Abstract
Sleep is widespread across the animal kingdom. However, most comparative sleep data exist for terrestrial vertebrates, with much less known about sleep in amphibians, bony fishes, and invertebrates. There is an absence of knowledge on sleep in cartilaginous fishes. Sharks and rays are amongst the earliest vertebrates, and may hold clues to the evolutionary history of sleep and sleep states found in more derived animals, such as mammals and birds. Here, we review the literature concerning activity patterns, sleep behaviour, and electrophysiological evidence for sleep in cartilaginous (and bony) fishes following an exhaustive literature search that found more than 80 relevant studies in laboratory and field environments. Evidence for sleep in sharks and rays that respire without swimming is preliminary; evidence for sleep in continuously swimming fishes is currently absent. We discuss ways in which the latter group might sleep concurrent with sustained movement, and conclude with suggestions for future studies in order to provide more comprehensive data on when, how, and why sharks and rays sleep.
References
1.
Andrews
KS
, Williams
GD
, Farrer
D
, Tolimieri
N
, Harvey
CJ
, Bargmann
G
, et al. Diel activity patterns of sixgill sharks, Hexanchus griseus: the ups and downs of an apex predator
. Anim Behav
. 2009
;78
(2
):525
–36
. 0003-34722.
Appelbaum
L
, Wang
GX
, Maro
GS
, Mori
R
, Tovin
A
, Marin
W
, et al. Sleep-wake regulation and hypocretin-melatonin interaction in zebrafish
. Proc Natl Acad Sci USA
. 2009
Dec
;106
(51
):21942
–7
.
[PubMed]
0027-84243.
Árnason
BB
, Þorsteinsson
H
, Karlsson
KÆ
. Absence of rapid eye movements during sleep in adult zebrafish
. Behav Brain Res
. 2015
Sep
;291
:189
–94
.
[PubMed]
0166-43284.
Aserinsky
E
, Kleitman
N
. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep
. Science
. 1953
Sep
;118
(3062
):273
–4
.
[PubMed]
0036-80755.
Aulsebrook
AE
, Jones
TM
, Rattenborg
NC
, Roth
TC
2nd, Lesku
JA
. Sleep ecophysiology: integrating neuroscience and ecology
. Trends Ecol Evol
. 2016
Aug
;31
(8
):590
–9
.
[PubMed]
0169-53476.
Barker
SM
, Peddemors
VM
, Williamson
JE
. A video and photographic study of aggregation, swimming and respiratory behaviour changes in the Grey Nurse Shark (Carcharias taurus) in response to the presence of SCUBA divers
. Mar Freshwat Behav Physiol
. 2011
;44
(2
):75
–92
. 1023-62447.
Barnett
A
, Payne
NL
, Semmens
JM
, Fitzpatrick
R
. Ecotourism increases the field metabolic rate of whitetip reef sharks
. Biol Conserv
. 2016
;199
:132
–6
. 0006-32078.
Borbély
AA
. A two process model of sleep regulation
. Hum Neurobiol
. 1982
;1
(3
):195
–204
.
[PubMed]
0721-90759.
Brett
JR
, Blackburn
JM
. Metabolic rate and energy expenditure of the spinydogfish, Squalus acanthias
. J Fish Res Board Can
. 1978
;35
(6
):816
–21
. 0015-296X10.
Brown
CE
, Muir
BS
. Analysis of ram ventilation of fish gills with application to skipjack tuna (Katsuwonus pelamis)
. J Fish Res Board Can
. 1970
;27
(9
):1637
–52
. 0015-296X11.
Bruce
BD
, Bradford
RW
. The effects of shark cage-diving operations on the behaviour and movements of white sharks, Carcharodon carcharias, at the Neptune Islands, South Australia
. Mar Biol
. 2013
;160
(4
):889
–907
. 0025-316212.
13.
Campbell
SS
, Tobler
I
. Animal sleep: a review of sleep duration across phylogeny
. Neurosci Biobehav Rev
. 1984
;8
(3
):269
–300
.
[PubMed]
0149-763414.
Carey
FG
, Kanwisher
J
, Brazier
O
, Gabrielson
G
, Casey
J
, Pratt
H
Jr. Temperature and activities of a white shark. Carcharodon carcharias
. Copeia
. 1982
;1982
(2
):254
–60
. 0045-851115.
Carey
F
, Scharold
J
, Kalmijn
AJ
. Movements of blue sharks (Prionace glauca) in depth and course
. Mar Biol
. 1990
;106
(3
):329
–42
. 0025-316216.
Carey
FG
, Teal
JM
, Kanwisher
JW
. The visceral temperatures of mackerel sharks (Lamnidae)
. Physiol Zool
. 1981
;54
(3
):334
–44
. 0031-935X17.
