Review - Indian Academy of Sciences

0 downloads 0 Views 432KB Size Report
Nov 6, 2013 - such as the dinosaurs have to deal with large gravitational forces, but in ... isotope chemistry has led to an elaborate protocol for using O18/O16 stable isotopes for palaeotemperature .... suggests a periodicity probably connected to the lunar ..... (2005) Dinosaur coprolites shed light on the early evolution of.

Review Biomineralization: Some complex crystallite-oriented skeletal structures ASHOK SAHNI 98 Mahatma Gandhi Marg, Lucknow 226 001, India (Email, [email protected]) The present review focuses on some specific aspects of biomineralization with regard to the evolution of the first focused visioning systems in trilobites, the formation of molluscan shell architecture, dental enamel and its biomechanical properties and the structure of the calcified amniote egg, both fossil and recent. As an interdisciplinary field, biomineralization deals with the formation, structure and mechanical strength of mineralized skeletonized tissue secreted by organisms. Mineral matter formed in this way occurs in all three domains of life and consists of several mineral varieties, of which carbonates, phosphates and opaline silica are the most common. Animals and plants need mechanical support to counteract gravitational forces on land and hydrostatic pressure in the deep ocean, which is provided by a skeletonized framework. Skeleton architecture mainly consists of basic elements represented by small usually micrometer- to nanometer-sized crystallites of calcite and aragonite for carbonate systems and apatite crystallites for phosphatic ones, and then these building blocks develop into structured more complex frameworks. As selective pressures work towards optimizing stress and response, the orientation, morphology and structural arrangement of the crystallites indicates the distribution of the stress field of the biomineralized tissue. Large animals such as the dinosaurs have to deal with large gravitational forces, but in much smaller skeletonized organism such as the coccoliths, a few micrometer in diameter made up of even smaller individual crystallites, van der Waals forces play an increasingly important role and are at present poorly understood. Skeleton formation is dependent upon many factors including ambient water chemistry, temperature and environment. Ocean chemistry has played a vital role in the origins of skeletonization, 500 to 600 million years (ma) ago with the dominance of calcium carbonate as the principal skeleton-forming tissue and with phosphates and silica as important but secondary materials. The preservation of calcareous skeletons in deep time has resulted in providing interesting information: for example, the number of days in the Devonian year has been established on the basis of well-preserved lunar (annual) cycles, and isotope chemistry has led to an elaborate protocol for using O18/O16 stable isotopes for palaeotemperature measurements in the geological past. Stable isotopes of dental apatite have helped to establish ecological shifts (terrestrial to wholly marine) during the evolution of the Cetacea. Biomineralization as a field of specialization is still searching for its own independent identity, but gradually, its importance is being realized as a model for engineering applications especially at the nanometer scale. [Sahni A 2013 Biomineralization: Some complex crystallite-oriented skeletal structures. J. Biosci. 38 925–935] DOI 10.1007/s12038-013-9390-z

1.

Introduction

Biomineralization is an interdisciplinary field that deals with the formation, structure and function of mineral matter secreted by organisms. The biomineral phase represents the fundamental building block of all calcified tissue, both fossil and recent, and all three domains of life possess biominerals in some form or the other, but it is only the eukaryotes that Keywords.

form mineralized skeletons. This field is therefore a great unifying and integrating force in studying organically mineralized tissue (Lowenstam and Weiner 1989) and has witnessed a strong resurgence of interest with the advent of scanning electron microscopy (Boyde 1964; Koenigswald and Sander 1997; Sahni 1988). In general terms, mineralized tissue usually retains its integrity and identity through deep time in the context of chemistry and physical structure so that

Oriented crystallite; biomineral; skeletal structures

http://www.ias.ac.in/jbiosci

Published online: 6 November 2013

J. Biosci. 38(5), December 2013, 925–935, * Indian Academy of Sciences

925

926

Ashok Sahni

anatomical details can be easily observed. Occasionally, fossil mineral tissue is altered by ‘diagenesis’, which is a process that occurs post burial and usually involves chemical alteration both at ambient and high temperatures. However, whenever this happens, enough evidence is left in the form of crystal overgrowth, dissolution and distortion for this process to be identified as such. In contrast to mineralized tissue, soft cellular material on fossilization may undergo severe modification and alteration. Silicified fossil wood is a case in point. Starting with the ‘Big Bang’ of complex multicellular life some 600 million years ago, skeletons originated to serve several functions: to provide mechanical support for organisms in various environments, to protect organisms against increased predation, to act as attachment surfaces for muscles and lastly to serve as a chemical reservoir for essential elements and for removal of metabolic wastes (Kazmieraczak et al. 1985). The present review focuses on four specific and diversified aspects of skeletal structure to illustrate how crystallite orientations are fundamental in the building of biomineralized complexes ranging from vision in trilobites, molluscan and amniote shell architecture, and the formation of dental enamel. One of the aims of this overview is to bring into sharper focus the present status of the discipline which foresees a brighter future for all those who wish to study the origins, structure and functionality of mineral matter secreted by organisms. Biomineralization is usually associated with the skeletal frame of an organism whether internal (endoskeletons) or external (exoskeletons) but also gives rise to special structures such as teeth, eggs and ear bones (such as the otoliths of fish). Although several biominerals have been identified, in this review, only the major skeleton forming minerals such as calcite and aragonite (calcium carbonate) found in invertebrates, or hydroxyapatite (calcium phosphate) occurring in vertebrates and opaline silica common in mainly marine organisms such as sponges, radiolarians and diatoms, will be considered. Most protistan clades possessing skeletons are silica-based. Microscopic opaline silica nodules called phytoliths are also found in many terrestrial plants such as grasses and serve as mechanical support. For invertebrates with calcareous skeletons, the mineral calcite is dominant, but in some cases, aragonite is also present as, for example, in corals, many mollusks and in turtle eggshells (Bajpai et al. 1997). In order to understand functionality of the skeleton or of a biomineralized tissue such as dental enamel, mollusk shells or calcified eggshells, it is essential to look at the structure as a whole but at different scales of observation, starting with the primary building block, the oriented crystallite, and then examine the more complex and structured framework in the light of growth and the biological functions that need to be performed. This process is a complicated task and selection pressures have found innovative ways to accomplish this for diverse forms of life through deep time, ranging from the gravityJ. Biosci. 38(5), December 2013

