Desenvolvimento de Dentes Catfishes

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Morphology and Development of Teeth and EpidermalBrushes in Loricariid Catfishes

Tom Geerinckx,* Joris De Poorter, and Dominique Adriaens

Evolutionary Morphology of Vertebrates, Ghent University-UGent, 9000 Ghent, Belgium

ABSTRACT Loricariidae or suckermouth armored cat-fishes are one of several aquatic taxa feeding on epilithicand epiphytic algae. Their upper and lower jaws bearexquisitely curved teeth, which usually are asymmetri-cally bicuspid. The enlarged lower lip carries papillaewith keratinous unicellular epidermal brushes or unculi.Teeth, and probably unculi too, assist in scraping food offsubstrates. Their morphology, growth, and replacement isexamined and compared among several loricariid species,using cleared and stained specimens, serial sections, andSEM. Apart from the general tooth form and crownshape, the anterior layer of soft tissue on the lower shaftregion, present in several species, appears to be a specia-lization for enhancing the mobility of individual teethwhen scraping on uneven surfaces. During early onto-geny, a transition from simple conical to mature toothoccurs. The first unculi appear together with the firstteeth carrying a bicuspid crown, 2 days after the first ex-ogenous feeding, but synchronous with the completeresorption of the yolk sac. J. Morphol. 268:805814,2007. 2007 Wiley-Liss, Inc.

KEY WORDS: dentition; Loricariidae; ontogeny; sucker-mouth armored catfishes; unculi

Brush- and gouge-like devices are ideal for scra-ping food off substrates, and are most often found inaquatic organisms, particularly aquatic insect lar-vae (Arens, 1994), amphibian larvae (Orton, 1953;Wassersug and Yamahita, 2001), and fishes. In allthese cases the diet primarily consists of adherentalgae. Examples in teleosts are the rake-like den-ticles of the osmeriform ayu (Howes and Sanford,1987; Uehara and Miyoshi, 1993), the tooth-likekeratinous hooks of Gyrinocheilidae (Ono, 1980;Benjamin, 1986), spatulate teeth of certain Cichli-dae (Vandervennet et al., 2006) and Mochokidae,and the scraping teeth of species of the Loricariidae

or suckermouth armored catfishes. The latter fa-mily exhibits the most exquisite and diverse teethforms (e.g., Muller and Weber, 1992; Schaefer andStewart, 1993; Delariva and Agostinho, 2001): theS- or Z-shaped recurved teeth are generally asym-metrically bicuspid, but, in some taxa, have onecusp only. Teeth of the related loricarioid, scolopla-cid, and astroblepid families are usually symmetri-cally bifid (Schaefer, 1990), although shape varia-tion exists (e.g., Cardona and Guerao, 1994). Teethare absent in adults of the more basal callichthyids,while simple conical teeth have been found in small

juveniles (Huysseune and Sire, 1997a). While manygenera of the basal loricarioid trichomycterids haverather conical teeth, Henonemus has (unicuspid)recurved teeth, reminiscent of loricariid teeth(DoNascimiento and Provenzano, 2006).

Loricariidae are able to attach onto surfacesusing a not well understood process allowing respi-ration during attachment, and scrape off algae andother food with their ventrally oriented upper andlower jaws. Ono (1980) and Roberts (1982) describedunicellular keratinous lip projections or unculi onthe surface of the expanded lower lip of loricariids.These epidermal projections might serve as abra-sive brushes or protective structures for the associ-ated taste buds. Ono (1980) studied the internalmicrostructure of the loricariid unculi. Unicellularand multicellular keratinous structures are foundin several teleostean orders, with functions oftenrelated to reproduction, protection, abrasion, adhe-sion, and hydrodynamics (Branson, 1962; Wileyand Collette, 1970; Roberts, 1973, 1982; Arratia,1987; Arratia and Huaqun, 1995; Chen and Arratia,1996).

In this article we describe the morphology of lori-cariid teeth and unculi, their growth, and theirshape during early ontogeny. Results are then dis-cussed in view of the possible role of both structuresin feeding.

MATERIALS AND METHODS

Teeth and lips of several loricariid species were examined,using the clearing and staining method of Taylor and Van Dyke(1985), and SEM (Table 1): Ancistrus cf. triradiatus, Pterygo-plichthys lituratus, Panaque nigrolineatus, Otocinclus vestitus,Rineloricaria parva, Farlowella acus, and Sturisoma aureum.All species were obtained commercially. After sedation in MS 222

Contract grant sponsor: FWO; Contract grant number: G.0355.04;Contract grant sponsor: Institute for the Promotion of Innovationthrough Science and Technology in Flanders (IWT-Vlaanderen).

*Correspondence to: Tom Geerinckx, Evolutionary Morphology ofVertebrates, Ghent University-UGent, K.L. Ledeganckstraat 35,9000 Ghent, Belgium. E-mail: [email protected]

Published online 11 July 2007 inWiley InterScience (www.interscience.wiley.com)DOI: 10.1002/jmor.10547

JOURNAL OF MORPHOLOGY 268:805814 (2007)

2007 WILEY-LISS, INC.


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the specimens were fixed in a 4% buffered formalin solution (at

neutral pH).Ancistruscf. triradiatuswas selected for the ontogenetic study.

