Paleontological Society
The Mesozoic Marine Revolution: Evidence from Snails, Predators and Grazers
Author(s): Geerat J. Vermeij
Reviewed work(s):
Source: Paleobiology, Vol. 3, No. 3 (Summer, 1977), pp. 245-258
Published by: Paleontological Society
Stable URL: http://www.jstor.org/stable/2400374 .
Accessed: 10/03/2013 16:48
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .
http://www.jstor.org/page/info/about/policies/terms.jsp
.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of
content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms
of scholarship. For more information about JSTOR, please contact [email protected].
.
Paleontological Society is collaborating with JSTOR to digitize, preserve and extend access to Paleobiology.
http://www.jstor.org
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
Paleobiology.
1977.
vol. 3, pp. 245-258.
The Mesozoic marine revolution: evidencefrom
snails, predatorsand grazers
Geerat J. Vermeij
Abstract.-Tertiary and Recent marine gastropods include in their ranks a complement of
mechanically sturdy forms unknown in earlier epochs. Open coiling, planispiral coiling, and
umbilici detract from shell sturdiness,and were commoner among Paleozoic and Early Mesozoic gastropods than among younger forms. Strong external sculpture, narrow elongate apertures, and apertural dentition promote resistance to crushing predation and are primarily associated with post-Jurassicmesogastropods, neogastropods, and neritaceans. The ability to
remodel the interiorof the shell, developed primarilyin gastropods with a non-nacreous shell
structure,has contributed greatly to the acquisition of these antipredatoryfeatures.
The substantial increase of snail-shell sturdiness beginning in the Early Cretaceous has
accompanied, and was perhaps in response to, the evolution of powerful, relatively small,
shell-destroyingpredators such as teleosts, stomatopods, and decapod crustaceans. A simultaneous intensificationof grazing, also involving skeletal destruction, brought with it other
fundamental changes in benthic communitystructurein the Late Mesozoic, including a trend
toward infaunalization and the disappearance or environmental restrictionof sessile animals
which cannot reattach once they are dislodged. The rise and diversificationof angiosperms
and the animals dependent on them for food coincides with these and other Mesozoic events
in the marine benthos and plankton.
The new predators and prey which evolved in conjunction with the Mesozoic reorganization persisted through episodes of extinction and biological crisis. Possibly, continental
breakup and the wide extent of climatic belts during the Late Mesozoic contributed to the
conditions favorable to the evolution of skeleton-destroyingconsumers. This tendency may
have been exaggerated by an increase in shelled food supply resulting from the occupation
of new adaptive zones by infaunal bivalves and by shell-inhabitinghermit crabs.
Marine communities have not remained in equilibrium over their entire geological history.
Biotic revolutions made certain modes of life obsolete and resulted in other adaptive zones
becoming newly occupied.
GeeratJ. Vermeij. Departmentof Zoology. University
of Maryland,College Park,Maryland
20742
Accepted: February 21, 1977
Introduction
When we view the historyof life fromits
beginningssome three billion years ago, we
seem to witness a pattern of comparatively
sudden revolutionsinterspersedwith long intervalsof relative quiescence. The most notable revolutions,the development of hard
parts in the Early Paleozoic and the marine
events of the Late Mesozoic, are not the instantaneous take-overs or inventions with
which we identifyrevolutionsin human history,but lasted tens of millionsof years; yet,
these episodes are shortrelative to the hundreds of millionsof yearswhen comparatively
littlefundamentalchange took place in communityorganization.
In the Early Cambrian, diverse marine
groups developed skeletonsof calcium phosphate, calcium carbonate, and silica. Some
groups were earlier in this developmentthan
others (for a review see Stanley 1976a), but
by the Middle Cambrian most groups which
were to play an importantrole in the fossil
record had become skeletonized. By early
Ordoviciantime,marinecommunitieshad acquired fundamental characteristics which
theywould retainformorethanthreehundred
millionyears duringthe remainderof the Paleozoic and Early Mesozoic. During this
period, reefscame and went (for reviews see
Newell 1971; and Copper 1974), and groups
diversifiedand declined; but mostmarinebenthiccommunitieswere dominatedby epifaunal
1977 The Paleontological Society
Copyr.?
All rightsreserved
US ISSN 0094-8373
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
246
VERMEIJ
(surface-dwelling)or semi-infaunalelements
(Stanley 1972,1977).
Then, inexplicably,thingsbegan to change.
Beginning in the Jurassicand oontinuingat
an accelerated pace in the Cretaceous,
changesin life habits tookplace which fundamentally altered relationshipsamong organisms in shallow-watermarine communities.
These currentsof change were unaffectedby,
or only temporarilydelayed, by episodes of
extinction,including the crisis at the end of
the Cretaceous (Maastrichtian-Daniantransition). Stanley (1977) and Meyer and McCurda (1977) have already treated some
aspectsof thisreorganization,
and I have speculated on some curious changes in shell geometrywhichaffectedgastropodsin the Mesozoic (Vermeij 1975). The consensusreached
fromthese investigationsis that the intensity
of predationhas increased substantiallysince
theMiddle Mesozoic.
In this paper, I shall expand upon this
theme. From furtherevidence of skeletal geometryand otherdata, I shall argue that predation as well as grazing has intensifiedand
become more destructiveto skeletons;and I
shall ask, mostlyin vain, what triggeredthis
Mesozoic reorganization.
of the genera in the largely Paleozoic and
Early Mesozoic superfamilyPleurotomariacea
had umbilicate shells, while only 58 to 60%
of the genera in the Mesozoic and Cenozoic
Trochacea possess umbilici (Vermeij 1975).
Non-umbilicate shells with often relatively
high spires, placed by Knight et al. (1960)
in the Murchisoniacea, Subulitacea, and
Loxonematacea,were presentfromLate Cambrian or Early Ordovician time onward; but
the great expansion of the largely non-umbilicate mesogastropods and neogastropods
did not take place until the latterhalf of the
Mesozoic. Thus, archaeogastropodsstill predominated in Triassic faunas, but Jurassic
and Cretaceous assemblages already contained a large diversityof mesogastropods.
Siphonate neogastropods and higher mesogastropods constitutethe majority in some
Late Cretaceous and nearly all Cenozoic gastropod assemblages (Sohl 1964).
The trendin the reductionin frequencyof
umbilicate shells seems to reflect an overall increase in the mechanical resistance of
shells to crushing(Vermeij 1976). The large
umbilicusand highwhorlexpansionrate (W)
render the West Indian trochid Cittarium
pica vulnerableto predationby crabs at larger
shell diameters than the taxonomicallyand
ecologically related western Pacific Trochus
Trends in GastropodMorphology
niloticus,which has a lower W and a smaller
Tertiaryand Recent marinegastropodsdif- umbilicus(Vermeij 1976).
ferfromMesozoic and especially fromPaleoSeveral additional features of gastropod
zoic snails in many architecturalways and shell architecture
supportthethesisthatpredainclude in their diverse ranks a complement tion intensitydue to crushing enemies has
of mechanicallysturdyformsquite unknown increased since the Middle Mesozoic. The diin earliertimes. First,the incidence of shells versity,and especially the size, of bilaterally
possessingan umbilicus (cavity in the base of symmetrical(usually umbilicate) coiled shells
the cell created by the incompleteoverlap of among the gastropods has dramaticallydeadjacent whorls) has significantlydecreased creased since the Late Cretaceous (Vermeij
in the course of geological time (Vermeij 1975). Today, such planispiral shells are
1975). Paleozoic gastropod faunas were foundprincipallyin freshwater and on land,
heavily dominatedby archaeogastropodsand where theymay stillattaindiametersas much
by bilaterallysymmetrical
bellerophontaceans. as 5 cm. In the sea, however,all planispirally
(For the purposes of this paper, I shall here coiled snails are small (usually less than 0.5
regard Bellerophontaceaas belonging to the cm in diameter), and most are found among
algae, understones,or in the plankton. Predaclass Gastropoda,and follow for convenience
tionby shell crushingseemsto be unimportant
the classificationalscheme of Taylor and Sohl for very small snails (see e.g.