defying giant dinosaurs weighing some 70 to 80 tons to micrometer-sized coccoliths (Young et al. 1999) and other even smaller microbiota influenced by yet poorly characterized van der Waals forces. Several biomineralized systems show a high degree of selforganization starting with basic components such as crystallites and then enlarging to increasing complexity encompassing the entire skeleton. At present it is unclear (and beyond the scope of this work) to resolve issues concerned with the mechanism leading to a self-ordered system of skeletal architecture and whether natural selection controls self organization or not (Kaufmann 1993). At present it appears that a Darwinian gradualistic adaptive evolutionary approach would be enough to explain the observed structures. In cases where the temporal constraints are good and species diversification is fairly rapid, as, for example, in whale evolution (Roe et al. 1998), it is easier to ascribe this process to adaptive evolution rather than to systems of self organization. 2.

Skeletonization: Origins and special features

Multicellular life began with a ‘Big Bang’ over 600 million years ago after nearly 2.8 billion years of the earth was inhabited by unicellular organisms, and soon after, several organisms belonging to diverse phyla developed skeletons. Murdock and Donoghue (2011) and Dove (2013) give a comprehensive review on the advent of skeletonization. Initially around 600 million years or so only some eukaryote phyla developed skeletons, but 50 million years later calcareous skeletonization became much more common, and by the Ordovician, it was quite prevalent (Pruss et al. 2010). An interesting event is recorded by Bengtson and Zhao (1992) that no sooner had some organisms developed skeletons, opportunistic borers developed the capability of penetrating them. The process of skeletonization has to be seen in the light of early ocean chemistry and what were the most easily available skeleton building materials: then, as now, carbonates were abundant whereas phosphates were more limited. Donoghue and Sansom (2002) have discussed the origin and early evolution of vertebrate skeletonization. Apatite is a hard biomaterial forming the phosphatized skeletons of some early invertebrates such as brachiopods and was retained by the vertebrates but the cost (in terms metabolic trade-off) for apatite skeletons was rather high. A possible reason may lie in the fact that the solubility, availability and precipitation differs for phosphate and carbonate skeletal systems. Carbonates are by far the most common skeleton builders. Silica, the hardest of the biomineralized materials, is a distant third as a skeleton builder and forms the framework for siliceous sponges and a variety of microorganisms such as radiolaria and diatoms. Biomineralized skeletons of fossil organisms have been used to obtain interesting data in deep time, ranging from the

Complex crystallite-oriented skeletal structures number of days in a Devonian year, to palaeotemperature measurements including the recognition of ancient environments and the ecological shifts that took place during phyletic evolution: The fact that some animals with calcareous skeletons such as corals retain a faithful record of their growth has been used in exceptionally wellpreserved specimens to calculate the number of days in a Devonian year (Wells 1963; Scrutton 1964). On the basis of diurnal, monthly and annual cycles recorded in the calcareous exoskeleton of a fossil coral, Scrutton (1964) suggests a periodicity probably connected to the lunar breeding cycles corresponding to 13 lunar months of 30.5 days each for the Middle Devonian, which has more days in the year than at present. Urey (1947) was one of the first to give a theoretical model for establishing a palaeotemperature scale. Later, he and his co-workers using oxygen isotopes from molluscan shells were able to calculate temperatures at which the shell formed in the ocean (Epstein et al. 1953; Goodwin et al. 2003). Present day studies have built on these foundations and made palaeotemperature measurements a sophisticated science (Goodwin et al. 2003). In a pioneering study DeNiro and Epstein (1978) established how carbon isotopes could be used for inferring the diets of mammals. Using fossil dental enamel (= bioapatite) Thewissen et al. (1996) and Roe et al. (1998) demonstrated how cetacean (whale) evolution took place from a four legged terrestrial ancestor to typically marine forms. They based their studies on stable isotopes of carbon and oxygen of tooth enamel using three comparative groups: modern whales living in the open ocean, recent freshwater delphinids and an evolving group of primitive whales in India and Pakistan that showed a transition from freshwater to marine conditions. Dentitions of early whales including enamel structure also confirms this (Sahni 1981; Sahni and Koenigswald 1997). Bera et al. (2010) have shown ecological and environmental shifts using fossil dental enamel material. 3.

