158 J. A. CRAME & B. R. ROSEN
Causes of Cenozoic biodiversification
It would appear then that if we are to find a satis-
factory explanation for the global Cenozoic bio-
diversification event, it must be one that involves
a synchronous increase at all four basic levels
(i.e. alpha, beta, gamma and delta diversity). In
other words this must be a process that allows
both an increase in the numbers of taxa within
individual habitats as well as increased differen-
tiation between these habitats on a variety of
geographical scales. For example, at one of the
very simplest levels it has been postulated that
the Cenozoic rise in biodiversity could be linked
to a global rise in trophic resources provided by
the radiation of the angiosperms (Bambach
1977). Even in the marine realm the increased
flux of plant detritus through river systems may
have raised benthic productivity. Similarly, it has
been suggested that oceanic nutrient cycling
may have been influenced by changes in the
global thermohaline circulation system brought
about by the formation of Antarctic deep
bottom waters at the Eocene-Oligocene bound-
ary (Bambach 1977).
Such ideas are indeed appealing, and we
should not lose sight of the fact that there may
well have been times of abrupt increase in both
terrestrial and marine productivity through
Earth history. Nevertheless it is by now well
established that there is not necessarily a direct
link between increased productivity and
increased biodiversity. An increase in produc-
tivity can trigger an increase in biomass, but
there is no reason why this should not, in
turn, just be within one or a small number of
species. Something else is required to generate
a large number of new taxa from a rise in
productivity (Blackburn & Gaston 1996). We
also have to bear in mind that any potential
mechanism for Cenozoic global biodiversifica-
tion must explain the greater relative production
of new taxa in the low- than in the high-latitude
regions. In their discussion of the origin and
diversification of major taxonomic groups,
Jablonski & Bottjer (1990) identified five basic
explanations for global radiations. We might
rationalize these into two main types: intrinsic
and extrinsic.
Intrinsic mechanisms of diversification
One of the simplest explanations for global
Cenozoic diversification would be that it rep-
resents the coincidental expansion of a series of
unrelated clades. Although key adaptive break-
throughs, such as mantle fusion and the develop-
ment of posterior siphons in bivalves, or the
development of plants with flowers, undoubtedly
occurred well before the Cenozoic Era, it may
have taken periods of tens of millions of years for
such clades to build up substantial numbers of
taxa (Jablonski & Bottjer 1990). Once certain
groups became established in the latest Meso-
zoic/earliest Cenozoic they may in turn have
triggered the automatic radiation of others.
Angiosperm assemblages would have provided a
variety of novel terrestrial habitats, and the rapid
development of coral reefs, sea-grass beds and
mangroves at this time could have promoted
diversification in shallow, tropical seas (Verrneij
1977).
It is also possible that intense biological inter-
actions between various taxonomic groups were
a driving force behind diversification. In particu-
lar, if biological hazards due to competitors and
predators have increased through time, then so
may the responses of various prey taxa to them.
The net result is a sort of 'evolutionary arms
race', with first one group gaining a numerical
ascendancy, and then the other (Vermeij 1987,
1994). This special form of co-evolutionary
relationship, known as escalation, emphasizes
the importance of enemies as agents of natural
selection: over periods of geological time
enemy-related adaptations bring about long-
term evolutionary trends in the morphology,
ecology or behaviour of other organisms. It is
essentially a tropical phenomenon and is
particularly well represented in species-rich
groups, such as angiosperms, arthropods, verte-
brates and molluscs, that have highly developed
competitive and defensive capabilities (Vermeij
1987). Striking examples would appear to be the
co-radiation of angiosperms and pollinating
insects in the terrestrial realm, and the link
between durophagous predators and both
deeper-burrowing infauna and more heavily
ornamented epifauna in the marine one.
Although escalation seems to be an intuitively
satisfying explanation for certain tropical radia-
tions, some doubts have been raised as to its
widespread efficacy. For example, Vermeij
(1987) himself drew attention to the low inci-
dence of damage repair within many infaunal
bivalve groups, and the high-resolution fossil
record in general has comparatively few
examples of gradual morphological change
induced within a prey lineage (Hansen et al. 1999;
Dietl et al 2000; Miller 2000). Many biotic tran-
sitions within the fossil record could equally
well be interpreted as the replacement of -
incumbent taxa by some form of fundamental
environmental change (Jablonski 2000). Non-
competitive expansions may be just as common
through geological time (Benton 1999).
