Throughout an animal’s life, species may occupy different environments and exhibit distinct life stages, known as ontogenetic shifts. The life histories of most sharks (class: Chondrichthyes) are characterized by these ontogenetic shifts, which can be defined by changes in habitat and diet as well as behavioral changes at the onset of sexual maturity. In addition, fishes experience indeterminate growth, whereby the brain and body grow throughout the organism’s life. Despite a presupposed lifelong neurogenesis in sharks, very little work has been done on ontogenetic changes in the brain, which may be informative about functional shifts in sensory and behavioral specializations. This study quantified changes in brain-body scaling and the scaling of six major brain regions (olfactory bulbs, telencephalon, diencephalon, optic tectum, cerebellum, and medulla oblongata) throughout ontogeny in the Atlantic sharpnose shark, Rhizoprio-nodon terraenovae. As documented in other fishes, brain size increased significantly with body mass throughout ontogeny in this species, with the steepest period of growth in early life. The telencephalon, diencephalon, optic tectum, and medulla oblongata scaled with negative allometry against the rest of the brain throughout ontogeny. However, notably, the olfactory bulbs and cerebellum scaled hyperallometrically to the rest of the brain, whereby these structures enlarged disproportionately as this species matured. Changes in the relative size of the olfactory bulbs throughout ontogeny may reflect an increased reliance on olfaction at later life history stages in R. terraenovae, while changes in the relative size of the cerebellum throughout ontogeny may be indicative of the ability to capture faster prey or an increase in migratory nature as this species moves to offshore habitats, associated with the onset of sexual maturity.

1.
Aicardi
S
,
Amaroli
A
,
Gallus
L
,
Di Blasi
D
,
Ghigliotti
L
,
Betti
F
, et al.
Quantification of neurons in the olfactory bulb of the catsharks Scyliorhinus canicula (Linnaeus, 1758) and Galeus melastomus (Rafinesque, 1810)
.
Zoology (Jena)
.
2020
Aug
;
141
:
125796
.
[PubMed]
1873-2720
2.
Altman
J
,
Das
GD
.
Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats
.
J Comp Neurol
.
1965
Jun
;
124
(
3
):
319
35
.
[PubMed]
0021-9967
3.
Ari
C
.
Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives
.
Open Anat J
.
2011
;
3
(
1
):
1
13
.
4.
Atema
J
.
Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors
.
Biol Bull
.
1996
Aug
;
191
(
1
):
129
38
.
[PubMed]
0006-3185
5.
Aya
F
,
Corpuz
M
,
Laron
M
,
Garcia
L
.
Larval and early juvenile development of silver therapon, Leiopotherapon plumbeus (Actinopterygii: Perciformes: Terapontidae), reared in mesocosms
.
Acta Ichthyol Piscat
.
2017
;
47
(
4
):
347
56
. 0137-1592
6.
Barks
SK
,
Calhoun
ME
,
Hopkins
WD
,
Cranfield
MR
,
Mudakikwa
A
,
Stoinski
TS
, et al.
Brain organization of gorillas reflects species differences in ecology
.
Am J Phys Anthropol
.
2015
Feb
;
156
(
2
):
252
62
.
[PubMed]
0002-9483
7.
Barton RA, Capellini I. Maternal investment, life histories, and the costs of brain growth in mammals. Proc Natl Acad Sci USA. 2011 Apr;108(15):6169–74.
8.
Bauchot
R
,
Bauchot
ML
,
Platel
R
,
Ridet
JM
.
The brains of Hawaiian tropical fishes: brain size and evolution
.
Copeia
.
1977
;
1
(
1
):
42
6
. 0045-8511
9.
Bauchot
R
,
Diagne
M
,
Ribet
JM
.
Post-hatching growth and allometry of the teleost brain
.
J Hirnforsch
.
1979
;
20
(
1
):
29
34
.
[PubMed]
0021-8359
10.
Bethea
D
,
Carlson
J
,
Buckel
J
,
Satterwhite
M
.
Ontogenetic and site-related trends in the diet of the Atlantic sharpnose shark Rhizoprionodon terraenovae from the northeast Gulf of Mexico
.
Bull Mar Sci
.
2006
;
78
:
287
307
.0007-4977
11.
Bonfil
R
,
de Anda
D
,
Mena
R
. (
1990
): Shark Fisheries in Mexico: The Case of Yucatan as an Example. In: Elasmobrances as Living Resources: Advances in Biology, Systematics, and the Status of the Fisheries (Jr. HP, Gruber S, Taniuchi T, eds), pp 427-441. Silver Spring MD: NOAA Technical Report NMFS 90. NOAA/NMFS.
12.
Brandstätter
R
,
Kotrschal
K
.
Life history of roach, Rutlius rutilus (Cyprinidae, Telestei)
.
Brain Behav Evol
.
1989
;
34
(
1
):
35
42
.
[PubMed]
0006-8977
13.
Brandstätter
R
,
Kotrschal
K
.
