THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW OF A BIOLOGICAL ‘ARMS RACE’

SUBHENDU BARDHAN 1 and DEVAPRIYA CHATTOPADHYAY 2

1. Department of Geological Sciences, Jadavpur University, Kolkata. 2. Department of Earth Sciences, Indian Institute of Technology, Bombay.

A B S T R A C T Vermeij (1977) in a brilliant introspection notices a sudden escalation of bloody battle between marine predators and their prey in Mesozoic. This rise of extensive predation set the evolutionary trend of many benthic groups, which continue even today. Though prey communities responded to a single cause, evolution followed diverse lines. Vermeij deals mainly with the different morphological trends of gastropods. We, here, in a preliminary investigation bring together subsequent case studies and notions ingrained in literature to see the impact of the Mesozoic marine revolution on other invertebrate groups. The effect appears to be quite stunning and holistic. It made the marine life wonderful for the second time in the history. Impact of the Mesozoic marine revolution was felt at different hierarchical levels and modes of evolution appeared punctuational, involving species selection. While intense predation pressure thoroughly reorganized the prey community, it did not ensue extinction at higher levels, like the mass extinction events caused by abiotic factors. Mass extinction events appear to have derailed the evolved trends of benthic communities by taking toll of the adaptive forms, which arose in response to the Mesozoic marine revolution. But, same antipredatory trends persist in the stragglers across the mass crisis boundaries, says K-T. This large-scale adaptive trend has puzzled Gould (1990).

INTRODUCTION particular direction because they gain advantage in which natural selection is Life has two extremities – it the driving force. The great originates and eventually dies. Between palaeontologist, Simpson (1953) these two end points, life grows in case proclaimed, “all long- and most short of an individual. At higher levels, i.e., range trends consistent in direction are species, genus or clade, life evolves. adaptively oriented.” Against this view of During evolution, life’s progress may panadaptation, many recent workers have assume a direction known as advocated a non-adaptive explanation of evolutionary trend. Evolutionary trend the evolutionary trends. For example, may be defined as “persistent directional Stanley (1975) envisaged that the evolutionary changes” [see Glossary, Mc evolutionary trends operate at many Namara (ed.), 1990, p. 353]. Various taxonomic levels (i.e., hierarchical) and patterns of evolutionary trends emerge in that species selection instead of natural lineages that are the artifacts of many selection, is causally responsible for the factors. Palaeontologists, for example, large-scale macroevolutionary trend debate continuously whether these trends within any evolutionary lineage. Within- are adaptive or not. species change has nothing to do with the In the early days ever since directionality of the lineage and Darwin, evolutionary trends were seen microevoltuon is ‘decoupled’ from basically as an adaptationist programme. macroevolution. Gould (1990) suggested Organisms evolve and change in a speciation and sorting as the source of

Indian Journal of Earth Sciences, Vol-30, No. 1-4,1 p. 1-28, 2003 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY evolutionary trends. According to him THE MESOZOIC MARINE (Gould, 1988), changes of variance can EVOLUTION explain many trends. However, one biotically driven During Mesozoic especially in the attribute appears to be the trend-setter for Jurassic, there suddenly arose many many groups. It is the Mesozoic marine groups of organisms in the seas as well as revolution as envisaged by Vermeij on the lands who were capable of killing (1977). The Mesozoic seas witnessed efficiently other organisms, thus posed as sudden appearance of a plethora of formidable predators. Majority of marine predatory taxa and this sent a red alert to predatory groups were small in size, but the rival prey camp. Shallow marine powerfully built and capable of benthic habitat was red with jaws and destroying shells of prey communities. claws of fishes and crabs. Every new They adapted various feeding types – acquisition of weaponry of the offenders shell crushing, spearing, wrenching was countered by the victims by extracting of soft parts from shell etc. deploying various novel means of They mainly colonized in shallow water predatory avoidance. This protracted war environments and adopted visually resulted in a thorough organizational hunting strategies. Prey communities, shake-up within the prey communities which included mostly benthic and many evolutionary trends quickly organisms, were badly affected, and appeared, which Vermeij (1987) has underwent a thorough shake up. Every called “escalation”, but all showed morphological acquisition of the defensive strategies. However to Gould’s predators was countered by the (1990, p.22) utter surprise, this development of characters, useful to hypothesis is based on adaptation and predatory avoidance in prey progression in Darwinian sense. communities. Powerful eyes capable of Gastropods became mechanically sturdy, discerning colours and strong jaws increasingly spinose and developed many capable of shell-crushing were other features as defensive measures disillusioned by the stunning mimicry, against shell crushing. Bivalves and camouflage or infaunalization within echinoids increasingly took refuge within sediments and “the increase in shell the sediments and thereby becoming thickness and spinosity of snails matched infaunas. Ammonites and nautiloids with growing strength in the claws of evolved shell rugosity to elude the jaws crab predators” (Gould, 1990, p.22). This of death. Many other groups also sustained hide-and-seek games between responded to this great and sudden prey and predator led to the development escalation of predation pressure. Does the of enormous pile of arsenal in both Mesozoic marine revolution pertain to camps, which is uniquely coined as any single, sustained trend to every major biological ‘arms race’ by Vermeij, group? No, it is rather the response of (1977). The impact of sudden rise of many taxa to a single cause (sudden rise predation was so far-reaching that many of predators), but in their own ways. organisms crossed their ecological Therefore, while the Mesozoic marine thresholds. Gastropods were forced to revolution affected all organisms prone to venture on land (i.e., Pulmonata) or predation, there appeared many remained afloat as nektoplanktons directional trends with some even (Pteropoda) during the Jurassic since opposite in nature. It is not all pervasive, aquatic, especially benthic environments like Cope’s Rule (Stanley, 1973) became inimical due to predation. showing a single, large-scale trend across Bivalves had to make excursion again to many taxonomic groups. the fresh water bodies as shallow marine

2 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW

Predators Apperance Mode of feeding

Asteroidea (including star fish) Late Ordovician Extraoral and intraoral digestion; molluscivore.

Dipnoi (fresh water lungfishes) Devonian Crushing; durophagous. Heterodontidae (sharks) Jurassic Crushing; durophagous. Batoidea (rays) Jurassic Crushing; durophagous. Teleostei (Bony fishes) Triassic Crushing, wrenching, swallowing whole; durophagous.

Stomatopoda (Crustacean) Jurassic Hammering and spearing; durophagous.

Palinuridae (spiny lobsters) and Nephropidae Jurassic Crushing; durophagous. (lobsters) Brachyura (crabs) Jurassic Crushing, apertural extraction; durophagous.

Aves (birds) Late Jurassic Crushing, swallowing whole, wrenching; molluscivores.

Cephalopoda (Ammonitina, Nautilina and Jurassic Crushing; durophagous. Belemnites) Muricacea (gastropods) Early Drilling, apertural extraction. Cretaceous Naticea (gastropods) Triassic Drilling. Other Neogastropoda Early Apertural extraction; molluscivores. Cretaceous Cynatidae (Mesegastropods) Late Cretaceous Apertural extraction; molluscivores.

Actinaria (sea anemones) No fossil Swallowing whole. records

Table 1. Appearance and mode of feeding of the predators which evolved during the Mesozoic (modified after Vermeij, 1977)

environments were infested with dreaded 2000, for nautiloids). But, in literature, predators. evidences of the effect of the Mesozoic Vermeij (1977) in his seminal marine revolution are implicit in other paper listed the origination of various groups. Here, we shall assess the kinds predators belonging to different historical consequences of the bloody taxonomic groups, which employ battles between the predators and the different feeding strategies (see Table 1). major marine prey communities.

