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A quantitative analysis of ferric iron in butterflyfish teeth (Chaetodontidae, Perciformes) and the relationship to feeding ecology
Canadian Journal of Zoology
Abstract
Despite much work on the iron compounds found on invertebrate and vertebrate teeth, no interspecific quantitative analyses of iron compounds in fish teeth have ever been conducted, nor in any vertebrate has such a study related the iron concentrations to the feeding ecology. This study reveals that ferric iron exists on the tooth cap of eight species of chaetodontid butterflyfishes. The iron layer appears early in tooth development and is darkest, and presumably more concentrated, towards the tooth tip. There are significant differences among the eight species, with those that feed on harder prey having more iron than those that feed on softer-bodied prey. Furthermore, there exist differences among the species that correlate with the degree of morphological specialization for feeding on hard-bodied prey. The iron layer, which has been shown by others to be harder than the underlying enameloid, probably represents a specialization to harden the teeth, resisting abrasion and cracking.
... In addition, different species from various families (e.g. Acanthuridae, Aracanidae, Balistidae, Chaetodontidae, Cichlidae, Esocidae, Helostomatidae, Ostraciidae, Tetraodontidae) also possess a thin superficial layer, commonly named the cuticle, covering the enameloid and often red-pigmented (Garant, 1969;Herold, 1975;Motta, 1987;Suga et al., 1989). The redpigmentation has been described as an iron-rich or iron oxide deposit and its presence is mainly thought to be phylogenetic rather than environmental (Suga et al., 1991(Suga et al., , 1989. ...
... Apart from the tooth arrangement and shape, we expect other possible changes in tooth features between divergent feeding habits. In teleosts, the relationships between tooth microstructure and composition with diet has been rarely examined as well as the function, microstructure, composition and formation of the cuticle (but see Farina et al., 1999;Motta, 1987). ...
In any vertebrate group, tooth shape is known to fit with a biological function related to diet. However, little is known about the relationships between diet and tooth microstructure and composition in teleost fishes. In this work, we describe the external morphology, internal microstructure and elemental composition of the oral teeth of three representative species of the family Serrasalmidae having different feeding habits (herbivorous vs. omnivorous vs. carnivorous). We used backscattered-electron imaging and low vacuum environmental scanning electron microscope to compare the organization and mineralization of tooth layers as well as energy dispersive X-ray microanalysis and Raman microspectrometry to investigate the elemental composition, Ca/P ratio and mineralogy of the most superficial layers. Oral teeth of each serrasalmid species have the same internal organization based on five distinctive layers (i.e. pulp, dentine, inner enameloid, outer enameloid and cuticle) but the general tooth morphology is different according to diet. Microstructural and compositional variation of the cuticle and iron-enrichment of superficial layers were highlighted between herbivorous and carnivorous species. Iron is more concentrated in teeth of the herbivorous species where it is associated with a thicker cuticle explaining the more intense red-pigmentation of the cutting edges of oral teeth. The iron-enrichment is interpreted as a substitution of Ca by Fe in the hydroxyapatite. These traits are discussed in the light of the evolutionary history of the family. Further considerations and hypotheses about the formation and origin of the mineralized tooth layers and especially the iron-rich superficial layers in teleost fishes are suggested.
... Similarly, dental morphology and patterning more directly determine what food resources can be procured. The bristle-shaped iron-tipped teeth in chaetodontid jaws [58] have been proposed to be an ancestral biting adaptation [59,60]. Indeed, this appears to be a generalized trait for chaetodontoid (bristle-toothed) fishes (Chaetodontidae, Pomacanthidae and Micrognathidae) that form a major part of the coral reef ichthyofauna [30]. ...
... Specializations to teeth and lips may also be important in shaping the abilities of corallivores to harvest digestible elements from the abrasive calcium carbonate matrix of stony corals. Such specializations include bristle-like teeth tipped with iron-invested caps in butterflyfishes [58,59], fused oral beaks for tough gouging bites in parrotfishes [6,34], and fleshy self-lubricating lips for mucus extraction in tube-lipped wrasses [71]. Regardless of the mechanism, Chaetodon species have somehow managed to overcome these challenges, allowing the group to enjoy a period of high net-diversification since the Miocene [72]. ...