Brain growth patterns in four European cyprinid fish species (Cyprinidae, Teleostei): roach (Rutilus rutilus), bream (Abramis brama), common carp (Cyprinus carpio) and sabre carp (Pelecus cultratus)
.
Brain Behav Evol
.
1990
;
35
(
4
):
195
211
.
[PubMed]
0006-8977
14.
Burnham
KP
,
Anderson
D
.
Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach
. 2nd ed.
New York (NY)
:
Springer
;
2002
.
15.
Burnham KP, Anderson DR, Huyvaert KP. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. 2011;65:23–35.
16.
Cadwallader
P
.
Relationship between brain morphology and ecology in New Zealand Galaxiidae, particularly Galaxias vulgaris (Pisces: salmoniformes)
.
N Z J Zool
.
1975
;
2
(
1
):
35
43
. 0301-4223
17.
Camilieri-Asch
V
,
Yopak
KE
,
Rea
A
,
Partridge
JC
,
Mitchell
JD
,
Collin
SP
(
2020
):
Convergence of olfactory inputs within the central nervous system of a cartilaginous and a bony fish: an anatomical indicator for olfactory sensitivity.
Brain Behav Evol. accepted with minor revisions.
18.
Carlson
J
,
Baremore
I
.
Changes in biological parameters of Atlantic sharpnose shark Rhizoprionodon terraenovae in the Gulf of Mexico: evidence for density-dependent growth and maturity?
Mar Freshw Res
.
2003
;
54
(
3
):
227
34
. 1323-1650
19.
Carlson
J
,
Heupel
M
,
Bethea
D
,
Hollensead
L
.
Coastal habitat use and residency of juvenile Atlantic sharpnose sharks
.
Estuaries Coasts
.
2008
;
31
(
5
):
931
40
. 1559-2723
20.
Cavanaugh
J
.
Unifying the derivations for the Akaike and corrected Akaike information criteria
.
Stat Probab Lett
.
1997
;
33
(
2
):
201
8
. 0167-7152
21.
Compagno
LJ
.
FAO Species Catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. II. Carcharhiniformes
.
Rome, Italy
:
FAO Fisheries Synopsis
;
1984
.
22.
Coppock
AG
,
Gardiner
NM
,
Jones
GP
.
Sniffing out the competition? Juvenile coral reef damselfishes use chemical cues to distinguish the presence of conspecific and heterospecific aggregations
.
Behav Processes
.
2016
Apr
;
125
:
43
50
.
[PubMed]
0376-6357
23.
Corfield
JR
 Jr
,
Price
K
,
Iwaniuk
AN
,
Gutierrez-Ibañez
C
,
Birkhead
T
,
Wylie
DR
.
Diversity in olfactory bulb size in birds reflects allometry, ecology, and phylogeny
.
Front Neuroanat
.
2015
Jul
;
9
:
102
.
[PubMed]
1662-5129
24.
Deacon
TW
.
Fallacies of progression in theories of brain-size evolution
.
Int J Primatol
.
1990
;
11
(
3
):
193
236
. 0164-0291
25.
Deaner
RO
,
Isler
K
,
Burkart
J
,
van Schaik
C
.
Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates
.
Brain Behav Evol
.
2007
;
70
(
2
):
115
24
.
[PubMed]
0006-8977
26.
Demski
LS
,
Northcutt
RG
. The brain and cranial nerves of the white shark: An evolutionary perspective. In:
Klimley
AP
,
Ainley
DG
, editors
.
Great White Sharks: The Biology of Carcharodon carcharias
.
San Diego (CA)
:
Academic Press
;
1996
. pp.
121
30
.
27.
Dudley
SF
,
Anderson-Reade
MD
,
Thompson
GS
,
McMullen
PB
.
Concurrent scavanging off a whale carcass by great white sharks, Carcharodon carcharias, and tiger sharks, Galeocero cuvier
.
Fish Bull
.
2000
;
98
:
646
9
.0096-0985
28.
Endres
CS
,
Lohmann
KJ
.
Detection of coastal mud odors by loggerhead sea turtles: a possible mechanism for sensing nearby land
.
Mar Biol
.
2013
;
160
(
11
):
2951
6
. 0025-3162
29.
Eriksson
PS
,
Perfilieva
E
,
Björk-Eriksson
T
,
Alborn
AM
,
Nordborg
C
,
Peterson
DA
, et al.
Neurogenesis in the adult human hippocampus
.
Nat Med
.
1998
Nov
;
4
(
11
):
1313
7
.
[PubMed]
1078-8956
30.
Ernst
A
,
Alkass
K
,
Bernard
S
,
Salehpour
M
,
Perl
S
,
Tisdale
J
, et al.
Neurogenesis in the striatum of the adult human brain
.
Cell
.
2014
Feb
;
156
(
5
):
1072
83
.
[PubMed]
0092-8674
31.
Fishelson
L
,
Baranes
A
.
