
):
1267
82
.
29.
Neuringer
AJ
.
Animals respond for food in the presence of free food
.
Science
.
1969
;
166
(
3903
):
399
401
.
30.
Rosenberger
K
,
Simmler
M
,
Nawroth
C
,
Langbein
J
,
Keil
N
.
Goats work for food in a contrafreeloading task
.
Sci Rep
.
2020
;
10
(
1
):
22336
12
.
31.
Ogura
T
.
Contrafreeloading and the value of control over visual stimuli in Japanese macaques (Macaca fuscata)
.
Anim Cogn
.
2011
;
14
(
3
):
427
31
.
32.
Menzel
EW
.
Chimpanzees (Pan troglodytes): problem seeking versus the bird-in-hand, least-effort strategy
.
Primates
.
1991
;
32
(
4
):
497
508
.
33.
Cerqueira
M
,
Millot
S
,
Castanheira
MF
,
Félix
AS
,
Silva
T
,
Oliveira
GA
, et al
.
Cognitive appraisal of environmental stimuli induces emotion-like states in fish
.
Sci Rep
.
2017
;
7
(
1
):
13181
.
34.
Cerqueira
M
,
Millot
S
,
Felix
A
,
Silva
T
,
Oliveira
GA
,
Oliveira
CCV
, et al
.
Cognitive appraisal in fish: stressor predictability modulates the physiological and neurobehavioural stress response in sea bass
.
Proc Biol Sci
.
2020
;
287
(
1923
):
20192922
.
35.
Cerqueira
M
,
Millot
S
,
Silva
T
,
Félix
AS
,
Castanheira
MF
,
Rey
S
, et al
.
Stressor controllability modulates the stress response in fish
.
BMC Neurosci
.
2021
;
22
(
1
):
48
.
36.
Okuno
H
.
Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers
.
Neurosci Res
.
2011
;
69
(
3
):
175
86
.
37.
Kawashima
T
,
Okuno
H
,
Bito
H
.
A new era for functional labeling of neurons: activity-dependent promoters have come of age
.
Front Neural Circuits
.
2014
;
8
:
37
.
38.
Ganz
J
,
Kroehne
V
,
Freudenreich
D
,
Machate
A
,
Geffarth
M
,
Braasch
I
, et al
.
Subdivisions of the adult zebrafish pallium based on molecular marker analysis
.
F1000Res
.
2014
;
3
(
3
):
308
.
39.
Bateson
M
,
Desire
S
,
Gartside
SE
,
Wright
GA
.
Agitated honeybees exhibit pessimistic cognitive biases
.
Curr Biol
.
2011
;
21
(
12
):
1070
3
.
40.
Mendl
M
,
Brooks
J
,
Basse
C
,
Burman
O
,
Paul
E
,
Blackwell
E
, et al
.
Dogs showing separation-related behaviour exhibit a “pessimistic” cognitive bias
.
Curr Biol
.
2010
;
20
(
19
):
R839
40
.
41.
Lagisz
M
,
Zidar
J
,
Nakagawa
S
,
Neville
V
,
Sorato
E
,
Paul
ES
, et al
.
Optimism, pessimism and judgement bias in animals: a systematic review and meta-analysis
.
Neurosci Biobehav Rev
.
2020
;
118
:
3
17
.
42.
Mendl
M
,
Burman
OHP
,
Parker
RMA
,
Paul
ES
.
Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms
.
Appl Anim Behav Sci
.
2009
;
118
(
3–4
):
161
81
.
43.
Laubu
C
,
Louâpre
P
,
Dechaume-Moncharmont
FX
.
Pair-bonding influences affective state in a monogamous fish species
.
Proc R Soc A B
.
2019
;
286
(
1904
):
20190760
.
44.
Berlinghieri
F
,
Rizzuto
G
,
Kruizinga
L
,
Riedstra
B
,
Groothuis
TGG
,
Brown
C
.
Are lateralized and bold fish optimistic or pessimistic
.
Anim Cogn
.
2024
;
27
(
1
):
42
.
45.
Alvarado
MV
,
Felip
A
,
Espigares
F
,
Oliveira
RF
.