The diversity of fishes on coral reefs is influenced by the evolution of feeding innovations. For instance, the evolution of an intramandibular jaw joint has aided shifts to corallivory in Chaetodon butterflyfishes following their Miocene colonization of coral reefs. Today, over half of all Chaetodon species consume coral, easily the largest concentration of corallivores in any reef fish family. In contrast with Chaetodon, other chaetodontids, including the long-jawed bannerfishes, remain less intimately associated with coral and mainly consume other invertebrate prey. Here, we test (i) if intramandibular joint (IMJ) evolution in Chaetodon has accelerated feeding morphological diversification, and (ii) if cranial and post-cranial traits were affected similarly. We measured 19 cranial functional morphological traits, gut length and body elongation for 33 Indo-Pacific species. Comparisons of Brownian motion rate parameters revealed that cranial diversification was about four times slower in Chaetodon butterflyfishes with the IMJ than in other chaetodontids. However, the rate of gut length evolution was significantly faster in Chaetodon, with no group-differences for body elongation. The contrasting patterns of cranial and post-cranial morphological evolution stress the importance of comprehensive datasets in ecomorphology. The IMJ appears to enhance coral feeding ability in Chaetodon and represents a design breakthrough that facilitates this trophic strategy. Meanwhile, variation in gut anatomy probably reflects diversity in how coral tissues are procured and assimilated. Bannerfishes, by contrast, retain a relatively unspecialized gut for processing invertebrate prey, but have evolved some of the most extreme cranial mechanical innovations among bony fishes for procuring elusive prey. © 2017 The Author(s) Published by the Royal Society. All rights reserved.
... Iron also strengthens the immune system and has important roles in electron transfer, cell respiration, cell proliferation and differentiation. It has been suggested that iron plays a role in both enamel development and mechanical properties of enamel (30). ...
Objective: Heavy metals threaten life by accumulating in the body via various sources as water,air and foods. Smoking is one of the important factors that causes this problem. Despite there is an abundant number of studies showing the detrimental effects of smoking on periodontal health, the mechanisms that cause these harmful effects is not clearly known yet. The main aim of our study is to discover whether heavy metal deposition on the tooth surface is related to the disease-causing potential of smoking. Materials and Method: Total of 80 individuals consist of 43 women and 37 men were included in this study. The participants were divided into 4 groups of 20 individuals each according to the results from clinical examination and anamnesis. Plaque index, gingival index, pocket depth, bleeding on probing and clinical attachment level were recorded clinically. The teeth indicated for extraction were collected. Cd, Pb, Ni, Cr and Fe depositions on teeth were measured by ICP-OES device. Kolmogorov-Smirnov, Student T, Mann Whitney U, One way ANOVA, Kruskal Wallis, Ki-Kare, Pearson, and Spearman tests were performed for the statistical analysis. Results: Smoking increases the accumulation of heavy metals such as Cd, Ni, Cr, and Pb. The Pb level was higher in both the smoking group and the periodontitis group, compared with the control group. Fe levels were found high in the non-smoking healthy group. Cr and Fe levels were found higher in women while Cd level was higher in men. Positive correlations were found between Pb and plaque index, gingival index, pocket depth and bleeding on probing; and also between Ni and plaque index. ( p=0.000, p=0.009, p=0.025, p=0.011, p=0.019) Conclusion: In conclusion, our study explored the connection between heavy metal deposition on tooth surfaces and the disease-causing potential of smoking. Smoking has been identified as a significant factor in the increased accumulation of heavy metals, including Cd, Ni, Cr, and Pb. The higher Pb levels seen in both the smoking and periodontitis groups, compared to the control group, suggest a potential link between Pb accumulation and periodontal health. Additionally, differences based on gender were observed, with women showing higher Cr and Fe levels, while Cd levels were more elevated in men. The positive correlations between Pb and various periodontal indices, along with the correlation between Ni and plaque index, shed light on the potential influence of heavy metal deposition on periodontal health. While our findings enhance our understanding of the interplay between smoking, heavy metal deposition, and oral health, further research is needed to fully comprehend the underlying mechanisms. Such insights could lead to interventions aimed at minimizing the adverse effects of heavy metal accumulation on oral health.
... head of the first supraneural longer and much flattened). The fossil described herein cannot be aligned with the subgenera Roaops, Exornator, and Lepidochaetodon, since their two supraneurals are consolidated into a single bone, and especially with Lepidochaetodon whose oral jaws contain two different types of teeth (labial teeth are significantly larger and stouter than lingual ones; Motta 1985Motta , 1987Blum 1988). Tetrachaetodon can be distinguished from all the other subgenera, including †Blumchaetodon subgen. ...