Ontogenesis and cytomorphology of the nasal olfactory organs in the Oman shark, Iago omanensis (Triakidae), in the Gulf of Aqaba, Red Sea
.
Anat Rec
.
1997
Nov
;
249
(
3
):
409
21
.
[PubMed]
0003-276X
32.
Fuchs
R
,
Winkler
H
,
Bingman
V
,
Ross
J
,
Bernroider
G
.
Brain geometry and its relation to migratory behavior in birds
.
J Adv Neurosci Res
.
2014
;
1
(
1
):
1
9
.
33.
Fuiman
L
. (
1988
)
Vulnerability of Atlantic herring larvae to predatory fishes.
In:
Program and Abstracts of the Annual Meeting of the American Association of Ichthyologists and Herpetologists
, p
96
.
34.
Gardiner
JM
,
Whitney
N
,
Hueter
RE
. (
2014
) Smells like home: Olfactory contributions to homing behavior in blacktip sharks. In: Joint Meeting of Ichthyologists and Herpetologists and the American Elasmobranch Society, Chattanooga, TN.
35.
Gheusi
G
,
Cremer
H
,
McLean
H
,
Chazal
G
,
Vincent
JD
,
Lledo
PM
.
Importance of newly generated neurons in the adult olfactory bulb for odor discrimination
.
Proc Natl Acad Sci USA
.
2000
Feb
;
97
(
4
):
1823
8
.
[PubMed]
0027-8424
36.
Gonda
A
,
Herczeg
G
,
Merilä
J
.
Population variation in brain size of nine-spined sticklebacks (Pungitius pungitius)—local adaptation or environmentally induced variation?
BMC Evol Biol
.
2011
Mar
;
11
(
1
):
75
.
[PubMed]
1471-2148
37.
Gonzalez-Voyer
A
,
Kolm
N
.
Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids
.
PLoS One
.
2010
Dec
;
5
(
12
):
e14355
.
[PubMed]
1932-6203
38.
Gozlan
R
,
Burnard
D
,
Britton
J
,
Andreou
D
.
Evidence of female preference for hidden sex signals in distant fish species
.
Behav Ecol
.
2013
;
25
(
1
):
53
7
. 0198-5841
39.
Grandel
H
,
Kaslin
J
,
Ganz
J
,
Wenzel
I
,
Brand
M
.
Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate
.
Dev Biol
.
2006
Jul
;
295
(
1
):
263
77
.
[PubMed]
0012-1606
40.
Grubbs
R
. Ontogenetic Shifts in Movements and Habitat Use. In:
Carrier
J
,
Musick
J
,
Heithaus
M
, editors
.
Sharks and Their Relatives II: Biodiversity, Adaptive Physiology, and Conservation
.
Boca Raton
:
CRC Press
;
2010
.
41.
Harahush
BK
,
Hart
NS
,
Collin
SP
.
Ontogenetic changes in retinal ganglion cell distribution and spatial resolving power in the brown-banded bamboo shark Chiloscyllium punctatum (Elasmobranchii)
.
Brain Behav Evol
.
2014
;
83
(
4
):
286
300
.
[PubMed]
1421-9743
42.
Hasler
A
,
Scholz
AT
,
Horrall
RM
.
Olfactory imprinting and homing in salmon
.
Am Sci
.
1978
May-Jun
;
66
(
3
):
347
55
.
[PubMed]
0003-0996
43.
Helfman
G
,
Collette
B
,
Facey
D
.
The Diversity of Fishes
.
Oxford
:
Blackwell Science
;
1997
.
44.
Herculano-Houzel
S
.
The human brain in numbers: a linearly scaled-up primate brain
.
Front Hum Neurosci
.
2009
Nov
;
3
:
31
.
[PubMed]
1662-5161
45.
Herculano-Houzel
S
.
Coordinated scaling of cortical and cerebellar numbers of neurons
.
Front Neuroanat
.
2010
Mar
;
4
:
12
.
[PubMed]
1662-5129
46.
Hinsch
K
,
Zupanc
GK
.
Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis
.
Neuroscience
.
2007
May
;
146
(
2
):
679
96
.
[PubMed]
0306-4522
47.
Hinterleitner
S
,
Platzer
U
,
Wieser
W
.
Development of the activities of oxidative, glycolytic and muscle enzymes during early larval life in three families of freshwater fish
.
J Fish Biol
.
2006
;
30
(
3
):
315
26
. 0022-1112
48.
Huber
R
,
Rylander
MK
.
Brain morphology and turbitity preference in Notropis and related genera (Cyprinidae, Teleostei)
.
Environ Biol Fishes
.
1992
;
33
(
1-2
):
153
65
. 0378-1909
49.
Huber
R
,
van Staaden
MJ
,
Kaufman
LS
,
Liem
KF
.
Microhabitat use, trophic patterns, and the evolution of brain structure in African cichlids
.
Brain Behav Evol
.