Trilobites and the first vision apparatus

Of the many remarkable ways in which selective pressures have shaped the diversity of organs and organisms themselves, the evolution of vision must rank as one of the most outstanding. The evolution of focused vision in multicellular organisms had a remarkable origin over 542 million years ago and is exemplified by a group of extinct arthropods called trilobites. In fact an exceptionally wellpreserved enigmatic fossil Anomalocaris from the Burgess Shale suggests that focused vision may have arisen even earlier (Paterson et al. 2011) than that of the trilobites themselves. The trilobites ruled the earth for more than 300 million years and occupied most of the available niches in

927

the ocean from tidal sand to open sea. As one of the most complex swimming animals of their time, eye sight (and locomotion) was an important component in their evolutionary process both for those trilobites who were vicious predators and others who were their poor prey! However, many bottom dwelling, sand-burrowing and mud-grubbing trilobites lost their vision and were blind. Using the birefringent mineral calcite, trilobites were able to evolve sophisticated visioning systems finely focused in aqueous medium some 500 million years ago. A birefringent mineral is one in which light splits into two pathways, giving rise to two distinct and usually overlapping images, and there is only one crystallographic axis in which a single image forms, that is along the C-Axis. The basic lens unit of this early visioning system is therefore a transparent calcite crystallite (variety Iceland Spar) oriented specifically along the C-axis of the crystallite. Lenses in some trilobites were grouped into compound arrays with prominent crescentshaped to bulbous eyes (figure 1D). Clarkson (Clarkson 1979; Clarkson et al. 2006) pioneered studies on diverse trilobite vision systems and described three distinct types based on lens shape, spacing and the degree of coverage by the corneal membrane. The earliest and most generalized is known as abathochroal, found in the earliest known eodiscid trilobites from China (Xi-Guang and Clarkson 1990) and consists of a corneal membrane limited to the edge of the lens with thin sclera comprising of exoskeleton cuticle. This type is similar to schizochroal eyes which have fewer and larger lenses each separated by a corneal membrane and thick sclera. In contrast, holochroal eyes are the commonest vision systems in trilobites and consist of several hundred lenses (about 30–100 μm in diameter) and are covered by a single corneal membrane. The usual problem of spherical aberration and maintaining focused vision in the ocean is a difficult task because of turbidity, salinity and light intensity differences in general, but trilobites managed to overcome these difficulties and evolved the ‘intralensar bowl’ (Lee et al. 2007; Torney et al. 2008) having a different refractive index than the couplet lens and therefore ‘upstaged’ the work of Des Cartes and Hugyens, who devised the same type of lenses in the era of human intelligence, a few hundred years ago and several million years after the extinction of the last trilobite (Clarkson and Levisetti 1975)! There has been much discussion on the properties of the intralensar bowl and it appears that at least for some trilobite species the lenses had an interface with an undulating intralensar surface which corrected for spherical aberration (Horvath 1996). Torney et al. (2008) using the electron backscatter technique have demonstrated that some species had calcite lenses with a chemically different intralensar bowl to correct aberration; other species appear to have a more complex structure whereby light was fed to the mineral calcite through an outer J. Biosci. 38(5), December 2013

928

Ashok Sahni

ƒFigure 1.

Generalized schematic diagram showing general features and the structure of the trilobite eye. (A) Oriented transparent crystallite of calcite (var. Iceland Spar) aligned along C-axis. Light entering the crystallite (a few micrometers in length) in any other direction than the C-axis will split into two components causing ‘double imaging’. (B) Calcite lens with intralensar bowl, refractive index (R.I.) of the intralensar bowl is 1.63 slightly less than that of the rest of the lens (R.I.= 1.66). (C) Compound lenses arranged in symmetrical array, some mm across. (D) The bulbous schizochroal eyes of Phacops ( width of cephalon about a cm across) as seen from the anterior. This personal specimen is ‘rolled’, i.e. head and tail are juxtaposed in an effort to protect the soft ventral area.

unit having radially arranged C-axes, a novel crystallographic solution to a problem in functional morphology. It should be borne in mind that directional sight requires either a spherical apparatus for the lens or an array of lenses such as those found in a compound eye. The trilobites evolved diversely shaped eyes which consist of large arrays ranging from globular, crescent to high convex dishes (Clarkson et al. 2006). Some eyes were located on stalks so that the animal could lie concealed in the water with only the eyes scanning the water horizon above. Through time, diverse animals groups evolved their own visioning systems with materials other than calcite. Recently, however, calcite microlenses serving as photoreceptors have been discovered in the brittle stars (Aizenberg et al. 2001). It is therefore interesting to observe how the birefringent calcite biomineral was used for over 300 million years to form arthropod eye lenses and is still used as a form of photoreceptor by marine echinoderms. 4.

Molluscan shell structures: Some insights

Molluscan shells have played an important role in the development of the field of biomineralization simply because of their ready availability, ease of study and the fact that mollusks are found in a variety of environments and have extremely varied shell structures adapted to ecologically specific environments (Carter 1980). Additionally, the discipline has an obvious application in the pearl industry where oysters belonging to the family Pteriidae and other Bivalvia have been cultured to produce commercially viable products (Dakin 1913; Simkiss and Wada 1980). In this regard studies on the formation of nacre had an early start (Wada 1972) and it has recently been shown (Fryda et al. 2009) that the controlling mechanisms for nacre formation have been stable in deep time since the Triassic. Taylor and Layman (1972) in a comprehensive review have discussed the mechanical properties of bivalve shells, giving a detailed account of their varied shell structure and the adaptation to specific habitats and environments. The last four decades have seen a quantum increase in the number of articles dealing with form, function J. Biosci. 38(5), December 2013

Complex crystallite-oriented skeletal structures and structural aspects of invertebrate shell structure using advanced imaging and theoretical modeling techniques and instrumentation (Aizenberg et al. 2001; Checa 2002; Ubukata 2005). In this brief overview, issues dealing with modern approaches to understand structural complexities of shell architecture and the general control of molluscan neural systems on form, shape and ornamentation patterns of shells will be touched upon. Chen et al. (2004) have shown the application of bivalve structures to the ceramic industry and how biomimetics can help to solve engineering problems. Chateignera et al. (2000) used X-ray diffraction to characterize the crystallite architecture of many molluscan groups including the monoplacophorans, bivalves, gastropods and cephalopods, and came to the conclusion that the textural patterns in the forms studied can be quantitatively determined based on a few parameters with area specific parts of the shell having different strength capabilities and with diverse crystallographic orientations. Boettigera et al. (2009), in an important study, integrated data from the neural system of the mollusks that secretes the shell, namely, the tongue-like mantel, and showed how the nerve fibres control the shell making processes for each of the different segments. Checa (2000) discussed the crystallographic orientations of the calcite crystallites in some unionids and showed how the texture and the structure of the shell can be characterized using X-ray diffractometer in terms of crystal orientation of the Bragg diffraction planes 001 and 112 across long shell distances. Calcite is one of the most common building blocks of the skeleton and produces a variety of robust and stress resistant structures both in thin and thick-shelled molluscs.

