Some 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 3 3 Editor: O. Otero degré de minéralisation de leurs tissus osseux, respectivement 1,06 à 1,39 gHA/cm et 1,04 à 1,33 gHA/cm , 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) (Tremato- 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 c e d e x 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 fishLepidonotothen and Champsocephalus Me u n i e r e t a l .

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) Me u n i e r e t a l . Bone and teeth histology of Southern Ocean fishLepidonotothen 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- slices (12.5 μm thick) of pure aluminium (99.99%) of cres- socephalus gunnari are covered by a periostic layer consti- cent thickness. The exposure parameters were 20 KV under tuted either of globular osteoblasts on the active growing 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, 3 were expressed in g of hydroxyapatite per cm 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 fishLepidonotothen and Champsocephalus Me u n i e r e t a l .

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 fish (Meunier, 1988; Castanet et al., 1993). They (transmitted natural light). One can see a curved sharp tooth (arrow) and sev- 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 eralized. section of the dentary (microradiography) showing that the degree of min- 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- Both species have sharp slightly curved teeth on phy). Detail showing the heterogeneity of the mineralization. Scale bars: A, 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) Me u n i e r e t a l . Bone and teeth histology of Southern Ocean fishLepidonotothen 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 Panfiliet 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). vascular canals (Fig. 3B). Despite the specific environmental condition for abiotic parameters (low temperature, important depth), Lepidonoto- then squamifrons and Champsocephalus gunnari present nor- Discussion mal physiologic activity according to the histological char- acteristics of their bony tissues. Effectively, mean values of Our study points clearly to the acellularity of the bony the degree of mineralization in teleost fishes range from 0.80 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 tissues in various teleostean fishes with cellular (cel) or acellular (acel) bone. another deep-sea fish but in other environmen- 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). Ictalurus melas pectoral spiny ray cel 1.1 0.87-1.33 Finally, the histological organization of teeth Cyprinus carpio vertebra cel 0.88 0.71-1.08 in both species is similar to the descriptions cur- 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 Bone and teeth histology of Southern Ocean fishLepidonotothen and Champsocephalus Me u n i e r e t a l . nier, 2015; Meunier et al., 2013, 2015). 3-D imaging (X-ray Duhamel G., 1981. - Caractéristiques biologiques des principa- CT scan) appears however compulsory to ascertain the pres- les espèces de poissons du plateau continental des îles Kergue- len. Cybium, 5(1): 19-32. ence of such an organization in L. squamifrons (e.g. Germain DUHAMEL G., 1991 - The biological and demographic peculiari- et al., 2016; Texereau et al., 2018). ties of the icefishChampsocephalus gunnari Lönnberg, 1905 from the Kerguelen plateau. In: Biology of Antarctic Fishes (Di Prisco G., Maresca R. & Tota B., eds), pp. 40-53. Springer Ver- lag, Berlin, Heidelberg. Conclusion DUHAMEL G., 1995. - New data on spawning, hatching and growth of Champsocephalus gunnari on the shelf of the Ker- The skeleton and teeth of the grey notothen and of the guelen Islands. CCAMLR Sci., 2: 21-34. mackerel icefish shows the normal histological organization DUHAMEL G. & HUREAU J.C., 1985 - The role of zooplankton in the diets of certain sub-antarctic marine fishes.In: Antarctic of teleostean fishes with acellular bone. Their specific eco- Nutrient Cycles and Food Webs (Siegfried W.R., Condy P.R. & logical niche in deep cold waters onto the shelf and on the Laws R.M., eds), pp. 421-429. Springer Verlag, Berlin, Heidel- slope does not affect the histological features of their bones berg. DUHAMEL G. & OZOUF-COSTAZ C., 1985 - Age, growth and and teeth as far as investigate with current methods of obser- reproductive biology of Notothenia squamifrons Günther, 1880 vation and mineralization quantification. Moreover, the skel- from the Indian sector of the Southern Ocean. 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