He (1977) documented in detail GASTROPODA the responses of the gastropods in the event of rapid increase in the intensity of Vermeij (1977) gave a detailed predation pressure. He also briefly account of different solutions offered by mentioned the reactions of other hapless the gastropods against predation since preys. Since then, there is no serious and Jurassic. They developed diverse trends, comprehensive attempt to evaluate the exploited every opportunity to evade evolutionary trends within the other prey predation. Gastropods are preyed upon by lineages except some well studied, but various durophagous (shell crushing) isolated case histories (e.g., Ward, 1981, animals and many of them appeared for ammonites; Roy, 1994, for a subset of during the Jurassic (see Table 1). gastropods and Bardhan and Halder, Besides, many extinct Mesozoic groups such as Ichthyosaur, mososaurid lizard

3 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY and ptychodontoid sharks were also appeared rapidly in post-Jurassic believed to be the important predators, mesogastropods, neogastropods and which achieved durophagy by that time neritaceans. Spines not only increase the (see Vermeij, 1977 and references effective size of a shell (thus small therein). Gastropods are hunted by the predators can be avoided), but also predators right from their early ontogeny strengthen it against any breakage and through out the phylogeny! Think of (Vermeij, 1974). Narrow, elongated great internal asymmetry of gastropods, aperture effectively restricts the entry of which is known as torsion. Torsion predators such as crabs, muricids and occurs at planktotrophic larval (valiger) some other neogastropods which indulge stage and it brings the anus over the in apertural extraction of soft parts of the mouth, thus causing a great sanitation victims as feeding mode. These novelties problem. This inherent disadvantage is have been the predominant trends of borne by the gastropods since the many gastropods since Cretaceous. Cambrian. But, at the same time the twist Vermeij (1977) noted apertural dentition of the internal organs due to torsion as primarily an anti-crushing device, but enables gastropods to develop operculum it appears that dentition seems to provide at the posterior tip of foot. It allows some sort of a holdfast for the soft body mouth to first enter the shell when parts against apertural extraction. Co- threatened by an approaching predator occurrence of slit-like aperture with and the operculum comes last to conceal denticulated lips in many groups e.g. the aperture (see Stanley, 1975). Torsion Cypraea (Cowrie), Cassis (helmet shell) thus protects the animal right from the and cymatiids (tritons) or collumelar valiger stage. A fortress is always plica e.g. in Turbinella (the great Indian vulnerable in the absence of doors. For blowing conch, also used as bangles by the gastropod shell operculum is the married women) speaks for its additional fitting trap door! The most dominant function. External features being species evolutionary trend seen in the gastropod specific and easily recognizable, were phylogeny from the Jurassic onward was targeted extensively by the predators and against shell crushing. There was a therefore, there was a tendency to decreasing trend of evolute, planispiral conceal it by a mantle envelope (e.g., and umbilicate forms in Cypraea) or losing it altogether (e.g., archaeogastropods since the Jurassic. nudibranchs) as seen in present day Non-umbilicate mesogastropods and oceans. Remarkably, this trend also neogastropods also greatly evolved in the developed since Jurassic (see Portmann, later half of the Mesozoic (Vermeij, 1967). This phenomenon has been 1977). Open coiling, large umbilicus and interpreted as failure of the shell to act as high whorl expansion rate make a place of refuge. The shell loss is gastropods more prone to shell crushing commonly associated with a great speed (Vermeij, 1976). These forms are even or development of an obnoxious and found today, mainly in fresh water or acidic secretion as a means of protection land where shell-crushing predators are (Vermeij, 1977; Peel, 1987). lesser. Such forms, if present in marine Subclass Pulmonata, include environment are generally small in size, terrestrial gastropods or secondarily fresh evidently to avoid durophagy. If the jaws water dwelling groups. They evolved and (fishes) and claws (decapod crustacea) quickly diversified during the Mesozoic. were the order of the Mesozoic seas, They are detorted groups with mantle gastropods responded by developing cavity vascularized to act as air breathing mechanically more sturdy shells. Thick lung. This rapid change and ecological shell, strong nodes and elaborate spines breakthrough in a molluscan group to

4 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW become land dweller are significant. We ontogeny of benthic gastropods, acts as a believe that this is no coincidence that swimming device. It is studded with their origination took place in Mesozoic numerous cilia, which by means of when intense predation pressure made the continuous stirring helps in swimming. marine substrate nearly inimical for Pteropods retain all these larval features benthic groups and perhaps forced some including pelagic life, but they are adult. of them to venture on land. It is worth This clearly indicates that they were noting that some prosobranchs and paedomorphically, especially opisthobranchs also began to inhibit land progenetically derived and thus escape and fresh water at the same time. It is benthic life mode during the late evident that marine substrates became ontogeny of their ancestors. Intensity of increasingly inhospitable as many predation was such that every order of predators although appeared in the opisthobranchs and prosobranchs had Jurassic, achieved durophagy in the their pelagic representatives. Cretaceous or later in the Early Tertiary. Besides, there were many grazers and BIVALVIA browsers, e.g., teleostean (bony fish) or holostean (the pycnodonts), sea urchins Bivalves, a major class of (echinoids) and many gastropods. Mollusca, constitute the dominant Majority of them continue even today. benthic prey community of today’s The fishes which feed on algae, have oceans. Scores of millions of dead shearing dentition capable of breaking off bivalve shells litter the intertidal areas to the protruding parts or crushing the suggest their great success. If we look whole shell of smaller size. Sea urchins closely, we shall see that majority of are chief destroyers of today's coral reef them are siphonate infaunas – a and associated fauna. Many morphological as well as ecological opisthobranchs and prosobranchs are novelty, which was not present right from grazers and carnivorous, feeding on their appearance in the Cambrian. cniderians and other benthic animals. As Bivalves are headless, eyeless and retain a result benthic habitat became very many other characters of primitive stressful since the Cretaceous. The molluscs. They are simple, yet they are gastropod evolution reached its real acme ecologically specialized and diverse. If in the Tertiary with the great diversity and abundance are the measures diversification of siphonate of evolutionary success of any animal neogastropods. Along with them evolved group, bivalves are the ‘advanced’ group another new ecologic group i.e., and ‘progressive’ too (see also Gould, pteropods in the early Tertiary. They 1986). were tiny, pelagic opisthobranchs found Diversity at any hierarchic level in great numbers in rock record as deep- (e.g. genus or family) in the bivalve water pteropod ooze. We speculate that phylogeny has increased ever since the evolution of pteropods took place as an Ordovician. Even the great mass escape reaction from benthic ecology in extinction events could not perturb the response to intense grazing. Many ever-increasing trend. Sudden demise of gastropods pass through different many groups was quickly replenished by plankotrophic larval stages during a burst of evolution, thereby restoring the ontogeny. In valiger stage of larval background value (see Miller, 1990, fig. development when torsion occurs, they 6.1D). Therefore, it will not be have a thin nucleus shell with a peculiar understood from the diversity curve that wing-like organ called velum. Velum, what was the impact of the Mesozoic which is modified into foot during adult marine revolution in the bivalve

5 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY community since the Jurassic. The effect above the substrate. Stanley (1968) lies elsewhere. described the development of siphon as During Palaeozoic, especially the key innovation of the Mesozoic after the great burst of radiation in the bivalves. Siphon and the presence of Ordovician, bivalves adapted to various strong, muscular foot enabled the bivalves to become deep infauna. Great number of bivalve superfamilies having characterized by heterodont and desmodont dentition evolved during the early Mesozoic. Clarkson (1999, p. 212) observed, “Indeed the second great expansion of the bivalves during the early Mesozoic and continuing through out the Cenozoic was directly due to the fact that they could burrow”. But why did this great diversification wait for a long time (siphonate groups although many of them were mucous feeders, originated in the Fig. 1. Changes of diversity of siphonate and Late Palaeozoic, see Stanley, 1977, 1979) non-siphonate burrowing bivalves through and take place only during the Jurassic ages (after Stanley, 1977). (see Fig.1)? We have already mentioned

that intense grazing and shell crushing by the predators that made life hard for the modes of life and feeding strategies. benthic preys during the Late Mesozoic. These were mainly epifaunal, The sudden rise of predation sent a red endobyssate and shallow burrowing alert to the whole benthic community and groups, having adapted to both triggered a thorough reorganization of the suspension and deposit feeding types. earlier morphology and ecology. Many Throughout Palaeozoic, although relative groups, for example, gastropod resorted diversity fluctuated, endobyssate group to planktonic life or made excursion to dominated the adaptive landscape of fresh water or even to land. But the most bivalves. After the Permian-Triassic dominant trend taken up by many boundary mass extinction episode and unrelated groups, even different phyla, especially from Jurassic onwards, the was the infaunalization during Jurassic relative percentage of the endobyssate and Creataceous times. Many gastropods group fell dramatically and diversity of even adapted infaunal life habit and free burrowing ecologic group increased underwent great diversification (Vermeij, greatly (Stanley, 1968, 1977). Earlier, the 1977). An entirely new morpho-ecologic infaunal groups had included mainly group, showing great diversity, evolved mucous-feeding bivalves (e.g. within the echinoids, i.e., Irregularia Lucinaceae) or very shallow burrowers (Kier, 1974, 1987 and see below) and that lay near the sediment-water Stanley (1977) noted a dramatic rise of interface. It was in early Mesozoic times the siphonate, infaunal bivalves. that the bivalves with true siphon Both Stanley (1977, p.200) and flourished. Siphon is formed by the Vermeij (1977, p. 225) were not certain fusion of the posterior parts of the mantle to single out predation as the prime and has a tubular and muscular extension. causal factor for bivalve diversity. It allows the burrowing bivalves to Stanley (1979, p. 293) saw basically communicate with the external world predation as a ‘braking mechanism’,