It is a medium-sized, mostly herbivorous and easily reared lori-cariid. Its teeth are extremely curved. Eggs were obtained fromadults kept in a 24268C aquarium (30130 cm). At differenttime intervals eggs and free-living embryos were sedated andfixed in a paraformaldehydeglutaraldehyde solution. One sub-adult and three free-living embryonic specimens of this specieswere selected for serial sectioning (section thickness 2 or 5 lm),using Technovit 7100 as plastic embedding medium, a Reichert-Jung Polycut microtome, and toluidin blue stain for visuali-zation. One specimen of Pterygoplichthys lituratus, Otocinclusvestitus, and Farlowella acus was serially sectioned as well(Table 1).

Scanning electron micrographs were taken of teeth and lip tis-sues of all examined species and of five ontogenetic stages ofAncistrus cf. triradiatus. After isolation of the tissue samples

from the in toto fixed specimens (see earlier), the material wasdehydrated and critically point-dried with CO2 using a BalzersCPD 020, and gold coated using a Balzers SCD 040. The materialwas then examined using a Jeol JSM-840 scanning electronmicroscope (15 kV; magnification up to 15,0003).

RESULTSMorphology and Growth of Teeth

Upper and lower jaws of loricariids are orientedso that the teeth point ventrally, touching the sub-strate to which the fish is attaching (Fig. 1). Adult

Ancistrus cf. triradiatusspecimens carry one row of4067 emergent teeth per premaxilla (n 7, mean 55), and 5879 teeth per dentary (n 7, mean 69). No distinct differences were noted in toothshape for each jaw, except for those on the lateralside being somewhat smaller. Teeth are Z-shaped,

and are composed of a thick, curved base (which iscovered by the jaw epithelium), a thin lower shaft,a thicker upper shaft, and a curved bicuspid crown(Fig. 2C). The base is movably connected to the jawbone. The base and the shaft form an angle of about908, as do the shaft and the crown. The small la-teral cusp has an angle of 11081508 to the maincusp, and is about half as long. The anterior regionof the lower shaft is not calcified, but is composed ofsoft material. A distal protuberance of this softlayer, seen only in A. cf. triradiatus, is stained bluewith alcian blue and purple (metachromatic) withtoluidin blue (Fig. 2C,I). Manipulating individualteeth of freshly killed A. cf. triradiatus specimens

reveals that the lower shaft can actually bend up to908with respect to the tooth base (Fig. 3). Such con-siderable bending as shown in this figure (herecaused by manipulation with tweezers) probablyseldom occurs in natural circumstances, as the liptissue, situated behind the teeth, hinders such ex-cessive movement (e.g., Fig. 5A). Manipulatedbending in the opposite, anterior direction, invaria-bly causes breaking after bending only about 108208.

One row of teeth emerges from the jaw epithe-lium (Figs. 1 and 2H). The jaws are essentially bas-ket-shaped; the lower jaw also has a lateral handlearticulating with the quadrate and consisting of the

angulo-articular and part of the dento-mentomecke-lium (Geerinckx et al., 2007). Tooth germs are

TABLE 1. Specimens used in the present study

SpeciesSL

(mm)Age

(dPF) Method

Ancistrus cf. triradiatus 6.1 4 SS (2 lm)Ancistrus cf. triradiatus 6.7 4 SEMAncistrus cf. triradiatus 8.0 7 SS (2 lm)

Ancistrus cf. triradiatus 8.2 6 SEMAncistrus cf. triradiatus 9.8 8 SEMAncistrus cf. triradiatus 10.2 10 SEMAncistrus cf. triradiatus 10.2 14 SS (2 lm)Ancistrus cf. triradiatus 10.7 14 SEMAncistrus cf. triradiatus 33.5 160 SS (5 lm)Ancistrus cf. triradiatus 69.6 ? (adult) CSAncistrus cf. triradiatus 75.0 ? (adult) CSAncistrus cf. triradiatus 76.6 ? (adult) CSAncistrus cf. triradiatus 85.4 ? (adult) CSAncistrus cf. triradiatus 94.0 ? (adult) CSAncistrus cf. triradiatus 101.9 ? (adult) CSAncistrus cf. triradiatus 114.6 ? (adult) CSPterygoplichthys lituratus 63 ? (subadu lt) SS (5 lm)Pterygoplichthys lituratus 94 ? (subadul t) SEMPterygoplichthys lituratus 150 ? (subadult) CSPanaque nigrolineatus 71 ? (subadult) CS

Panaque nigrolineatus 76 ? (subadu lt) SEMOtocinclus vestitus 22 ? (adult) SS (5 lm)Otocinclus vestitus 24 ? (adult) CSOtocinclus vestitus 28 ? (adult) SEMFarlowella acus 124 ? (adult) CSFarlowella acus 125 ? (adult) SEMFarlowella acus 125 ? (adult) SS (5 lm)Rineloricaria parva 75 ? (adult) CSRineloricaria parva 76 ? (adult) SEMSturisoma aureum 85 ? (adult) CSSturisoma aureum 86 ? (adult) SEM

CS, clearing and staining; dPF, days post-fertilization; SEM,scanning electron microscopy; SL, standard length; SS, serialsectioning.