5.

Dental enamel

Tooth enamel has been a focus of attention since the 19th century as relevance to evolution and dental anatomy necessitated a comprehensive approach to the formation, structure and architecture of individual teeth and complete dentitions in the context of human and other mammalian enamel diversity (Boyde 1964; Koenigswald and Sander 1997). In dental systems as well, selective pressures work at all levels of complexity as they do in Mollusks, discussed earlier. Analogous to the calcite crystallites used by mollusks and other marine organisms to build their shell structure, the mineral bioapatite is the fundamental building block of all vertebrate skeletal structures (Selvig 1970) with a few notable exceptions, namely, fish ear bones (= otoliths) and, of course, amniote eggshells. The bio-apatite crystallite is now a focus of attention and it has been characterized using Raman spectroscopy (Thomas et al. 2011) and represents the fundamental building block of teeth and bones giving basic

929

information on structure and biomechanics. Dumont et al. (2011) have examined whether the sizes of the apatite crystallites is the same in large and small animals such as the giant sauropod dinosaurs and the small mammal. Similarly, Mishra and Knothe-Tate (2008) conducted studies on several fossil forms to find out the relationships between osteons (bone cells) and Haversian Canal diameters with reference to body weights. They have demonstrated that with increasing weight or size of the animal, the osteon and Haversian Canal size diameter decreases per unit body weight. These are fundamental issues in skeleton architecture which are only now being examined. One of the hardest biomaterials known, the study of dental enamel has been influenced greatly by individual contributions (Korvenkontio 1934; Shobusawa 1952; Boyde 1964) as well as some dedicated work at the institutional level, for example, the Steinmann Institute of the University at Bonn, where for over four decades, research on biomineralization and mammalian dental enamel diversity has been undertaken (Koenigswald 1997a, b). As a result, there is a high level of understanding of the biomechanics, the functional gross and fine architectural framework of the teeth of various mammalian group (Rensberger and Koenigswald 1980; Koenigswald et al. 1987; Koenigswald 2004; Koenigswald 2012; and Koenigswald and Sander 1997 and articles therein) at various observational scales of study and at different levels of complexity (Koenigswald and Clemens 1992). The structure and function of teeth and the dentition, in fact the whole skull, is specifically optimized for diet. It is interesting to note that the diet dictates the way the enamel is strengthened at all levels of complexity even in phyletically unrelated groups. For example, the response of selective pressures for mammals eating grass is normally by the possession of evergrowing incisors and hypsodonty (increase in tooth height) and a complex characteristic internal crystallite structure (Sahni 1986; Koenigswald 2004). This fact is illustrated by the similarity of architectural plans for building efficient dentitions for eating grasses which have a high silica content in the case of rodents (Koenigswald 2004) and an unrelated extinct group of primitive mammals (gondwanatheres) in the Indian latest Cretaceous (Prasad et al. 2005; Krause et al. 1997; Patnaik et al. 2001). Of the vast literature encompassing the field the current section, in this brief review, I will focus on two aspects in which I have been interested (Sahni 1979, 1988) : the evolution of mammalian dental enamel (Sahni 1987) and the characteristics of rodent dental enamel (Sahni 1986) which by structural design is one of the most complex and sophisticated systems known. This evolutionary complexity has come about because, unlike reptiles that continuously grow and shed their teeth, the origin of enamel structure in mammals is a result of the fact that we have only one set of deciduous teeth. In the permanent dentition, teeth come in J. Biosci. 38(5), December 2013

930

Ashok Sahni

contact through life (occlude) and therefore must last until the life of the animal. There is need therefore for reinforcement and support of these structures (Sander 1997; Sahni 1987) against fracture and continued occlusion stress during mastication. The teeth in mammals in both the upper and lower dentitions have evolved special structures known as ‘prisms’ in order to counteract the stresses. Prisms are basically ‘ bundles’ of similarly oriented bio-apatite crystallites (some nanometer in size) of varying shapes ranging from circular, elongate to keyhole shaped. The prisms are surrounded by the interprismatic layer oriented usually at an angle to the plane of the prismatic layer, a condition that is technically known as decussation, leading to what appears to be a closely knit interwoven architecture (figure 2B, C and D). Rodent enamels are one of the hardest biomaterials known and their mechanical properties have been studied

in some detail. Rodents are known from the early Tertiary onwards (Sahni 1980; Kotlia and Sahni 1993; Koenigswald 2004) and have the same basic body form since their early evolution and this includes the shape of the skull and the fact that since the teeth are ever-growing, the skull and lower jaw are suitably modified with the incisors having a grooved space to accommodate them (figure 2A). The pointed apex of the incisor is maintained as it forms the interface between the harder enamel which is made up of structured apatite crystallites and the dentine which is more porous and more prone to wear. In any abrasive action the enamel will erode less than the dentine and therefore the point will remain ever-sharp. Rodent enamel has been studied by several workers mainly because it is easy to do so as the incisors grow throughout life. It also provides insights into the mechanism by which apatite crystallites are secreted from cells known as ameloblasts. These prisms