1997
;
50
(
3
):
167
82
.
[PubMed]
0006-8977
50.
Hubold
G
.
Spatial distribution of Pleuragramma antarcticum (Pisces: Nototheniidae) near the Filchner and Larsen Ice Shelves (Weddell Sea, Antarctica)
.
Polar Biol
.
1984
;
3
(
4
):
231
6
. 0722-4060
51.
Hueter
R
. (
1980
): Physiological optics of the eye of the juvenile lemon shark (Negaprion brevirostris). MSc Thesis, The University of Miami. 145 pp.
52.
Iaskin
VA
.
[Seasonal changes in hippocampus size and spatial behaviour in mammals and birds]
.
Zh Obshch Biol
.
2011
Jan-Feb
;
72
(
1
):
27
39
.
[PubMed]
0044-4596
53.
Iribarne
L
,
Castelló
ME
.
Postnatal brain development of the pulse type, weakly electric gymnotid fish Gymnotus omarorum
.
J Physiol Paris
.
2014
Apr-Jun
;
108
(
2-3
):
47
60
.
[PubMed]
0928-4257
54.
Isler
K
.
Brain size evolution: how fish pay for being smart
.
Curr Biol
.
2013
Jan
;
23
(
2
):
R63
5
.
[PubMed]
0960-9822
55.
Ito
H
,
Ishikawa
Y
,
Yoshimoto
M
,
Yamamoto
N
.
Diversity of brain morphology in teleosts: brain and ecological niche
.
Brain Behav Evol
.
2007
;
69
(
2
):
76
86
.
[PubMed]
0006-8977
56.
Iwaniuk
AN
,
Hurd
PL
,
Wylie
DR
.
Comparative morphology of the avian cerebellum: I. Degree of foliation
.
Brain Behav Evol
.
2006
;
68
(
1
):
45
62
.
[PubMed]
0006-8977
57.
Jacobs
LF
.
From chemotaxis to the cognitive map: the function of olfaction
.
Proc Natl Acad Sci USA
.
2012
Jun
;
109
Suppl 1
:
10693
700
.
[PubMed]
0027-8424
58.
Janvier
P
.
Early Vertebrates
.
Oxford, UK
:
Oxford University Press
;
1996
.
59.
Jerison
HJ
.
Evolution of the Brain and Intelligence
.
New York (NY)
:
Academic Press
;
1973
.
60.
Kajiura
SM
,
Cornett
AD
,
Yopak
KE
. Sensory Adaptations to the Environment: Electroreceptors as a case study. In:
Carrier
JC
,
Musick
JA
,
Heithaus
MR
, editors
.
Sharks and Their Relatives II: Biodiversity, Adaptive Physiology, and Conservation
.
New York (NY)
:
CRC Press
;
2010
.
61.
Kempster
RM
,
Garza-Gisholt
E
,
Egeberg
CA
,
Hart
NS
,
O’Shea
OR
,
Collin
SP
.
Sexual dimorphism of the electrosensory system: a quantitative analysis of nerve axons in the dorsal anterior lateral line nerve of the blue-spotted Fantail Stingray (Taeniura lymma)
.
Brain Behav Evol
.
2013
;
81
(
4
):
226
35
.
[PubMed]
1421-9743
62.
Kihslinger
RL
,
Nevitt
GA
.
Early rearing environment impacts cerebellar growth in juvenile salmon
.
J Exp Biol
.
2006
Feb
;
209
(
Pt 3
):
504
9
.
[PubMed]
0022-0949
63.
Kolm
N
,
Gonzalez-Voyer
A
,
Brelin
D
,
Winberg
S
.
Evidence for small scale variation in the vertebrate brain: mating strategy and sex affect brain size and structure in wild brown trout (Salmo trutta)
.
J Evol Biol
.
2009
Dec
;
22
(
12
):
2524
31
.
[PubMed]
1010-061X
64.
Kotrschal
K
,
Adam
H
,
Brandstätter
R
,
Junger
H
,
Zaunreiter
M
,
Goldschmid
A
.
Larval size constraints determine directional ontogenetic shifts in the visual system of teleosts: a mini‐review
.
J Zool Syst Evol Res
.
1990
;
28
(
3
):
166
82
. 0947-5745
65.
Kotrschal
A
,
Rogell
B
,
Bundsen
A
,
Svensson
B
,
Zajitschek
S
,
Brännström
I
, et al.
Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain
.
Curr Biol
.
2013
Jan
;
23
(
2
):
168
71
.
[PubMed]
0960-9822
66.
Kotrschal
K
,
van Staaden
MJ
,
Huber
R
.
Fish brains: evolution and environmental relationships
.
Rev Fish Biol Fish
.
1998
;
8
(
4
):
373
408
. 0960-3166
67.
Krubitzer
L
,
Dooley
JC
.
Cortical plasticity within and across lifetimes: how can development inform us about phenotypic transformations?
Front Hum Neurosci
.
2013
Oct
;
7
:
620
.