Unexpected appetitive events promote positive affective state in juvenile European sea bass
.
Sci Rep
.
2023
;
13
(
1
):
22064
.
46.
Faustino
AI
,
Oliveira
GA
,
Oliveira
RF
.
Linking appraisal to behavioral flexibility in animals: implications for stress research
.
Front Behav Neurosci
.
2015
;
9
:
104
.
47.
Espigares
F
,
Martins
R
,
Oliveira
R
.
A behavioural assay to investigate judgment bias in zebrafish
.
Bio Protoc
.
2022
;
12
(
4
):
e4327
.
48.
Espigares
F
,
Optimistic and pessimistic cognitive judgement bias modulates the stress response and cancer progression in zebrafish
.
bioRxiv
.
2024
.
49.
Espigares
F
,
Alvarado
MV
,
Faísca
P
,
Abad-Tortosa
D
,
Oliveira
RF
.
Pessimistic cognitive bias is associated with enhanced reproductive investment in female zebrafish
.
Biol Lett
.
2022
;
18
(
12
).
50.
Espigares
F
,
Abad-Tortosa
D
,
Varela
SAM
,
Ferreira
MG
,
Oliveira
RF
.
Short telomeres drive pessimistic judgement bias in zebrafish
.
Biol Lett
.
2021
;
17
(
3
):
rsbl.2020.0745
.
51.
Sharot
T
,
Guitart-Masip
M
,
Korn
CW
,
Chowdhury
R
,
Dolan
RJ
.
How dopamine enhances an optimism bias in humans
.
Curr Biol
.
2012
;
22
(
16
):
1477
81
.
52.
Charpentier
CJ
,
Bromberg-Martin
ES
,
Sharot
T
.
Valuation of knowledge and ignorance in mesolimbic reward circuitry
.
Proc Natl Acad Sci U S A
.
2018
;
115
(
31
):
E7255
64
.
53.
Rygula
R
,
Papciak
J
,
Popik
P
.
Trait pessimism predicts vulnerability to stress-induced anhedonia in rats
.
Neuropsychopharmacology
.
2013
;
38
(
11
):
2188
96
.
54.
Brandl
HB
,
Pruessner
JC
,
Farine
DR
.
The social transmission of stress in animal collectives
.
Proc Biol Sci
.
2022
;
289
(
1974
):
20212158
.
55.
Kikusui
T
,
Winslow
JT
,
Mori
Y
.
Social buffering: relief from stress and anxiety
.
Philos Trans R Soc Lond B Biol Sci
.
2006
;
361
(
1476
):
2215
28
.
56.
Gilmour
KM
,
Bard
B
.
Social buffering of the stress response: insights from fishes
.
Biol Lett
.
2022
;
18
(
10
):
20220332
.
57.
Culbert
BM
,
Gilmour
KM
,
Balshine
S
.
Social buffering of stress in a group-living fish
.
Proc R Soc A B
.
2019
;
286
(
1910
):
20191626
.
58.
Schumann
S
,
Mozzi
G
,
Piva
E
,
Devigili
A
,
Negrato
E
,
Marion
A
, et al
.
Social buffering of oxidative stress and cortisol in an endemic cyprinid fish
.
Sci Rep
.
2023
;
13
(
1
):
20579
.
59.
Yusishen
ME
,
Yoon
GR
,
Bugg
W
,
Jeffries
KM
,
Currie
S
,
Anderson
WG
.
Love thy neighbor: social buffering following exposure to an acute thermal stressor in a gregarious fish, the lake sturgeon (Acipenser fulvescens)
.
Comp Biochem Physiol Mol Integr Physiol
.
2020
;
243
:
110686
.
60.
Mommer
BC
,
Bell
AM
.
A test of maternal programming of offspring stress response to predation risk in threespine sticklebacks
.
Physiol Behav
.
2013
;
122
:
222
7
.
61.
Pagnussat
N
,
Piato
AL
,
Schaefer
IC
,
Blank
M
,
Tamborski
AR
,
Guerim
LD
, et al
.
One for all and all for one: the importance of shoaling on behavioral and stress responses in zebrafish
.
Zebrafish
.
2013
;
10
(
3
):
338
42
.
62.