Figure 2. (A) Skull structure of the common rat illustrating the structure of the dentitions and the pointed upper and lower incisors. Cranial components, jaw structure, attachment areas for jaw musculature, the diastema between the incisors and the molars make an effective grass-eating machine. (B) Schematic section of the apex of a rodent incisor in black penciled outline showing the orientations of the apatite crystallites at the tip and internally in the basal enamel. Enamel thickness is variable, typically between 100–200 μm. The dentine which is non-crystalline provides a softer cutting edge in contrast to the enamel which leads to an ever-sharpened apex. (C) Intertwined (=decussating) prisms form a hardened structure. (D) Prisms and interprisms in a primitive multituberculate mammal showing bundles of crystallites occurring as rounded prisms with intervening rows of crystallites at an angle to the circular prisms (Sahni 1979). (E) Typical bioapatite crystallite of enamel, bone crystallites are relatively smaller. J. Biosci. 38(5), December 2013

Complex crystallite-oriented skeletal structures and interprismatic layers form opposing rows either one row, a few rows or several rows thick giving the enamel its great strength (figure 2B and C). The biomineral apatite is considerably more load-resistant than biocalcite. It forms not only the delicate structures associated with mammalian enamel but also is able to support considerable weight in limbs of large animals such as elephants and dinosaurs.

6.

Eggshell structure

The calcareous shell-covered amniote egg is perhaps the acme of the evolutionary process, a self-contained living entity that allows reproduction of life. Recent studies have focused on the crystallographic structure of the avian and dinosaurian eggshell (Sakae et al. 1995; Dalbeck and Cusack 2006). My interest in eggshells in general was sparked by finds of dinosaur eggshells during field work in Montana for my doctoral dissertation (Sahni 1972). This experience was useful when, a decade later, we are able to find complete

931

nests of sauropods in India (Jain and Sahni 1985; Srivastava et al. 1986; Sahni et al. 1994). Additional studies showed that the nesting sites were spread over an area of exceeding 10000 km2 extending from Kutch in the far west, through the central peninsular regions, to Andhra Pradesh and Tamil Nadu (Kohring et al. 1996). It is beyond the scope of this brief overview to discuss the various types of structures in calcified eggshells, which are characteristic for crocodiles, lizards, turtles, dinosaurs and birds, all of which have a fossil records in India (Sahni et al. 1994). In fact, the finds of thin shelled 65 ma eggshells from Kutch and Maharashtra belonging to ornithoid dinosaurs, possibly to primitive birds and to gekkonid lizards (Sahni et al. 1984) resulted in a resurgence of interest in eggshell structure. Within the dinosaurs themselves there are several eggshell types, in particular the ‘ornithoid’, with a structure that is indistinguishable from that of birds. It is sometimes possible using scanning electron microscopy to find out if a preserved dinosaur nest had viable embryos as the inner (mammillary surface) of the shell tends to get ‘cratered’; that is, the calcium is leached out as the bones of the embryo grow

Figure 3. Sauropod eggshell structure of the parataxon Megaloolithus. (A) Complete egg from Balasinor, Kheda district in Gujarat, about 16 cm in diameter. (B) Enlarged view of one egg in a nest to illustrate the shell structure occurring as a raised rim. (C) Microstructure of the eggshell, external surface to top of page showing spheroliths, incremental arched striations terminating in an external node. (D) shows about two spheroliths composed of biocalcite crystallites arranged with their C-axis oriented radially outwards. The spheroliths impart strength to the egg supported by the C-axis orientations of the biocalcite which has the highest compressive strength. The calcite crystallites act as one large crystal crystallographically and produce a uniaxial interference figure indicating that this plane is perpendicular to the c-axis. (E) The same view in polarized light showing a tangentially-sectioned spherolith(s) with a rounded air canal, a few micrometers in diameter abutting it at the top right. Air canal diameters are quite variable in different species. J. Biosci. 38(5), December 2013

932

Ashok Sahni

larger (Srivastava et al. 1986; Sahni et al. 1994). This inference calls for caution as other chemical reactions through time (diagenesis) may result in the same condition. As the growing embryo within the shell lives and breathes, the structure, density and location of the air canals is a characteristic feature of eggshell structure (figure 3E). Younger bird eggshells have also been studied: Fossil ostrich eggs in India and their fine structure suggested that these ratite birds had an origin in Gondwanaland and India was one of the centres of diversification some 10 million years ago (Patnaik et al. 2009). Ostriches persisted in India at least till the Late Pleistocene (Kumar et al. 1990; Sahni et al. 1990). In India, two type of eggs and nests are most common: one with spherical eggs, Megaloolithus (Sahni et al. 1994) and the other with elongated eggs, Ellipsoolithus (Loyal et al. 2000). The load stress response for the spherical eggs was worked out using finite element analysis, demonstrating that the size of the eggs, and in particular the shape of the spheroliths, and the degree of fusion with neighbouring spheroliths impart mechanical strength (Srivastava et al. 2005). The oval to ellipsoidal eggs are interesting for at least two reasons: they represent meat-eating dinosaurs and show how nest-laying behaviour incorporates biomechanical principles. It is known from nests of the Mongolian dinosaur Protoceratops and other dinosaurs having elongated eggs that these are laid vertically so that their polar axis is perpendicular to the ground surface. This gives them added support against crushing loads. The biomechanical support for eggshells comes largely from the C-axis orientation of biocalcite. Air canals and porous air-filled spaces are critical for providing oxygen for the growing embryo, and this is provided for in calcareous eggshells by channels or porous tissue within the calcareous biomineralized tissue.

7.