[PubMed]
1662-5161
68.
Kruska
DCT
(
1988
): The brain of the basking shark (Cetorhinus maximus). Brain Behav Evol 32:353-363.s
69.
Kudo
H
,
Shinto
M
,
Sakurai
Y
,
Kaeriyama
M
.
Morphometry of olfactory lamellae and olfactory receptor neurons during the life history of chum salmon (Oncorhynchus keta)
.
Chem Senses
.
2009
Sep
;
34
(
7
):
617
24
.
[PubMed]
0379-864X
70.
Kullback
S
,
Leibler
R
.
On information and sufficiency
.
Ann Math Stat
.
1951
;
1
(
1
):
79
86
. 0003-4851
71.
Ladage
LD
,
Riggs
BJ
,
Sinervo
B
,
Pravosudov
VV
.
Dorsal cortex volume in male side-blotched lizards (Uta stansburiana) is associated with different space use strategies
.
Anim Behav
.
2009
Jul
;
78
(
1
):
91
6
.
[PubMed]
0003-3472
72.
Lefebvre
L
.
Brains, innovations, tools and cultural transmission in birds, non-human primates, and fossil hominins
.
Front Hum Neurosci
.
2013
Jun
;
7
:
245
.
[PubMed]
1662-5161
73.
Leyhausen
C
,
Kirschbaum
F
,
Szabo
T
,
Erdelen
M
.
Differential growth in the brain of the weakly electric fish, Apteronotus leptorhynchus (Gymnotiformes), during ontogenesis
.
Brain Behav Evol
.
1987
;
30
(
3-4
):
230
48
.
[PubMed]
0006-8977
74.
Lisney
TJ
,
Bennett
MB
,
Collin
SP
.
Volumetric analysis of sensory brain areas indicates ontogenetic shifts in the relative importance of sensory systems in elasmobranchs
.
Raffles Bull Zool
.
2007
;
14
:
7
15
.0217-2445
75.
Lisney
TJ
,
Collin
SP
.
Relative eye size in elasmobranchs
.
Brain Behav Evol
.
2007
;
69
(
4
):
266
79
.
[PubMed]
0006-8977
76.
Lisney
T
,
Wagner
H
,
Collin
S
.
Ontogenetic shifts in the number of axons in the olfactory tract and optic nerve in two species of deep-sea grenadier fish (Gadiformes: Macrouridae: Coryphaenoides)
.
Front Ecol Evol
.
2018
;
6
:
168
. 2296-701X
77.
Lisney
TJ
,
Yopak
KE
,
Camilieri-Asch
V
,
Collin
SP
.
Ontogenetic shifts in brain organization in the bluespotted stingray Neotrygon kuhlii (Chondrichthyes: dasyatidae)
.
Brain Behav Evol
.
2017
;
89
(
2
):
68
83
.
[PubMed]
1421-9743
78.
Loefer
J
,
Sedberry
G
.
Life history of the Atlantic sharpnose shark (Rhizoprionodon terraenovae) (Richardson, 1836) off the southeastern United States
.
Fish Bull
.
2003
;
101
:
75
88
.0096-0985
79.
Long
DJ
,
Jones
RE
. White shark predation and scavenging on cetaceans in the eastern North Pacific Ocean. In:
Klimley
AP
,
Ainley
DG
, editors
.
Great White Sharks: The Biology of Carcharodon carcharias
.
San Diego (CA)
:
Academic Press
;
1996
. pp.
293
307
.
80.
Manzon
R
,
Docker
M
. Lamprey Metamorphosis.
Lampreys: Biology, Conservation and Control
.
New York (NY)
:
Springer
;
2015
. pp.
139
214
.
81.
Masuada
R
.
Behavioral ontogeny of marine pelagic fishes with the implications for the sustainable management of fisheries resources
.
Aqua-Biosci Monogr
.
2009
;
2
(
2
):
1
56
. 1882-3203
82.
McCallum
ES
,
Capelle
PM
,
Balshine
S
.
Seasonal plasticity in telencephalon mass of a benthic fish
.
J Fish Biol
.
2014
Nov
;
85
(
5
):
1785
92
.
[PubMed]
0022-1112
83.
Mcfarland
W
. The visual world of coral reef fishes. In:
Sale
PF
, editor
.
The Ecology of Fishes on Coral Reefs
.
San Diego (CA)
:
Academic Press
;
1991
. pp.
16
38
.
84.
Ming
GL
,
Song
H
.
Adult neurogenesis in the mammalian central nervous system
.
Annu Rev Neurosci
.
2005
;
28
(
1
):
223
50
.
[PubMed]
0147-006X
85.
Mink
JW
,
Blumenschine
RJ
,
Adams
DB
.
Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis
.
Am J Physiol
.
1981
Sep
;
241
(
3
):
R203
12
.
[PubMed]
0002-9513
86.
Montgomery
JC
,
Bodznick
D
,
Yopak
KE
.
