Table Of ContentSome histological data on bone and teeth in the grey notothen
(Lepidonotothen squamifrons) and in the mackerel icefish
(Champsocephalus gunnari) (Notothenioidei; Perciformes; Teleostei)
by
François J. Meunier* (1), Frédérique LecoMte (2) & Guy DuhaMeL (1)
abstract. – the grey notothen (Lepidonotothen squamifrons) and the mackerel icefish (Champsocephalus gun-
nari) (Notothenioidei; Perciformes; Teleostei) are two Southern Ocean acellular boned fishes whose bones show
cyclical growth marks. the degree of mineralization of their bony tissues, respectively 1.06 to 1.39 gha/cm3
and 1.04 to 1.33 gha/cm3, is close to the values of better known acellular boned fishes like the wolffish, the
anglerfish or the horse mackerel. The histological characteristics of bony tissues are not fundamentally different
from those observed in other marine acellular boned fishes.
résumé. – Quelques données histologiques sur les tissus osseux et les dents du colin austral (Lepidonotothen
squamifrons) et du poisson des glaces (Champsocephalus gunnari) (notothenioidei ; Perciformes ; teleostei).
© SFI Le colin austral (Lepidonotothen squamifrons) et le poisson des glaces (Champsocephalus gunnari) sont
Received: 9 Nov. 2017 deux espèces de l’océan austral à os acellulaire et dont certains os présentent des marques de croissance. Le
Accepted: 8 Dec. 2017 degré de minéralisation de leurs tissus osseux, respectivement 1,06 à 1,39 gha/cm3 et 1,04 à 1,33 gha/cm3,
Editor: O. Otero
est proche des valeurs connues pour des espèces communes comme le loup de l’atlantique, la baudroie ou le
chinchard. Les caractéristiques histologiques de leurs tissus osseux ne sont pas fondamentalement différentes de
celles observées chez d’autres poissons marins à os acellulaire.
Key words
Lepidonotothen
Champsocephalus
acellular bone
teeth
Mineralization
histology the grey notothen, Lepidonotothen Bertin (1936) considered that deep water may induce
squamifrons (Günther, 1880) (ttrreemmaattoo-- rickets, and Kock (1980) hypothesised that bones of Champ-
minae; Nototheniidae), and the mackerel icefish, Champso- socephalus gunnari are weakly calcified. These two South-
cephalus gunnari Lönnberg, 1905 (channichthyinae; noto- ern Ocean fishes, that live in relative deep depth and in cold
theniidae), are two Southern Ocean marine fishes that both waters, thus appear as good models to describe and inves-
belong to the Perciformes (nelson et al., 2016; Betancur-r tigate an eventual effect of depth and cold on histologi-
et al., 2017). they are found abundant on the Kerguelen cal characteristics of their skeletal tissues. however, to our
Plateau (KP, indian sector of the Southern ocean), where knowledge, the histological structure of their skeleton (bones
they have represented an important part of the commer- and teeth) has never been studied. in that frame, we provide
cial resource (hureau and Duhamel, 1980; Duhamel, 1981; here a comparative study of various bones and of teeth of
Duhamel et al., 2011). they live at depths of 200 m to 400 m these two notothenioids to document an eventual action of
in cold waters, ranging from 1.5°c to 4°c, of the Polar Fron- depth and temperature on the histological characteristics of
tal Zone (Park and Vivier, 2011). adults of C. gunnari inhab- their skeletal tissues in these sub-polar fishes.