Concluding remarks

In this short overview, I have merely touched upon certain topics in which I have been interested. My own perspective on biomineralization as a palaeontologist stems from my interest in fossils which are usually preserved because they are biomineralized hard tissues (Kobayashi et al. 1993). I have tried to stress the fact that in order to get a overall idea of the functional importance of a specific element, it is necessary to look at all observational scales and all levels of complexity to understand the way in which selective pressures operate with crystallite orientations being the most basic and important; and furthermore, I have attempted to show that interest in this interdisciplinary area is picking up (Bouligand 2004) with more workers using modern techniques to characterize the crystallographic, biomechanical form– J. Biosci. 38(5), December 2013

function relationships with regard to engineering applications and the control of neural systems on biomineral formation and crystallite orientation under stress-field conditions. The introduction of mathematical models and cellular automata (Fowler et al. 1992; Ermentrout et al. 1986; Boettiger et al. 2009) are providing new insights into studies of shell growth, ornamentation, and mechanical support. In our pigeonholed world, many fields on the periphery of major disciplines suffer as they do not get the same recognition and support as mainstream subjects; biomineralization happens to be a case in point. However, this field has much to offer as organisms large and small (particularly the latter) provide insights that cannot be obtained from any other sources. Biomineralization is currently facing a crisis of identity: it has the potential of generating interest across disciplines, but for the time being, is generally neglected and marginalized except for the efforts by some dedicated individuals, laboratories and institutions. Acknowledgements I wish to thank Prof Rajeev Patnaik (Chandigarh) for all his help. It was the support of many other students of mine in the 1980s and early 1990s who helped to develop the field in this country. I would like to record my deep appreciation to Professors Alan Boyde and Wighart von Koenigswald and the late Professor H K Erben for enduring interactions, and to Prof Duncan Murdock for his considered suggestions. Unknown reviewers have provided insights that have added materially to this review and I thank them for their painstaking efforts.

References Aizenberg J, Tkachenko A, Weiner S, Addadi L and Hendler G 2001 Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature 412 819–822 Bajpai S, Srinivasan S and Sahni A 1997 Fossil turtle eggshells from intertrappean beds of Duddukuru, Andhra Pradesh. J. Geol. Soc. India 49 209–213 Bengtson S and Zhao Y 1992 Predatorial borings in Late Precambrian mineralized Exoskeletons Science 257 267–369 Bera MK, Bhattacharya K, Sarkar A, Samanta A, Kumar K and Sahni A 2010 Oxygen isotope analysis of bone and tooth enamel phosphate from palaeogene sediments: experimental; techniques and initial results. J. Geol. Soc. India 76 275–282 Boettiger A, Ermentrout B and Ostera G 2009 The neural origins of shell structure and pattern in aquatic mollusks. Proc. Natl. Acad. Sci. USA 106 6837–6842 Bouligand Y 2004 The renewal of ideas about biomineralisations. C.R. Palevol. 3 617–628 Boyde A 1964 The structure and development of mammalian enamel. PhD thesis, University of London

Complex crystallite-oriented skeletal structures Carter JG 1980 Guide to bivalve shell microstructures; in: Skeletal growth of aquatic organisms. Biological records of environmental change (eds) DC Rhoads and RA Lutz (New York: Plenum Press) pp 645–673 Checa A 2000 A new model for periostracum and shell formation in Unionidae (Bivalvia, Mollusca). Tissue Cell 32 405–416 Checa A 2002 Fabricational morphology of oblique ribs in bivalves. J. Morphol. 254 195–209 Chen B, Peng X, Wang JG and Wua X 2004 Laminated microstructure of Bivalva shell and research of biomimetic ceramic/polymer composite. Ceramics Int. 30 2011–2014 Chateignera D, Hedegaard C and Wenk H-R 2000 Mollusc shell microstructures and crystallographic textures. J. Struct. Geol. 22 1723–1735 Clarkson ENK 1979 The visual system of trilobites. Palaeontology 22 1–22 Clarkson ENK and Levisetti R 1975 Trilobite eyes and optics of Descartes and Huygens. Nature 254 663–667 Clarkson ENK, Levi-Setti R and Horvath G 2006 The eyes of trilobites: The oldest preserved visual system. Arthropod Struct. Dev. 35 247–259 DeNiro M and Epstein S 1978 Influence of diet on distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42 495–506 Dakin WJ 1913 Pearls (London: Cambridge University Press) Dalbeck P and Cusack M 2006 Crystallography (electron backscatter diffraction) and chemistry (electron probe microanalysis) of the avian eggshell. Crystal Growth Des. 6 2558–2562 Dumont MA, Kostka A, Sander PM, Borbely A and KaysserPyzalla A 2011 Size and size distribution of apatite crystals in sauropod fossil bones. Palaeogeogr. Palaeoclimatol. Palaeoecol. 310 108–116 Donoghue PCJ and Sansom IJ 2002 Origin and early evolution of vertebrate skeletonization. Microsc. Res. Tech. 59 352–372 Dove PM 2013 The rise of skeletal biominerals. Elements 6 37–42 Ermentrout B, Campbell JG and Ostera G 1986 A model for shell patterns based on neural activity. The Veliger 28 369–388 Epstein S, Buchbaum HA and Lowenstam HA 1953 Revised carbonate-water isotopic temperature scale Bull. Geol. Soc. Am. 64 1315–1326 Fowler DR, Meinhard H and Prusinkiewicz P 1992 Modeling seashells. Comput. Graph. 26 379–387 Fryda J, Bandel K and Frydov B 2009 Crystallographic texture of Late Triassic gastropod nacre: evidence of the long-term stability of the mechanism controlling its formation. Bull. Geosci. 84 745–754 Goodwin DH, Schoene BR and Dettman DL 2003 Resolution and fidelity of oxygen isotopes as paleotemperature proxies in bivalve mollusk shells: models and observations. PALAIOS 18 110–125 Horvath G 1996 Lower lens unit in Schizochroal trilobite eyes reduces reflectivity: on the possible optical function of the intralensar bowl. Hist. Biol. 12 83–93 Jain SL and Sahni A 1985 Dinosaurian eggshell fragments from the Lameta Formation of Pisdura, Chandrapur District, Maharashtra. Geosc. J. 6 211–220