6 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW which slows down the evolutionary rate deeper water, which is less frequented by of speciation and/or promote extinction. the predators. But, many regular While explaining the gradual decline of nautiloids and ammonites along with the endobyssate bivalves during the belemnites survived till the end of Palaeozoic, he attributed predation as the Cretaceous and faced the brunt of the sole cause. Many higher taxa according sudden rise of predators during the to him (Stanley, 1979, p. 293) radiated in Mesozoic. How did they respond to such the absence of predation. Again, hostility? We here examine all the major elsewhere, he (p. 204) suggested that subclasses of the Mesozoic cephalopods. predation pressure of less intensity can accelerate diversification. However, Ammonidea: concomitant rise of many predatory animals and great expansion of many Contoured frequency diagrams of benthic prey communities during the Raup and Stanley (1985, fig8-2, 8-3) Jurassic deserve special notice. elaborated later by Ward (1981, fig. 2.6) Moreover, many of these prey showed show that the best-fit design adapted by parallel evolutionary trends towards ammonites throughout their career is an infaunalization at the same time. For involute form with elliptical whorl gastropods and echinoids, it is section. Functionally, this streamlined convincingly shown that predation was shape is hydrodynamically more the cause. Modern bivalves are devoured efficient, allowing ammonites a quicker by the every predator that arose in the movement in the water. In addition, it Jurassic (see Table1). They are killed by may appear that like in the gastropods, means of crushing, spearing, swallowing open coiling of cephalopods is vulnerable of the whole body and more importantly to predation. In contrast, involute shell, by drilling predators. Two important which protects the more fragile early predatory drilling gastropods i.e, whorls, might have been a defensive muricids and naticids achieved this measure against predation during the capacity in Cretaceous. Many dead Mesozoic. But older groups, such as the, bivalve shells of the present day oceans Late Paleozoic order Goniatitina were bear characteristic boring marks made by more involute (see Raup and Stanley, these drilling gastropods. 1985, fig. 8-3) than the true Mesozoic Infaunalization includes invasion ammonites. Contemporary nautiloids into two ecological regimes – soft were also more involute than the sediments and hard substrates. In soft Jurassic-Cretaceous ammonites (see sediments digging is done by muscular Ward, 1981, Fig. 7). Besides, many foot. Hard bottom penetration is achieved evolute ammonites persisted and through mechanical boring by shell diversified, and heteromorphs were rotation or acid secretion. It is not an abundant in the post-Triassic oceans. It accident that boring bivalves also seems that shifting of morphospace appeared in the Jurassic (Pojeta, 1987). within ammonite phylogeny towards the optimally designed involute shape speaks CEPHALOPODA for rather better hydrodynamic efficiency and distinction of adaptive peaks of Vermeij (1977) noted the nautiloids and ammonites was the result existence of heteromorph (irregular of the biotic competition (see also Ward, coiling) shell within the Palaeozoic and 1980). Ammonite’s planispiral baüplan the Mesozoic cephalopods and speculated has a finite limit and is constrained that if these forms had continued today mainly by growth. Variation in shell form they would have been restricted to the occurs by the interplay of three Raupian

7 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY parameters i.e., degree of involution (D, impact with the substrate (Westermann, distance of generating curve), inflation 1971, 1990), sexual display (Kennedy (W, rate of whorl expansion) and shape and Cobban, 1976) and camouflage of the generating curve (S) (Kennedy and (Cowen et al., 1973). Cobban, 1976) and the gross shell form While all these functions of shows homeomorphism, which is ammonite ornamentation are feasible, common place in phylogenetic history of Ward (1981) has singled out predation as the sole cause for the increasing shell rugosity in the Mesozoic ammonites, which evolved as a defensive adaptation. Ribbing on ammonite shell increases resistance against shell breakage; for the same shell thickness, corrugated part would be stronger than smooth shell against the point-load exerted by toothed predator (Westermann, 1971). Kauffman and Kesling (1960) reported a famous case where a specimen of Placenticeras mecki of the Cretaceous was bitten several times by mosasaur reptile. The shell was punctured, but not crushed. Though genus Placenticeras has numerous species, except one species in Bagh, central India, none have their apertural margin preserved (see Klinger and Kennedy 1989; Gangopadhyay and Bardhan, 1998). This indicates perhaps that they had been suffered from extensive predation. Bagh Sea in India

during the Coniacian was deep inland and Fig. 2. Frequency distributions of categories of rib placid in nature. This attributed to less patterns of ammonites during Late Palaeozoic and Mesozoic (modified after Ward, 1981) hostility of the normal marine predators

and a single species, i.e., P. kaffrarium

almost monopolized the Bagh sea. It has the ammonites. Ward (1984), therefore, many specimens having their peristome explored the possible counter measures intact (see for detail, Bardhan et al, taken up by the ammonites against 2002). predation in another line of investigation Apertural breakage of ammonite – shell sculpture. Ammonites are shell by decapod crustaceans and brilliantly ornamented by ribs, tubercles repairing of the injuries have also been and spines and in the past they were the reported (Roll, 1935; Thiermann, 1964 in collectors’ pride. Palaeontologists Ward, 1981). Many ammonite fossils interpreted functional significance of have been found with shell injuries done ammonites shell sculpture in various by predators or by defensive efforts of ways ranging from hydrodynamic their prey (Ward and Wicksten, 1980). efficiency (Chamberlain and The nature of ribbing during Mesozoic Westermann, 1976), withstanding was mostly radial. This would align the ambient hydrostatic pressure (Spath, brekage parallel to the peristome margin 1919), better buoyancy regulation and cause less damage to the body (Teichert, 1967; Kennedy and Cobban, chamber. Apertural thickening by 1976), resistant against predation and