it the shelf or top bank while L. squamifrons are found on the
slope (hureau, 1970; Duhamel, 1981). Moreover, C. gunnari
is a short living species (4 to 6 years maximum on the KP), MaTerial aNd MeThodS
while L. squamifrons lives longer (14 to 15 years) (Duhamel,
1981, 1991, 1995; Duhamel and hureau, 1985). they both Material
forage on pelagic organisms but their preys differ consider- Lepidonotothen squamifrons: 10 specimens (tL: 190 to
ably: crustaceans (hyperiid amphipods, euphausiacea) for 415 mm); Champsocephalus gunnari: 10 specimens (tL:
C. gunnari; Cnidarians (jellyfishes), Ctenarians, Thaliacea 135 to 305 mm). all have been collected from the Kergue-
for L. squamifrons (Duhamel et al., 2005). len islands shelf (northern part of the Kerguelen Plateau) by
(1) uMr 7208 (Mnhn-cnrS-irD-Sorbonne université-ucBn) Borea, Département adaptations du Vivant, Muséum national
d’histoire naturelle, cP 026, 43 rue cuvier, 75231 Paris cedex 05, France. [[email protected]]
(2) 6 quartier Beauregard, 27530 ezy-sur-eure, France. [[email protected]]
* corresponding author [[email protected]]
Cybium 2018, 42(1): 91-97.
Bone and teeth histology of Southern Ocean fish Lepidonotothen and champsocephalus Meunier et al.
table i. – Lengths and various techniques used on the studied spec-
imens of Lepidonotothen squamifrons and Champsocephalus gun-
nari. histol = classical histology with demineralized bones; Gro
Sec = ground section on undecalcified bones; SL = standard length;
TL = total length; μ X Q = quantitative microradiography.
Length (mm) histol Gro Sec µ X Q
Lepidonotothen
1 195 tL X X
2 205 tL X
3 250 tL X
4 227 SL X
5 255 SL X
6 259 tL X X
7 333 tL X X
8 415 tL X X
9 380 tL X
10 190 tL X
Champsocephalus
1 273 tL X
2 278 tL X X
3 280 tL X X
4 286 tL X X
5 305 tL X X
6 252 SL X
7 150 SL X
8 135 SL X
9 267 SL X
10 260 SL X
Figure 1. – Lepidonotothen squamifrons (227 mm SL). cross sec-
trawling. table i gives the length of the specimens and the tion of the dental (aPS-Groat-Pic). a: Bony tissue is deprived of
techniques applied on each one. The specimens were firstly osteocytes. arrows point to vascular cavities. B: Detail of an erosive
cavity showing active osteoclasts (arrowheads). the arrows point
frozen and then put in alcohol 70°. For the present study, we
to osteoblastic canaliculi. C: Champsocephalus gunnari (150 mm
sampled several bones included toothed bones: vertebrae, SL) (aZan). Bony tissue is deprived of osteocytes and osteoblas-
lower jaws, premaxillae, ceratohyals and spiny rays. tic canaliculi are seen (arrowheads). Scale bars: A = 250 μm; B,
C = 25 μm.
Methods
Histology 50-75 μm in thickness. The sections were microradiographed
the bones were dehydrated in a graded series of ethanol, with a cGr Sigma generator, and then observed under trans-
infiltrated, and embedded in wax. Transversal and longitu- mitted natural and polarized light with a Zeiss axiovert 35
dinal sections (7.5-10 μm thick) were stained with various microscope.
dyes: aPS-Groat-Pic, Gabe, aZan (according to Martoja
and Martoja, 1967), and then examined by light microscopy Quantitative microradiography
(natural transmitted light). We have also observed unstained the measurement of the mean degree of mineralization
sections with polarized light. of bone may be quantitatively evaluated by exposing an alu-
minium calibration step-wedge and a plane-parallel calcified
Ground sections tissue section simultaneously to the same beam of X-rays
the bones were dehydrated in graded series of alcohol (Baud, 1957; Boivin and Baud, 1984). We determine then,
till absolute ethanol, transferred to acetone, and embedded from the resulting microradiograph, the thickness of alu-
in stratyl polymer (chronolite 2195). transversal and lon- minium that produces the same X-ray absorption as a given
gitudinal sections (150-200 μm thick) were cut on the vari- region of the bone tissue section. the data obtained on the
ous bones with an isomet sawing machine and ground to bony tissues were compared with those of the standard alu-
92 Cybium 2018, 42(1)
Meunier et al. Bone and teeth histology of Southern Ocean fish Lepidonotothen and champsocephalus
Figure 2. – Lepidonotothen squami-
frons. a: cross section of the premax-
illa (microradiography). B: cross sec-
tion of the dental (microradiography).