Fig. 1. Ventral view of head of adultAncistrus cf. triradiatusshowing the upper and lower jaws with tooth rows (arrows).Dark zones on jaws are the epithelium covering the replace-ment tooth rows. Scale bar is 5 mm.

806 T. GEERINCKX ET AL.

Journal of MorphologyDOI 10.1002/jmor


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found deep inside the basket; growing teeth migrate

within the basket. The individual tooth germs arenot found in bony crypts; serial sections show thatthe bases of emergent teeth are connected to thebone via soft tissue, most probably containing alarge amount of collagen. Thus the development iscompletely extraosseous, as in other siluriformsand many other teleosts (Trapani, 2001). In the pre-maxilla, there is a progression of less- to more-developed teeth from posterior to anterior (viceversa for dentary). An anteroposterior cross-sectionthrough the jaws (Fig. 4) clearly shows this progres-sion, but at the same time gives the false impres-

sion of the presence of numerous replacement tooth

rows (up to 20). Serial sections, however, reveal thepresence of only about four successive teeth in onetooth family: the arrows on Figure 2J show thereplacement teeth originating from two distinctloci; an epithelial track connects the subsequentreplacement teeth. A tooth becomes erected after ithas been fully formed (Fig. 4): it penetrates the jawepithelium, thereby rotating 408808 (large arrow-heads on Fig. 5A indicate emerging teeth). This pos-sibly rather sudden tooth movement leaves trail-like scars in the weak jaw epithelium (small arrow-heads on Figs. 2H and 5A). Once in use, the crown

Fig. 2. Representative teethof lower jaw. A: Otocinclus ves-

titus. B: Sturisoma aureum. C:Ancistrus cf. triradiatus. D:Farlowella acus. E: Pterygo-plichthys lituratus. F: Rinelori-caria parva. G: Panaque nigro-lineatus. Scale bar for AG is500 lm. H: Section through leftpremaxilla of a 33.5 mm A. cf.triradiatus, showing emergentteeth (below) and replacementtooth rows. Arrowheads pointat scars left by emerging tooth.I: Detail of H, showing sectionsof the upper shaft (1), transi-tion zone between upper andlower shaft, with distal protu-berance (2), and lower shaft (3).

J: Detail of premaxill aryreplacement teeth with indica-tion of two series of successivereplacement teeth (indicated bywhite and black horizontalarrows, respectively). The verti-cal arrows indicate the lociwhere each series originates.Scale bars for HJ are 50 lm.o-mx, os maxillare; o-pmx, ospraemaxillare; t-g, tooth germs;t, (erected) teeth.

TEETH AND EPIDERMAL BRUSHES IN LORICARIIDAE 807



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is worn and consequently shortened; Figure 5Bshows obvious signs of wear caused by scraping onsubstrates.

Previous authors have described the diversity innumber and shape of teeth in various loricariids(Muller and Weber, 1992; Delariva and Agostinho,2001). We limit our description to the most remark-able shape observations. The teeth of Pterygoplich-

thys lituratus and Otocinclus vestitus resemblethose ofAncistrus cf. triradiatus, but the soft layerin the lower shaft region is thinner, lacking the dis-tal protuberance (Figs. 2A,E and 5C,D). Long spa-tulate crowns with almost similarly sized cuspscharacterize Sturisoma aureum and Farlowellaacus (Figs. 2B,D and 5E,F). Panaque nigrolineatushas sturdy, unicuspid, spoon-shaped teeth (Figs. 2G

and 5G). Both unequally sized cusps of the teeth ofRineloricaria parva are pointed (Figs. 2F and 5H).Teeth in the latter two species are least curved andlack the soft layer. They appear to be rigid, whileteeth of all other species can bend to a certaindegree between the lower shaft and the base. While

1525 apparent replacement tooth rows are seen atfirst sight in adult specimens of all specimens (Fig.4), only about four are present (as observed on se-rial sections ofP. lituratus and Farlowella acus), asin A. cf. triradiatus. Analogous to this, the 78apparent replacement rows seen in O. vestitusactually represent only two rows. One to two rowsare probably present in P. nigrolineatus(5 apparentrows), andR. parva(4 apparent rows).

Tooth Shape During Early Ontogeny

Ancistrus cf. triradiatus hatches 56 days afterfertilization. The yolk sac is depleted after an addi-

tional 45 days. Ingested food particles are foundin the intestine from 3 to 4 days after hatching. Thefirst teeth appear on the premaxilla and eruptbefore hatching, at 4 days after fertilization.The (59) premaxillary teeth are conical, bearingno resemblance at all to the adult tooth shape(Fig. 6A). Analogous to the appearance of the skinodontodes, these first teeth are observed before thesupporting bone materializes (Geerinckx et al.,2007).