Hobson 1974;
(1962). Runnegar and Pojeta (1974) have Stein et al. 1975) and is likelyto be of greater
presented argumentsin favor of transferring consequence forsnails living on exposed rock
the bellerophontsto the Monoplacophora;see surfacesthan forthose living among algae or
also Golikovand Starobogatov(1975) forfur- underrocks (Vermeij 1974). In the lattertwo
ther discussion.) I have estimatedthat 74% habitats,constraintson rapid looomotionand
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
247
visual detectionlimitthe activitiesof such po- mals a measure of protectionfrompotential
tentialcrushingpredatorsas fishesand crabs. predators (see for example McLean and
Planispiral coiling among planktonic gastro- Mariscal 1973).
Open coiling was apparently much compods may be related to theirswimmingmode
of life and seems to be associated with rapid moner in the Paleozoic and Early Mesozoic
locomotion. Most planktonicpredators,more- than now. From various sources (Knight et
over,do not appear to use crushingas a means al. 1960; Wanberg-Eriksson1964; Yochelson
1971), I have counted some 18 to 20 genera
of prey capture.
Pre-Cretaceousseas, in contrast,oftensup- of Paleozoic, and 2 genera of Triassic gastroported large planispiral or near-planispiral pods with open coiling. Some of these, such
snails (Macluritacea, Euomphalacea, Bellero- as the Paleozoic Macluritella and various
phontacea, Pleurotomariacea,etc.), most of euomphalids,may have rested on soft muds
which were probablymembersof the benthic (Yochelson 1971), while others (e.g. the
epifauna (Vermeij 1975). At least in some Platyceratidae and the Late Devonian and
macluritaceansand euomphalaceans,theplani- Triassic Tubinidae) may have been sedentary
spiral geometrywas not associated with rapid reef-associatedforms (Bowsher 1955; Knight
locomotionbut ratherwith a sedentarymode et al. 1960).
of life on quiet bottoms(Yochelson 1971).
Paleozoic nautiloids and Mesozoic amRex and Boss (1976) have summarizedthe monoids also included in their ranks many
taxonomicdistributionof the 15 Recent spe- shells withopen and sometimesirregularcoilcies of gastropods exhibiting open coiling. ing, which could not have been well suited
Open coiling is defined by Rex and Boss for rapid swimming (Kummel and Lloyd
(1976) as regular coiling based on the loga- 1955). The only Recent externallyshelled
rithmicspiral, in which adjacent whorls do cephalopod (genus Nautilus) has rathertight
not touch one another;thus, such groups as coiling, and the only living cephalopod with
Vermicularia, Siliquaria, and Vermetidae, open coiling (Spirula) lives at moderwhose coilingis irregularand non-logarithmic, ate depthsand has an essentiallyinternalshell.
are excluded. Of the 15 Recent species, only It is very likely that the fragileopen coiling
8 are marine,3 are found in freshwater,and of fossil cephalopods would, if these animals
4 are terrestrial.From estimates of Recent were alive today, restrict them to great
molluscan species numbers given by Boss depths or to other marginal habitats where
(1971), I calculate that open coilingis found shell-destructive
predationis rare.
in about 1 out of every2,200marinegastropod
The ability to remodel the interiorof the
species, 1 out of every 1,000 fresh-waterspe- shell has contributedgreatlyto the increased
species sturdinessof Late Mesozoic and especially
cies, and 1 out of every3,750terrestrial
of shelled gastropod. The fresh-waterforms Cenozoic gastropods (Mesogastropoda, Neowith open coiling all occur in cold lakes, gastropoda,and Neritacea). Carriker(1972)
where crushing predation is rare (Vermeij has suggestedthatthe externalspinesof many
and Covich 1977). Most of the marineopen- muricidshells are resorbed by the left edge
coiled snails are found either in very deep of the mantle as the exteriorof the shell is
water (Lyocyclus, Epitonium) or in sand as- obliteratedfromview by theencroachinginner
sociated with cnidarians (Spirolaxis, Epi- lip duringspiral growth. Spines of this type
tonium). The habits of Extractrixand Cal- serveto increasethe effectivesize of the shell,
lostracum are not known but are probably and often strengthenit against crushing or
sandy or muddy, judging fromthe distribu- other destruction (Vermeij 1974 and refertion of other members of their respective ences therein). Without resorption or refamilies (Cancellariidae and Turritellidae). modeling, these spines and other collabral
Predation throughcrushingis probably rela- sculptural elements (those parallel to the
tively uncommon in most of these environ- outer lip) would protrudeinto the aperture
ments. Bright (1970), for instance, found and, if large enough,mightinterferewith refew shelled invertebratesin the diet of 81 tractionof the body into the shell. Although
deep-sea fish individuals he examined from such protrusionsare actually known in some
the Gulf of Mexico, and these were ingested fresh-watershells (e.g. Biomphalaria) and
whole. Cnidarians often give associated ani- land snails (Helicodiscus and other genera),
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
248
VERMEIJ
they are apparentlyexceedinglyrare among Jurassicand younger Neritidae (Neritacea);
marine gastropods. In the archaeogastropods and Jura-Cretaceous
high-spirednerineaceans.
(excluding Neritacea), where resorptionap- Yet, it is primarilythe Cretaceous and Cenopears to be poorly developed or altogether zoic mesogastropods and neogastropods in
absent,thisproblemcan be avoided by either which nodes, spines, and collabral ribs have
(1) covering the sculpture with a thick in- been most elaborately developed. Some
ductural glaze, or (2) producing shells with contemporaneoustrochid,turbinid,and cyclosreduced whorl overlap so that interference trematid archaeogastropods have also prowithpreviouslybuilt sculptureis minimal(see duced such sculpture(recall the trochidTecalso Vermeij 1973). The firstsolution de- tus, for example), but theirnumbersare less
mands a relativelybroad apertureand would impressive.
restrictthe sculptured surface to the body
Similarly, extensive development of prowhorl. Examplesofthesecond solution,which tectivedentitionon the innerface of the outer
implies a tall spire that can oftenbe cracked lip is predominantlya post-Jurassicinnovaby predators,are provided by the sometimes tion which, in such groups as Neritidae,
open-coiled, stronglyribbed mesogastropod Muricidae, and many other mesogastropods
Epitonium and by the trochidarchaeogastro- and neogastropodswould be impracticalif it
pod Tectus, which is sculpturedwith one or could not be secondarilyresorbed as the pomore spiral rows of knobs on the upper face sition of the growingedge moves in a spiral
of the whorlsand is furthercharacterizedby a direction. Withoutremodeling,teeth restrictspire unusuallyhigh for an archaeogastropod ing accessibilityinto the aperture could be
(apical half-angleof Palauan T. triseriatais developed only in the adult stage of species
26.30).
with determinategrowth,when spiral growth
In view of these and other limitationsim- has ceased. Indeed, such teethare commonly
posed by general shell geometryon sculpture seen in cowries (Cypraeidae), helmet shells
(see also Vermeij 1971, 1973), it is perhaps (Cassidae), and many tritons(Cymatiidae),
not surprisingthat few Paleozoic snails had as well as in many Paleozoic nautiloids and
shells in which nodes, spines, or strong col- Mesozoic ammonoids. These molluscs forlabral ridges were the dominant sculptural feited the luxuryof aperturaldefense during
elements. Examples of periodicallyproduced the active spiral phase of growth,when most
collabral lamellae are knownin some bellero- gastropods are particularly vulnerable to
phonts (the Middle to Upper Ordovician predation.