We describe here a new bony fish assemblage collected from a fossiliferous outcrop located in Perarolo, Berici Hills, Venetian Southern Alps. The fossiliferous deposits pertain to the Rupelian (lower Oligocene) Castelgomberto Calcarenite and are indicative of a tropical marine shallow water setting associated with coral reefs. The assemblage is characterized by diminutive putative cryptobenthic fishes, including a single goby (family Gobiidae) and several cardinalfishes of the subfamily Pseudamiinae (family Apogonidae). Furthermore, a new apogonine of the extinct tribe †Eoapogonini, a new butterflyfish (family Chaetodontidae), and an indeterminate viviparous brotula belonging to the ophidiiform family Dinematichthyidae, are also present, and likely represented part of the epibenthic community. Some of the taxa described herein are among the first occurrences within their respective lineages in the fossil record. The Perarolo taxa document the first Oligocene coral reef fish assemblage known to date. Four taxa are described as new: †Arconiapogon deangelii gen. et sp. n., †Chaetodon (Blumchaetodon) wattsi subgen. et sp. n., †Oligopseudamia iancurtisi gen. et sp. n., and †Oniketia akihitoi gen. et sp. n.
... This may be due to an increase in wear at the tip during the lifetime of the tooth as a result of its durophagous diet. Ferric iron has been reported in butterflyfish teeth (Chaetodontidae, Perciformes) and found in higher concentrations forspecies who specialize in feeding on hard-bodied prey [69] . ...
The relationship between diet, bite performance, and tooth structure is a topic of common interest for ecologists, biologists, materials scientists, and engineers. The highly specialized group of biters found in Serrasalmidae offers a unique opportunity to explore their functional diversity. Surprisingly, the piranha, whose teeth have a predominantly cutting function and whose main diet is soft flesh, is capable of exerting a greater bite force than a similarly sized pacu, who feeds on a hard durophagous diet. Herein, we expand our understanding of diet specialization in the Serrasalmidae family by investigating the influence of elemental composition and hierarchical structure on the local mechanical properties, stress distribution, and deformation mechanics of teeth from piranha (Pygocentrus nattereri) and pacu (Colossoma macropomum). Microscopic and spectroscopic analyses combined with nanoindentation and finite element simulations are used to probe the hierarchical features to uncover the structure-property relationships in piranha and pacu teeth. We show that the pacu teeth support a durophagous diet through its broad cusped-shaped teeth, thicker-irregular enameloid, interlocking interface of the dentin-enameloid junction, and increased hardness of the cuticle layer due to the larger concentrations of iron present. Comparatively, the piranha teeth are well suited for piercing due to their conical-shape which we report as having the greatest stiffness at the tip and evenly distributed enameloid.
Statement of Significance
The hierarchical structure and local mechanical properties of the piranha and pacu teeth are characterized and related to their feeding habits. Finite element models of the anterior teeth are generated to map local stress distribution under compressive loading. Bioinspired designs from the DEJ interface are developed and 3D printed. The pacu teeth are hierarchical structured and have local mechanical properties more suitable to a durophagous diet than the piranha. The findings here can provide insight into the design and fabrication of layered materials with suture interfaces for applications that require compressive loading conditions.
... Tooth pigmentation is quite common in nature. Several vertebrate taxa have been used as model to study this diversity, including shrews, salamanders and fish (Motta, 1987;Sparks et al., 1990;Clemen, 1988;Suga et al., 1992;Anderson and Miller, 2011). In rodent dentition, this natural variability is especially visible on incisors. ...
The evolution of the vertebrate dentition is among the most exciting topics in the evo-devo field, with particular attention being drawn to the mouse model. The mouse dentition includes four ever-growing incisors and twelve molars with a specific cusp pattern. Incisors and molars develop according to a tightly regulated molecular network.The ERK-MAPK cascade is involved at various stages of tooth development. Molar tooth phenotype comparisons in mutant mice for genes acting at various levels of the cascade highlighted a dental phenotype signature, which consists in the presence of a supernumerary tooth and shared cusp pattern defects. Some of these recall characters present in fossil rodents, supporting the ERK-MAPK as a good candidate to explain some evolutionary trends of the rodent dentition. By working on a mouse line over-expressing one of this pathway inhibitor in the oral epithelium, I perfect our understanding of Fgf gene role in specifying signaling center formation at the right stage, and in achieving correct mineralization.When considering evergrowing incisors, mouse dentition is also dynamic at the lifetime scale. I monitored the ageing process of the mouse upper incisors, and provided a chronology of occurrence of the variety of age-related defects display. These defects are set up from the six months on, the most frequent abnormality being the presence of an enamel groove along the surface of the incisor. Using Next Generation Sequencing technologies, I detected transcriptomic changes in the stem cell niches affecting cell proliferation and metabolism, as well as the stem cell niche functioning. The correlation found between the groove occurrence and a large immune response in dental tissues expands our concern for dental stem cell ageing.