933

Kaufmann SA 1993 The origins of order: self organization and selection in evolution (New York: Oxford University Press) pp 1–709 Kazmieraczak J, Ittekkot V and Degens ET 1985 Biocalcification through time: environmental challenge and cellular response Palaeont. Zeitshrift 59 15–33 Kobayashi I, Mutvei H and Sahni A 1993 Fossil hard tissues: structure. formation and evolution; in Symposium Volume 29th IGC, Kyoto (Tokyo: Tokai University Press) pp 1–214 Koenigswald Wv 1997a Brief survey of the enamel diversity at the schmelzmuster level in Cenozoic placental mammals; in Tooth enamel microstructure (eds) Wv Koenigswald and PM Sander (Rotterdam: Balkema) pp 137–161 Koenigswald Wv 1997b Evolutionary trends in the differentiation of mammalian enamel ultrastructure; in Tooth enamel microstructure (eds) Wv Koenigswald and PM Sander (Rotterdam: Balkema) pp 203–235 Koenigswald Wv 2004 Enamel microstructure of rodent molars, classification, and parallelisms, with a note on the systematic affiliation of the enigmatic Eocene rodent. Protoptychus J. Mammal. Evol. 11 30–36 Koenigswald Wv 2012 Unique differentiation of radial enamel in Arsinoitherium (Embrithopoda, Tethytheria). Hist. Biol. 25 1–10 Koenigswald Wv and Clemens WA 1992 Levels of Complexity in the microstructure of mammalian enamel and their application in the study of systematic. Scan. Microscopy 6 195–218 Koenigswald Wv and Sander PM 1997 Tooth enamel microstructure (Rotterdam: Balkema) pp 1–280 Koenigswald Wv, Rensberger JM and Pretzschner HM 1987 Changes in the tooth enamel of Paleocene mammals allowing increased diet diversity. Nature 328 150–152 Kohring R, Bandel K, Kortum D and Parthasarthy S 1996 Shell structure of a dinosaur egg from the Maastrichtian of Ariyalur (Southern India). Neues Jahrbuch Geologie und Palaeontologie 1 48–64 Korvenkontio VA 1934 Mikroskopische Untersuchungen an Nagerincisiven unter Hinweis auf die Schmelzstruktur der Backenzahne. Ann. Zool. Soc. Zool. Bot. Fennicae Vanamo. 2 1–274 Kotlia BS and Sahni A 1993 Enamel ultrastructure of fossil and extant. Arvicolids Proc. 29 166 Krause DW, Prasad GVR, Koenigswald Wv, Sahni A and Grine FG 1997 Cosmopolitanism amongst Gondwana Late Cretaceous mammals. Nature 390 504–507 Kumar G, Sahni A, Pancholi RK and Narvare G 1990 Archaeological discoveries and a study of Late Pleistocene ostrich eggshells and egg shell objects in India. Man Environ. 16 29–40 Lee MR, Torney C and Owen AW 2007 Magnesium-rich intralensar structures in schizochroal trilobite eyes. Palaeontology 50 1031–1037 Loyal RS, Mohabey DM, Khosla A and Sahni A 2000 Status and palaeobiology of the Late Cretaceous Indian theropods with description of a new theropod eggshell oospecies, Ellipsoolithus khedaensis, from the Lameta Formation (District Kheda, Gujarat), Western India. GAIA Geosci. J. (Portugal) 15 1–9 Lowenstam HA and Weiner S 1989 On biomineralization (New York: Oxford University Press) 324 p

J. Biosci. 38(5), December 2013

934

Ashok Sahni

Mishra S and Knothe-Tate ML 2008 Comparative study of bone micro- architecture of some mammalian bones. The Palaeobotanist 57 299–302 Murdock DJE and Donoghue PCJ 2011 Evolutionary origins of animal skeletal biomineralization. Cells Tissues Organs 194 98– 102 Patnaik R, Sahni A, Cameron D, Pillans B, Chatrath P, Simons E, Williams M and Bibi F 2009 Ostrich-like eggshells from a 10.1 million year old Miocene ape locality, Haritalyangar (Himachal Pradesh) India. Curr. Sci. 96 1485–1495 Patnaik R, Sahni A and Prasad GVR 2001 Tooth Enamel microstructure of a Late Cretaceous Gondwanatherian mammal from India. J. Palaeont. Soc. India 46 15–23 Paterson JR, Garcia-Belido DC, Lee MSY, Brock GA, Iago JB and Edgecombe GE 2011 Acute vision in the giant Cambrian predator Anomalocaris and the origin of compound eyes. Nature 480 237–240 Prasad V, Strömberg CAE, Alimohammadian H and Sahni A (2005) Dinosaur coprolites shed light on the early evolution of grasses and grazers. Science 310 :1177–1180 Pruss S, Finnegan S, Fischer WW and Knoll AH 2010 Carbonates in skeleton-poor seas: New insights from Cambrian and Ordovician strata of Laurentia. Palaios 25 73–84 Rensberger JM and Koenigswald Wv 1980 Functional and phylogenetic interpretation of enamel microstructure in rhinoceroses. Paleobiology 6 477–495 Roe LJ, Thewissen JGM, Quade J, O’Neil JR, Bajpai S, Sahni A and Hussain TS 1998 Isotopic approaches to understanding the terrestrial-to-marine transition of the earliest Cetaceans; in Emergence of whales (ed) JGM Thewissen (New York: Plenum Press) pp 399–422 Sakae T, Mishima H, Suzuki K, Kozawa Y and Sahni A 1995 Crystallographic and chemical analyses of eggshell of Dinosaur (Sauropod Titanosaurids sp.). J. Fossil Res. Jpn. 27 50–54 Sahni A 1972 The vertebrate fauna of the Judith river formation. Bull. Am. Museum Natural Hist. 147 323–412 Sahni A 1979 Enamel Ultrastructure of certain North American Cretaceous mammals. Palaeontographica A. Stuttgart 166 7–4 9. Sahni A 1980 SEM studies of Indian Eocene and Siwalik rodent enamels. Geosci. J. 1 21–30 Sahni A 1981 Enamel ultrastructure of fossil mammalia: Eocene archaeocete from Kutch. J. Palaeont. Soc. India 25 33–37 Sahni A 1986 Enamel structure of early mammals and its role in evolutionary relationships among rodents. Proc. Int. Symp. Analysis Evol. Relation. Rodents PARIS NATO-ASI Series 92 133–150 Sahni A 1987 Evolutionary Aspects of reptilian and mammalian enamel structure. Scan. Microsc. Int. 1 1903–1912 Sahni A 1988 Application of electron microscopy to problems in Palaeontology and biomineralisation; in Micropalaeontology of shelf sequences of India (ed) P Kalia (Papyrus Publishing House: New Delhi) pp 1–11 Sahni A and Koenigswald Wv 1997 The enamel structure of some fossil and recent whales from the Indian subcontinent; in Tooth enamel microstructure (eds) Wv Koenigswald and PM Sander (Rotterdam: Balkema) pp 177–191