Phragmolites,the Middle Ordovician to SiluThe firstsnail withouter-lipdentitionseems
rian Temnodiscus,and the nearlyopen-coiled to be the Middle PermiansubulitidLabridens
Middle Silurian Pharetrolites). Collabral (Knight et al. 1960). The only other gastrothreads often associated with nodes or even pod with labial teeth to have evolved before
spines were developed in the Lower to Mid- the Late Cretaceous is the Upper Jurassicto
dle PermianportlockiellidTapinotoniariaand Upper CretaceoustrochidChilodonta. Within
by various Upper Devonian open-coiled Tu- the internallyresorbingNeritidae (Woodward
binidae. The high-spiredPseudozygopleuridae 1892), which arose during the Triassic, the
of theCarboniferousand Permianwere usually firstgenera to show dentitionon the outer
characterized by evenly spaced collabral lip (Myagrostoma,Velates, and Nerita) date
ridges.
fromsedimentsof Late Cretaceous age, when
In the pre-CretaceousMesozoic we see a most of the higher mesogastropodsand neolarger number of gastropods with collabral gastropods also differentiated
or expanded.
sculpture: some Triassic and JurassicHeliIn Conus, Olivella, Bullia, Ellobiidae, and
cotomidae (Macluritacea); Triassic Porcel- possibly other snails with markedlynarrow
liidae, Zygitidae, and Jurassic Pleuroto- and elongate apertures,extensiveinternalremariidae (Pleurotomariacea); open-coiled sorption of whorl partitions (Fischer 1881;
Triassic Tubinidae (Oreostomatacea); some Crosse and Fischer 1882; Morton1955) seconTurbinidae (Trochacea), Middle Triassic and darilywidens the shell cavityto accommodate
youngerCirridae and Amberleyidae(Amber- the visceral mass while at the same time efleyacea); high-spired Triassic and Jurassic fectivelyrestrictingentryinto the aperture.
Zygopleuridae (Loxonematacea), Middle Before the Cretaceous, relativelylong, nar-
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
249
row aperturesare knownin but a few isolated eitherwith great speed (cephalopods, heterogenera: the Lower Carboniferous opistho- pod gastropods) or with toxicityor unpalatbranch Acteonina, the Lower Carboniferous ability (many nudibranchs,onchidiids, perto Lower Permian Soleniscus and Middle haps some fissurellids?). Even in cowries
Permian Labridens (Subulitiidae), and the (Cypraeidae), in which the well-developed
Lower Jurassicto Upper Cretaceous neritid shellis oftencoveredduringlifewiththe manPileolus (see Knightet al. 1960). The great- tle, Thompson (1969) demonstrated the
est diversityof snails with slit-likeapertures existenceof acid-secretingcells whichmay disis found in the post-Jurassiccypraeids,vexil- couragepredationby fishes. (See also Thomplids, conids, mitrids, olivids, columbellids, son 1960). Thus, internalizationand loss of
marginellids,and even strombids.
the shellmayhave been alternativesolutionsto
It may thus be concluded that Neritacea, the problem of increased predation intensity
mesogastropods,and especially neogastropods on molluscs.
have, by evolving and taking advantage of
the capacity to remodel the shell interior, GastropodPredators
significantlybroadened the range of shell
There is good reason to believe that the
types that were available to earlier archaeoincrease
in snail-shellsturdinessbeginningin
gastropods. In particular, remodeling has
enabled these snails to acquire combinations the Cretaceous and continuingthrough the
of shortspires,narrowapertures,strongexter- Tertiaryhas accompanied, and was perhaps
nal sculpture,and apertural dentitionwhich in responseto, the evolutionof powerful,relarenderthe shellrelativelyimperviousto preda- tively small, shell-destroying(durophagous)
tion by crushing or other shell-destructive predators. Table 1 summarizesthe geological
modes of attack. In most archaeogastropods, origins of the major groups of present-day
possession of one architecturalantipredatory molluscivores,and shows that most of these
attributecompromisesanother,so thattheshell are in the Mesozoic era. Withinthe majority
is rarely as well defended (in a geometrical of durophagous groups (for example, in the
sense) as in many post-Jurassicsiphonate teleosts,brachyurans,birds, and drillinggastropods), the ability to destroyor penetrate
snails.
In passing, it is worth noting that all the shellswas not perfecteduntilLate Cretaceous
gastropodsin which internalremodelinghas time or even later (Sohl 1969; Vermeij 1977),
been employed extensively have a non- long afterthese groups firstarose. The Asnacreous shell structure. Currey and Taylor teroidea (sea stars) are the only group of
(1974) have shownthatnacre is in manyways importantRecent molluscivoreswith a known
mechanicallytougherand strongerthan other pre-Mesozoichistory,and theydo not employ
methodsto
typesof shell microarchitecture,
yet nacre ap- crushingor othershell-destructive
obtain
their
molluscan
prey.
Sea
stars inpears to be the primitivecondition in most
molluscanclasses (Taylor 1973). The intrigu- terpretedto have employed extraoraldigesing possibilitythatthe advantagesof remodel- tion co-occur with intraorallydigesting sea
ing in non-nacreousshells could have con- stars in Upper Ordovician rocks (see Carter
tributedto the replacementthroughtime in 1968).
There were, of course, durophagouspredamany lineages of the nacreous type of structure with other forms of microarchitecture torswhich affectedshelled molluscsin Paleozoic and Mesozoic communitiesbut are no
deserves furtherinvestigation.
Portmann (1967) and many others have longerwith us today. Several Late Devonian
pointedout thatthe externalshellhas been in- arthrodiresand arthrodirerelatives (e.g. Myternalized or entirelylost in a large number lostoma and the ptyctodonts)had jaw dentiof gastropod and cephalopod lineages. This tion in the formof a crushingpavement,as
loss is interpretedby these authors as a de- did a number of Late Devonian to Permian
emphasis of the shell as a protectivedevice. hybodontsharks. Some of the latterwere apIt is, of course,impossibleto know how wide- parentlyquite small fishes(e.g. Chondrenchespread thisloss was in the course of Paleozoic lys and Helodus) (Romer 1966). Hybodont
and Mesozoic history;but it does seem that sharksmay have been responsibleforthe disshell loss in Recent molluscs is associated articulation and shell breakage observed
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
250
VERMEIJ
1.
Origins and modes of predation used by
recent molluscivores.
TABLE
Asteroidea; extraoraland intraoraldigestion; arose and
became molluscivores Late Ordovician; Carter
(1968)
Dipnoi (fresh-waterlungfishes); crushing; arose and
became durophagous in Devonian; Thomson (1969)
Heterodontidae (sharks); crushing; arose and became durophagous in Jurassic; Romer (1966)
Batoidea (rays); crushing; arose Jurassic, became
durophagous in Cretaceous; Bigelow and Schroeder
(1953)
Stomatopoda (crustaceans); hammering and spearing; arose Jurassic, may have achieved durophagy
by late Cretaceous; Holthuis and Manning (1969)
Palinuridae (spiny lobsters) and Nephropidae (lobsters); crushing; arose Jurassic. date of acquisition
of durophagy uncertain; George and Main (1968)
Brachyura (crabs); crushing, apertural extraction;
arose Jurassic, achieved durophagy by Latest Cretaceous or Paleocene; Glaessner (1969), Stevcic
(1971), Vermeij (1977)
Aves (birds); crushing, swallowing whole, wrenching; arose Late Jurassic, were molluscivorous by
Late Eocene; Cracraft (1973)
Muricacea (gastropods); drilling, apertural extraction; arose Albian (Early Cretaceous), drilling by
Campanian (Late Cretaceous); Sohl (1969)
Naticacea (gastropods); drilling; arose Triassic, drilling by Campanian (Late Cretaceous); Sohl (1969)
Other Neogastropoda; apertural extraction; arose
Early Cretaceous, molluscivory certainly established by Late Cretaceous; Sohl (1964, 1969)
Cynatiidae (Mesogastropoda); apertural extraction;
arose and became molluscivorous Late Cretaceous;
Sohl (1969)
Actinaria (sea anemones); swallowing whole; nothing
known of fossilrecord
Teleostei (bony fishes); crushing, wrenching, swallowing whole; arose Triassic, durophagy by Late
Cretaceous or earliest Tertiary; Schaefferand Rosen
(1961)
amongsome thick-shelled
trigoniacean,heterodont,and taxodont-hinged
bivalvesin the Park
City Formationof the Lower Permianof Wyoming (Boyd and Newell 1972). Earlier in
the Paleozoic, cephalopods may have been importantmolluscivores,but no record of their
activitiesremains.