Synopsis
Whether distantly related organisms evolve similar strategies to meet the demands of a shared ecological niche depends on their evolutionary history and the nature of form–function relationships. In fishes, the visual identification and consumption of microscopic zooplankters, selective zooplanktivory, is a distinct type of foraging often associated with a suite of morphological specializations. Previous work has identified inconsistencies in the trajectory and magnitude of morphological change following transitions to selective zooplanktivory, alluding to the diversity and importance of ancestral effects. Here we investigate whether transitions to selective zooplanktivory have influenced the morphological evolution of marine butterflyfishes (family Chaetodontidae), a group of small-prey specialists well known for several types of high-precision benthivory. Using Bayesian ancestral state estimation, we inferred the recent evolution of zooplanktivory among benthivorous ancestors that hunted small invertebrates and browsed by picking or scraping coral polyps. Traits related to the capture of prey appear to be functionally versatile, with little morphological distinction between species with benthivorous and planktivorous foraging modes. In contrast, multiple traits related to prey detection or swimming performance are evolving toward novel, zooplanktivore-specific optima. Despite a relatively short evolutionary history, general morphological indistinctiveness, and evidence of constraint on the evolution of body size, convergent evolution has closed a near significant amount of the morphological distance between zooplanktivorous species. Overall, our findings describe the extent to which the functional demands associated with selective zooplanktivory have led to generalizable morphological features among butterflyfishes and highlight the importance of ancestral effects in shaping patterns of morphological convergence.
Structural elements called “scales” in fish have a structure and chemical content closer to teeth than to any other scale type. Scales exist in many shapes and sizes, and serve as protection (mechanical and anti-bacterial), camouflage, and plumage for marine fishes. In addition to protective properties, scales provide these animals with locomotive and, in the case of lateral lines, sensory abilities. A fish’s locomotion is aided by the shape of scales, which help create a laminar flow of water around the animal. These properties are partially determined by the hierarchically composite-based structure of scales. Discussed in this chapter are numerous mineral-based composites and unique biological materials such as enamel, enameloid, dentines, cosmine, ganoine, hyaline and their derivatives. Also discussed is the diversity and structure of extinct and extant fish scales, scutes and denticles.
Previous studies by the authors have revealed that fluoride and iron concentrations in the enameloid of the teeth of some teleostean fishes are very high compared with those in human enamel, and that their concentrations are related to the phylogeny of the fishes rather than to the environmental water, tooth morphology, and feeding habits. In order to trace the origin of the concentration.mechanism of these elements into the enameloid in the evolutionary history of the bony fishes, electron microprobe investigations of tooth fluoride and iron were made in this study in non-teleostean bony fishes which are ancestral to or distantly diverged from the teleostean lineage, i.e., the dipnoan lungfishes, the crossopterygian coelacanth, the primitive antinopterygian polypterids (bichers and reedfishes), gars, and bowfin.
A high fluoride concentration in the entire layer of the enameloid, as seen in many teleostean fishes, was found only in the bowfin, in which the concentration was about 3.5% in the surface layer and about 2.2% in the inner layer. Fluoride concentration was from 0.17% to 0.70% in the enamel of lungfishes and coelachanth and in the enameloid of polypterids and gars. On the other hand, a high iron deposition,at the outer layer of enameloid (0.5%–1.3%) was detected in polypterids, gars, and bowfin, while the enamel in lungfishes and coelacanth did not contain any detectable amounts of iron under the analytical conditions of this study.
Based on these results, the mechanisms of high fluoride and iron concentrations seem to have been acquired only in actinopterygians, and the origin of the high fluoride concentration could be traced back to the pre-teleostean stage of actinopterygian evolution while the high iron concentration mechanism seemed to originate as far back as the cladistian (polypterid) stage.
It is well known that the fluoride has an ability to promote precipitation and growth of apatite crystal and to make its crystallinity higher due to its incorporation into crystal lattice. On the other hand, excess uptake of fluoride during tooth development interferes with the functions of the hard tissue forming cells, especially, the enamel forming cells, and, finally, induces hypomineralization of enamel (mottled enamel). Fluoride in the teeth, especially, in human enamel, under normal and various pathological conditions, has been examined by many investigators mainly in connection with dental caries [1, 2]. On the other hand, deposition of histologically detectable amount of iron in the enamel of amphibians, reptiles and some mammals and in the enameloid of some fishes has been known for many years. It has been considered that the iron minerals act as hardening agents on the surface of enamel and enameloid [3–5].