The cerebellum and cerebellum-like structures of cartilaginous fishes
.
Brain Behav Evol
.
2012
;
80
(
2
):
152
65
.
[PubMed]
1421-9743
87.
Montgomery
JC
,
Sutherland
BW
.
Sensory development of the Antarctic silverfsh Pleuragramma antarcticum: A test for the ontogenetic shift hypothesis
.
Polar Biol
.
1997
;
18
(
2
):
112
5
. 0722-4060
88.
Morales-Nin
B
,
Geffen
A
,
Pérez-Mayol
S
,
Palmer
M
,
González-Quirós
R
,
Grau
A
.
Seasonal and ontogenic migrations of meagre (Argyrosomus regius) determined by otolith geochemical signatures
.
Fish Res
.
2012
;
128
:
154
65
. 0165-7836
89.
Mull
C
,
Yopak
KE
,
Dulvy
N
.
Does more maternal investment mean a larger brain? Evolutionary relationships between reproductive mode and brain size in chondrichthyans
.
Mar Freshw Res
.
2011
;
62
(
6
):
567
75
. 1323-1650
90.
Mull
CG
,
Yopak
KE
,
Dulvy
NK
.
Maternal investment, ecological lifestyle, and brain evolution in sharks and rays
.
Am Nat
.
2020
Jun
;
195
(
6
):
1056
69
.
[PubMed]
0003-0147
91.
Näslund
J
,
Aarestrup
K
,
Thomassen
S
,
Johnsson
JI
.
Early enrichment effects on brain development in hatchery-reared Atlantic salmon (Salmo salar): no evidence for a critical period
.
Can J Fish Aquat Sci
.
2012
;
69
(
9
):
1481
90
. 0706-652X
92.
Näslund
J
,
Larsen
M
,
Thomassen
S
,
Aarestrup
K
,
Johnsson
J
.
Environment-dependent plasticity and ontogenetic changes in the brain of hatchery-reared Atlantic salmon
.
J Zool (Lond)
.
2017
;
301
(
1
):
75
82
. 0952-8369
93.
Nevitt
GA
,
Losekoot
M
,
Weimerskirch
H
.
Evidence for olfactory search in wandering albatross, Diomedea exulans
.
Proc Natl Acad Sci USA
.
2008
Mar
;
105
(
12
):
4576
81
.
[PubMed]
0027-8424
94.
Ngwenya
A
,
Patzke
N
,
Spocter
MA
,
Kruger
JL
,
Dell
LA
,
Chawana
R
, et al.
The continuously growing central nervous system of the Nile crocodile (Crocodylus niloticus)
.
Anat Rec (Hoboken)
.
2013
Oct
;
296
(
10
):
1489
500
.
[PubMed]
1932-8486
95.
Nilsson
GE
,
Routley
MH
,
Renshaw
GM
.
Low mass-specific brain Na+/K+-ATPase activity in elasmobranch compared to teleost fishes: implications for the large brain size of elasmobranchs
.
Proc Biol Sci
.
2000
Jul
;
267
(
1450
):
1335
9
.
[PubMed]
0962-8452
96.
Northcutt
RG
.
Elasmobranch central nervous system organization and its possible evolutionary significance
.
Am Zool
.
1977
;
17
(
2
):
411
29
. 0003-1569
97.
Northcutt
RG
. Brain Organization in the Cartilaginous Fishes. In:
Hodgson
ES
,
Mathewson
RF
, editors
.
Sensory Biology of Sharks, Skates, and Rays
.
Arlington (VA)
:
Office of Naval Research
;
1978
. pp.
117
94
.
98.
Northcutt
RG
.
Brain variation and phylogenetic trends in elasmobranch fishes
.
J Exp Zool Suppl
.
1989
;
2
S2
:
83
100
.
[PubMed]
1059-8324
99.
Nosal
AP
,
Chao
Y
,
Farrara
JD
,
Chai
F
,
Hastings
PA
.
Olfaction contributes to pelagic navigation in a coastal shark
.
PLoS One
.
2016
Jan
;
11
(
1
):
e0143758
.
[PubMed]
1932-6203
100.
Olivera-Pasilio
V
,
Lasserre
M
,
Castelló
ME
.
Cell proliferation, migration, and neurogenesis in the adult brain of the pulse type weakly electric fish, Gymnotus omarorum
.
Front Neurosci
.
2017
Aug
;
11
:
437
.
[PubMed]
1662-4548
101.
Packard
A
.
Cephalopods and fish: limits of convergence
.
Biol Rev Camb Philos Soc
.
1972
;
47
(
2
):
241
307
. 0006-3231
102.
Pinheiro
J
,
Bates
D
. DebRoy, S., Sarkar, D. & R Core Team (
2014
) nlme: Linear and nonlinear mixed effects models. R Package Version 3.1–117. Available at http://CRAN.Rproject.org/package=nlme
103.