8 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW internal ridges (i,e. pseudoconstriction, utilities were either suppressed or played see Westermann, 1990) increased the a secondary role. The ornamental mechanical strength against the shell rugosity was channelised to serve only crushing. Presence of spine at the one function i.e., protection. peristome is primarily seen as either a If the ratio between the rib width mechanical protection against apertural and the shell diameter of ammonites extraction of the soft parts by the exceeds 0.05, the hydrodynamic predators (Kennedy and Cobban, 1976) efficiency of the shell decreases like that of gastropods (see Vermeij; (Chamberlain in Ward, 1981). The 1977) or as a sensor because these spines coarsely ornate Jurassic and Cretaceous are mainly hollow and delicate ammonites had greater magnitude than (Westermann, 1990). Ward (1981) has this critical value, and thus seemed to shown an evolutionary trend of the have sacrificed speed for protection. increasing strength of ammonoid shell- Many ammonites were thoroughly ribbing during the Mesozoic (Ward, ornamented, but shell ornamentation on 1981, present fig. 2) and highest their phragmocones rather lowered the incidence of nodose and spinose forms strength against the ambient hydrostatic occur during the Cretaceous. His main pressure. A smooth shell with circular argument was the timing of appearance whorl section was the most adaptive of the increasing strength of shell design (Westermann, 1990). Yet, the rugosity. While ribs of varying strength ornamentation in young was crucial for were present since Palaeozoic, there was survival against predation. a dramatic increase of the ribbing Ornamentation may also be an strength in the Middle Jurassic, which expression of the genetic variability continued with accelerated pace till the within a population. Many ammonite end of Cretaceous. He therefore, species show great intraspecific variation. supported Vermeij (1977) and mentioned Often there is a positive correlation that the trend of shell rugosity in between the degree of inflation and ammonites also orchestrated the trend in strength of ornamentation (Westermann, other invertebrate groups. 1966). The Coniacian Placenticeras We have mentioned about the kaffrarium of the Indo-Madagascan other usages of the ammonite shell Faunal province shows stunning sculpture and they appear to be also quite intraspecific variation – from smooth, reasonable. Presence of ribbed shell slender and oxyconic umkwelanense might convert the nature of water flow variant to tumid kaffrarium variant with from laminar to turbulent boundary layer three rows of tubercles – leading to an flow, thereby increasing the ornamental polymorphism (Klinger and “streamlining” and hydrodynamic Kennedy, 1989; Bardhan et. al., 2002). efficiency (Chamberlain and The ornate variant here clearly had an Westermann, 1976). The prominent extra adaptive edge over the smooth spines are hollow or even septate in some sympatric variant. Widely variable cases (see Kennedy and Cobban, 1976) to populations were not generally under increase buoyancy. We believe that the strong selection pressure (Seilacher, ornamentation of ammonites initially 1972). But in later phylogeny of the evolved to serve various functions or it family Placenticeratidae, a trend of had multiple uses. The function of the increasing rugosity and body size (the same sculpture also differs from taxon to youngest species during the Campanian taxon (Westermann. 1990). But, due to attained diameter of about 1 m, see the escalation of predation during the Emami et. al, 1984 in Klinger and Mesozoic marine revolution, the current Kennedy, 1989), which were

9 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY hypermorphically derived (Kennedy and Jurassic is often called the “Age of Wright, 1985), was set. In a well- Ammonites” (more than 650 genera developed sexually dimorphic species, highest ever for any period). The great microconch is generally strongly and sudden diversification of the new and ornamented up to the end of the body last order Ammonitina was associated chamber whereas the macroconchiate with many new novelties other than body chamber may be devoid of any suture. One was the prevalence of strong ornament (Callomon, 1963, Jana, 2002). and widespread sexual dimorphism. In But this genetic character of microconch sexual dimorphism, the sexes are not may be transmitted to descendant species, only separate, the males and the females which has both sexual morphs thoroughly differ from each other at least in size. ornamented. In this way higher This size dimorphism of ammonites is taxonomic group may appear through known as early as from the Devonian. macroevolution (cf. Stanley, 1979). Such However, from the Jurassic onward was the case for subfamily level dimorphism is characterised by size, transition from Macrocephalitiane to nature of coiling and ornamentation. The Eucycloceratinae during the Middle males that are smaller (called Jurassic (Jana 2002, Jana et al., in press). microconch) are not only more strongly There are many similar instances where ornamented than the larger females ornaments had appeared intrinsically, not (called macroconch), they have bizarre as a product of natural selection. But, structures like the rostrum, and lappets these sculptures were later co-opted as etc., at the aperture and are more defensive measures against predation aberrantly coiled. The disparity between (Bardhan and Halder, 2000). Gould and two sexes is so great that palaeontologists Vrba (1982) decribed this phenomenon took about 100 years to understand that as “exaptation”. Prominent and slender they are the two sexual variants of same spines on body chamber might develop biological species. The microconchiate merely due to ontogenetic scaling characters are variously interpreted as (Checa, 1985). These spines as in sexual characters, sexual display (see productid brachiopods, then played a Kennedy and Cobban, 1976) or helps in secondary role for protection and perhaps mate recognition (Jana 2002; Jana et al., as camouflage (Westermann, 1990). in press). Westermann (1990) believes Isolated mutations or developmental that well developed dimorphism implies constraints (mainly heterochrony) ecological niche partitioning. Majority of initially induced important morphological the ammonite groups are currently changes and trends are ‘exaptive interpreted as having nectobenthic life expansion’ (cf. Gould, 1990) guided by mode in shallow water where they faced extrinsic factors (here biological, i.e, stiff competition for food. He mentions predation). Dommergues (1990) that the shallow water ammonites are described such trends in many Jurassic strongly dimorph while the pelagic ammonites. groups (e.g. phylloceratids and Ammonite diversity patterns have lytoceratids) have no or poorly developed a fluctuating history; after a sudden crush dimorphism. Ammonites inhabited in the at Permo-Triassic boundary, the diversity shallow water shelf environments since roared to explosive adaptive radiation the Palaeozoic. Though there had been no during the Mesozoic. The Palaeozoic ecological shift during the Jurassic, yet goniatiids gave rise to Triassic ceratiids we get pronounced shell dimorphism in from which rapidly evolved the true all Jurassic and Cretaceous families ammonites (having ammonitic suture) (Donovan et. al., 1981; Klinger and after the end-Triassic mass extinction. Kennedy, 1989).

10 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW

Vermeij (1977, 1987) has shown predatory groups. Other molluscs solved that the great predation during the it by various ways as discussed above. Mesozoic marine revolution did not act Ammonites responded by increasing the as an agent of death in the long run; strength of ornament and great instead, prompted great diversification of diversification. This was possible many new and existing groups in which because ammonites adopted a new kind sex prevails. Evolution of sex is primarily of reproductive strategy ― strong, seen as a caterer of evolutionary ornamental dimorphism. It is remarkable radiation. It provides wide range of that records of the earliest sexual genetically derived intraspecific variation dimorphism in other cephalopods such as within a population upon which natural nautiloids (see Bardhan and Halder, selection or drift can work. The Late 2000) and coleoids (Doyle, 1985) Precambrian metazoan evolution is appeared in the Jurassic (see discussion perhaps associated with the origin of sex below). (Schopf et. al., 1973) and so also the Did ammonites belong only to the Cambrian explosion of all the modern prey community? The order Ammonitina day bisexual phyla (Stanley, 1979). The that appeared only during the Jurassic Mesozoic ammonites were not only had many novelties. These are diverse, they were characterised by rapid widespread and elaborate sexual turn over and equally dominant dimorphism just mentioned and the evolutionary bursts, which made them calcified jaw structure known as aptychi. “biological stopwatches”. Excellent Early ammonites had chitinous anaptychi biostratigraphic zonation of the Jurassic from which the Jurassic aptychi evolved System of rocks is possible only because and eventually replaced it. This change of the scores of short-lived, ephemeral over as well as the various types of ammonite species or genera. We believe strongly ornamented calcitic aptychi that even within bisexuality, dimorphism suggests a new kind of feeding strategy has more evolutionary potential because (Kennedy and Cobban, 1976). here, outbreeding takes place between Structurally aptychi resemble jaws of parents who are quite dissimilar, resulting present day Nautilus or octopuses which more variation in the population. More are active hunters of the bottom dwelling ornamental rugosity of microconchs crustaceans. Crabs resist nautiloid would play major role in the evolution predation by chelae and often break the within lineages and there would be a peristome of the Nautilus in a manner phylogenetic slant towards the increasing much similar to that found in the strength of the shell sculpture, if these ammonite shells. Ward (1981) has were found to be resistant to crushing. therefore reasons to speculate that the This exactly happened during the ammonites especially of the Cretaceous Jurassic. Stanley (1979) stresses that sex used to prey heavily on various and large plays more important role in size crustaceans. Claws in crabs, spines macroevolution. Rapid origination of in lobsters and other armors arose higher categories is only possible by primarily as defense adaptation and they quick speciation events, which again can later turned into formidable predators (for only be accomplished by sexual taxa. The detail, see Crustacean section). early Middle Jurassic times witnessed the We also believe that ammonites appearance of many superfamilies being most diverse in the Jurassic park showing evolutionary increase of shell under the sea and having been equipped sculpture. Nektobenthic habitats of the with prehensile tentacles, well developed shallow water were for the first time jaws, eyes and a capacity to have infested with many rapidly rising extensive and complex courtship ritual (if

11 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY lappets are a product of sexual selection), perhaps serving no functional purpose. were intelligent and important predatory Subsequently, the nautiloid ribs became animals. They adopted visually hunting progressively stronger, extending all strategies like fish and occupied higher around the shell like those of the level at the food web. As it often occurs, contemporary ammonites. The frequency the hunter becomes a victim of other of the ribbed taxa and the strength of group, ammonites took care of defense ribbing increased in later nautiloids by increasing the shell rugosity. Many (fig.3), paralleling the trend in ammonites aptychus closely conform the apertural (Ward, 1981). This is believed to be an outline of the ammonites, but anaptychi never closely match. This led Kennedy and Cobban (1976) and others to believe that aptychi acted secondarily as an operculum to protect soft parts from any possible attacker (for different view see Lehmann, 1981).