Probable Mesozoic durophages include the
remarkableTriassic marineplacodont reptiles
(von Huene 1956), the Triassic ichthyosaur
Omphalosaurus;the Late Cretaceousmososaurid lizards, especially the genus Globidens
(see Kauffmanand Kesling 1960); and the
Cretaceous ptychodontoid sharks (Romer
1966). Kauffman (1972) believes ptychodonts to have been importantpredators on
inoceramidbivalves (see also Speden 1971)
and has described some suggestive toothmarkson these large shells. Tooth-markson
the rostraof Jurassicbelemnitesfromsouthwest Germanyare also thoughtto have been
made by various fishes (Riegraf 1973).
It is, of course,difficultto assess the impact
of extinctpredators;yet, the large numberof
taxa which have perfecteddurophagyin the
Cenozoic suggeststhat shell-crushinghas become a relatively more importantform of
predationon molluscsover the course of time.
Westermann(1971) noted that the frequency
of repaired shell injuries among Mesozoic
ammonoidswas less than the 19% frequency
reportedby Eichler and Ristedt (1966) for
juvenile Recent Nautilus pompilius. Preliminary resultsfromstudies on repaired injuries
in high-spiredCretaceous and Cenozoic gastropod shells (Vermeij, Zipser, and Dudley,
in preparation) point to the same conclusion.
Moreover,drillingappears to be a relatively
new form of predation invented by gastropods and octopods in the Late Cretaceous
(Sohl 1969). Problematical perforationsin
Paleozoic shells, especially brachiopods,
seem in most cases to have been made after
death of the affected animal and therefore
did not constitutepredation (Carriker and
Yochelson1968; Sohl 1969). Even if the boreholes observed by Rohr (1976) in Silurian
brachiopods of the genus Dicaelosia were
made duringthe life of the brachiopod,they
occur in less than 3% of the population, and
were thus extremelyrare compared to the
holes made in Tertiaryshells.
Infaunalizationand Grazing
Stanley (1977) has summarizedadditional
changes in the compositionand structureof
marinebenthic communitiesthroughgeological time. Foremost among the long-term
trends recognized by him is what may be
labeled an infaunalizationof soft-bottom
benthic animals, which becomes particularly
noticeableduringthe Late Cretaceous. In the
Paleozoic, many brachiopods and stalked crinoids lived on the surfaceof,or were partially
buried in, subtidal muds. In the Mesozoic,
the epifaunal reclining habit is commonly
seen in inoceramidbivalves. From the Late
Cretaceous onward, however,these epifaunal
and semi-infaunalelementshave been largely
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
251
replaced by infaunalforms(see also Rhoads survivingcrinoidsin shallow water are post1970). Among bivalves, for example, there Permian comatulids which can change their
has been a relative decrease in the diversity position at will and are able to attach themof endobyssate (bysally attached semi-infau- selves facultativelyby means of the cirri (see
nal) formssince the Ordovician, and a cor- also Meyer and McCurda 1976).
responding dramatic increase in infaunal
Increased epifaunal predation may well be
siphonate bivalves since the Paleozoic and partly responsible for these far-reaching
especially the Late Mesozoic (Stanley 1968, changes in benthic community structure
1970, 1972, 1977). Gastropodsand echinoids (Stanley 1977; Meyer and McCurda 1977),
exhibiteda similar,disproportionateinfaunal but I am inclinedto thinkthatheavier grazing
diversification
in the Jurassicand Cretaceous pressureshave had a moreprofoundinfluence
(Kier 1974; Stanley 1977). All these changes (see also Garrett1970). Two groupswhichtomay reflect intensificationof predation or day contain quantitativelyimportantgrazers,
other sources of mortalityat and above the the teleostean fishes and echinoid echinosediment-water
interface.
forces
derms,have apparentlybeen significant
A furtherindication of this comes from in shallow-watercommunitystructureonly
architecturalchanges in the epifauna itself. since the Late Mesozoic. Teleosts arose in the
Waller (1972) noted thatmostPaleozoic pec- Triassic,but the criticalmorphologicalbreaktinacean bivalves (scallops) were character- throughspermitting
themto browse algae, nip
ized by prismatic shell structure;sculpture coral polyps, and scrape hard surfaces were
consistedof radial thickenings(costae). Dur- not perfecteduntil the Cretaceous (Schaefing the Mesozoic, shallow-waterpectinaceans fer and Rosen 1961). The pycnodonts,an
leading to the present-dayPectinidae became early (Jura-Cretaceous)holosteanexperiment
increasinglycharacterizedby a foliated cal- in grazing and browsing,had teeth perhaps
citic structure,which permittedthe develop- adapted for breakingoffprotrudingparts of
ment of radial crinkles or folds (plicae).
invertebrates(Romer 1966). (In a reinterpreThese, in turn, permit the necessarily thin tation of pycnodonts,Thurmond (1974) sugshell of these swimmingbivalves to be but- gests that the Jura-CretaceousGyrodusgroup
tressed against what Waller (1972) believed was characterized by a shearing dentition,
to be an ever increasing number of shell- while the European TertiaryPycnodus group
destroying
predators.
had strictlycrushingteethadapted forfeeding
Brachiopodstoday are foundmostlyin cryp- on small shelledinvertebrates.)However, the
tic temperateand deep-sea environmentsbut scarids,acanthurids,kyphosids,and othertypiin the Paleozoic and pre-Cretaceous Meso- cal grazersand browsersof tropicalreefs are
zoic were dominantelementsof hard- as well apparentlyof latestCretaceous or,moreprobas soft-bottom
epifaunal assemblages. C. W. ably, of earliestTertiaryextraction(see Hiatt
Thayer has pointed out to me that, when a and Strassburg 1960; Romer 1966; Hobson
brachipod which normallylives attached by 1974). These fisheshave a profoundimpact
a peduncle becomes dislodged by some ex- not only upon the algae which they eat, but
ternal agent, it cannot reattach itself and is equally on other epifaunal organismswhich
thereforefar more likelyto die than is a bys- are scraped or sheared offthe rock along with
sally attached bivalve, which can in principle the algae (see, for example, Stephensonand
re-establishitselfafterbeing tornloose. It is Searles 1960).
thesebyssallyattachedbivalves,togetherwith
Sea urchins (Echinoidea) arose no later
the post-Permianoysters and other bivalves than the Late Ordovician but were not comcemented with one valve to the underlying mon in intertidalor shallow-watercommunisubstratum,that have come to predominate ties untilthe latterhalfof the Mesozoic (Kier
in Mesozoic and Cenozoic epifaunal assem- 1974; Bromley1975). For example,theywere
blages. In the same way, stalked crinoidsare not the importantdestroyersof reeflimestone
today restrictedto the deep sea but were im- in the Paleozoic that they are in reefs of the
portant constituentsof Paleozoic shallow- present day (Newell 1957; Copper 1974).
water bottom communities. They probably Like grazing fishes, echinoids scrape rocks
cannot reattachonce dislodged and gave way bare of macroscopicalgae and epifaunal anito otherorganismsin the Mesozoic. The only mals and are known to have a profoundin-
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
252
VERMEIJ
fluence on the compositionand architecture
of tropical as well as temperatehard-bottom
communities(see e.g. Sammarco et al. 1974;
Dayton 1975). The Aristotle'sLantern, with
whichhard surfacesare scraped by the urchin,
began its developmentas the perignathicgirdle in the Permianbut was not perfecteduntil
shortlybefore the Maastrichtianin the Late
Cretaceous, at which time the pentaradial
traces characteristicof modernechinoid grazing first became common in shallow-water
communities(Bromley1975).