Carlson
J
, Goldman
K
, Lowe
C
. Metabolism, energetic demand, and endothermy. In: Carrier
JC
, Musick
JA
, Heithaus
MR
, editors. Biology of sharks and their relatives. CRC Mar Biol Series
. Volume 1
. Boca Raton
: CRC Press
; 2004
. pp. 203
–24
. 18.
Carlson
JK
, Parsons
GR
. The effects of hypoxia on three sympatric shark species: physiological and behavioral responses
. Environ Biol Fishes
. 2001
;61
(4
):427
–33
. 0378-190919.
Casterlin
ME
, Reynolds
WW
. Diel activity patterns of the smooth dogfish shark, Mustelus canis
. Bull Mar Sci
. 1979
;29
(3
):440
–2
.0007-497720.
Chapman
DD
, Pikitch
EK
, Babcock
EA
, Shivji
MS
. Deep-diving and diel changes in vertical habitat use by Caribbean reef sharks Carcharhinus perezi
. Mar Ecol Prog Ser
. 2007
;344
:271
–5
. 0171-863021.
22.
Clark
E
, Kristof
E
. Deep-sea elasmobranchs observed from submersibles off Bermuda, Grand Cayman, and Freeport, Bahamas. In: Pratt
HL
Jr, Gruber
SH
, Taniuchi
T
, editors. Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of fisheries
. Volume 90
. Seattle
: NOAA Tech Rep NMFS
; 1990
. pp. 269
–84
.23.
Clarke
C
, Lea
J
, Ormond
R
. Reef-use and residency patterns of a baited population of silky sharks, Carcharhinus falciformis, in the Red Sea
. Mar Freshw Res
. 2011
;62
(6
):668
–75
. 1323-165024.
Clarke
TA
. The ecology of the scalloped hammerhead shark, Sphyrna lewini, in Hawaii
. Pac Sci
. 1971
;25
:133
–44
.0030-887025.
Collin
SP
. Scene through the eyes of an apex predator: a comparative analysis of the shark visual system
. Clin Exp Optom
. 2018
Sep
;101
(5
):624
–40
.
[PubMed]
0816-462226.
Compagno
LJ
. Sharks of the order Carcharhiniformes. 1st Reprint (2003
). New Jersey: The Blackburn Press; 1988.27.
Compagno
LJ
. Systematics and body form. In: Hamlett
WC
, editor. Sharks, skates and rays: the biology of elasmobranch fishes
. Volume 1
. Baltimore
: John Hopkins University Press
; 1999
. pp. 1
–42
.28.
Cortés
E
, Gruber
SH
, Cortes
E
. Diet, feeding habits and estimates of daily ration of young lemon sharks, Negaprion brevirostris (Poey)
. Copeia
. 1990
;1990
(1
):204
–18
. 0045-851129.
Dubin
RE
, Baker
JD
. Two types of cover-seeking behavior at sunset by the princess parrotfish, Scarus taeniopterus, at Barbados, West Indies
. Bull Mar Sci
. 1982
;32
(2
):572
–83
.0007-497730.
Duboué
ER
, Borowsky
RL
, Keene
AC
. β-adrenergic signaling regulates evolutionarily derived sleep loss in the Mexican cavefish
. Brain Behav Evol
. 2012
;80
(4
):233
–43
.
[PubMed]
1421-974331.
Duboué
ER
, Keene
AC
, Borowsky
RL
. Evolutionary convergence on sleep loss in cavefish populations
. Curr Biol
. 2011
Apr
;21
(8
):671
–6
.
[PubMed]
0960-982232.
Dudgeon
CL
, Lanyon
JM
, Semmens
JM
. Seasonality and site fidelity of the zebra shark, Stegostoma fasciatum, in southeast Queensland, Australia
. Anim Behav
. 2013
;85
(2
):471
–81
. 0003-347233.
Ebert
DA
. Observations on the predatory behaviour of the sevengill shark Notorynchus cepedianus
. S Afr J Mar Sci
. 1991
;11
(1
):455
–65
. 0257-761534.
Enger PS. The electroencephalogram of the codfish (Gadus callarias). Acta Physiol Scand. 1957 Apr;39(1):55–72.
35.
Falcón
J
, Besseau
L
, Sauzet
S
, Boeuf
G
. Melatonin effects on the hypothalamo-pituitary axis in fish
. Trends Endocrinol Metab
. 2007
Mar
;18
(2
):81
–8
.
[PubMed]
1043-276036.
Finstad
WO
, Nelson
DR
. Circadian activity rhythm in the horn shark, Heterodontus francisci: effect of light intensity
. Bull South Calif Acad Sci
. 1975
;74
(1
):20
–6
.0038-387237.
Fitzpatrick
R
, Abrantes
KG
, Seymour
J
, Barnett
A
. Variation in depth of whitetip reef sharks: does provisioning ecotourism change their behaviour?
Coral Reefs
. 2011
;30
(3
):569
–77
. 1432-097538.