Nautiloidea:

Among the post-Triassic nautiloids, many genera are characterized by transverse ornamentation, believed to have evolved independently in many families. Tintant and Kabamba (1983, Fig. 3. Frequency distributions of categories of 1985) and Tintant (1989) attributed this rib patterns, (1) fine, (2) moderate and (3) to adaptation. According to them ribbing strong in species of Jurassic-Cretaceous evolved gradually in response to a change nautiloids (after Bardhan and Haldar, 2000) in the habitat. Bardhan and Halder (2000), on the other hand, believe that ribs were formed by crowding of growth adaptive response to the Mesozoic lines, as a corollary to changes in body marine revolution (Bardhan and Halder, size during paedomorphic evolution. 2000). Ribbing, though not adaptive at Initially the ribs had no direct functional first in the nautiloids, was subsequently significance. Detailed study of the origin co-opted as a defensive adaptation. The and the nature of ribbing patterns in evolution of this structure is a good Paracenocerous, one of the earliest post- example of exaptation (Gould and Vrba, Triassic genera, led them to draw some 1982). general conclusions about the phylogenetic history of ribbing in Coleoidea: nautiloids. These ribs appeared suddenly in a species, P. jumarense in the Late The subclass Coleoidea of Bathonian of Kutch, Gujarat, in a manner Cephalopoda is represented in the present compatible with the punctuational model day seas by the squids, cuttlefishes and of evolution (Gould and Eldredge, 1993). octopuses. They are dibranchiate, having Some other contemporary genera are also internal shells. In octopus it is lost found to have similar ribbing patterns. altogether. Except belemnites the fossil The ribs were initially weak and record of Coleoids is poor. Coleoids restricted to either the flanks or the venter doubtfully appeared in Devonian of the adult body chamber. They evolved (Engeser, 1990). Recently, Engeser and essentially as an evolutionary by product, Bandel (1988) and Engeser (1990)

12 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW revised the coleoid classification and equipped with the armour, i.e., their subdivided them into two orders, extinct rostrum, evolved not only in the Ealy Belemnoidea and Neocoleoidea [it has Jurassic, they also rapidly diversified. two extant groups, the Octopodifarmis Predation on belemnites was perhaps (eg. Octopus) and Decapodifarmis intense. Rostra of many species bore (squids, sepia etc)]. Belemnoidea were injury marks those were subsequently represented during the Paleozoic by repaired (Bandel and Kulicki, 1985). aulacoceratids and phragmoteuthids. The Holder (1973) found tooth scratches Triassic aulacoceratids e.g., Aulacoceras probably made by marine saurians on the and Ausseites, had covering, called guard live belemnite rostrum. They are believed or rostrum, on the tip of the to have been extensively predated by the phragmocone. The rest of the Mesozoic marine reptiles such as phragmocone along with the small guard Icthyosaur and large toothed fishes was believed to be enclosed by the (Ager, 1976). Jurassic sharks were also mantle as found in the endoskeleton of eminently suited to a bellemnite diet. In a the present day coleoids. Aulacoceratids famous discovery from the Lias of and phragmoteuthids continued up to the Germany, a Mesozoic shark belonging to Early Jurassic (Engeser and Bandel, the genus Hybodus, has been found to 1988). Belemnites sensu stricto suddenly contain more than 200 belemnite rostra in appeared during the Jurassic and its stomach (Jordan et al., 1975) continued upto the end of the Cretaceous. Belemnites were also active predators; In belemnites, body chamber was they fed on smaller organisms (Morton, reduced to pro-ostracum and the guard 1971; Young and thompson, 1976). became an enormously large, a massive, Belemnites, equipped with hooks on all bullet-shaped cylinder of solid calcite. It ten arms and eyes with lens (Engeser and resides at the posterior part and encloses Bandel, 1988; Engeser, 1990) were the whole phragmocone. Phragmocone is capable of visual hunting. All recent a hydrostatic organ and is also present in coleoids are active predators, feeding on other cephalopods such as nautiloids, bivalves, crustaceans and small fishes. It ammonoids and orthocone cephalopods. is, therefore, believed that the Mesozoic Some workers believe that orthocone belemnites occupied an important cephalopods were vertical migrants in position as carnivores in the trophic water. Addition of external thickening as chain. guard initially acted as a counter weight Since, they were also extensively to maintain a horizontal disposition of the predated by large fishes and reptiles, body while swimming. But, why the rostrum which enclosed phragmocone Jurassic-Cretaceous belemnites had completely in belemnites, evolved massive guards covering the whole rapidly as a defense mechanism. skeleton? It is conceived that the guard or Significantly, the Jurassic belemnites the rostrum in the Triassic Aulacoceras were also found to be sexually was used not only to counterbalance the diamorphic (Doyle, 1985). Like buoyant phragmocone but also to protect ammonites and nautiloids, they too young shell (Swinnerton, 1950) — a step seemed to employ sex as an adaptive against high juvenile mortality owing to strategy to diversify (Donovan and predation. So it can be considered to be a Harcock, 1967; Stevens, 1973). They case of exaptation. To protect only young continued with much vigor till the end of was not enough when predation pressure Cretaceous when, like many other taxa, accelerates. Aulacoceratids became they fell victim to the major mass extinct in the early Jurassic. It is extinction event. This catastrophy shifted significant that belemnites being better the evolutionary trend within the

13 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY phylogeny of Coleoidea. Neocolioidea diverse (see Rowell and Grant, 1987, which remained insignificant during the present fig.4) and they dominated the Cretaceous, suddenly went into great entire shallow water community adaptive radiation at the beginning of throughout Palaeozoic. The Permian Tertiary (Engeser, 1990). They quickly brachiopods underwent a great adaptive diversified, perhaps to exploit all the radiation. They were not only diverse and vacated niches left by the ammonites and the most abundant fossils of the shallow belemnites, once their formidable deposits of the world, they also made an competitors. Subsequently, evolution important ecological breakthrough. progressed mainly in two directions. One Brachiopods are filter-feeder, sessile was the reduction of guard. The shell benthos. They have various life modes; underwent rapid degeneration resulting in majority employ pedicle as means of the total loss of the shell. Another trend attachment. Many strophomenides and led to the early loss of rostrum, decrease some spiriferides were free lying. Less in phragmocone size and finally, the common brachiopods are encrusted and development of lanceolate pro-ostracum, epiplanktonic inhabits. During the which is still found in present day squid, Permian, productides crossed the Loligo. previous ecological threshold to invade a Intensity of predation appeared new zone i.e., infaunal niches. not to have been stalled after the K-T Productides adapted to quasi- to fully boundary mass extinction since there infaunal life. The spines in adult pedicle arose different kinds of predators in the valve helped them anchor firmly within Tertiary marine waters (Vermeij, 1980). sediments, and a concave brachial valve The reduction of shell or its received sediments settling from above. internalization, also took place in many In Waagenoconcha, a Permian genus, gastropod groups of the Tertiary, as a brachial valve developed small, delicate reaction against extensive predation on spines to prevent removal of sands from shelled prey. This loss has been the surface by strong currents (Grant, interpreted as a de-emphasis of the shell 1966). Brachiopods thus would, become as a protecting device. It is commonly fully covered and be well camouflaged associated with great speed (e.g., squids) (Clarkson, 1999, fig.7.17e). This clearly or with toxicity and unpalatability. indicates that productides adapted to infaunal life for protection and competed BRACHIOPODA well with the nonsiphonate infaunal What are the attributes that bivalves. Besides, other groups showed control diversity, evolutionary trends and ‘great evolutionary plasticity’ and dominance of a lineage? The great colonised in reef environment. Many of decline of brachiopods from the major them looked bizarre, ‘unbrachiopod-like’, shallow water benthic constituents of but all were highly adapted to their Palaeozoic to highly reduced ones in Late respective niches (Rudwick and Cowen, Mesozoic onwards, has been explained 1968). by causal factors, like their competition Alas, brachiopods were worst hit with bivalves, and the evolutionary by the great Permo-Triassic mass consequence of their great dying because extinction and productides became of the Permo-Triassic boundary mass completely extinct. Extinction thus extinction. removed the best-adapted taxa from the Brachiopods appeared during the brachiopod phylogeny. Rhynchonellides, Cambrian and then quickly diversified in terebratulides and few others managed to to three subphyla, which still continue. straddle past the crisis boundary and By the Devonian, brachiopods were most subsequent brachiopod evolution was