Grazing chitonsand gastropods,which today have less impact on the epifauna than
do sea urchinsand teleosts (Stephenson and
Searles 1960; Dayton 1975), have probably
been present in shallow-waterand intertidal
communitiessince the Early Cambrian. Althoughcertaindeeply scouringlimpets (postPermian Acmaeidae and Patellidae) may be
able to graze the algal turfto a lower height
than can othergastropods,I doubt that grazto
ing gastropodshave contributednmaterially
the demise of the brachiopods and stalked
crinoids,or to their restrictionto crypticor
deep-waterenvironments.The relativeimpact
of other, post-Paleozoic and usually postCretaceous, grazers among crabs, mammals,
birds, and reptileshas not been investigated
thoroughlyeven in Recent communitiesand
cannot be evaluated for ancient assemblages.
Other Mesozoic Changes
Reefs have developed at various times in
reefsdiffer
the Phanerozoic,but post-Jurassic
in many importantways fromall earlier versions of this community.Not only were rockdestroyingfishes and echinoids absent or
unimportantin Paleozoic reefs,but the structure of modern reefs is far more cavernous
than that of Paleozoic and perhaps even Late
Cretaceous rudist reefs (Jackson et al. 1971;
Kauffman and Sohl 1974). Copper (1974)
has noted that such fast-growingpalmate or
highlybranched reef builders as the presentday acroporid and pociloporid corals were
unknownin Paleozoic reefs. Skeletonsof this
type probably contributeheavily to the creation of caves and other intersticesand did
not arise among corals until later in the Cretaceous. Possibly they reflect more intense
competitionforlightthan was typical of reef
buildersin earlier epochs.
Two ecologically important communities,
the sea-grass bed and the mangrove swamp
or mangal,were not presentbeforeLate Cretaceous time (see Brasier 1975). The flowering plants which give these communitiestheir
names possess rootswhich stabilize and baffle
the sediment,thus providinga habitat for a
great diversityof marineorganisms.
In benthic communitiesas a whole, many
groups (echinoids, gastropods,bivalves, crustaceans, fishes) seem to have diversifieddramatically beginning in the Middle Jurassic
and continuingthroughthe Cretaceous and
Tertiary periods. This diversificationis so
widespread and pervasive that I am inclined
to concur with Valentine (1969) that it is a
real phenomenonand not merelythe consequence of preservationalbiases (see Raup
1972 fora carefuldiscussionon thispoint).
The alterationswhich affectedmarinecommunitiesduringthe Mesozoic were not limited
to the benthos. Beginning in the Jurassic,
therewas a markedexpansionin the diversity
of marine microplankton,including the appearance of the firstplanktonicForaminfera
and Coccolithophorida; planktonic diatoms
joined the assemblagein the Cretaceous (for a
review see Lipps 1970).
Events on land are more spread out over
geological time than were those in the sea.
With the evolution of endothermyamong
therapsid reptiles in the Permian and probably dinosaursin the Triassic came important
alterationsin trophic energy transferwhich
were to persist,witha shortexceptionalperiod
in the Paleocene, to the presentday (Bakker
1972, 1975). Dinosaurs evolved cursorial
(fast-running)habitsby Middle or Late Triassic time,and large cursorialvertebrateswere
importantconstituentsof terrestrialcommunities throughoutthe rest of the Mesozoic and
Cenozoic, again exceptingthe Paleocene (Bakker 1975). The only events on land which
coincide in time with the Late Mesozoic maline reorganizationare the evolution in the
Early Cretaceous of angiosperms,theirrapid
rise to dominancein the Late Cretaceous and
Cenozoic (Muller 1970), and the unprecedented radiation of insects which pollinated
their flowers and ate their leaves (Ehrlich
and Raven 1964). The diversificationof
birdsmay also be related to the rise of angiospermsand insects (Morse 1975).
Not all groups were, however, affectedby
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
253
scene are more likelyto become extinctor to
be pushed into marginal habitats than are
thosewhichcan successfullycoexistwithpredators and competitors. In other words, the
processwhich Stanley (1975, 1977) has called
species selection may well account for the
long-termtrendtoward greaterpredator-prey
and competitor-competitor
coadaptation. If
this same species selection is to account for
the Late Mesozoic communityreorganization
(Stanley 1977), then it is surprisingthat the
various seemingly independent events contributingto it did not take place at widely differenttimes but rather took place more or
less in concert;and we mustwonder why the
eithercame so
criticaladaptive breakthroughs
late
in
time
or
lay
dormant
for
tens
to hundreds
Discussion
of millionsof years before spawning a major
Throughoutgeological time,therehas been diversification.In otherwords, the Mesozoic
a tendencyin many skeletonized groups for revolution,recognizedby the preferentialsurmorphologicallysimple, unadorned formsto vival of powerfulconsumersand well-armed
give rise to, or to be replaced by, types with prey over species less well adapted to predamore elaborate skeletons. These elaborate tion, reflectsunusually intense species selecformsare thenlargelyobliteratedin the major tion; it upset the status quo which had been
episodes of extinction,and the process begins established since the Early Paleozoic. The
anew. Thus,Valentine(1973) has commented species selectionwhich prevailed during this
thatthe skeletonsof Lower Cambrianbrachio- long intervalof "equilibrium"produced more
pods, trilobites,and molluscsare oftensimple powerful or more elaborate variations on a
("grubby,"in his terminology),while Permian few adapted themes but produced very few
representativesoften have elaboratelysculp- new themes. Thus, I envision one of a few
tured or otherwisehighly"specialized" skele- physicalor geographicaleventsas havingpertons. After the Permo-Triassic extinctions, mitteda degree of speciationand coevolution
Early Triassic fossils are once again simple, that would not have been possible under earwhile Cretaceous skeletonsare often bizarre lierconditions.
and, in the case of ammonoidswith complex
In the Early Paleozoic, we can point to
suturesor irregularcoiling,even a bit rococo. several events which could have triggered,
The frequentextinctionswhich have ravaged or at least greatlyspeeded up, the diversificathe planktonicworld have affectedprimarily tion of the Metazoa and the developmentof
the elaborate and the adorned forms,and it hardpartsin manyoftheirlineages. Skeletoniis generallythe morphologicallyconservative zation in the Cambrian is broadly correlated
types which survive and rediversifyafteran with the demise of stromatolites
and with the
episode of extinction (Lipps 1970; Cifelli greater activityof grazers, small burrowers,
1976; Fischer and Arthur1977).
and perhaps predators (Garrett 1970; AwraIs this gradual process of skeletal elabora- mik 1971; Stanley 1973). Rhoads and Morse
tionand specializationcomparableto the revo- (1971) have conjecturedthat these developlutionaryevents in the Early Paleozoic and mentswere made possible when the dissolved
Late Mesozoic? I believe not. The long-term oxygen concentrationexceeded about 1 ml
skeletal specializationmay be one expression 02 per liter of water, since calcificationat
of a continuingprocess of coevolutionor co- lower dissolved oxygenconcentrationswould
adaptation,in which predatorsincrease their have unacceptably compromisedother comprey-capturingefficiency,while the prey are peting functionsinvolvingcalcium (see also
continuallyseeking ways to evade, repel, or Towe 1970). Stanley(1976b) has furthersugotherwisethwarttheir enemies. Species less gested that the inventionof sex late in the
well adapted to the constantlychangingbiotic Precambrian promoted both speciation and
the Mesozoic reorganization. S. A. Woodin
has pointed out to me that,judging fromthe
meagerfossilrecord,mostpolychaetefamilies
were established in the Early Paleozoic and
thatno significantor detectablemorphological
changes have taken place among the worms
since then. Nuculacean bivalves, inarticulate
brachiopods,and other groups characteristic
of physiologicallystressed or marginal environmentsseem also to have remainedmuch
the same morphologicallythroughtime. Althoughfurther,more detailed studies are required, it seems that the most profound
changes affectedcommunitiesin physiologicallyfavorableenvironments.
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
254
VERMEIJ
adaptive radiation,diversifying
what by mod- created conditionsfavorableto the revolution
ern standardsmust have been a monotonous (for a review of climate see Cracraft1973).
biota.