Fuss
T
, Bleckmann
H
, Schluessel
V
. Visual discrimination abilities in the gray bamboo shark (Chiloscyllium griseum)
. Zoology (Jena)
. 2014
Apr
;117
(2
):104
–11
.
[PubMed]
1873-272039.
Gleiss
AC
, Gruber
SH
, Wilson
RP
. Multi-channel data-logging: towards determination of behaviour and metabolic rate in free-swimming sharks. In: Nielsen
JL
, Arrizabalaga
H
, Fragoso
N
, Hobday
A
, Lutcavage
M
, Sibert
J
, editors. Tagging and tracking of marine animals with electronic devices
. New York
: Springer
; 2009
. pp. 211
–28
. 40.
Gleiss
AC
, Wright
S
, Liebsch
N
, Wilson
RP
, Norman
B
. Contrasting diel patterns in vertical movement and locomotor activity of whale sharks at Ningaloo Reef
. Mar Biol
. 2013
;160
(11
):2981
–92
. 0025-316241.
Goldshmid
R
, Holzman
R
, Weihs
D
, Genin
A
. Aeration of corals by sleep-swimming fish
. Limnol Oceanogr
. 2004
;49
(5
):1832
–9
. 0024-359042.
Goley
PD
. Behavioral aspects of sleep in pacific white-sided dolphins (Lagenorhynchus obliquidens, Gill 1865) 1
. Mar Mamm Sci
. 1999
;15
(4
):1054
–64
. 0824-046943.
Graeber
RC
, Ebbesson
SO
. Visual discrimination learning in normal and tectal-ablated nurse sharks (Ginglymostoma cirratum)
. Comp Biochem Physiol A Comp Physiol
. 1972
May
;42
(1
):131
–9
.
[PubMed]
0300-962944.
Gravett
N
, Bhagwandin
A
, Sutcliffe
R
, Landen
K
, Chase
MJ
, Lyamin
OI
, et al. Inactivity/sleep in two wild free-roaming African elephant matriarchs - Does large body size make elephants the shortest mammalian sleepers?
PLoS One
. 2017
Mar
;12
(3
):e0171903
.
[PubMed]
1932-620345.
Gruber
SH
, Nelson
DR
, Morrissey
JF
. Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon
. Bull Mar Sci
. 1988
;43
(1
):61
–76
.0007-497746.
Hart
NS
, Lisney
TJ
, Collin
SP
. Visual communication in elasmobranchs. In: Ladich
F
, Collin
SP
, Moller
P
, Kapoor
BG
, editors. Communication in fishes
. Plymouth
: Science Publishers
; 2006
. pp. 337
–92
.47.
48.
Heithaus
M
, Dill
L
, Marshall
G
, Buhleier
B
. Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem
. Mar Biol
. 2002
;140
(2
):237
–48
. 0025-316249.
Holland
K
, Lowe
C
, Peterson
J
, Gill
A
. Tracking coastal sharks with small boats: hammerhead shark pups as a case study
. Mar Freshw Res
. 1992
;43
(1
):61
–6
. 1323-165050.
Holland
KN
, Wetherbee
BM
, Peterson
JD
, Lowe
CG
. Movements and distribution of hammerhead shark pups on their natal grounds
. Copeia
. 1993
;1993
(2
):495
–502
. 0045-851151.
Holts
D
, Bedford
DW
. Horizontal and vertical movements of the shortfin mako shark, Isurus oxyrinchus, in the Southern California Bight
. Mar Freshw Res
. 1993
;44
(6
):901
–9
. 1323-165052.
Huber
R
, Ghilardi
MF
, Massimini
M
, Ferrarelli
F
, Riedner
BA
, Peterson
MJ
, et al. Arm immobilization causes cortical plastic changes and locally decreases sleep slow wave activity
. Nat Neurosci
. 2006
Sep
;9
(9
):1169
–76
.
[PubMed]
1097-625653.
Hur
SP
, Takeuchi
Y
, Itoh
H
, Uchimura
M
, Takahashi
K
, Kang
HC
, et al. Fish sleeping under sandy bottom: interplay of melatonin and clock genes
. Gen Comp Endocrinol
. 2012
May
;177
(1
):37
–45
.
[PubMed]
0016-648054.
Iglesias
TL
, Boal
JG
, Frank
MG
, Zeil
J
, Hanlon
RT
. Cyclic nature of the REM sleep-like state in the cuttlefish Sepia officinalis
. J Exp Biol
. 2019
Jan
;222
(Pt 1
):jeb174862
.
[PubMed]
0022-094955.
Iigo
M
, Tabata
M
. Circadian rhythms of locomotor activity in the goldfish Carassius auratus
. Physiol Behav
. 1996
Sep
;60
(3
):775
–81
.
[PubMed]
0031-938456.