Six days after fertilization, half a day after ha-tching, similar teeth are still present on the pre-maxilla, and identical teeth have appeared on thedentary as well. One replacement tooth row is pres-

ent (7 days PF; arrows on Fig. 7A). Serial sectionsshow that, as in adults, these teeth are connected tothe bone via soft (collagenous) tissue. At 8 days newteeth possess a flattened, unicuspid tip (arrowheadson Fig. 6B); the curvature between the base and theshaft has now developed. Consequently, these newteeth are recurved backward (Fig. 6B), instead ofslightly forward (conical teeth on Fig. 6A). A rudi-

Fig. 3. Tooth of Ancistrus cf. triradiatus with indication ofbendable lower shaft portion. The stippled line represents thenearly maximum extent of bending. See text for details.

Fig. 4. Medial view on ananteroposterior cross-sectionthrough the right (A) upperand (B) lower jaw of a 75 mmSL Ancistrus cf. triradiatus,indicating emergent tooth andthe apparent multiple series ofreplacement tooth. Notice thatthere are actually only aboutfour replacement teeth peremergent tooth. The stippledlines indicate the approximateposition of the jaw epithelium.Position of the substrate is indi-cated by a horizontal line. Scalebar is 1 mm.




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mentary bicuspid crown is present on some teeth at10 days (both cusps are indicated by arrowheads onFig. 6C). The curvature between the shaft and thecrown, added to the one between the base and theshaft, results in the first Z-like teeth. Only 14 daysafter fertilization bicuspid crowns are present(Fig. 6D); cartilage resorption has made place foralready 34 replacement rows (arrows on Fig. 7B).This is already the maximum of tooth rowsobserved in Ancistrus cf. triradiatus. The numberof teeth has risen to 1317 teeth for each of the four

jaw bones. Already some of the teeth appear to

have a damaged crown. As opposed to the numberof replacement rows, the number of teeth progres-sively increases during further ontogeny.

Pharyngeal teeth are present in all examinedspecies [as opposed to Alexanders (1965) statementthat they are absent]; they are cone-shaped. Theirnumber more or less correlates with body size,without any further substantial difference betweenspecies. In Ancistrus cf. triradiatus, the first pha-ryngeal teeth appear at 3 days after hatching(Geerinckx et al., 2007), and about 30 teeth arepresent per single jaw quadrant.

Fig. 5. Loricariid tooth crowns.SEM. A: Anterior view of den-tary teeth of Ancistrus cf. trira-diatus (large arrowheads indi-cate emerging teeth; smallarrowheads indicate scars left byemerging teeth). B: Ventralclose-up of heavily worn dentarytooth crown of same species

(arrowheads indicate wear zone).C: Ventral close-up of dentarytooth crown of Pterygoplichthyslituratus. D: Ventral view ofdentary tooth crowns of Otocin-clus vestitus. E: Ventral view ofdentary tooth crowns of Sturi-soma aureum. F: Ventral view ofdentary tooth crowns of Farlo-wella acus. G: Anterior view ofdentary tooth crown of Panaquenigrolineatus. H: Ventral view ofdentary tooth crowns of Rinelori-caria parva. Scale bars are 50 lm.




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Morphology and Growth of Unculi

Unicellular epidermal brushes or unculi arefound in a field on the top of labial papillae of thelower lip. In some species with unculi not all papil-lae bear unculi; unculi are rare on the upper lip. Inthose cases where taste buds are present on thepapillae as well, the unculi are found rostrally tothese. Counts of unculi on five randomly chosenpapillae, and height measurements of 10 randomlychosen unculi at the scanning electron microscope

yielded the following ranges: Ancistrus cf. triradia-tus: 4080 unculi per papilla, sometimes coveringthe whole top of the papilla, height 715 lm, unculislender with the tip curved rostrally (Fig. 8A); Pte-rygoplichthys lituratus: 2550 unculi per papilla,height 1216 lm, straight with a slightly flattenedtip (Fig. 8B); Panaque nigrolineatus: several hun-dreds of unculi per papilla, also covering the sidesof the papilla, height 510 lm, broad with a flat-tened tip (Fig. 8C); Sturisoma aureum: 2035unculi per papilla, height 812 lm, tip flattened;

Farlowella acus: 4070 unculi per papilla, height

1217 lm, sometimes covering whole top of papilla,unculi slender, tip straight (not flattened) (Fig. 8D);

Rineloricaria parva: no unculi present on papillae;and Otocinclus vestitus: 4070 unculi per papilla,height 24 lm, unculi broad, and tip extremely flat-tened (Fig. 8E).

Epidermal cell diameter is 812 lm in all spe-cies. Taste buds are numerous on the papillae in R.parva, rare inF. acus,O. vestitus, andP. nigrolinea-tus (arrowheads on Fig. 8C,E), and absent on many(but not all) papillae in the other species. Unculiappear to be replaced when parts of the upper epi-dermal layer of the lip are shed, as seen in A. cf.triradiatus (Fig. 8F). Figure 8F, as well as Figure 9,suggest that the shedding occurs more or less perpapilla. In the specimen in Figure 9, only three ofthe total amount of papillae was in an obvious pro-cess of shedding.