Faustino
AI
,
Tacão-Monteiro
A
,
Oliveira
RF
.
Mechanisms of social buffering of fear in zebrafish
.
Sci Rep
.
2017
;
7
(
1
):
44329
.
63.
Jesuthasan
SJ
,
Mathuru
AS
.
The alarm response in zebrafish: innate fear in a vertebrate genetic model
.
J Neurogenet
.
2008
;
22
(
3
):
211
28
.
64.
Akinrinade
IDF
Oxytocinergic modulation of social information use in threat perception in zebrafish
;
2020
.
65.
Hall
D
,
Suboski
MD
.
Visual and olfactory stimuli in learned release of alarm reactions by zebra Danio fish (brachydanio rerio)
.
Neurobiol Learn Mem
.
1995
;
63
(
3
):
229
40
.
66.
Suboski
MD
,
Bain
S
,
Carty
AE
,
McQuoid
LM
,
Seelen
MI
,
Seifert
M
.
Alarm reaction in acquisition and social transmission of simulated-predator recognition by zebra danio fish (Brachydanio rerio)
.
J Comp Psychol
.
1990
;
104
(
1
):
101
12
.
67.
Pinho
JS
,
Castilho
M
,
Sollari
JS
,
Oliveira
RF
.
Innate chemical, but not visual, threat cues have been co-opted as unconditioned stimulus for social fear learning in zebrafish
.
Genes Brain Behav
.
2020
;
19
(
8
).
68.
Verheijen
FJ
.
Transmission of a flight reaction amongst a school of fish and the underlying sensory mechanisms
.
Experientia
.
1956
;
12
(
5
):
202
4
.
69.
Manassa
RP
,
McCormick
MI
.
Social learning improves survivorship at a life-history transition
.
Oecologia
.
2013
;
171
(
4
):
845
52
.
70.
Cordi
V
,
Ortubay
S
,
Lozada
M
.
Visual cues during the alarm reaction of Gymnocharacinus bergi (Pisces, Characidae)
.
J Appl Ichthyol
.
2005
;
21
(
6
):
487
91
.
71.
Akinrinade
I
,
Kareklas
K
,
Teles
MC
,
Reis
TK
,
Gliksberg
M
,
Petri
G
, et al
.
Evolutionarily conserved role of oxytocin in social fear contagion in zebrafish
.
Science
.
2023
;
379
(
6638
):
1232
7
.
72.
Peen
NF
,
Duque-Wilckens
N
,
Trainor
BC
.
Convergent neuroendocrine mechanisms of social buffering and stress contagion
.
Horm Behav
.
2021
;
129
:
104933
.
73.
Jung
T
,
Jang
M
,
Noh
J
.
Role of medial prefrontal cortical neurons and oxytocin modulation in the establishment of social buffering
.
Exp Neurobiol
.
2021
;
30
(
1
):
48
58
.
74.
Pace
SA
,
Lukinic
E
,
Wallace
T
,
McCartney
C
,
Myers
B
.
Cortical–brainstem circuitry attenuates physiological stress reactivity
.
J Physiol
.
2024
;
602
(
5
):
949
66
.
75.
Keysers
C
,
Knapska
E
,
Moita
MA
,
Gazzola
V
.
Emotional contagion and prosocial behavior in rodents
.
Trends Cogn Sci
.
2022
;
26
(
8
):
688
706
.
76.
Baden
T
.
Circuit mechanisms for colour vision in zebrafish
.
Curr Biol
.
2021
;
31
(
12
):
R807
20
.
77.
Key
B
.
Why fish do not feel pain
.
Anim Sentience
.
2016
;
1
(
3
):
1
.
78.
Striedter
G
.
Lack of neocortex does not imply fish cannot feel pain
.
Anim Sentience
.
2016
;
1
(
3
):
15
.
79.
Brown
C
.
Comparative approach to pain perception in fishes: commentary on key on fish pain
.
Anim Sentience
.
2016
;
1
(
3
):
1
7
. Available from: https://researchers.mq.edu.au/en/publications/comparative-approach-to-pain-perception-in-fishes-commentary-on-k (Accessed 07 Jun 2024).
You do not currently have access to this content.