Jaggard
J
, Robinson
BG
, Stahl
BA
, Oh
I
, Masek
P
, Yoshizawa
M
, et al. The lateral line confers evolutionarily derived sleep loss in the Mexican cavefish
. J Exp Biol
. 2017
Jan
;220
(Pt 2
):284
–93
.
[PubMed]
0022-094957.
Jaggard
JB
, Stahl
BA
, Lloyd
E
, Prober
DA
, Duboué
ER
, Keene
AC
. Hypocretin underlies the evolution of sleep loss in the Mexican cavefish
. eLife
. 2018
Feb
;7
:e32637
.
[PubMed]
2050-084X58.
Jouvet
M
, Michel
F
, Courjon
J
. Sur un stade d’activite electrique cerebrale rapide au tours du sommeil physiologique
. C R Seanc Sot Biol.
1959
;153
:101
–5
.59.
Karmanova
H
, Belich
A
. Temporal organization of “wakefulness-primary sleep” cycle in the dwarf catfish Ictalurus nebulosus
. J Evol Biochem Physiol
. 1983
;19
:131
–6
.0022-093060.
Karmanova
I
, Belich
A
, Lazarev
S
. An electrophysiological study of wakefulness and sleep-like states in fish and amphibians. In: Laming
PR
, editor. Brain mechanisms of behaviour in lower vertebrates
. Cambridge
: Cambridge University Press
; 1981
. pp. 181
–202
.61.
Karmanova
IG
, Titkov
ES
, Popova
DI
. [Species characteristics of the diurnal periodicity of rest and activity in Black Sea fish]
. Zh Evol Biokhim Fiziol
. 1976
Sep-Oct
;12
(5
):486
–8
.
[PubMed]
0044-452962.
Kavanau
JL
. Vertebrates that never sleep: implications for sleep’s basic function
. Brain Res Bull
. 1998
Jul
;46
(4
):269
–79
.
[PubMed]
0361-923063.
Kazimi
N
, Cahill
GM
. Development of a circadian melatonin rhythm in embryonic zebrafish
. Brain Res Dev Brain Res
. 1999
Oct
;117
(1
):47
–52
.
[PubMed]
0165-380664.
Klimley
A
, Butler
S
, Nelson
D
, Stull
A
. Diel movements of scalloped hammerhead sharks, Sphyrna lewini Griffith and Smith, to and from a seamount in the Gulf of California
. J Fish Biol
. 1988
;33
(5
):751
–61
. 0022-111265.
Klimley
AP
, Nelson
DR
. Diel movement patterns of the scalloped hammerhead shark (Sphyrna lewini) in relation to El Bajo Espiritu Santo: a refuging central-position social system
. Behav Ecol Sociobiol
. 1984
;15
(1
):45
–54
. 0340-544366.
Kruger
JL
, Gravett
N
, Bhagwandin
A
, Bennett
NC
, Archer
EK
, Manger
PR
. Sleep in the Cape mole rat: a short-sleeping subterranean rodent
. Brain Behav Evol
. 2016
;87
(2
):78
–87
.
[PubMed]
1421-974367.
Lesku
JA
, Aulsebrook
AE
, Kelly
ML
, Tisdale
RK
. Evolution of sleep and adaptive sleeplessness. In: Dringenberg
HC
, editor. Handbook of sleep research
. Cambridge
: Academic Press/Elsevier
; 2019
.[in press]. 68.
Lesku
JA
, Ly
LM
. Sleep origins: restful jellyfish are sleeping jellyfish
. Curr Biol
. 2017
Oct
;27
(19
):R1060
–2
.
[PubMed]
0960-982269.
Lesku
JA
, Rattenborg
NC
, Valcu
M
, Vyssotski
AL
, Kuhn
S
, Kuemmeth
F
, et al. Adaptive sleep loss in polygynous pectoral sandpipers
. Science
. 2012
Sep
;337
(6102
):1654
–8
.
[PubMed]
0036-807570.
Lesku
JA
, Vyssotski
AL
, Martinez-Gonzalez
D
, Wilzeck
C
, Rattenborg
NC
. Local sleep homeostasis in the avian brain: convergence of sleep function in mammals and birds?
Proc Biol Sci
. 2011
Aug
;278
(1717
):2419
–28
.
[PubMed]
0962-845271.
Leung
LC
, Wang
GX
, Madelaine
R
, Skariah
G
, Kawakami
K
, Deisseroth
K
, et al. Neural signatures of sleep in zebrafish
. Nature
. 2019
Jul
;571
(7764
):198
–204
.
[PubMed]
0028-083672.
Libourel
PA
, Barrillot
B
, Arthaud
S
, Massot
B
, Morel
AL
, Beuf
O
, et al. Partial homologies between sleep states in lizards, mammals, and birds suggest a complex evolution of sleep states in amniotes
. PLoS Biol
. 2018
Oct
;16
(10
):e2005982
.
[PubMed]
1544-917373.
