Journal of the Geological Society, London, Vol. 159, 2002, pp. 1–4. Printed in Great Britain.
occurrence? Logically one could argue that any absence from
the fossil record, however local, however temporary, is a
Lazarus effect because the duration required for the Lazarus
effect is not defined.
Taxonomic abundance varies, both locally and globally,
when plotted against time, and at its lowest ebb a taxon may
‘disappear’ from the fossil record; at times of biotic crisis such
disappearing acts may last for several million years. If the
taxon does not reappear then it is assumed to be extinct. Crisis
periods resulting in mass extinctions of graptolites, also result
in other graptolite species becoming rare and/or geographically
restricted.
Lazarus taxa, refugia and
relict faunas: evidence from
graptolites
R. B. RICKARDS 1 & A. J. WRIGHT 2
Department of Earth Sciences, The University,
Downing Street, Cambridge CB2 3EQ, UK
School of Geosciences, University of Wollongong,
New South Wales 2522, Australia
The end-Ordovician crisis event. The end-Ordovician mass
extinction (Fig. 1) peaks in the extraordinarius Biozone where
only three forms have been recorded: Climacograptus extraordinarius (Sobolevskaya 1974), Glyptograptus sp., and ?Climacograptussp. The first of these does not survive the end of the
biozone and the others are doubtful records. Species of Normalograptus possibly comprise Lazarus taxa as both N. normalis (Lapworth) and N. angustus (Perner) have been widely and
commonly recorded both above and below the extraordinarius
Biozone but not within it. However, unpublished research by
one of us (R.B.R.) suggests that the Ordovician and Silurian
representatives of Normalograptus are specifically distinct.
Thus the genus Normalograptus may be considered a Lazarus
taxon but evolution of the species lineages probably took place
during the crisis period. An evolutionary explosion beginning
in the persculptus Biozone (Fig. 1) derived either from C.
extraordinarius, perhaps unlikely in view of its alreadyspecialized thecae, or from an as yet unrecognized Glyptograptus sp., possibly itself a Lazarus taxon, or at least very rare at
the level of the extraordinarius Biozone. The biodiversity plots
of Figure 1 show a striking recovery when plotted at the level
of species per biozone. However, when plotted at species per
part biozone it is seen that the burgeoning assemblages show a
dip in the lower part of the acuminatus Biozone. The same
biomodal biodiversity record is also seen in the recovery period
immediately following the end-Wenlock (Silurian) crisis event
(Fig. 2). Such blips may represent a faltering of the adaptive
radiation phase as early niche exploiters were replaced by
long-term successful lineages. The main recovery period following the end-Ordovician crisis occurred in about a million
years, by which time the marine transgression of the shelves
was complete (end-acuminatus Biozone). This is not in accord
with recent work by Kirchner & Weil (2000) (see also Erwin
2000) where a recovery period of up to 10 million years is
suggested, although their analyses were carried out at a much
higher taxonomic level. The onset of the crisis period may have
been much shorter (see the increase in extinction rate at the end
of the anceps Biozone). A similar situation obtained at the
end-Wenlock event (Fig. 2) where the recovery period took
about a million years up to and including the lower nilssoni
Biozone, whilst the decline into the crisis occurred in only
0.25 Ma.
L
azarus taxa are considered to be end members of a
common phenomenon and their usefulness is questioned. Mass extinctions are survived by a small
number of evolutionary lineages, which give rise to the
increase in biodiversity during the recovery phase; and by a small
number of species which survived in geographically small, isolated refugia, perhaps marginal to the main environment in crisis.
Refugia may give rise to relict faunas, as in the case of early
Ludlow graptolites of New South Wales, Australia, but most
elements of a relict fauna are short-lived in evolutionary terms.
Keywords: graptolites, Lazarus taxa, refugia, relict faunas, biotic
recoveries.
The aim of this paper is to discuss the end-Ordovician and
end-Wenlock (Silurian) extinction events, and subsequent recoveries, in terms of the planktic graptoloids which provide
useful information on such concepts as Lazarus taxa, refugia
and relict faunas.