Again, however,it must be recalled that mild
What featuresmade the Middle Mesozoic climaticepisodes may have characterizedthe
earth so special that skeletal destructionde- Devonian and perhaps otherPaleozoic epochs
veloped or became more importantamong withoutinitiatingmajor upheavals in marine
both predatorsand grazersin shallow benthic community organization. Furthermore,inenvironments?In attemptingto account for tense grazing and predation by crushingare
the concomitantburstof biotic diversification typicalof Recent tropicalmarineassemblages
in the Middle and Late Mesozoic, Valentine despite a steep latitudinalgradientin climate
(1969) and Valentine and Moores (1970) and the large extentof temperateand polar
pointed to the breakup of continentsbegin- oceanic waters.
ningin theJurassicand to the gradual steepenIn short,continentalbreakup and long-lasting of the latitudinalclimaticgradientduring ing favorableclimatemay have created condithe Tertiary. These tectonic and climatic tions favorable to the evolution of skeletonevents created biogeographical provinces destroyingpredators and well-armoredprey
where only one or a few had existed before and had far-reaching
consequencesforbenthic
and thuspromotedgeographicalisolationand marinecommunitiesas a whole. Whetherthe
subsequent speciation. Moreover, the result- Mesozoic era differedfundamentally
fromthe
ing constantraisingand loweringof geographi- Paleozoic in these respectsremainsto be decal barrierswould have led to even more iso- termined,and the problem of dormantadaplation, differentiation,
and eventual contact tive breakthroughsis not yet satisfactorily
with species which had previously evolved solved.
under differentbiological regimes. This conLipps and Mitchell (1976) and Fischer and
tinual biological rearrangementand oppor- Arthur(1977) have independentlypointed to
tunityfor speciation could promote coevolu- the diversificationof very large open-ocean
tionand coadaptationand speed up the spread predatorsduringMesozoic and Tertiarypolyof a major adaptive breakthrough.
taxic episodes. During these timesof high diSpeciation would have been even more versityand reduced oceanic circulation,the
favoredif ocean circulation(and thus plank- prey populations upon which the very large
tonic larval dispersal) were reduced during predators depended must have been large
periodsof high diversity(polytaxicepisodes), enough and stable enough to permitexploitaas has been suggestedby Fischer and Arthur tion by a specialized animal. Many of the gi(1977). Slow circulationand high diversity, ganticconsumersbecame extinctduringoligomoreover,were generallyassociated withhigh taxic episodes (periods of low diversityand
stands of sea level and, therefore,with large more rapid oceanic circulation) and were
areas available foroccupation by benthicand thereforeonlyephemeralelementsin the complanktonicmarine life (Fischer and Arthur munity. In this way, they differimportantly
1977; Valentine and Moores 1970). It is im- from the benthic products of the Mesozoic
portantto remember,however,that episodes revolution,since these animals persisted in
of provinciality
had occurredin earlierepochs spiteof theperiodiccrisesthatbeset the biotic
-the Late Ordovician and Permian,for ex- world as a whole. The resourcesupon which
ample-without resultingin the kind of re- the new predators depended were therefore
organizationof communitieswitnessedin the more permanent and more reliable through
Mesozoic.
time.
The events which shaped the Mesozoic
The gradual occupation of new adaptive
revolutionprobably took place in a tropical zones may have contributedto the evolution
setting,since some of the most characteristic of new and more specialized predators. Stansymptoms(intense grazingby teleosts,preda- ley (1968) has documented the invasion of
tion by crushing) are today predominantly deep sedimentsby shelled bivalves. Though
warm-waterphenomena (Earle 1972; Vermeij this invasion began in the Early Paleozoic, it
1977). Hence, one could argue that the per- was primarilya Mesozoic phenomenonassocihaps unusually benign climate during much ated with the evolution of siphons through
of the Mesozoic (at least in polytaxictimes) mantle-lobefusion. This ecological expansion
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
255
mayhave led to an overallincreasein the avail- criteriafor hermit-craboccupation would be
abilityand abundance of prey protectedby a established,then the proportionof hermited
hard shell. Whethersuch an expansionwas in- shells in a given fossil assemblage may give
dependentof, or correlatedwith,the appear- some relativeindicationof the extentto which
ance of more specialized predatorsremainsan the supply of shelled prey is constitutedby
hermitcrabs.
open question.
The evolution of hermitcrabs would not
Anotherexample of a possible increase in
shelled food supply,and of the occupation of explain why drilling was developed among
a new adaptive zone, is the evolutionand di- predatorygastropods and octopods, since at
versificationof hermit crabs (Paguridea). least gastropodsdo not normallydrillhermited
These crustaceans,which are knownfromthe shells. However, the adaptive expansion of
Jurassiconward (Glaessner 1969), normally the bivalves may possibly be connected with
live in the discarded shells of snails but do the developmentof thisnew methodof predanot usually feed on the previous adult in- tion.
Finally, the consequences of the Mesozoic
habitantsof theirdomiciles. As a result,hermit crabs could have enormouslyextended communityreorganizationunderscorethe fact
the ecological life-spanof the average snail that what ecologists perceive as long-term
shell, thereby dramatically increasing the equilibria in communitiesmay fromtime to
shakenby revolutionary
numberand abundance of shelled prey. This timebe fundamentally
effect,which would be particularlystrongin events. Not onlyis the functionalarchitecture
the tropics (where most hermitcrabs live to- of componentspecies in a communityaffected
day), could permitpredatorsto specialize on by these events but so are such community
shelled prey where such specializationwould properties as species diversityand trophic
have been trophicallyunfeasible before the structure.Certain modes of life become obhermitcrabs arose. The propensityof shell- solete or restrictedto a small numberof marcrushing fishes, crabs, and other predators ginal environments,while other adaptive
(which take both hermitcrabs and snails) to zones are newly occupied and previouslyunattacklivinggastropodpreytoo large forthem tapped resources are newly exploited. From
to crush,a commonphenomenontoday (Ver- present evidence, it seems that periods of
meij 1976; Miller 1975), would be encouraged equilibrium have been interruptedby deif attackson hermitedshells of equal size are stabilizingrevolutionsand that these revolusometimessuccessful. In such cases, the her- tions are not strictlyconnected with the mamited shell may have been weakened by bor- jor bioticcrises.
ing organisms,or the crab may be somewhat
too large forits shell,thus being more vulner- Acknowledgments
able to successfulattackthanis the livingsnail
I am deeply indebted to Robert Bakker,
whichbuiltthe shell. Indeed, Rossi and Parisi
(1973) have shown that hennited shells are Alfred Fischer, Jeremy Jackson, Douglas
more vulnerable to crushing by the crab Morse, Norman Sohl, Steven Stanley,Thomas
Eriphia verrucosathan are conspecificshells Waller, Ellis Yochelson,and Edith Zipser for
inhabitedby livingsnails. Shell characteristics helpful discussions and criticisms. The empromotingresistanceto predators might be- pirical data underlyingmany of the conclucome morestronglyselectedforas morepreda- sions of thispaper were obtained with the assistanceof GrantsFA-31777and DES74-22780
tors assault the living shelled snail.
Justhow much hermitcrabs have added to of the Oceanography Section, National Scithe ecological life-spanof a given gastropod ence Foundation; and a fellowshipfromthe
shell may be difficultto assess in the fossil John Simon Guggenheim Memorial Foundarecord,but it may be possible to show whether tion.
a given fossilshell was inhabitedby a hermit
crab beforebeing preservedin the sediment. LiteratureCited
If, in any assemblage, most fossils bear evidence of havingbeen carriedby a hermitcrab, AWRAMIK, S. M. 1971. Precambian columnar stramatolite diversity: reflection of metazoan appearit may be concluded that the ecological lifeance. Science. 174:825-827.
span of the shell is relativelylong. If reliable BAKKER, R. T. 1972. Anatomical and ecological
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
256
VERMEIJ
evidenceof endothermy
in dinosaurs.Nature.238: EICHLER, R. AND H. RISTEDT. 1966. Untersuchun81-85.
gen zur Fruhontogenievon Nautilus pompilius
BAKKER, R. T. 1975. Experimental
and fossilevi(Linne). Palaontol.Z. 40:173-191.
dence for the evolutionof tetrapodbioenergetics. FISCHER, A. G. AND M. A. ARTHUR. 1977. Secular
pp. 365-399. In: Gates,D. and R. Schmerl,eds.
variationin pelagic realms. In: Enos, P. and H.