14 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW directed to their ways. They diversified them resulted in the ultimate community during the Jurassic, and by the replacement (Steele-Petrovic, 1979). Cretaceous they were abundant in shelf Gould and Galloway (1980) alternatively, environment including shallow waters, attributed the bivalvian take over to but were localized. Since then, the another causal factor — the evolutionary brachiopods lost their dominance in shelf aftermath of the end-Permian extinction habitat, which was instead successfully crisis, which took the toll of majority of colonized by bivalves. Brachiopods are the brachiopods. The bivalves, however, now found in deep and cold seas. While were less severely affected (fig.1). there were 4500 fossil genera, and they Bivalves, the first among the survivors, are currently restricted to only 100 living then rapidly monopolized the vacated genera. This speaks for a great fall of shallow water niches left by the Permian brachiopods. Benton (1983) also mentioned that competition as well as catastrophic demise might be responsible for such a large-scale faunal replacement. During Palaeozoic, especially in the Permian, brachiopods were not only diverse and abundant, they also successfully competed with the bivalves for both infaunal and epifaunal habitats. “Brachiopods dominated the level- bottom nearshore and shelf habitats during Palaeozoic time, but they were able to share a number of habitats (especially in the nearshore region) with bivalves [italics ours] and a long-term equilibrium was set up”(Clarkson, 1999, p.50) In fact, living side by side with bivalves, the Mesozoic terebratulides and Fig. 4. Changes of diversity of Brachiopoda rhynchonellides were the commonest with time (after Rowell and grant, 1987) fossils in many shelf habitats, such as, in

the classical Jurassic section of Kutch, India (personal observation). The dwindle of brachiopods actually started their diversity and a shift of ecology from from late Mesozoic. We, therefore find shallow to deep waters since the no reason why won’t the surviving Mesozoic. brachiopods compete with bivalves to Why did brachiopods fail to colonize the substrate? It was really a bad reestablish their supremacy in shallow luck and not a bad gene (cf, Raup, 1991) water environments? Many hypotheses that the productides were completely have been put forward to explain their wiped out during the end Permian crisis. dwindling and ecological exclusion from Had it not been the case, they could have the shelf area. Competition with the been formidable competitors of the bivalves, especially with infaunal siphonate bivalves during the Mesozoic. siphonate groups, is considered to be the Stanley (1979) singled out one of the likely causes. Siphonate predation as the likely cause for the bivalves are more efficient filter feeder decline of brachiopods. Clarkson (1999) and physiologically superior to considered that the rise of starfish in the brachiopods; a fierce fighting between Mesozoic might have been responsible

15 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY for the decline of brachiopods. We, here, on opposite sides of a spherical test), emphasize that many other predators dominated by cidaroids. They were which appeared due to the Mesozoic ornamented with large tubercles, spines marine revolution, for example, drilling and simple ambulacral plates. They all gastropods, also exerted much pressure were epifaunal, living on substrate since on the epifaunal brachiopods they could not burrow. During the great (Grant,1987). Terebratulides were end-Permian mass extinction event, all extensively predated and Ovcharenko Palaeozoic echinoid taxa died; only the (1969) reported from the Middle Jurassic genus, Miocidaris straddled past the P-T of Pamir, a predation-driven evolutionary boundary. For the major part of the trend within a lineage i.e., Kutchithyris. Triassic, echinoids remained small and We know that the punctate brachiopods less diverse. Then, in the Late Triassic- can reduce predation of the boring Early Jurassic, the stragglers went on a organisms by means of the presence of spectacular adaptive radiation and various proteins and lipids in their cacae. produced an entirely new stock that is But this ability to repel predators was not known as noncidaroid regular echinoids achieved by the punctate brachiopods in (fig. 5). They are distinguished from Palaeozoic (Grant, 1987)! We have Palaeozoic cidaroids in having compound already mentioned that bivalves ambulacral plates and more tuberculate overcame the danger by adapting more to interambulacral plates. They are also infaunal life. The Mesozoic brachiopods epifaunal. Soon, during the Early were fixosessile (having strong pedicle Jurassic, they gave rise to a new group, attachment) and, thus, phylogenetically which lost pentameral symmetry of the constrained (cf. Seilacher, 1972) not to primitive echinoids ―the Irregularia. develop the burrowing ability. They The irregular echinoids were finally gave way shallow water areas to characterised by a dominant bilateral the bivalves and migrated to the placid symmetry and migration of the periproct deep and cold water as we find them from the apical disc to the lower surface. today. These morphological innovations enabled Look at the inarticulate Lingula, the irregular echinoids to become which is a living fossil since the infaunal, which subsequently gave the Cambrian and has a wide ecological echinoid evolutionary history a slant range covering shelf and basinal regions towards this new group. Many taxa since in the past (Cherns, 1979) to the present the Jurassic independently became day brackish to intertidal environments irregulars to adapt for an infaunal mode (Craig, 1951). The modern level- bottom of life. They dominate the present day near shore habitat is infested with seas. bivalves and Lingula survives! Lingula Echinoids have many predators has “weathered the storm” of extinction, like fishes, crabs, mammals and birds; competition and predation better because even the man prefers their palatable eggs. of the fact that it could efficiently Some echinoids devour other members. burrow. For example, in the present day ocean, large, regular echinoids eat sand-dollar (a ECHINOIDEA type of asteroid) from the edges like a biscuit. The Post-Palaeozoic cidaroids are It is the largest class within the “improved regulars” being larger in size Phylum Echinodermata that appeared and more spinuous; they dominated the during the Ordovician. All Palaeozoic Triassic. But, during the Jurassic a major taxa were regular echinoids (having change took place. The noncidaroid pentameral symmetry; mouth and anus regulars developed compound ambulacral

16 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW

Fig. 5. The stratigraphic range chart of echinoderm classes. Note appearance of irregular echinoids during Jurassic.

enabling them to build up large spines infaunalization of irregular echinoids as attached to the ambulacra (Kier, 1987). the reflection of intensification of Large spines in regular echinoids were predation at or above the sediment-water primarily for protection from the predators interface. It is interesting to note that the and for locomotion. Even some used bivalves also solved the same predation spines to bore within hard substrate to pressure by increasingly adapting to an conceal themselves from predators. The infaunal mode of life since the Jurassic. regular echinoids of the tropics, where The true siphonate groups emerged during predation is more intense, employ that time. Irregular echinoids poisonous spines as defense adaptation. superimposed bilateral symmetry over the Pedicellariae, nothing but modified spines, pentamerous baüplan, native to old are the Jurassic acquisitions, consequent regulars. Periproct came out of the apical to the beginning of the “arms races”. The system and migrated towards posterior; pincers, besides performing other likewise peristome shifted towards functions, prevent small predators; some anterior. This made revolution as it use poison to repel larger attacker, say, a offered better sanitation within the starfish (Kier, 1987). burrows. Like bivalves the echinoids had to take care of problems related to communication with the external world Kier (1987, p. 669) observed that, for food and respiration. The bivalves “ The most significant post-Palaeozoic solved it by innovating siphon and the development was the evolution of the echinoids used their versatile tube feet, irregular echinoids during the Early which among multiple uses, serve Jurassic”. Vermeij (1977) related the respiration and feeding. Other significant