The term Lazarus taxon was coined by Flessa & Jablonski
(1983) and expanded by Jablonski (1986). Urbanek (1993,
1998) and Wignall & Benton (1999) related Lazarus taxa to
biotic crises and subsequent recovery. Wignall & Benton (1999,
p. 453) defined Lazarus taxa as: ‘At times of biotic crisis many
taxa go extinct, but others only temporarily disappear from the
fossil record, often for intervals measured in millions of years,
before reappearing unchanged’. Earlier work supports the
concept though without using the name Lazarus taxon (e.g.
Batten 1973; Waterhouse & Bonham-Carter 1976; Paul 1982).
But how useful is the concept of a Lazarus taxon? In the first
place it is implicit that the taxon must have survived somewhere, but during the time of biotic crisis was not preserved.
There are two ways, not mutually exclusive, that this might
occur: the taxon might have become either very rare or
geographically restricted (e.g. coelacanths). Both factors would
decrease preservational potential. However, a single record of
the taxon, discovered in rocks deposited during the crisis
period, immediately cancels its status as a Lazarus taxon. So is
a Lazarus taxon anything more than an extreme manifestation
of a taxon’s low abundance plotted against time?
Recorded at the level of species per biozone, then the
Lazarus effect may occupy one or more biozones. Suppose it
occupied three biozones, and then someone discovered a
single record in the middle of the three biozones. Do we then
have two shorter Lazarus effects separated by a ‘normal’
Graptolite Lazarus taxa. In his analysis of oligophyly,
Urbanek (1998, pp. 551 & 554) identified the Monograptus
uncinatus lineage as demonstrating a Lazarus effect in that
species of this group were absent from the nassa / dubius
Biozone (see Fig. 2): so he gives it the notation N = (1), that is,
at time t = 0 the number of taxa is 1, except that the Lazarus
effect requires that the 1 be bracketed. However, this case
exemplifies the point we made in the introductory paragraphs,
1
2
R. B. RICKARDS & A. J. WRIGHT
Fig. 1. Global graptolite biodiversity
changes, recorded at species level, across
the end-Ordovician mass extinction/crisis
event. Solid line, number of species per
biozone; dashed line, number of species
per part biozone, where possible; broad
diagonal shading, number of new species
per biozone; narrow diagonal shading,
number of extinctions per biozone or
part biozone (anceps Biozone) for the
anceps to basal triangulatus biozones;
possible Lazarus taxa are excluded from
the extraordinarius Biozone; mean
duration per biozone is 1.1 Ma
(Ordovician 1.6 Ma; Silurian 0.5 Ma);
mean duration per part Biozone is
0.70 Ma (Ordovician 1.1 Ma; Silurian
0.4 Ma)
Fig. 2. Global graptolite biodiversity
changes, recorded at species level across
the end-Wenlock (Silurian) mass
extinction/crisis event. Uppermost solid
line, number of species per biozone;
dashed line, number of species per part
biozone where global subdivisions of
biozones are recognized; heavier solid
line, number of new species per part
biozone; dotted line, number of
extinctions per part biozone; possible
Lazarus taxa are excluded from the
nassa / dubius Biozone (full explanation
in text); mean duration per biozone at
this level is 0.6 Ma; mean duration of
biozonal subdivisions is 0.25 Ma.
because hooked monograptids of this type have been recorded,
albeit rarely, from the Lake District and North Wales (UK)
(Rickards 1967; Warren et al. 1984) and New South Wales
(Australia) (Rickards et al. 1995). The concept of a Lazarus
taxon in this case fails. It is far more sensible and helpful to
describe the uncinatus group at that time as very rare and
geographically restricted.
A better example of a Lazarus taxon concerns the genus
Cyrtograptus. This occurs abundantly, with reasonable species
diversity, up to and including the lundgreni Biozone (Wenlock)
but has never been recorded in the nassa/dubius Biozone or the
ludensis Biozone. The genus reappears as a single species with
extremely restricted geographical occurrence (Rickards et al.
1995), and is known only from one region of New South Wales
(Quarry Creek district), from the nilssoni Biozone of the early
Ludlow. A peculiar feature of the genus in New South Wales is
that, in all the species so far identified from the Wenlock and
Ludlow, thecal cladia (branches) are extremely rare. Normally
cladia are taken as diagnostic of the genus. But individual
species can still be identified, e.g. C. lundgreni, the eponymous
biozonal fossil of the late Wenlock. There can be no doubt that
cyrtograptids in the Wenlock and early Ludlow Series of New
South Wales rarely had thecal cladia. Many specimens have
been found: it is most certainly not a preservational artefact
(see below).