C: cross section of a dorsal spiny ray
(microradiography). d: cross section
of a caudal vertebra (microradiography)
showing the numerous vertebral bony
arches fixed on the centrum. e: Detail
of a section of a caudal vertebra (Polar-
ized light showing the fibrous organiza-
tion of bone and two vascular canals
(arrowheads). F: Same section than
Fig. e observed in transmitted natural
light. the vascular canals are surround-
ed by a reversal line (arrows). G: Detail
of a section (polarized light) in a ver-
tebral centrum showing growth marks.
Scale bars: A = 500 μm; B = 250 μm;
C, D, E, F = 200 μm; G = 50 μm. A:
415 mm tL; B-D, G: 333 mm tL; e, F:
250 mm tL.
minium and the bone mineral density was calculated with reSulTS
the formulae of Sissons et al. (1960a, b).
We used bone sections of 100 ± 1 μm in thickness. The Bony tissues
sections were microradiographed with a standard of thin the bones of Lepidonotothen squamifrons and Champ-
socephalus gunnari are covered by a periostic layer consti-
slices (12.5 μm thick) of pure aluminium (99.99%) of cres-
tuted either of globular osteoblasts on the active growing
cent thickness. the exposure parameters were 20 KV under
surface or flat osteoblasts on the resting surfaces. in both
7 ma X-rays during 60 minutes with a distance of 40 cm
species, bony tissues are totally deprived of osteocytes
from the X-rays source. the X-rays are the radiation kα
(Figs 1, 2A-C), so these species are acellular boned fishes.
of copper with a nickel filter. The exposed high-resolution
there are osteoblastic processes penetrating the bony tis-
films (Kodak SO 343) were developed 5 minutes at 20°C.
sue in the two species (Fig. 1B, c). the various bones are
the measurements of optical densities of the microradiog-
constituted of relatively large vascular cavities surrounded
raphies were done with a histophotometer Zeiss. the results
by more or less thin bony trabeculae (Figs 1a, 2a, B, 3c,
were expressed in g of hydroxyapatite per cm3 of bone tissue 4a), especially the vertebrae that show many bony trabecu-
(for more details see Baud, 1957; castanet, 1979; Boivin and lae inserted around the chordal centrum (Figs 2D, 4D). the
Baud, 1984; Meunier, 1984). For each microradiography we bones are submitted locally to remodelling. Bony tissue is
measured 50 to 100 points per section. first eroded by osteoclasts (Fig. 1B) and eventually replaced
Cybium 2018, 42(1) 93
Bone and teeth histology of Southern Ocean fish Lepidonotothen and champsocephalus Meunier et al.
Figure 3. – Lepidonotothen squami-
frons. a: horizontal section (microra-
diography) showing several cross sec-
tions of teeth on the right and the lower
jaw on the left. B: horizontal section
(microradiography) taken lower than
Fig. a. the wall of the pulp cavity of
the central tooth (*) is crossed by vas-
cular canals. We can see three very
young non-functional teeth (arrow-
heads). C: cross section of the lower
jaw (microradiography) showing a
young erupted tooth (arrow) and a fall-
en tooth (*). d: Detail of a functional
tooth showing the unmineralized liga-
ment (arrowhead). e: cross section of
the jaw showing a tooth bud inserted in
an alveola (arrow), beside a functional
tooth (arrowhead). F, G: cross section
of a tooth (respectively in transmitted
natural and polarized light. the more
lateral dentinous tissue is striated, indi-
cating the presence of odontoblastic
canaliculi. (Scale bars: A, D = 250 μm;
B, F, G = 150 μm; C = 500 μm;
e = 1 mm. (a, B, F, G: 259 mm tL; c:
415 mm tL; D, e: 190 mm tL).