Certain populations of the fluviatile Mexican fish genus Ilyodon (family Goodeidae), in a few tributaries of two adjacent river systems, are sharply dichotomous with respect to suites of trophic specializations. These trophic types have been considered specifically distinct; they are easily differentiated, by eye, as adults and breed true in the laboratory. Nondichotomous populations are found in other tributaries of the same rivers. In a sample from the Rio Terrero, a tributary of the R. Tuxpan (R. Coahuayana), five of 30 allozyme loci surveyed were identically polymorphic in both trophic types. All genotype (zygotic) frequencies were in agreement with those predicted by Hardy-Weinberg equilibria, and agreement was maintained when the data from the two types were pooled. Conspecificity of the trophic types appears to be the most straightforward interpretation of the data: the sharp trophic differences are probably a discontinuous polymorphism segregating within a local population of a single biological species. The relationships of the trophic types in a sample from the Rio de Comala seem more complex. Of five loci polymorphic in both types, significant differences between the types were detected in the allelic frequencies of one locus and in the genotypic frequencies of a second. In one of the types, highly significant heterozygote deficiencies were detected at two loci. A Wahlund effect (subdivision with respect to genotype frequencies at both loci) is suggested as the best explanation for simultaneous deficiencies at two loci. Thus, there is a possibility that one of the types consists of two or more genetically distinct populations. Dichotomous Ilyodon populations may have evolved from continuous ones in special habitats by disruptive selection favoring extreme trophic phenotypes, followed by the establishment of clear-cut polymorphisms probably encoded by supergenes. The final step in the process may be the acquisition by the trophic types of reproductive isolation in sympatry
Certain populations of the goodeid fish Ilyodon occur as bimodal (dichotomous) assemblages of broad and narrow mouthed individuals. These have previously been given species status (I. xantusi and I. furcidens, respectively). Progeny of females inseminated in the field and from laboratory crosses show that each morph (broad and narrow) occasionally produces offspring of the opposite type. These morphs are therefore considered components of a morphological (presumably trophic) polymorphism in mouth width within a single biological species. The genetic basis of the polymorphism is not clear; both disruptive selection and ecophenotypic factors may be responsible for the development of young fish into dichotomous adult populations. A greater proportion of intermediate individuals was observed in broods reared in laboratory conditions than was detected in the field sample. Unknown environmental factors may determine the unimodal or bimodal morphology distributions seen in populations of Ilyodon throughout their range.
Preliminary data are presented on the physical properties and the mineralogy of the material in denticle caps of chitons. The X-ray diffraction patterns of the denticle material indicate the presence of magnetite, or possibly maghemite. This is the first indication that magnetite or possibly maghemite is precipitated by a biologic agent in sea water. Hence, the origin of magnetite reported in recent and fossil marine deposits will have to be re-examined. The hardness of the denticle material (Ca. 6 on the Mohs scale) explains why chitons are effective erosional agents of rock surfaces, particularly of limestone. From the biologic point of view the possibility is considered that the magnetic properties of the denticle caps may serve as a guidance system for the so-called homing instinct of chitons.
The structure, morphology, composition, and organization of inorganic solids in the radula teeth of the limpet Patella vulgata have been studied by electron microscopy, electron diffraction, and e.d.X.a. of fractured, acid-treated, and sectioned tissue. Minerals first appear in the tooth base and comprise: amorphous and poorly crystalline granular, particulate, and sheet-like phases of variable composition (Fe, Si, P, Ca); irregular laths of crystalline goethite; and single crystals of prismatic goethite. The presence of localized Si and P may inhibit goethite crystallization in many regions of the tooth base. Mineralization of the tooth cusp begins with goethite impregnation of the posterior region. Crystals are deposited in the form of thin fibrous strands (15-20 nm width) with the [001] crystallographic axis initially parallel to the posterior tooth wall. Mineralization proceeds by an increase in the number and thickness of the crystals within the posterior region. In contrast, the anterior zone is only partly impregnated with crystals aligned parallel to the long axis of the cusp. The mature crystals are well ordered, acicular in morphology but with extensive growth distortions, and organized along regularly interspaced (30-50 nm) electron-dense filaments within the cusp. Removal of iron reveals the presence of silica-impregnated fibres, folded sheets, and tubular structures (often 30-60 nm in diameter) within essentially intact teeth. We propose that goethite crystallization and organization is regulated, in part, by spatial constraints established by an ordered filamentous organic matrix and that silica impregnates the matrix components at a later stage in mineralization thus maintaining the structural integrity of the organic tissue.