Silurian biserial graptolites may also exhibit instances of
apparent Lazarus taxa. Thus Jaeger (1978) described a remarkable climacograptid, of Normalograptus type, from the
LAZARUS TAXA, REFUGIA AND RELICT FAUNAS
hercynicus Biozone (Devonian) of Thuringia. These forms are
last seen in the late Llandovery Silurian some 32 biozones
earlier! It is possible that this example fits into the ‘quality of
the fossil record’ group as defined by Wignall & Benton (1999)
but it is much more likely, given the considerable time gap,
that the Devonian form has a different evolutionary origin. A
less spectacular example is that of Neoglyptograptus sussmilchi
Rickards et al. (1995), a Glyptograptus-like species. Glyptograptus itself is last seen in the late Llandovery at least eight
biozones earlier. Neoglyptograptus may also have a different
evolutionary origin, possibly derived from a retiolitid species.
It seems to us that these examples, as well as the points raised
in the introduction, indicate the fragility of the whole concept of the Lazarus taxon, even when it is attempted to relate
it to a time of biotic crisis: if rarity=zero, within a species’
(acro)zonal occurrence, then it becomes a Lazarus taxon.
Graptolite refugia. A refugium is a site to which species run, or
places in which they happen to be when the world closes in. In
their recent appraisal of refugia Wignall & Benton (1999)
considered that at times of biotic crisis refugia are small ‘areas
of sanctuary to which species flee at times of environmental
stress in their normal habitat’ (see also Jablonski & Flessa
1986; Jablonski & Harries 1996; Erwin 1996). Whilst one can
imagine that Homo spp. might adopt such a strategy is it not
more likely that, for example, ocean plankton might find
themselves in a sanctuary, passively or accidentally, when
times elsewhere were hard? This also carries the implication
that such sanctuaries would be physically or ecologically
marginal to the main environment normally occupied by the
species, because it is the main environment which is challenged
(see also Hallam & Wignall 1997, pp. 14–15). A consequence
of this might be that some adaptation may already have taken
place in response to the special conditions of the refuge: for
some reason, possibly hydrodynamic, cyrtograptids in New
South Wales did not require thecal cladia, whereas in the rest
of the world they did. The only reasonable alternative to this is
that the extinction-causing stress does not occur in the refuge.
The graptolite record suggests that in refugia some evolution
was taking place. Thus Monoclimacis ludlowensis, Monograptus uncinatus and Cyrtograptus elegantulus differ from their
pre-Lazarus ancestors of the same species groups. The region
of Orange in New South Wales may well be a refugium of
some significance in that robust monograptids were present
here during the time of the ludensis Biozone, as were
monograptids referred to Testograptus (to date recorded only
from New South Wales), probably cladia-less cyrtograptids
and monoclimacids (in that they recurred only here after the
crisis).
The Silurian environment of New South Wales, at the end of
the Wenlock, consisted of a series of north–south, deep
troughs, with rises and islands separating them, and a varied
distribution of volcanic and clastic rocks. There were also
considerable differences between coeval graptolite faunas of
New South Wales and those of the more open depositional
basin of Victoria in both the Ordovician and Silurian
(Rickards et al. 2000, 2001). It is possible that the trough and
rise system provided some isolation from the more open ocean
environments and hence some possibilities of refugia developing during crisis events. If such crises involved a lowering of
the sea level and exposure of shelf seas, the deep trough
system, with its narrow marginal environments may have
already developed species relatively unaffected by sea-level
change.
3
Graptolite relict fauna. The early Ludlow (nilssoni Biozone)
fauna of the Quarry Creek district near Orange, New South
Wales, is the only example which we are able to describe as a
relict fauna. The age is beyond question (see Rickards
et al. 1995; Rickards & Wright 1999). The full relict component of Wenlock elements, associated with 16 taxa comprising
the Ludlow fauna.