Lima
SL
, Rattenborg
NC
, Lesku
JA
, Amlaner
CJ
. Sleeping under the risk of predation
. Anim Behav
. 2005
;70
(4
):723
–36
. 0003-347274.
Lisney
TJ
, Theiss
SM
, Collin
SP
, Hart
NS
. Vision in elasmobranchs and their relatives: 21st century advances
. J Fish Biol
. 2012
Apr
;80
(5
):2024
–54
.
[PubMed]
0022-111275.
Lyamin
OI
, Lapierre
JL
, Kosenko
PO
, Kodama
T
, Bhagwandin
A
, Korneva
SM
, et al. Monoamine release during unihemispheric sleep and unihemispheric waking in the fur seal
. Sleep (Basel)
. 2016
Mar
;39
(3
):625
–36
.
[PubMed]
0302-512876.
Lyamin
OI
, Manger
PR
, Ridgway
SH
, Mukhametov
LM
, Siegel
JM
. Cetacean sleep: an unusual form of mammalian sleep
. Neurosci Biobehav Rev
. 2008
Oct
;32
(8
):1451
–84
.
[PubMed]
0149-763477.
McKibben
JN
, Nelson
DR
. Patterns of movement and grouping of gray reef sharks, Carcharhinus amblyrhynchos, at Enewetak, Marshall Islands
. Bull Mar Sci
. 1986
;38
(1
):89
–110
.0007-497778.
McLaughlin
R
, O’Gower
A
. Life history and underwater studies of a heterodont shark
. Ecol Monogr
. 1971
;41
(4
):271
–89
. 0012-961579.
Meffert
P
. Ultrasonic recorder for locomotor activity studies
. Trans Am Fish Soc
. 1968
;97
(1
):12
–7
. 0002-848780.
Metcalfe
JD
, Butler
PJ
. Changes in activity and ventilation in response to hypoxia in unrestrained, unoperated dogfish (Scyliorhinus canicula L.)
. J Exp Biol
. 1984
Jan
;108
(1
):411
–8
.
[PubMed]
0022-094981.
Morrissey
JF
, Gruber
SH
. Home range of juvenile lemon sharks, Negaprion brevirostris
. Copeia
. 1993
;1993
(2
):425
–34
. 0045-851182.
Mukhametov
LM
, Supin
AY
, Polyakova
IG
. Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins
. Brain Res
. 1977
Oct
;134
(3
):581
–4
.
[PubMed]
0006-899383.
Myrberg
AA
Jr, Gruber
SH
. The behavior of the bonnethead shark, Sphyrna tiburo
. Copeia
. 1974
;1974
(2
):358
–74
. 0045-851184.
Nakano
H
, Matsunaga
H
, Okamoto
H
, Okazaki
M
. Acoustic tracking of bigeye thresher shark Alopias superciliosus in the eastern Pacific Ocean
. Mar Ecol Prog Ser
. 2003
;265
:255
–61
. 0171-863085.
Nath
RD
, Bedbrook
CN
, Abrams
MJ
, Basinger
T
, Bois
JS
, Prober
DA
, et al. The jellyfish Cassiopea exhibits a sleep-like state
. Curr Biol
. 2017
Oct
;27
(19
):2984
–2990.e3
.
[PubMed]
0960-982286.
Nelson
DR
, Johnson
RH
. Diel activity rhythms in the nocturnal, bottom-dwelling sharks, Heterodontus francisci and Cephaloscyllium ventriosum
. Copeia
. 1970
;1970
(4
):732
–9
. 0045-851187.
Nelson
D
, Johnson
R
. Behavior of the reef sharks of Rangiroa, French Polynesia
. Nat Geo Res Rep.
1980
;12
:479
–99
.88.
Nelson
DR
, McKibben
JN
, Strong
WR
Jr, Lowe
CG
, Sisneros
JA
, Schroeder
DM
, et al. An acoustic tracking of a megamouth shark, Megachasma pelagios: a crepuscular vertical migrator
. Environ Biol Fishes
. 1997
;49
(4
):389
–99
. 0378-190989.
Nir
Y
, Staba
RJ
, Andrillon
T
, Vyazovskiy
VV
, Cirelli
C
, Fried
I
, et al. Regional slow waves and spindles in human sleep
. Neuron
. 2011
Apr
;70
(1
):153
–69
.
[PubMed]
0896-627390.
Nobili
L
, Ferrara
M
, Moroni
F
, De Gennaro
L
, Russo
GL
, Campus
C
, et al. Dissociated wake-like and sleep-like electro-cortical activity during sleep
. Neuroimage
. 2011
Sep
;58
(2
):612
–9
.
[PubMed]
1053-811991.
Nixon
AJ
, Gruber
SH
. Diel metabolic and activity patterns of the lemon shark (Negaprion brevirostris). J Exp Zool A Comp
. Exp Biol
. 1988
;248
(1
):1
–6
.