Perspectivesof BiophysicalEcology. Springer-Ver- Cook, eds., Soc. Econ. Petr. Mineral. Special
lag; New York.
Publ. 25: In press.
BIGELOW, H. B. AND W. C. SCHROEDER. 1953. FISCHER, P. 1881. Note sur le genre Olivella. J.
Fishesof theWesternNorthAtlantic.PartII, SawConchyliol.
29:31-35.
fishes,guitarfishes,
skates and rays. Mem. Sears GARRETT, P. 1970. Phanerozoicstromatolites:
nonFound. Mar. Res. 1:1-585.
competitiveecological restriction
by grazing and
Boss, K. J. 1971. Criticalestimateof the number
burrowinganimals. Science. 169:171-173.
of RecentMollusca. Occas. Pap. on Mollusks,Mus. CEORGE, R. W. AND A. R. MAIN. 1968. The evoComp.Zool.3:81-135.
lutionof spinylobsters(Palinuridae): a studyof
BOUCOT, A. J. 1975. Evolutionand Extinction
Rate
evolutionin the marineenvironment.Evolution.
Controls.427 pp. ElsevierSci. Publ. Co.; Amster22:803-820.
dam,Netherlands.
GLAESSNER, M. F. 1969. Decapoda. pp. R399BOWSHER, A. L. 1955. Origin and adaptationof
R533. In: Moore, R. C., ed. Treatiseon Inverplatyceratidgastropods. Kansas Univ. Paleontol.
tebratePaleontology.Part R, Arthropoda4 (2).
Contrib.17 (Mollusca, Article5):1-11.
Univ. Kansas Press; Lawrence,Kansas.
BOYD, D. W. AND N. D. NEWELL.
1972. Taph- COLIKOv, A. M. AND Y. I. STAROBOGATOV. 1975.
onomyand diagenesisof a PermianfossilassemSystematics
ofprosobranch
gastropods.Malacologia.
blage fromWyoming.J. Paleontol.46:1-14.
15:105-232.
BRASIER, M. D. 1975. An outlinehistoryof sea- HIATT, R. W. AND D. W. STRASSBURG. 1960. Ecograss communities.Palaeontology.18:681-702.
logicalrelationships
of the fishfaunaon coral reefs
BRIGHT, T. J. 1970. Food of deep-sea bottom
of the MarshallIslands. Ecol. Monogr.30:65-127.
fishes. Texas A&M Univ. Oceanogr. Studies. 1: HOBSON, E. S. 1974. Feeding relationships of
245-252.
teleostean fishes on coral reefs in Kona, Hawaii.
BROMLEY, R. G. 1975. Comparative
analysisof fosFish. Bull.72:915-1031.
sil and Recentechinoidbioerosion.Palaeontology. HOLTHUIS, L. B. AND R. B. MANNING. 1969. Sto18:725-739.
matopoda. Pp. R535-R552. In: Moore, R. C.,
CARRIKER, M. R. 1972. Observationson the reed. Treatise on InvertebratePaleontology.Part
moval of spines by muricid gastropods during shell
R, Arthropoda 4 (2). Univ. Kansas Press; Lawgrowth. Veliger. 15:69-74.
rence, Kansas.
CARRIKER, M. R. AND E. L. YOCHELSON.
1968. Re- VON HUENE, F. R. 1956. Palaontologie und Phylocent gastropod boreholes and Ordovician cylindrigenie der niederen Tetrapoden. 716 pp. Gustav
cal borings. U.S. Geol. Surv. Prof. Pap. 593B:
Fischer; Jena, Deutschland.
B1-B23.
JACKSON, J. B. C., T. F. GOREAU,AND W. D. HARTCARTER, R. M.
1968. On the biology and palaeonMAN. 1971. Recent brachiopod-coralline
sponge
tology of some predatorsof bivalved Mollusca.
Paleogeogr.,Paleoclimatol.,Paleoecol. 4:29-65.
communities
and theirpaleoecologicalsignificance.
Science. 173:623-625.
CIFELLI,
R. 1976. Evolution of ocean climate and
JELEIZKY, J. A. 1965. Taxonomyand phylogeny
the record of planktonicForaminifera.Nature.
of fossilColeoidea (= dibranchiata). Geol. Surv.
264:431-432.
Pap. Can. 65-2:72-76.
COPPER,
P. 1974. Structure and development of KAUFFMAN, E. G. 1972. Ptychoduspredationupon
Early Paleozoic reefs. Second Int. Coral Reef Symp.
a CretaceousInoceramus.Palaeontology.15:4391:365-386.
444.
CRACRAFT,
J. 1973. Continental drift, paleoclima- KAUFFMAN, E. G. AND R. V. KESLING. 1960. An
ofbirds.
tology,and theevolutionand biogeography
Upper Cretaceous ammonite bitten by a mososaur.
J. Zool. London. 169:455-545.
Contrib.Mus. Paleontol.Univ. Mich. 15:193-248.
CROSSE,
H. AND P. FISCHER.
1882. Note comple- KAUFFMAN, E. G. AND N. F. SOHL. 1974. Strucmentaire sur la resorption des parois intemes du
ture and evolutionof AntilleanCretaceousrudist
teste chez Olivella. J. Conchyliol. 30:181-183.
frameworks.Verhandl. Naturf. Ges. Basel. 84:
CURREY, J. D. AND J. D. TAYLOR. 1974. The me399-467.
chanicalbehaviourof some molluscanhard tissues. KIER, P. M. 1974. Evolutionarytrendsand their
J. Zool. London. 173:395-406.
functionalsignificancein the post-PaleozoicechiDAYTON, P. K. 1975. Experimentalevaluationof
noids. J. Paleontol.,Paleontol.Soc. Mem. 5, 48,
ecological dominancein a rocky intertidalalgal
Part II of II: 1-95.
community.Ecol. Monogr.45:137-159.
LIPPS, J. H. AND E. MITCHELL.
1976. Trophic
EARLE, S. A. 1972. The influenceof herbivores
model for the adaptive radiations and extinctions
on the marineplantsof GreatLameshurBay, with
of pelagic marinemammals. Paleobiology2:147-
an annotated list of plants. Nat. Hist. Mus. Los
Angeles County Sci. Bull. 14:17-44.
1964. ButterP. R. AND P. H. RAVEN.
EHRLICH,
terfliesand plants: a studyin coevolution.Evolution.18:586-608.
155.
1973. ProMcLEAN, R. B. AND R. N. MARISCAL.
tection of a hermit crab by its symbiotic sea
anemone Calliactis tricolor. Experientia.29:128130.
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
MESOZOIC
MARINE
REVOLUTION
257
ceous species of Inoceramus. N.Z. J.Geol. Geophys.
D. L. AND B. MCCURDA. 1977. Adaptive
14:56-70.
radiationof the comatulidcrinoids. Paleobiology.
STANLEY, S. M. 1968. Post-Paleozoic
adaptiveradi3:74-82.
ation of infaunalbivalve molluscs-a consequence
MILLER, B. A. 1975. The biology of Terebra
of mantlefusionand siphonformation.
J.Paleontol.
gouldi Deshayes, 1859, and a discussionof life
42:214-229.
amongotherterebridsof similar
historysimilarities
STANLEY, S. M. 1972. Functionalmorphology
and
proboscistype. PacificSci. 29:227-241.
evolutionof byssallyattachedbivalve molluscs. J.
MORSE, D. H. 1975. Ecologicalaspectsof adaptive
Paleontol.46:165-212.
radiationin birds. Biol. Rev. 50:167-214.