Pollen
AA
,
Dobberfuhl
AP
,
Scace
J
,
Igulu
MM
,
Renn
SC
,
Shumway
CA
, et al.
Environmental complexity and social organization sculpt the brain in Lake Tanganyikan cichlid fish
.
Brain Behav Evol
.
2007
;
70
(
1
):
21
39
.
[PubMed]
0006-8977
104.
Pratt
HL
 Jr
,
Carrier
JC
.
A review of elasmobranch reproductive behavior with a case study on the nurse shark, Ginglymostoma cirratum
.
Environ Biol Fishes
.
2001
;
60
(
1/3
):
157
88
. 0378-1909
105.
Puzdrowski
RL
,
Gruber
S
.
Morphologic features of the cerebellum of the Atlantic stingray, and their possible evolutionary significance
.
Integr Zool
.
2009
Mar
;
4
(
1
):
110
22
.
[PubMed]
1749-4869
106.
Puzdrowski
RL
,
Leonard
RB
.
Variations in cerebellar morphology of the Atlantic stingray, Dasyatis sabina
.
Neurosci Lett
.
1992
Feb
;
135
(
2
):
196
200
.
[PubMed]
0304-3940
107.
Salas
CA
,
Yopak
KE
,
Warrington
RE
,
Hart
NS
,
Potter
IC
,
Collin
SP
.
Ontogenetic shifts in brain scaling reflect behavioral changes in the life cycle of the pouched lamprey Geotria australis
.
Front Neurosci
.
2015
Jul
;
9
:
251
.
[PubMed]
1662-4548
108.
Schmidt-Nielsen
K
.
Scaling: Why is Animal Size so Important?
Cambridge
:
Cambridge University Press
;
1984
.
109.
Sebens
KP
.
The ecology of indeterminate growth in animals
.
Annu Rev Ecol Syst
.
1987
;
18
(
1
):
371
407
. 0066-4162
110.
Shoji
T
,
Ueda
H
,
Ohgami
T
,
Sakamoto
T
,
Katsuragi
Y
,
Yamauchi
K
, et al.
Amino acids dissolved in stream water as possible home stream odorants for masu salmon
.
Chem Senses
.
2000
Oct
;
25
(
5
):
533
40
.
[PubMed]
0379-864X
111.
Smulders
TV
,
Sasson
AD
,
DeVoogd
TJ
.
Seasonal variation in hippocampal volume in a food-storing bird, the black-capped chickadee
.
J Neurobiol
.
1995
May
;
27
(
1
):
15
25
.
[PubMed]
0022-3034
112.
Sol
D
,
Székely
T
,
Liker
A
,
Lefebvre
L
.
Big-brained birds survive better in nature
.
Proc Biol Sci
.
2007
Mar
;
274
(
1611
):
763
9
.
[PubMed]
0962-8452
113.
Stabell
O
. Olfactory control of homing behaviour in salmonids. In:
Hara
T
, editor
.
Fish Chemoreception, Fish & Fisheries Series
.
Springer
;
1992
.
114.
Stephan
H
.
Methodische studien über den quantitativen vergleich architektonischer struktureinheiten des gehirns
.
Z Wiss Zool
.
1960
;
64
:
143
72
.
115.
Striedter
GF
.
Principles of Brain Evolution
.
Sunderland (MA)
:
Sinauer Associates, Inc.
;
2005
.
116.
Toyoda
J
,
Uematsu
K
.
Brain morphogenesis of the red sea bream, Pagrus major (teleostei)
.
Brain Behav Evol
.
1994
;
44
(
6
):
324
37
.
[PubMed]
0006-8977
117.
Tsuboi
M
,
van der Bijl
W
,
Kopperud
B
,
Erritzøe
J
,
Voje
K
,
Yopak
K
, et al.
Decoupling of brain size and body size facilitated the exceptional encephalization of mammals and birds
.
Nat Ecol Evol
.
2018
;
2
:
1492
500
.
[PubMed]
2397-334X
118.
Ueda
H
,
Kaeriyama
M
,
Mukasa
K
,
Urano
A
,
Kudo
H
,
Shoji
T
, et al.
Lacustrine sockeye salmon return straight to their natal area from open water using both visual and olfactory cues
.
Chem Senses
.
1998
Apr
;
23
(
2
):
207
12
.
[PubMed]
0379-864X
119.
Ullmann
JF
,
Cowin
G
,
Collin
SP
.
Quantitative assessment of brain volumes in fish: comparison of methodologies
.
Brain Behav Evol
.
2010
;
76
(
3-4
):
261
70
.
[PubMed]
1421-9743
120.
van Staaden
MJ
,
Huber
R
,
Kaufman
LF
,
Liem
KF
.
Brain evolution of cichlids in the African great lakes: brain and body size, general patterns, and evolutionary trends
.
Zoology
.
1995
;
98
:
165
78
.0944-2006
121.
von Bertalanffy
L
.
A quantitative theory of organic growth (inquiries on growth laws. II)
.