[PubMed]
0176-863892.
Omond
S
, Ly
LM
, Beaton
R
, Storm
JJ
, Hale
MW
, Lesku
JA
. Inactivity is nycthemeral, endogenously generated, homeostatically regulated, and melatonin modulated in a free-living platyhelminth flatworm
. Sleep (Basel)
. 2017
Oct
;40
(10
):
[PubMed]
0302-512893.
Papastamatiou
YP
, Wetherbee
BM
, O’Sullivan
J
, Goodmanlowe
GD
, Lowe
CG
. Foraging ecology of cookiecutter sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds
. Environ Biol Fishes
. 2010
;88
(4
):361
–8
. 0378-190994.
Pavan
C
. Observations and experiments on the cave fish Pimelodella kronei and its relatives
. Am Nat
. 1946
May-Jun
;80
(792
):343
–61
.
[PubMed]
0003-014795.
Peyrethon
J
, Dusan-Peyrethon
D
. Etude polygraphique du cycle veille-sommeil d’un téléostéen (Tinca tinca)
. C R Seances Soc Biol Fil
. 1967
;161
(12
):2533
–7
.
[PubMed]
0037-902696.
Pinheiro-da-Silva
J
, Tran
S
, Luchiari
AC
. Sleep deprivation impairs cognitive performance in zebrafish: A matter of fact?
Behav Processes
. 2018
Dec
;157
:656
–63
.
[PubMed]
0376-635797.
Pollard
D
, Lincoln Smith
M
, Smith
A
. The biology and conservation status of the grey nurse shark (Carcharias taurus Rafinesque 1810) in New South Wales, Australia
. Aquat Conserv
. 1996
;6
(1
):1
–20
. 1052-761398.
Randall
JE
. Food habits of reef fishes of the West Indies
. Stud Trop Oceanogr
. 1967
;5
:665
–847
.0081-872099.
Randall
JE
. Contribution to the biology of the whitetipreef shark (Triaenodon obesus)
. Pac Sci
. 1977
;31
:143
–64
.0030-8870100.
Rattenborg
NC
, van der Meij
J
, Beckers
GJ
, Lesku
JA
. Local aspects of avian non-REM sleep
. Front Neurosci
. 2019
Jun
;13
:567
.
[PubMed]
1662-4548101.
Rattenborg
NC
, Voirin
B
, Cruz
SM
, Tisdale
R
, Dell’Omo
G
, Lipp
HP
, et al. Evidence that birds sleep in mid-flight
. Nat Commun
. 2016
Aug
;7
(1
):12468
.
[PubMed]
2041-1723102.
Roberts
JL
. Ram gill ventilation in fishes. In: Sharp
GD
, Dizon
AE
, editors. The physiological ecology of tunas
. Volume 1
. Ney York
: Academic Press
; 1978
. pp. 83
–8
. 103.
Rowat
D
, Meekan
M
, Engelhardt
U
, Pardigon
B
, Vely
M
. Aggregations of juvenile whale sharks (Rhincodon typus) in the Gulf of Tadjoura, Djibouti
. Environ Biol Fishes
. 2007
;80
(4
):465
–72
. 0378-1909104.
Ruckebusch
Y
. The relevance of drowsiness in the circadian cycle of farm animals
. Anim Behav
. 1972
Nov
;20
(4
):637
–43
.
[PubMed]
0003-3472105.
Ryder
R
. Effects of ambient light variations on behavior of yearling, subadult, and adult walleyes (Stizostedion vitreum vitreum)
. J Fish Res Board Can
. 1977
;34
(10
):1481
–91
. 0015-296X106.
Sabbah
S
, Laria
RL
, Gray
SM
, Hawryshyn
CW
. Functional diversity in the color vision of cichlid fishes
. BMC Biol
. 2010
Oct
;8
(1
):133
.
[PubMed]
1741-7007107.
Scariotta
T
, Nelson
D
. Diel behaviour of the blue shark, Prionace glauca, near Santa Catalina Island. Calif
. Fish Bull
. 1977
;75
:519
–28
.0096-0985108.
Sekiguchi
Y
, Arai
K
, Kohshima
S
. Sleep behaviour: sleep in continuously active dolphins
. Nature
. 2006
Jun
;441
(7096
):E9
–10
.
[PubMed]
0028-0836109.
Shapiro
CM
, Hepburn
HR
. Sleep in a schooling fish, Tilapia mossambica
. Physiol Behav
. 1976
May
;16
(5
):613
–5
.
[PubMed]
0031-9384110.
Shein-Idelson
M
, Ondracek
JM
, Liaw
HP
, Reiter
S
, Laurent
G
. Slow waves, sharp waves, ripples, and REM in sleeping dragons
. Science
. 2016
Apr
;352
(6285
):590
–5
.
[PubMed]
0036-8075111.