Shape of Unculi During Early OntogenyEmbryonic specimens ofAncistruscf. triraditatus

have rudimentary papillae 1 day after hatching(Fig. 10A). First sloughing of epidermis occurs at 3

Fig. 6. Teeth of early stages of Ancistrus cf. triradiatusSEM. A: 4 days PF (6.7 mm SL; upper jaw). B: 8 days PF(9.8 mm SL; lower jaw). C: 10 days PF (10.2 mm SL; lowerjaw). D: Fourteen days PF (10.7 mm SL; upper jaw). Scale bars

are 10 lm.

Fig. 7. Serial sections through the left lower jaw of. (A) 7days PF old (8.0 mm SL) and (B) 14 days PF old (10.2 mm SL)Ancistrus cf. triradiatus. Cartilage resorption of the medial partof the Meckels cartilage has occurred between both stages.Arrows point to one tooth series (emergent tooth and replace-ment teeth originating from the same locus). Scale bars are100 lm. c-Meck, cartilago Meckeli; o-den-m, os dento-mento-meckelium; t-g, tooth germ; t, (erected) tooth.




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days after hatching (Fig. 10B). The first unculiappear together with the first well developed toothcusps, at 5 days after hatching (Fig. 10C,D). This isthe moment of complete resorption of the yolk sac.

DISCUSSION

As in several (but not all) otherAncistrusspecies,the number of dentary teeth in Ancistrus cf. trira-diatus is equal to (or slightly higher than) the num-ber of premaxillary teeth (Muller and Weber, 1992;Miquilarena et al., 1994; Fisch-Muller et al., 2001).No significant intraspecific differences between

both jaws were noted in the other examined species.The morphology of teeth of A. cf. triradiatusappears to be the most interesting of all loricariidsexamined by us and other authors thus far (e.g.,Schaefer, 1987; Muller and Weber, 1992; Schaeferand Stewart, 1993; Delariva and Agostinho, 2001;

Armbruster, 2004). The teeth are characterized by astrong Z-shaped curvature, the differentiation ofthe shaft in a thin lower and a thick upper portion,and the presence of an anterior layer of soft tissuealong the lower shaft. This layer has been found inall examined species except Panaque nigrolineatus

and Rineloricaria parva. The thicker distal protu-berance was found in A. cf. triradiatus only. Thehistological nature of the soft layer is unclear, butmight well have a strain-resistant function: ifthe crown jolts along a rough substrate during

Fig. 9. Serial section through some lower lip papillae ofAncistrus cf. triradiatus (33.5 mm SL). On two papillae areplacement epidermal layer with unculi is present, while thetop layer of the epidermis appears as if soon to be shed. Scalebar is 100 lm.

Fig. 8. Loricariid lower lippapillae and unculi. SEM. A:Rostrally inclined unculi of

Ancistrus cf. triradiatus (ante-rior toward bottom). B:Straight unculi of Pterygoplich-thys lituratus. C: Papilla of Panaque nigrolineatus bearingshort and sturdy unculi. D: Pa-pilla of Farlowella acus bearinglong and slender unculi. E:Short and flat unculi of Otocin-clus vestitus. F: Shedding ofepidermis of papilla of A. cf.triradiatus revealing new celllayer with partly developedunculi. Arrowheads on C and Eindicate taste buds. Scale barsare 20 lm.




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scraping, the anterior region of the tooth is prone tostrain, especially near the base of the lower shaft,where the bending occurs. A completely calcifiedtooth might easily break. Figure 2I suggests thatthe posterior lower shaft region (near the base) isfar from completely calcified: it is almost notstained by the toluidin blue stain (compare toothsection 3 to 1 and 2 on Fig. 2I). This might re-

present an elaborate adaptation to the fact that theshaft of loricariid teeth encounters sideward (ante-rior) forces instead of axial forces during feeding.The unmineralized (collagenous) attachment of thetooth base, present in most ostarioclupeomorph te-leosts (Fink, 1981), further increases the mobility ofthe individual tooth (with respect to the jaw bone).

The link between tooth shape and diet has beeninferred from several studies, with the general con-clusion that slender teeth are appropriate for scra-ping smaller particles from surfaces, while larger,stronger, and spatulate teeth are better for scrapingcoarser food items off hard surfaces (Delariva and

Agostinho, 2001). This is best illustrated by the two

extreme conditions. Robust teeth are present intaxa like Panaque and the Hypostomus cochliodongroup (Schaefer and Stewart, 1993; Armbruster,2004; this article), of which at least Panaque hasbeen proven to be able to eat and digest wood(Nelson et al., 1999). On the other hand, sometimescomplete absence of teeth is observed in some lori-cariines, a subfamily containing many detritus-feeders living on soft substrates (Salazar et al.,1982; Rapp Py-Daniel, 2000). The lack of the softtissue layer and the lesser mobility of the toothbase of Panaque nigrolineatus relative to the bone

might reflect the need for more robust, better an-chored and rigid (thus completely mineralized)teeth for scraping wood. The diet of the loricariine

Rineloricaria parva is less known; aquarium speci-mens were commonly observed on sand and gravel,when compared to the other species (stones, woodpieces, and plants were provided as well). Some

Loricaria species are known to feed more on small

animals and detritus on soft bottoms (as opposed tohard substrates) (Saul, 1975; Aranha et al., 1998;Reis and Pereira, 2000). More ecological data con-firming this forR. parvaare needed to substantiatethe hypothesis that this species scrapes less onhard substrates than the other loricariids examinedin this study. The lack of a soft layer in both P.nigrolineatus and R. parva also coincides with alow number of replacement tooth rows.