17 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY changes from epifaunal to infaunal life true reef builder and were present habit are the flattening and elongation everywhere. Reefs are massive, wave of the test, decrease in size, but increase resistant organic build up made by in number of tubercles and spines, diverse genera of corals and other development of petals and phyllodes groups. The Great Barrier Reef of and loss of teeth (see Kier, 1987 and Australia is a recent example of a huge present fig. 6). Burrowing echinoids organically built structure made by the scrape through sediments horizontally corals. It runs over several thousands of and assume the shape of a deep kilometers. More than 700 coral species burrowing bivalve in profile (see fig.6, live in the Indo-Pacific coral reefs. The c) ― a remarkable evolutionary success of scleractinians, ever since the convergence. Jurassic, is closely linked with their ability to make reefs. Reef formation involves presence of “groups of individuals structurally bound together in varying degree of skeletal and physiological integration” (Clarkson, 1999). Closely linked individuals act in a coordinated manner so that the whole reef can function as a single unit. It is a key physiological development. Massive and rapid growth of the coral

Fig. 6. Evolution of irregular echinoids reefs becomes possible for their one showing major morphological changes to remarkable ecological breakthrough, become infauna, during the Jurassic. An = anus. that is a symbiotic association of corals (modified after Kier, 1982) with algae (dianoflagellate and zooxanthellae). Algae enable corals to secrete more calcium carbonate and OTHER TAXA provide oxygen and food. But, why do they build reefs? Reef communities If the effects of the Mesozoic appeared throughout the geological marine revolution are far reaching in time and advantages of reef building are the groups mentioned above, how did mainly stability and protection. Almost other taxa respond to these phenomenal every predator of modern seas has a biotic stresses? Even a casual reading of share of diet on the corals. Fishes (e.g., this fossil records, reveals their parrot fish), reptiles (turtles) and stunning reactions. The effects in some starfish (Acanthaster) are dreaded of the other marine invertebrate predators of corals. A massive coral community are described in short colony is less vulnerable than solitary details. individuals. The ability to physically integrate them and to increase high Corals: carbonate productivity through algal symbiosis, appear to be the responses of Corals of the present day the corals against rapid rise of many tropical oceanic waters are dominated predators since the Jurassic. by the taxa belonging to the order Sclerectinia. They evolved during the Crinoidea: Middle Triassic and all post-Lower Triassic corals are included in the order. Crinozoans are primitively By the Middle Jurassic, corals became stalked echinoderms (pelmatozoans)

18 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW

Prey Defensive adaptation Appearance of Function antipredatory device Gastropoda Decreasing trend of evolute, panispiral Jurassic Against durophagy. and umbilicate forms. Sturdy shells with strong nodes and Jurassic Against durophagy. spines. Narrow, elongated and denticulated Cretaceous Against apertural extraction. aperture. Internallisation or complete loss of shell. Jurassic De-emphasis of shells as protective device and to avoid species-specific predation. Development of detorted groups Mesozoic Against marine predators. (Pulmonata), which made excursion to fresh water. Development of siphonate gastropod Diversification To avoid intense grazing in and/or infaunalisation. during Tertiary benthic ecology. Size reduction to become tiny, pelagic Early Tertiary To avoid intense grazing in opisthobranchs – pteropods. benthic ecology. Bivalvia Infaunalisation of true siphonate group Originated in the Intense predation in epifaunal including burrowing and boring. Early Mesozoic benthic ecology. Brachiopoda Shift in ecology from shelf to deep and Mesozoic To avoid intense predation in the cold seas. shelf region. Punctate brachiopods having various Mesozoic To repel predators. proteins and lipids in cacae. Echinoidea Development of Irregularia, rapid Early Jurassic To avoid intense predation in infaunalisation and modification of tube epifaunal benthic ecology. feet that helped in respiration and feeding. Large spines attached to the compound Jurassic Providing mechanical protection ambulacra. & helping in locomotion and boring within hard substrate. Poisonous spines Jurassic Against tropical predators. Pedicellariae Jurassic Prevent small predators. Coral Reef building capacity by the symbiotic End of Middle Defense adaptation against coral association with algae. Jurassic. crushing predators.

Crinoidea Appearance of first unstalked order Jurassic To move freely and to choose commatulida. suitable refuge. Bryozoa Appearance of Cheilistomata having Jurassic To avoid predation by providing calcified and integrated zooids. resistance.

Foraminifera Appearance of planktonic foraminifera. Middle Avoiding bioturbation and Jurassic. intense benthic grazing. Crustacea Rigid carapace. Jurassic Armour against durophagy and drilling. Chelae Jurassic To avoid predation by providing resistance. Evolution of hermit crabs taking refuge Jurassic To avoid predators who in discarded gastropod shells. swallowed the whole. Cephalopoda Ammonides and nautiloids having Jurassic Protection against durophagy. increasing shell rugosity. Evolution of belemnites and development Jurassic Against durophagy. of massive guard or rostrum.

Table 2: Appearance and function of the defensive adaptation of different prey communities which evolved during the Mesozoic.

19 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY with long arms and normally lack Mesozoic and may be intimately related complex respiratory structure. The to the rise of bioturbating animals. comatulid crinoids have, however, lost Recently Signor and Vermeij (1994) their stalks and become secondarily demonstrated that the planktic ecology free. It is only during Jurassic when the is a safe refuge from predation as well first unstalked order Comatulida as bioturbation for both adult and evolved which broke free from their larvae. It has been mentioned earlier, stalks in the early stages. They became because of the sudden rise of predation capable of moving away from predators especially on the benthic communities, and can hide in crevices (Stanley, many faunas took refuse within the 1979). Their great subsequent sediments. The triumph of siphonate diversification and dominance in the bivalves is a testimony of the present day sea may be seen as a occupation of this kind of new response to high intensity of predation ecological niche. Many other groups that started taking place only during also adapted the infaunal habit e.g., Jurassic (see also Ward, 1981). Irregular echinoids. Jurassic also witnessed the sudden increase in Bryozoa: burrowing activities (Stanley, 1979). Bryozoans, an important faunal Because of intense grazing by the constituent of present day marine predators and the churning by infaunal environment, were more diverse during preys, the marine substrate became very Paleozoic. After the great Permo- unstable and perhaps inimical to other Triassic extinction event, only one benthic groups. During Mesozoic, many group (Cyclostomata) managed to organisms, including the predators survive and flourished immediately in changed their early life mode strategy the absence of little competition. But a and adapted planktic larval stage e.g., new group (Cheilistomata) arose in brachyuran crabs and spiny lobster Jurassic; they were ecologically (Schram, 1982; Signor and Vermeij, superior in having increasing 1994). It is remarkable that the calcification, integration of the zooids undoubted fossil record of planktic and capability to live on different foraminifera came from the Middle habitats across the bathymetry. During Jurassic (Tappan and Loeblich, 1988). the end of Mesozoic, Clyclostomata started declining when competed with The Crustaceans: the group, cheilostome. McKenney and Many crustaceans e.g., decapods Jackson (1989) believed that great (crabs, lobsters) and stomatopods, arose diversity of the cheilostomes not only in the Jurassic and perhaps achieved lies in their adaptation to different durophagy by the Late Cretaceous ecology but they considered (Vermeij, 1977 and references therein). cheilostome colony as a living Initially they showed a strong predator mechanism to defend itself against the driven species selection (Stanley, predators. They also believed that 1979). The brachyuran crabs posses a decreasing relative diversity of Post- rigid carapace, used as armour as well Palaeozoic erect species is due to as a weapon like chelae. Hermit crabs increased predation pressure. are known from the Jurassic onwards. They solved the problem by taking The Planktons: refuge in discarded gastropod shells. Theyar (1983) suggested that This step, however, had other major diversification of planktic implications. This defense strategy organisms took place during the extended the ecological life span of