Shepard
EL
, Ahmed
MZ
, Southall
EJ
, Witt
MJ
, Metcalfe
JD
, Sims
DW
. Diel and tidal rhythms in diving behaviour of pelagic sharks identified by signal processing of archival tagging data
. Mar Ecol Prog Ser
. 2006
;328
:205
–13
. 0171-8630112.
Siegel
JM
. Rapid eye movement sleep. In: Kryger
M
, Roth
T
, Dement
WC
, editors. Principles and practices of sleep mechanisms
. Philadelphia
: WB Saunders
; 2016
. pp. 78
–95
.113.
Sigurgeirsson
B
, Thornorsteinsson
H
, Sigmundsdóttir
S
, Lieder
R
, Sveinsdóttir
HS
, Sigurjónsson
ÓE
, et al. Sleep-wake dynamics under extended light and extended dark conditions in adult zebrafish
. Behav Brain Res
. 2013
Nov
;256
:377
–90
.
[PubMed]
0166-4328114.
Sims
D
, Davies
S
, Bone
Q
. On the diel rhythms in metabolism and activity of post‐hatching lesser spotted dogfish, Scyliorhinus canicula
. J Fish Biol
. 1993
;43
(5
):749
–54
. 0022-1112115.
Sims
D
, Nash
J
, Morritt
D
. Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation
. Mar Biol
. 2001
;139
(6
):1165
–75
. 0025-3162116.
Sims
DW
, Southall
EJ
, Tarling
GA
, Metcalfe
JD
. Habitat‐specific normal and reverse diel vertical migration in the plankton‐feeding basking shark
. J Anim Ecol
. 2005
;74
(4
):755
–61
. 0021-8790117.
Sims
DW
, Wearmouth
VJ
, Southall
EJ
, Hill
JM
, Moore
P
, Rawlinson
K
, et al. Hunt warm, rest cool: bioenergetic strategy underlying diel vertical migration of a benthic shark
. J Anim Ecol
. 2006
Jan
;75
(1
):176
–90
.
[PubMed]
0021-8790118.
Singh
C
, Rihel
J
, Prober
DA
. Neuropeptide Y regulates sleep by modulating noradrenergic signaling
. Curr Biol
. 2017
Dec
;27
(24
):3796
–3811.e5
.
[PubMed]
0960-9822119.
Smith
K
, Scarr
M
, Scarpaci
C
. Grey nurse shark (Carcharias taurus) diving tourism: tourist compliance and shark behaviour at Fish Rock, Australia
. Environ Manage
. 2010
Nov
;46
(5
):699
–710
.
[PubMed]
0364-152X120.
Springer
S
. Field observations on large sharks of the Florida-Caribbean region. In: Gilbert
PW
, editor. Sharks and survival
. Boston
: Heath and Co.
; 1963
. pp. 95
–113
.121.
Standora
EA
, Nelson
DR
. A telemetric study of the behavior of free-swimming Pacific angel sharks, Squatina californica
. Bull South Calif Acad Sci
. 1977
;76
(3
):193
–201
.0038-3872122.
Starck
W
, Davis
W
. Night habits of fishes of Alligator Reef, Florida
. Ichthyologica.
1966
;38
(4
):313
–56
.123.
Stokesbury
MJ
, Harvey-Clark
C
, Gallant
J
, Block
BA
, Myers
RA
. Movement and environmental preferences of Greenland sharks (Somniosus microcephalus) electronically tagged in the St. Lawrence Estuary, Canada
. Mar Biol
. 2005
;148
(1
):159
–65
. 0025-3162124.
Stopa
RM
, Hoshino
K
. Electrolocation-communication discharges of the fish Gymnotus carapo L. (Gymnotidae: Gymnotiformes) during behavioral sleep
. Braz J Med Biol Res
. 1999
Oct
;32
(10
):1223
–8
.
[PubMed]
0100-879X125.
126.
Tauber
E
, Weitzman
E
. Eye movements during behavioral inactivity in certain Bermuda reef fish
. Commun Behav Biol
. 1969
;3
:131
–5
.0010-3608127.
Tefft
BC
. Acute sleep deprivation and culpable motor vehicle crash involvement
. Sleep (Basel)
. 2018
Oct
;41
(10
):
[PubMed]
0302-5128128.
Thiele
TR
, Donovan
JC
, Baier
H
. Descending control of swim posture by a midbrain nucleus in zebrafish
. Neuron
. 2014
Aug
;83
(3
):679
–91
.
[PubMed]
0896-6273129.
Titkov
E
. Characteristics of the daily periodicity of wakefulness and rest in the brown bullhead (Ictalurus nebulosus)
. J Evol Biochem Physiol
. 1976
;12
(4
):305
–9
.0022-0930130.
Tobler
I
. Phylogeny of sleep regulation. In: Kryger
MH
, Roth
T
, Dement
WC
, editors. Principles and practice of sleep medicine
. Philadelphia
: WB Saunders
; 2011
. pp. 112
–25
. 131.