The mineralized tooth portion of advanced actino-pterygians does not contain enamel (a purely epi-thelial product), but enameloid (to which ectome-senchymal tissue contributes) (Huysseune and Sire,1998). However, a soft tooth portion, as found in the

lower shaft of several loricariid species, has neitherbeen reported before, nor in any other teleost group.It is possible that the thin, hard part of the lowershaft near the base is not as intensely mineralizedas the remainder of the tooth. It is hard to find al-ternative explanations for the fact that this zonecan bend without immediately breaking. A possiblehypo-mineralization might be tested using micro-radiography.

No clear correlation, but a scale of different com-binations is found between tooth and unculus shapein the examined species. Of the loricariines, Farlo-

Fig. 10. Lower lip surface ofearly stages of Ancistrus cf.triradiatus SEM. A: 6 days PF(8.2 mm SL). B: 8 days PF(9.8 mm SL). C: 10 days PF(10.2 mm SL). D: Detail of firsttrue unculi (10 days old speci-men). Scale bars for AC are100 lm, for D, 5 lm.




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wella acus has slender teeth and unculi, and Sturi-soma aureum has similar teeth but sturdier unculi.Unculi are absent in Rineloricaria parva, whichhas pointed tooth cusps and no soft anterior layer.

Among the hypostomines, slender unculi co-occurwith relatively slender teeth in Pterygoplichthys

lituratus; unculi are somewhat thicker and ros-trally inclined, and teeth are somewhat narrower inAncistrus cf. triradiatus. Panaque nigrolineatus ischaracterized not only by the spoon-shaped teethwithout anterior soft layer, but also by numerousshort and flattened unculi. Unculi are even shorterand equally flattened, but less numerous in thehypoptopomatine Otocinclus vestitus, which hasfew and rather slender teeth. Unculi were not foundinOtocinclussp. by Ono (1980).

The interspecific shape diversity, and the rostralinclination of the unculi on the lower lip in Ancis-trus cf. triradiatus, corroborate the hypothesis thatunculi in loricariids may serve as abrasive struc-

tures (Ono, 1980). Ono (1980) mentioned the pre-sence of unculi on the upper lip of certain hyposto-mines; the upper lip is moved far less during scra-ping, and papillae are less numerous. She did notelaborate on the relative position of unculi andtaste buds on the upper lip papillae. Keratinization,though rare in teleosts, has been found in severaltaxa; we refer to Das and Nag (2006) for an over-view of such reports in teleosts and a histologicalexamination in keratinized spines ( unculi) in thecyprinid Garra gotyla gotyla. In the latter species,direction of the spines on the lower lip is opposite tothe unculus direction in A. cf. triradiatus. This, andthe distribution of the spines along the outer edge

of the lip, surrounding a central callus part, sug-gests a function in adhesion rather than in feeding.In most loricariids, the unculi might well serve bothfunctions.

It might be that the shedding of lip epidermiscontributes to a renewal of unculi. The sheddingof the epidermis of single papillae on Figures 8Fand 9 proves that such shedding does occur in

Ancistruscf. triradiatus, although similar processesin teleosts are not well treated in the literature.One could hypothesize that the abrasive function ofthe unculiferous papillae causes them to wear, ascenario in which shedding would be beneficial.

Unculus structure might be an underestimated

aspect of the adaptive radiation present in the lori-cariid family, next to shape, size, and number of theteeth, morphology and orientation of the jaws, andthe presence of labial filaments or fimbriae (RappPy-Daniel, 2000; Delariva and Agostinho, 2001;

Armbruster, 2004), and deserves a closer look in eco-logical studies where several loricariid species areoften found to live syntopically (Power, 1984; Buckand Sazima, 1995; Aranha et al., 1998; Delarivaand Agostinho, 2001). As pointed out by Zaret andSmith (1984), explanations for the small differences(and similarities) between ecologically important

structures like teeth and unculi of similar or relatedspecies, are not easy and will have to rely on a sig-nificant amount of ecological information includingpresent and past syntopy of the various species.

Generally the first tooth generations in teleostsconsist of simple, conical teeth, irrespective of the

adult tooth shape (Huysseune and Sire, 1997b; Sireet al., 2002; Vandervennet et al., 2006). Even lori-cariids are no exception, as observed in Ancistruscf. triradiatus. During further growth in the juve-nile and adult phases, only a weak allometry inshaft and crown length has been observed in sev-eralAncistrus and Hypostomus species (Muller andWeber, 1992). Schaefer and Stewart (1993) notedmore pronounced shape transitions (from standardbicuspid to unicuspid and spoon-shaped) in juve-niles of thePanaque dentex group.