Hum Biol
.
1938
;
10
:
181
213
.0018-7143
122.
Wagner
HJ
.
Sensory brain areas in mesopelagic fishes
.
Brain Behav Evol
.
2001
Mar
;
57
(
3
):
117
33
.
[PubMed]
0006-8977
123.
Wagner
HJ
.
Volumetric analysis of brain areas indicates a shift in sensory orientation during development in the deep-sea grenadier Coryphaenoides armatus
.
Mar Biol
.
2003
;
142
(
4
):
791
7
. 0025-3162
124.
Wanzenböck
J
,
Schierner
F
.
Prey detection in cyprinids during early development
.
Can J Fish Aquat Sci
.
1989
;
46
(
6
):
995
1001
. 0706-652X
125.
Werner
E
,
Hall
D
.
Ontogenetic habitat shifts in bluegill: the foraging rate-predation risk trade-off
.
Ecology
.
1988
;
69
(
5
):
1352
66
. 0012-9658
126.
Wisby
W
,
Hasler
A
.
Effect of olfactory occlusion on migrating silver salmon (O. kisutch)
.
J Fish Res Board Can
.
1954
;
11
(
4
):
472
8
. 0015-296X
127.
Wong
B
,
Fisher
H
,
Rosenthal
G
.
Species recognition by male swordtails via chemical cues
.
Behav Ecol
.
2005
;
16
(
4
):
818
22
. 0198-5841
128.
Yaskin
VA
.
Seasonal adaptive modification of the size of the hippocampus and the dynamics of spatial behavior in bank voles (Clethrionomys glareolus, Rodentia)
.
Zool Zh
.
2009
;
88
:
1365
76
.0044-5134
129.
Yopak
KE
.
Neuroecology of cartilaginous fishes: the functional implications of brain scaling
.
J Fish Biol
.
2012
Apr
;
80
(
5
):
1968
2023
.
[PubMed]
0022-1112
130.
Yopak
KE
,
Frank
LR
.
Brain size and brain organization of the whale shark, Rhincodon typus, using magnetic resonance imaging
.
Brain Behav Evol
.
2009
;
74
(
2
):
121
42
.
[PubMed]
1421-9743
131.
Yopak
K
,
Heel
K
,
Goh
G
,
Northcutt
R
,
Collin
S
.
Is bigger always better? Developing quantitative measures of cognitive ability in early vertebrates
.
Brain Behav Evol
.
2014
;
84
:
74
.
132.
Yopak
KE
,
Lisney
TJ
.
Allometric scaling of the optic tectum in cartilaginous fishes
.
Brain Behav Evol
.
2012
;
80
(
2
):
108
26
.
[PubMed]
1421-9743
133.
Yopak
KE
,
Lisney
TJ
,
Collin
SP
.
Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes
.
Brain Struct Funct
.
2015
Mar
;
220
(
2
):
1127
43
.
[PubMed]
1863-2653
134.
Yopak
KE
,
Lisney
TJ
,
Collin
SP
,
Montgomery
JC
.
Variation in brain organization and cerebellar foliation in chondrichthyans: sharks and holocephalans
.
Brain Behav Evol
.
2007
;
69
(
4
):
280
300
.
[PubMed]
0006-8977
135.
Yopak
KE
,
Lisney
TJ
,
Darlington
RB
,
Collin
SP
,
Montgomery
JC
,
Finlay
BL
.
A conserved pattern of brain scaling from sharks to primates
.
Proc Natl Acad Sci USA
.
2010
Jul
;
107
(
29
):
12946
51
.
[PubMed]
0027-8424
136.
Yopak
KE
,
McMeans
BC
,
Mull
CG
,
Feindel
KW
,
Kovacs
KM
,
Lydersen
C
, et al.
Comparative brain morphology of the Greenland and Pacific sleeper sharks and its functional implications
.
Sci Rep
.
2019
Jul
;
9
(
1
):
10022
.
[PubMed]
2045-2322
137.
Yopak
KE
,
Montgomery
JC
.
Brain organization and specialization in deep-sea chondrichthyans
.
Brain Behav Evol
.
2008
;
71
(
4
):
287
304
.
[PubMed]
1421-9743
138.
Yoshida
M
,
Tsuji
T
,
Mukuda
T
.
Relationship between brain morphology and life history in four bottom-dwelling gobiids
.
Zool Sci
.
2020
Apr
;
37
(
2
):
168
76
.
[PubMed]
0289-0003
139.
Zupanc
GK
.
Adult neurogenesis and neuronal regeneration in the central nervous system of teleost fish
.
Brain Behav Evol
.
2001
;
58
(
5
):
250
75
.
[PubMed]
0006-8977
140.
Zupanc
GK
.
Adult neurogenesis and neuronal regeneration in the brain of teleost fish
.
J Physiol Paris
.
2008
Jul-Nov
;
102
(
4-6
):
357
73
.
[PubMed]
0928-4257
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