Tobler
I
, Borbély
AA
. Effect of rest deprivation on motor activity of fish
. J Comp Physiol A Neuroethol Sens Neural Behav Physiol
. 1985
Dec
;157
(6
):817
–22
.
[PubMed]
0340-7594132.
Tomita
T
, Touma
H
, Murakumo
K
, Yanagisawa
M
, Yano
N
, Oka
S
, et al. Captive birth of tiger shark (Galeocerdo cuvier) reveals a shift in respiratory mode during parturition
. Copeia
. 2018
;106
(2
):292
–6
. 0045-8511133.
Tricas
TC
, Taylor
LR
, Naftel
G
. Diel behavior of the tiger shark, Galeocerdo cuvier, at French Frigate Shoals, Hawaiian Islands
. Copeia
. 1981
;1981
(4
):904
–8
. 0045-8511134.
van Alphen
B
, Yap
MH
, Kirszenblat
L
, Kottler
B
, van Swinderen
B
. A dynamic deep sleep stage in Drosophila
. J Neurosci
. 2013
Apr
;33
(16
):6917
–27
.
[PubMed]
0270-6474135.
Videler
J
, Koella
W
, Obál
F
, Schulz
H
. Sleep under sand cover of the labrid fish Coris julis
. Sleep
. 1986
;•••
:145
–7
.0161-8105136.
Vyazovskiy
VV
, Olcese
U
, Hanlon
EC
, Nir
Y
, Cirelli
C
, Tononi
G
. Local sleep in awake rats
. Nature
. 2011
Apr
;472
(7344
):443
–7
.
[PubMed]
0028-0836137.
Wardle
CS
. Swimming activity in marine fish. In: Laverack
MS
, editor. Physiological adaptations of marine animals
. Volume 1
. Scarborough
: The Co. of Biologists Ltd.
; 1985
. pp. 521
–40
.138.
Weber
VE
. Uber ruhelagen von fischen
. Z Tierpsychol
. 1961
;18
:517
–33
.0044-3573139.
Weihs
D
. Mechanically efficient swimming techniques for fish with negative buoyancy
. J Mar Res
. 1973
;31
:194
–209
.0022-2402140.
Weng
KC
, Block
BA
. Diel vertical migration of the bigeye thresher shark (Alopias superciliosus), a species possessing orbital retia mirabilia
. Fish Bull
. 2004
;102
(1
):221
–9
.0096-0985141.
Weng
KC
, O’Sullivan
JB
, Lowe
CG
, Winkler
CE
, Dewar
H
, Block
BA
. Movements, behavior and habitat preferences of juvenile white sharks Carcharodon carcharias in the eastern Pacific
. Mar Ecol Prog Ser
. 2007
;338
:211
–24
. 0171-8630142.
West
GJ
, Stevens
JD
. Archival tagging of school shark, Galeorhinus galeus, in Australia: initial results. In: Tricas
TC
, Gruber
SH
, editors. The behavior and sensory biology of elasmobranch fishes: an anthology in memory of Donald Richard Nelson
. Volume 20
. Dordrecht
: Springer
; 2001
. pp. 283
–98
. 143.
Whitney
NM
, Papastamatiou
YP
, Holland
KN
, Lowe
CG
. Use of an acceleration data logger to measure diel activity patterns in captive whitetip reef sharks, Triaenodon obesus
. Aquat Living Resour
. 2007
;20
(4
):299
–305
. 0990-7440144.
Yokogawa
T
, Marin
W
, Faraco
J
, Pézeron
G
, Appelbaum
L
, Zhang
J
, et al. Characterization of sleep in zebrafish and insomnia in hypocretin receptor mutants
. PLoS Biol
. 2007
Oct
;5
(10
):e277
.
[PubMed]
1544-9173145.
Yoshizawa
M
, Robinson
BG
, Duboué
ER
, Masek
P
, Jaggard
JB
, O’Quin
KE
, et al. Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish
. BMC Biol
. 2015
Feb
;13
(1
):15
.
[PubMed]
1741-7007146.
Zafar
N
, Morgan
E
. Feeding entrains an endogenous rhythm of swimming activity in the blind Mexican cave fish
. J Interdiscipl Cycle Res
. 1992
;23
:165
–6
. 0022-1945147.
Zhdanova
IV
. Sleep and its regulation in zebrafish
. Rev Neurosci
. 2011
;22
(1
):27
–36
.
[PubMed]
0334-1763148.
Zhdanova
IV
, Wang
SY
, Leclair
OU
, Danilova
NP
. Melatonin promotes sleep-like state in zebrafish
. Brain Res
. 2001
Jun
;903
(1-2
):263
–8
.
[PubMed]
0006-8993© 2019 S. Karger AG, Basel
2019
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.