In the lower jaw, we did not observe cartilageresorption at the level of formation of individualtooth germs of the first generations, as observed in

some cichlids by Huysseune (1990). This might berelated to the relatively large distance between thetooth germs (and the dentary bone anlage) andMeckels cartilage in the 8.0 mm Ancistrus speci-men. In the 10.2 mm specimen Meckels cartilage iscompletely resorbed at the level of the teeth, but wecannot infer a direct relation with the tooth germsthat now develop at the former location of the carti-lage (Fig. 7B).

In conclusion, we consider the teeth and lessknown unculi of Loricariidae to be highly diversetools, which most certainly are the result of anadaptive radiation. The unculi most probably havethe same function as the teeth, i.e., scraping food

off substrates, and as such, a comparable selectivepressure can be expected. The morphology and di-versity of teeth and unculi surely adds to the adap-tations to the broad ecological niche occupied bythis successful neotropical catfish family.

ACKNOWLEDGMENTS

Marleen Brunain made the high-quality histolo-gical sections. Rita Van Driessche and MarjoleinCouvreur are acknowledged for operating the scan-ning electron microscope. Authors thank two ano-nymous reviewers for their comments.

LITERATURE CITED

Alexander RMcN. 1965. Structure and function in the catfish.J Zool-Lond 148:88152.

Aranha JMR, Takeuti DF, Yoshimura TM. 1998. Habitat useand food partitioning of the fishes in a coastal stream of At-lantic Forest, Brazil. Rev Biol Trop 46:951959.

Arens W. 1994. Striking convergence in the mouthpart evolu-tion of stream-living algae grazers. J Zool Syst Evol Res32:319343.

Armbruster JW. 2004. Phylogenetic relationships of the sucker-mouth armored catfishes (Loricariidae) with emphasis on theHypostominae and the Ancistrinae. Zool J Linn Soc 141:180.




10/10

Arratia G. 1987. Description of the primitive family Diplomysti-dae (Siluriformes, Teleostei, Pisces): Morphology, taxonomyand phylogenetic implications. Bonn Zool Monogr 24:1120.

Arratia G, Huaqun L. 1995. Morphology of the lateral line sys-tem and of the skin of diplomystid and certain primitive lori-carioid catfishes and systematic and ecological considerations.Bonn Zool Monogr 36:1110.

Benjamin M. 1986. The oral sucker of Gyrinocheilus aymonieri

(Teleostei: Cypriniformes). J Zool-Lond 1:211254.Branson BA. 1962. Observations on the breeding tubercles of

some Ozarkian minnows with notes on the barbels of Hybop-sis. Copeia 1962:532539.

Buck S, Sazima I. 1995. An assemblage of mailed catfishes (Lor-icariidae) in southeastern Brazil: Distribution, activity, andfeeding. Ichthyol Explor Freshwater 6:325332.

Cardona L, Guerao G. 1994. Astroblepus riberae, una nuevaespecie de siluriforme cavernicola del Peru (Osteichthyes:Astroblepidae). Mem Biospeol XXI:2124.

Chen X, Arratia G. 1996. Breeding tubercles of Phoxinus (Tele-ostei: Cyprinidae): Morphology, distribution and phylogeneticimplications. J Morphol 228:127144.

Das D, Nag TC. 2006. Fine structure of the organ of attachmentof the teleost, Garra gotyla gotyla (Ham). Zoology 109:300309.

Delariva RL, Agostinho AA. 2001. Relationship between mor-

phology and diets of six neotropical loricariids. J Fish Biol58:832847.

DoNascimiento C, Provenzano F. 2006. The genus Henonemus(Siluriformes: Trichomycteridae) with a description of a newspecies from Venezuela. Copeia 2006:198205.

Fink WL. 1981. Ontogeny and phylogeny of tooth attachmentmodes in actinopterygian fishes. J Morphol 167:167184.

Fisch-Muller S, Mazzoni R, Weber C. 2001. Genetic and mor-phological evidence for two new sibling species of Ancistrus(Siluriformes: Loricariidae) in upper rio Tocantins drainage,Brazil. Ichthyol Explor Freshwater 12:289304.

Geerinckx T, Brunain M, Adriaens D. 2007. Development of theosteocranium in the suckermouth armored catfish Ancistruscf. triradiatus (Loricariidae, Siluriformes). J Morphol 268:254274.

Howes GJ, Sanford CPJ. 1987. Oral ontogeny of the Ayu, Plec-coglossus altivelis and comparisons with the jaws of other sal-

moniform fishes. Zool J Linn Soc 89:133169.Huysseune A. 1990. Development of the anterior part of the

mandible and the mandibular dentition in two species ofCichlidae (Teleostei). Cybium 14:327344.

Huysseune A, Sire J-Y. 1997a. Structure and development ofteeth in three armored catfish, Corydoras aeneus, C. arcuatusand Hoplosternum littorale (Siluriformes, Callichthyidae).Acta Zool-Stockholm 78:6984.