20 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW snail shell, thereby dramatically diverse. One of the remarkable aspects increasing the abundance of shelled of the Mesozoic marine revolution is prey. As a result, the predators that that both the predator and the prey were familiar with crustacean diet, had communities show sustained adaptive to develop shell-crushing devices. This trends as if the evolutionary energy was permitted the predators to specialise on concentrated on perfecting the acquired shelled prey where such speciallisation biomechanical designs for better would have been trophically unfeasible efficiency. Modernisation and before the hermit crabs arose (Vermeij, sophistication of arms and amours were 1977). the rules of the game. “……increasing Being well equipped, lobsters strength and efficiency in crab claws both chelate and armoured like shrimps, matched by growing intricacy and they swim only at a slower speed. sophistication of adaptive defenses in Shrimps developed morphologies for molluscan shells” (Gould, 2002, p.951). rapid propalsion as an escape One of the greatest fallout of the mechanism. Lobsters show a distinct Mesozoic marine revolution was the trend of strengthening the defensive ‘escalation’ of evolutionary tempo that devices, a move from buffer zone fueled rapid origination of many taxa. towards predatory camp. Recently Even in the human society (see the Tsudy et al (1998) observed news paper clipping at the outset) “arms morphological changes in a lobster race” initiates not only a tit-for-tat Hoploparia from the Late Cretaceous, policy, but also escalates piling up of Antactica. The spines of the older huge armaments within a short period species had gradually become absent of time. Vermeij (1977) has and delicately constructed claws have demonstrated this fundamental change been modified to robust ones in the in the community reorganization, younger species. This perhaps suggests involve very brief geological time a gradual transformation of the intervals, in comparison to a relative ancestral prey community to a stasis of the morphological consistency predatory descendant, since spines are that spanned for hundreds of millions of basically produced as a defensive, years. Gould (1990, 2002) admits that adaptation whereas robust and coarsely the Mesozoic marine revolution ornate claws appear to be a predatory produced trends, which were biotically acquisition. controlled and adaptive. He wonders that how could this trends be REMARKS accomplished; whether it is supposedly The above discussion suggests gradual, involving anagenetic escalation that the major organization of life, or it demands a punctuational especially of the marine communities, reinterpretation. He argued that this had assumed a new look since rapid modernization of the prey and the Mesozoic onwards. Every major group, predator can be explained by “ belonging to either prey or predator macroevolution as a process based upon community, responded to the Mesozoic geologically rapid production of high marine revolution. The prey level individuals by punctuational communities, which evolved defense speciation as the primary units of mechanism, underwent a great and change” (Gould, 2002, p. 950). rapid diversification (see Table. 2) and Jablonski and Bottjer (1990 a, b) those, which failed to adopt effective demonstrated that the evolutionary resistance, dwindled slowly or excluded innovations of the post-palaeozoic to placid areas where they became less major benthic invertebrates took place

21 SUBHENDU BARDHAN AND DEVAPRIYA CHATTOPADHYAY on the shelf region. The major novelties Permean resulted in large-scale at higher taxonomic level arose in the destruction of many shelf areas, and the onshore areas (nearshore to inner shelf), life on the earth received the biggest which dramatically increased since the jolt (about 97% of the marine species Jurassic. Vermeij (1977) stressed that died). Conversely, since the Jurassic the Jurassic predators mainly colonised onwards continents started rifting and in shallow water. He also envisioned consequently there arose a bewildering that this rapid coevolution of the prey array of taxa following the species-area and the predator could be explained by effect. Hallam (1973) recognized that macroevolutionary theory (Stanley, other factors such as increase of 1975, 1977). The driving force which ecological niches, reproductive Stanley called species selection, isolation between the population now explains the long-term trends acquired separated by oceanic barriers and by both the prey and the predators. competition among organisms to Stanley (1979) also believed that the occupy similar niches are responsible concomitant rise of the marine crabs, for the rapid increase in the diversity of teleost fishes and carnivorous the organisms during the continental gastropods in Late Mesozoic had a fragmentation. The diversity curve great effect on the rapid evolution of (Condie, 1989, Fig. 11.26) also reveals modern bivalves. The large-scale the exponential rise of invertebrate adaptive trends of bivalves and other families since the Jurassic. Vermeij marine prey communities may be (1977) also considered latitudinal explained by the species selection, steepening of the climatic gradient guided by predation, following Stanley (note that the length of continents were (1979, p.200-202). Recently, Miller longitudinally aligned) and the tropical (1998) and Jablonsky (1999) reaffirmed settings of the Mesozoic continents as that the escalation of arms race did take other causal factors. It is well place “far more abruptly” and recognized that the biotic diversity evolutionary trend is nothing but “a varies across latitude, attaining its summation of punctuational events”. widest range near the Equator. Besides, Why was Jurassic the time of Jurassic heralded an age after one of the life’s great reorganization? Vermeij major mass extinction events, the end- (1977) this time, sought answer not in Triassic. The mass extinction opened up the biotic factors but in a physical ecological opportunities for the attribute and its aftermath – continental survivors, and the might account for the fragmentation. Valentine and Moore diversity and novelties (cf. Jablonski (1970) have correlated the diversity of and Bottjer, 1990a). marine invertebrate with the patterns of continental assembly and break up POSTMORTEM throughout Phanerozoic (see Condie, Defense is the self-right. What 1989, Fig. 11.26). Aggregation of is significant is the “escalation” of the continents reduces habitable space, diversity of those who fought back. thereby causing fall of organic Those who failed did not go extinct but diversity. On the other hand, gradually lost diversity or slowly continental fragmentation increases migrated to placid areas. more habitable shelf areas and can The Mesozoic marine revolution promote rapid diversity. This is exactly has shifted the emphasis from the what happened time and again in the traditional Darwinian competition to Phanerozoic history of life. The predation as the likely biotic agent of formation of Pangea II in the end-

22 THE MESOZOIC MARINE REVOLUTION: AN OVERVIEW large-scale evolution, at least, since the Verlogsbuchhandlung, Stuttgart, Jurassic. p. 303-316 In ecological theory, predation Bardhan, S., Gangopadhyay, T.K. and may promote diversity in an organic Mondal. U. 2002: How far did community by relieving resource India drift during the Late limitation (Paine, 1966). The Mesozoic Cretaceous?- Placenticeras marine revolution may be seen as a kaffrarium Etheridge, 1904 scaled-up and complex version of the (Ammonoidea) used as a ecological theory in spaciotemporal measuring tape. Sedimentary background. Geology, 147, p.193-217 The Mesozoic marine revolution Bardhan, S. and Halder, S. 2000: did not pertain to any single, sustained Sudden origin of ribbing in trend to the prey communities, instead, Jurassic Paracenoceras there arose many trends which are (Nautiloidea) and its bearing on sometimes opposite in nature. the evolution of ribbing in post- Mass extinction event could not Triassic Nautiloids. Historical derail the antipredatory trends acquired Biology, 14, 153-168 by the prey. The large-scale trends have Benton, M. J. 1983. Large-scale been explained by species selection and replacement in the history of predation was the driving force. life. Nature, 302, 16-17. Jurassic marks the “Bioevent Callomon, J. H. 1963: Sexual par excellence” since it was the time of diamorphism in Jurassic continental fragmentation which ammonites. Leicester Literary increased the shelf areas. Onshore was and Philisophical society the site of major morphological transactions, 62, p. 21-56 innovation. Condie, K. C. 1989: Plate tectonics and crustal evolution, 3rd ed. ACKNOWLEDGEMENTS Pergamont press, 476p. Chamberlain, J. and Westermann, S. Das, Indian Statistical G.E.G. 1976: Hydrodynamic Institute, Kolkata and P. Roy, Jadavpur properties of cephalopod shell University helped at various stages. D. ornament. Paleobiology 2 Rudra, Kolkata critically read the Checa, A. 1985: Los Aspidaceratiforms manuscript and provided valuable en Europa ( Ammonitina, Faun. suggestions. Aspidoceratidae: Subfamilies Aspidoceratinae y REFERENCES: Physadoceratinae). Thesis, fac. Cien., Univ. Granada, 411p. Ager, D.V. 1976: The nature of the Cherns, L. 1979. The environmental fossil record. Proceedings of significance of Lingula in the Geological association, 87, p. Ludlow Series of the Wedsh 131-159 Borderland and Wales. Lethia, Bandel, K. and Kulicki, C. 1985: 12, p. 35-46. Belemnoteuthis polomica : A Clarkson, E.N.K. 1999: Invertebrate belemnite with an aragonitic Palaeontology and Evolution, rostrum. In Wiedmann, J. and Blackwell Science, UK, 452p. Kullmann, J. (eds), Cowen, R., German, R. and Wiggett, G. Cephalopods: Present and past. 1973: Camouflage patterns in Schweizerbartsche Nautilus and their implications

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