J. Biosci. 38(5), December 2013

Sahni A, Rana RS and Prasad GVR 1984 SEM studies of thin egg shell fragments, from the intertrappeans (Cretaceous-Tertiary transition) at Nagpur and Asifabad, Peninsular India. J. Palaeont. Soc. India 29 26–33 Sahni A, Kumar G, Bajpai S and Srinivasan S 1990 A review of Late Pleistocene ostriches (Struthio sp) in India. Man Environ. 15 41–47 Sahni A, Tandon K, Jolly A, Bajpai S, Sood A and Srinivasan S 1994 Upper Cretaceous dinosaur eggs and nesting sites from the Deccan Volcano - Sedimentary province of Peninsular India; in Dinosaur eggs and babies (eds) K Carpenter, KF Hirsch and JR Horner (Cambridge University Press) pp 204– 228 Sander MP 1997 Non-mammalian synapsid enamel and the origin of mammalian enamel prisms: the bottom-up perspective; in Tooth enamel microstructure (eds) Wv Koenigswald and PM Sander (Rotterdam: Balkema) pp 41–62 Selvig KA 1970 Periodic lattice images of hydroxyapatite crystals in bone and dental hard tissue, Calcif. Tissue Res. 6 227–236 Shobusawa M 1952 Vergleichende Untersuchungen ueber die Form der Schmelzprismen der Sa¨ugetiere. Okajimas Folia anat Jap. 24 371–392 Simkiss K and Wada K 1980 Cultured pearls – Commercialised biomineralisation. Endeavour New Ser. 4 32–37 Scrutton CT 1964 Periodicity in Devonian coral growth. Palaeontology 7 552–558 Srivastava S, Mohabey DM, Sahni A and Pant SC 1986 Upper Cretaceous dinosaur egg clutches from Kheda District, Gujarat, India: their distribution, shell ultrastructure and palaeoccology. Palaeontographica A 193 219–233 Srivastava R, Sahni A, Jafar SA and Mishra S 2005 Microstructure-dictated resistance properties of some Indian dinosaur eggshells: finite element modeling. Paleobiology 31 317–325 Taylor JD and Layman M 1972 The Mechanical Properties of the Bivalve (Mollusca) shell structures. Palaeontology 15 73–87 Thewissen JGM, Roe LJ, O'Neil JR, Hussain ST, Sahni A and Bajpai S 1996 Evolution of Cetacean osmoregulation. Nature 301 379–380 Thomas DB, Cushla M, McGoverin M, Fordyce E, Frew RD and Gordon KC 2011 Raman spectroscopy of fossil bioapatite — A proxy for diagenetic alteration of the oxygen isotope composition Palaeogeogr. Palaeoclimatol. Palaeoecol. 310 62–70 Torney C, Lee MR and Owen AW 2008 Peering into the eyes of trilobites using EBSD. In 15th International Conference on the Textures of Materials, 1-5 June 2008, Carnegie Mellon University Center, Pittsburgh, Pennsylvania USA (http:// eprints.gla.ac.uk/4523/) Ubukata T 2005 Theoretical morphology of bivalve shell sculptures. Paleobiology 31 643–655 Urey HC 1947 The thermodynamics of isotopic substances. J. Chem. Soc. 0 562–581 Xi-Guang Z and Clarkson ENK 1990 The eyes of the Lower Cambrian eodiscid trilobites. Palaeontology 33 911–932

Complex crystallite-oriented skeletal structures Young JR, Davis SA, Bown PR and Mann S 1999 Coccoliths ultrastructure and biomineralization. J. Struct. Biol. 126 195–215

935

Wada K 1972 Nucleation and growth of aragonite crystals in the nacre of some bivalve mollusks. Biomin. Res. Rep. 6 141–159 Wells JW 1963 Coral growth and geochronometry. Nature 197 948–950

MS received 23 March 2013; accepted 09 October 2013

Corresponding editor: DURGADAS P KASBEKAR

J. Biosci. 38(5), December 2013