Huysseune A, Sire J-Y. 1997b. Structure and development offirst-generation teeth in the cichlid Hemichromis bimaculatus(Teleostei, Cichlidae). Tissue Cell 29:679697.

Huysseune A, Sire J-Y. 1998. Evolution of patterns and proc-esses in teeth and tooth-related tissues in non-mammalianvertebrates. Eur J Oral Sci 106(Suppl 1):437481.

Miquilarena AM, Lopez HL, Aquino AE. 1994. Los Ancistrinae(Pisces: Loricariidae) de Argentina. In: De Castellanos ZA,editor. Fauna de Agua Dulce de la Republica Argentina.

Museo de la Plata 40. pp 149.Muller S, Weber C. 1992. Les dents de sous-familles Hypostomi-

nae et Ancistrinae (Pisces, Siluriformes, Loricariidae) et leurvaleur taxonomique. Rev Suisse Zool 99:747754.

Nelson JA, Wubah DA, Whitmer ME, Johnson EA, Stewart DJ.1999. Wood-eating catfishes of the genus Panaque: Gut micro-flora and cellulolytic enzyme activities. J Fish Biol 54:10691082.

Ono RD. 1980. Fine structure and distribution of epidermal pro-jections associated with taste buds on the oral papillae insome loricariid catfishes (Siluroidei: Loricariidae). J Morphol164:139159.

Orton GL. 1953. The systematics of vertebrate larvae. Syst Zool2:6375.

Power ME. 1984. Grazing response of tropical freshwater fishesto different scales of variation in their food. In: Zaret TM, edi-tor. Evolutionary Ecology of Neotropical Freshwater Fishes.The Hague: Dr. W. Junk Publishers. pp 2537.

Rapp Py-Daniel LH. 2000. Tracking evolutionary trends inSiluriformes (Teleostei: Ostariophysi). In: International Con-gress on the Biology of Fish, Aberdeen. Evolution SymposiumProceedings. Aberdeen: University of Aberdeen. pp 5772.

Reis RE, Pereira EHL. 2000. Three new species of the loricariidcatfish genus Loricariichthys (Teleostei: Siluriformes) fromsouthern South America. Copeia 2000:10291047.

Roberts TR. 1973. Interrelationships of ostariophysans. In:Greenwood PH, Miles RS, Patterson C, editors. Interrelation-ships of Fishes. London: Linnean Society of London, Aca-demic Press. pp 373395.

Roberts TR. 1982. Unculi (horny projections arising from singlecells), an adaptive feature of the epidermis of ostariophysanfishes. Zool Scr 11:5576.

Salazar FJM, Isbrucker IJH, Nijssen H. 1982. Dentectus bar-barmatus, a new genus and species of mailed catfish from theOrinoco basin of Venezuela (Pisces, Siluriformes, Loricarii-dae). Beaufortia 32:125137.

Saul WG. 1975. An ecological study of fishes at a site in UpperAmazonian Ecuador. Proc Acad Nat Sci Phila 127:93134.

Schaefer SA. 1987. Osteology of Hypostomus plecostomus (Lin-naeus) with a phylogenetic analysis of the loricariid subfami-lies (Pisces: Siluroidei). Contrib Sci 394:131.

Schaefer SA. 1990. Anatomy and relationships of the scoloplacidcatfishes. Proc Acad Nat Sci Phila 142:167210.

Schaefer SA, Stewart DJ. 1993. Systematics of the Panaquedentex species group (Siluriformes: Loricariidae), wood-eatingarmored catfishes from tropical South America. IchthyolExplor Freshwater 4:309342.

Sire J-Y, Davit-Beal T, Delgado S, Van der heyden C, Huys-seune A. 2002. First-generation teeth in nonmammalian line-ages: Evidence for a conserved ancestral character? MicroscRes Tech 59:408434.

Taylor WR, Van Dyke GC. 1985. Revised procedures for stain-ing and clearing small fishes and other vertebrates for boneand cartilage study. Cybium 9:107119.

Trapani J. 2001. Position of developing replacement teeth in te-leosts. Copeia 2001:3551.

Uehara K, Miyoshi S. 1993. Structure of comblike teeth of theAyu sweetfish, Plecoglossus altivelis (Teleostei: Isospondyli). I.Denticles and tooth attachment. J Morphol 217:229238.

Vandervennet E, Wautier K, Verheyen E, Huysseune A. 2006.From conical to spatulate: Intra- and interspecific changes intooth shape in closely related cichlids (Teleostei; Cichlidae:Eretmodini). J Morphol 267:516525.

Wassersug RJ, Yamahita M. 2001. Plasticity and constraints onfeeding kinematics in anuran larvae. Comp Biochem Physiol

Part A 131:183195.Wiley JL, Collette BB. 1970. Breeding tubercles and contact

organs in fishes: Their occurrence, structure and significance.Bull Am Mus Nat Hist 149:143216.

Zaret TM, Smith EP. 1984. On measuring niches and not mea-suring them. In: Zaret TM, editor. Evolutionary Ecology ofNeotropical Freshwater Fishes. The Hague: Dr. W. Junk Pub-lishers. pp 127137.



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