by new secondary bone constituting secondary oste-
ons (Fig. 2e, F). the mineralization looks normal
with the classic heterogeneity described in fish bone
(Figs 2a-c, 3c, 4c) (Meunier and François, 1992).
the mineralizing degree of bone in L. squamifrons
and C. gunnari is 0.82 to 1.51 gha/cm3 and 0.86 to
1.56 gha/cm3, respectively, with mean values 1.06
to 1.39 gha/cm3 and 1.04 to 1.33 gha/cm3, respec-
tively (tab. ii).
the extracellular matrix of bony tissues shows
alternating patterns of the collagenous matrix (Figs
2G, 4e). this characterizes seasonal growth of the Figure 4. – Champsocephalus gunnari. a: cross section of the dentary
(transmitted natural light). one can see a curved sharp tooth (arrow) and sev-
fish (Meunier, 1988; castanet et al., 1993). they
eral large vascular cavities (*) in the bony tissue. B: cross section of pre-
are clearly visible on the vertebrae as true growth maxilla showing two teeth (microradiography), that are fixed on their bony
marks. the cementing lines are weakly hypermin- support owing unmineralized ligaments (arrowheads). C: Detail of a cross
section of the dentary (microradiography) showing that the degree of min-
eralized.
eralization of bone is heterogeneous. d: cross section of a caudal vertebra
(microradiography) showing the numerous vertebral bony arches fixed on
Teeth the centrum. e: Longitudinal section of a caudal vertebra (microradiogra-
phy). Detail showing the heterogeneity of the mineralization. Scale bars: a,
Both species have sharp slightly curved teeth on
D = 200 μm; B = 250 μm; C = 100 μm; E = 500 μm. A, C, E: 278 mm TL; B:
their jaws (Figs 3c, D, 4a, B). each tooth is consti- 286 mm tL; D: 305 mm tL).
tuted of a dentine core with a thin external hyper-
mineralized enameloid layer (Figs 3a, B, D, 4a, B). alized ligaments (Figs 3D, 4a, B). teeth are replaced regu-
the dentinous tissue is crossed by odontoblastic canaliculi larly (Fig. 3c). the tooth bud is localized in an alveola at the
that are orthogonal to the wall of the pulp cavity (Fig. 3F, G): base of the functional tooth (Fig. 3B, e). the pulp cavity is
this is orthodentine. Teeth are fixed on the jaw with unminer- regularly circular (Fig. 3a). Yet in Lepidonotothen, the base
94 Cybium 2018, 42(1)
Meunier et al. Bone and teeth histology of Southern Ocean fish Lepidonotothen and champsocephalus
table ii. – Degree of mineralization (in g of hydroxyapatite/cm3) sub-families in the nototheniidae (Duhamel et al., 2014).
of the bony tissues in various bones of Lepidonotothen squamifrons
the presence of osteoblastic canaliculi in their bony tissue,
and Champsocephalus gunnari. M = mean value; Min-Max = mini-
mal and maximal values. probably participates to its nutrition in the absence of osteo-
cytes (Shahar and Dean, 2013; atkins et al., 2014; Sire and
M Min-Max
Meunier, 2017).
Lepidonotothen the successive growth marks observed on both species
Dentary 1.17 0.91-1.41 suggest that the grey notothen and the mackerel icefish are
Premaxillary 1.18 0.90-1.44 subject to a certain degree of seasonality of their metabolic
Maxillary 1.19 0.92-1.39 rates (Meunier and François, 1992; castanet et al., 1993;
Vertebrae 1.05 0.87-1.53 Panfili et al., 2002; and others). Such growth lines are also
Lepidotrichia 1.28 0.92-1.50 known in otoliths and scales of various notothenioidei,
Champsocephalus and were used for ageing fishes (Everson, 1980; Linkowski
Dentary 1.07 0.86-1.36 and Zukowski, 1980; Burchett, 1984; Duhamel and ozouf-
Premaxillary 1.17 0.95-1.56 costaz, 1985; horn, 2002). the strong seasonality of seston
Maxillary 1.16 0.91-1.52 and macrozooplankton biomass observed on the Kerguelen
Vertebrae 1.21 0.98-1.41 Plateau, peaking between november and april (hunt et al.,
Lepidotrichia 1.28 0.91-1.52 2011), certainly has implication on food webs dynamics and
may explain the pattern of growth marks in these two spe-
of teeth shows some discrete irregularities and transversal cific plankton feeder species (Duhamel and Hureau, 1985).