STANLEY, S. M. 1973. An ecologicaltheoryforthe
MORTON, J. E. 1955. The evolutionof the Elsudden originof multicellular
life in the late Prelobiidaewitha discussionon the originof the Pulcambrian. Proc. Nat. Acad. Sci. U.S.A. 70:1486monata. Proc. Zool. Soc. London. 125:127-168.
1489.
MiLT.ER, J. 1970. Palynologicalevidence of early
of angiosperms.Biol. Rev. 45:417- STANLEY, S. M. 1975. A theoryof evolutionabove
differentiation
the specieslevel. Proc. Nat. Acad. Sci. U.S.A. 72:
450.
646-650.
NEWELL, N. D. 1957. Paleoecology of Permian
reefsin the GuadalupeMountainsarea. Geol. Soc. STANLEY, S. M. 1976a. Fossil data and the Precambrian-Cambrian
evolutionarytransition.Am.
Am.Mem.67:407-436.
J.Sci. 276:56-76.
NEWELL, N. D. 1971. An outlinehistoryof tropiSTANLEY, S. M. 1976b. Ideas on the timing of
cal organicreefs. Am. Mus. Novit.2465:1-37.
metazoandiversification.
Paleobiology.2:209-219.
PORTMANN, A. 1967. Animal formsand patterns:
a study of the appearance of animals. 254 pp. STANLEY, S. M. 1977. Trends,rates,and patterns
SchockenBooks,New York.
of evolutionin the Bivalvia. In: Hallam, A., ed.
duringthe
RAUP, D. M. 1972. Taxonomicdiversity
Patternsof Evolution. Elsevier; Amsterdam.In
Phanerozoic. Science. 177:1065-1071.
press.
REx, M. A. AND K. J. Boss. 1976. Open coiling STEIN, R. A., J. F. KITCHELL, AND B. KNEZEVIC.
in Recentgastropods.Malacologia.15:289-297.
1975. Selective predation by carp (Cyprinus carpio
RHOADS, D. C. 1970. Mass properties,stability,
L.) on benthicmolluscsin Skadar Lake, Yugoand ecologyof marinemuds relatedto burrowing slavia. J.Fish. Biol. 7:391-399.
activity.In: Grimes,T. P. and J. C. Harper,eds. STEVCIC, Z. 1971. The mainfeaturesof brachyuran
Trace Fossils. Geol. J. Special Issue. 3:391-406.
evolution.Syst.Zool. 20:331-340.
1971. Evolution- STEPHENSON, W. AND R. B. SEARLES. 1960. ExperiRHOADS, D. C. AND J. W. MORSE.
ary and ecologic significanceof oxygen-deficient mentalstudieson the ecologyof intertidal
environmarinebasins. Lethaia. 4:413-428.
I. Exclusionof fishfrom
ments
at
Heron
Island.
RIEGRAF, W. 1973. Biszspuren auf Jurassischen
beach rock. Aust. J. Mar. Fresh-WaterRes. 11:
N. Jb. Geol. Palaontol.M.H.
Belemniten-rostren.
241-267.
8:494-500.
TAYLOR, D. W. AND N. F. SOHL.
1962. An outline
boringsin the
ROHR, D. M. 1976. Silurianpredator
of gastropodclassification.Malacologia. 1:7-32.
brachiopodDicaelosia fromthe CanadianArctic.J.
TAYLOR, J.D. 1973. The structural
evolutionofthe
Paleontol.50:1175-1179.
bivalve shell. Palaeontology.16:519-534.
ROMER, A. S. 1966. VertebratePaleontology.468
THOMPSON, T. E. 1960. Defensiveadaptationsin
pp. Univ. Chicago Press; Chicago, Ill.
opisthobranchs.
J. Mar. Biol. Assoc. U.K. 39:123Experimental
1973.
PARISI.
AND
V.
Rossi, A. C.
134.
studiesof predationby the crab Eriphiaverrucosa
on both snail and hermitcrab occupantsof con- THOMPSON, T. E. 1969. Acid secretionin Pacific
Ocean gastropods.Aust. J. Zool. 17:755-764.
specificgastropodshells. Boll. Zool. 40:117-135.
RUNNEGAR, B. AND J. P. POJETA, JR. 1974. Mollus- THOMSON, K. S. 1969. The biology of the lobefinnedfishes.Biol. Rev. 44:91-154.
can phylogeny: the paleontological viewpoint.
THU-RMOND, J. T. 1974. Lower vertebratefaunas
Science.186:311-317.
of the Trinitydivisionin north-central
Texas. GeoSAMMARCO, P. W., J.S. LEVINGTON, AND J. C. OGDEN.
MEYER,
1974. Grazing and controlof coral reef community
structureby Diadema antillarum Philippi (Echino-
science and Man. 8:103-129.
TOWE,K. N. 1970. Oxygen-collagen
priorityand
the earlymetazoanfossilrecord. Proc. Nat. Acad.
dermata: Echinoidea): a preliminarystudy. J.
Sci. U.S.A. 65:781-788.
Mar. Res. 32:47-53.
of taxonomicand
SCHAEFFER, B. AND D. E. ROSEN. 1961. Major VALENTINE, J. W. 1969. Patterns
adaptivelevels in the evolutionof the actinoptery- ecological structureof the shelf benthos during
Phanerozoictime. Palaeontology.12:684-709.
gian feedingmechanism.Am. Zool. 1:187-204.
paleoecology
Opisthobranchia VALENTINE, J. W. 1973. Evolutionary
SOHL, N. F. 1964. Neogastropoda,
of the Marine Biosphere. 511 pp. Prentice Hall
fromthe Ripley,Owl Creek,
and Basommatophora
Inc.; Englewood Cliffs,New Jersey.
and Prairie Bluff Formations. U.S. Geol. Surv.
Prof.Pap. 331-B:153B-344B.
VALENTINE,
J. W. AND E. M. MOORES. 1970. Platetectonicregulation
of faunaldiversity
and sea level:
SOHL, N. F. 1969. The fossilrecordof shellboring
a model. Nature.228:657-659.
by snails. Am. Zool. 9:725-734.
of shellsculpSPEDEN, I. C. 1971. Notes on New Zealand fossil VERMEIJ, G. J. 1971. The geometry
ture. Formaet Functio.4:319-325.
Mollusca-2. Predationon New Zealand Creta-
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions
258
VERMEIJ
and WXNBERG-ERKSSON, K. 1964. Isospira reticulata
J. 1973. Adaptation,versatility,
n.sp. from the Upper Ordovician Boda Limestone,
evolution.Syst.Zool.22:466-477.
Sweden. Geol. Forenings I Stockholm Fbrhandl.
VERMEIJ, G. J. 1974. Marine faunal dominance
86:229-237.
and molluscanshell form. Evolution.28:656-664.
and
VERMEIJ, G. J. 1975. Evolution and distribution WESTERMANN, G. E. G. 1971. Form,structure
functionof shell and siphunclein coiled Mesozoic
of left-handedand planispiralcoiling in snails.
ammonoids. Life Sci. Contrib.R. Ontario Mus.
Nature.254:419-420.
in
78:1-39.
VERMEIJ, G. J. 1976. Interoceanicdifferences
vulnerabilityof shelled prey to crab predation. WOODWARD, B. B. 1892. On the mode of growth
and the structure
of the shell in Velatesconoideus,
Nature.260:135-136.
Lamk., and otherNeritidae.Proc. Zool. Soc. LonVERMEIJ, G. J. 1977. Patternsin crab claw size:
don.528-540.
the geographyof crushing.Syst.Zool. 26: In press.
WALLER, T. R. 1972. The functionalsignificance YOCHELSON, E. L. 1971. A new Late Devonian
in the Pectinacea
gastropodand its bearing on problemsof open
of some shell microstructures
coilingand septation.Smithson.Contrib.Paleobiol.
(Mollusca: Bivalvia). Pp. 48-56. Int. Geol. Congr.
3:231-241.
24th Session,Montreal,Can. Sect. 7, Paleontol.
VERMEIJ, C.
This content downloaded on Sun, 10 Mar 2013 16:48:13 PM
All use subject to JSTOR Terms and Conditions