Despite the specific environmental condition for abiotic
vascular canals (Fig. 3B).
parameters (low temperature, important depth), Lepidonoto-
then squamifrons and Champsocephalus gunnari present nor-
mal physiologic activity according to the histological char-
diSCuSSioN
acteristics of their bony tissues. effectively, mean values of
the degree of mineralization in teleost fishes range from 0.80
our study points clearly to the acellularity of the bony
to 1.44 gha/cm3 with highest values found in marine fishes
tissues in both Lepidonotothen squamifrons and Champso-
with acellular bone (tab. iii; Meunier, 1984). the degree of
cephalus gunnari. Bone acellularity is present in all acan-
mineralization measured in the two species studied hereby
thomorphs with the exception of thunninae (Kölliker, 1859;
fit in the range of the values obtained in various Perciformes:
Moss, 1961, 1965; Weiss and Watabe, 1979; Meunier, 1987,
L. squamifrons and C. gunnari have well-mineralized bony
2011; Francillon-Vieillot et al., 1990; Sire and Meunier,
tissues. These results infirm the hypothesis of a weakly cal-
2017; and many others). This feature thus fits with the phy-
cified bone tissue in Champsocephalus gunnari, made by
logenetic position of the two species within Perciformes,
Kock (1980), and contradicts the idea that important depth
respectively the trematominae and the channichthyinae may induce rickets (Bertin, 1936). the latter
was also yet weakened by observations made in
table iii. – Degree of mineralization (in g of hydroxyapatite/cm3) of the bony
another deep-sea fish but in other environmen-
tissues in various teleostean fishes with cellular (cel) or acellular (acel) bone.
M = mean value; Min-Max = Minimal and Maximal values (from Meunier, tal context: Thermarces cerberus rosenblatt &
1984). cohen, 1986, a fish living near hydrothermal
Species Skeletal piece Bone M Min-Max vents (Meunier and arnulf, 2018).
Finally, the histological organization of teeth
Ictalurus melas pectoral spiny ray cel 1.1 0.87-1.33
in both species is similar to the descriptions cur-
Cyprinus carpio vertebra cel 0.88 0.71-1.08
rently observed notably in perciform fishes (e.g.
Cyprinus carpio dorsal spiny ray cel 1 0.87-1.17
Lison, 1954; Peyer, 1968; Schmidt, 1971; Shel-
Anguilla anguilla dental cel 0.98 0.75-1.16
lis and Berkowitz, 1976). The fixation of teeth
Esox lucius vertebra acel 1.15 0.84-1.36
with an unmineralized ligament corresponds to
Thunnus alalunga pectoral fin ray cel 1.08 0.87-1.37
the type 2 of Fink (1981). So, teeth are weakly
Euthynnus pelamis branchial arch cel 1.14 0.83-1.38
movable on their bony support when the fish
Lethrinus nebulosus dorsal fin ray acel 1.44 0.82-1.62
seizes its prey. however, the teeth of (Lepido-
Trachurus trachurus vertebra acel 1.11/1.33 0.85-1.56
notothen squamifrons show a peculiar morphol-
Coelorhinchus coelorhinchus dental acel 1.05 0.79-1.36
ogy at the base of the pulp cavity. the pulp wall
Nezumia aequalis dental acel 1.13 0.88-1.26 looks slightly pleated and therefore recalls teeth
Anarhichas lupus dental acel 0.93 0.80-1.04 of teleostean fishes, which have a plicidentine
Lophius americanus dental acel 1.13 0.93-1.37 organization of the simplexodont type (Meu-
Cybium 2018, 42(1) 95
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