Testograptus testis. This species is typically a late Wenlock
species and is often used as a label or ‘index’ to the testis or
lundgreni/testis Biozone. It occurs rarely in the ludensis Biozone (Rickards et al. 1995), and we have recently recovered it,
albeit rarely, with a good nilssoni Biozone assemblage, at
Mirrabooka Park in the Quarry Creek district.
Cyrtograptus elegantulus elegantulus and C. e. sparsus occur
uncommonly, with a rich nilssoni Biozone assemblage in
Quarry Creek (Rickards et al. 1995), and at Four Mile Creek
(Rickards & Wright unpublished). These are both cladia-less
forms and they closely resemble similar cyrtograptids from the
lundgreni/testis Biozone of the same area, which also lack
thecal cladia.
Monoclimacis ludlowensis occurs with a nilssoni Biozone fauna
in Quarry Creek and at Mirrabooka park in the same area. It
has already been discussed above in the section on Lazarus
taxa.
Of these four taxa only T. testis survives apparently unchanged, but all four have a pronounced Wenlock aspect to
them and are clearly survivors from that time. The species have
not been recorded from the nilssoni Biozone anywhere else in
the world; and the occurrence of the cladia-less cyrtograptids
in both the late Wenlock and early Ludlow of New South
Wales and nowhere else, suggests a particular hydrodynamic
niche, a refugium, in which the fauna lived and survived.
Therefore, the effect of the New South Wales refugium was to
allow a small number of typically Wenlock types to survive
into the early Ludlow. Equally clearly the species diversity of
these survivors, as well as their general rarity, suggests that
they were in decline. More commonly, other Wenlock species,
such as M. flemingii, (and subspecies) did not survive the
nassa / dubius crisis event, although their descendants did.
However, the M. flemingii species group gave rise to a major
Ludlow lineage, the uncinatus group, so in no sense could be
considered a relict species: that term must be restricted to those
forms which survived only for a short time, in this case less
than one million years, and which did not recover to provide
new lineages (holdover taxa).
Biotic recovery. Rickards et al. (1995) presented a global
biodiversity plot across the end-Wenlock crisis event. Figure 2
is a species-per-biozone plot through the same period. It shows
a double peak in the recovery, a feature also detected at the
end-Ordovician crisis event (Fig. 1). Therefore those graptolites which took advantage of the New South Wales refugium
survived not only the nassa / dubius crisis but a presumably
lesser crisis in the uppermost part of the ludensis Biozone,
immediately before the great diversity increase at the onset of
nilssoni Biozone times. This double trough/double peak observation may be relevant to one of the conclusions of Wignall &
Benton (1999, p. 456) concerning lag phases in recovery
periods. Had this small blip not been detected then one could
argue that the slow climb of the curve represented a lag phase,
and that it ‘may be viewed as a prolongation of the stressful
conditions that caused the mass extinction and not as some
intrinsic property of the recovery fauna’. In fact, it seems likely
4
R. B. RICKARDS & A. J. WRIGHT
to us that there could well be an intrinsic property of the
recovering fauna which resulted in both a lag phase and a
biodiversity blip. That intrinsic factor is adaptive evolutionary
change.
With the amelioration of the crisis at the onset of the early
Gleedon Chronozone, coupled with the global marine transgression, the relatively few surviving lineages would undergo
adaptive radiation and it is likely that this would go through a
period of mosaic evolution in which a variety of ‘options’ were
tried out by the evolving faunas. Mosaic evolutionary periods
are always followed by a fall off in speciation and then by a
fuller recover by lineages which would lead to major taxa (see
Kemp 1982; Rickards et al. 1995). Thus the lag phase discussed
by Wignall & Benton (1999) is not only to be expected but
should reflect the evolutionary patterns of the recovering
faunas. It is possible, however, that there were successive
pulses of harsh environmental conditions.
Conclusions. The concept of the Lazarus taxon, though catchy
in title, seems to us to serve no useful purpose, not only in
being at best an extreme instance of a common phenomenon,
but also because the gaps in the fossil record, even at times of
crisis, may well have alternative explanations. More important
is accurate plotting of biodiversity changes and species abundance through time, coupled with an appraisal of their palaeobiogeography. Refugia may be difficult to interpret in physical
terms for graptolite faunas, but it is very likely that they were
a major factor at times of crisis. One such refugium, in the
Quarry Creek/Mirrabooka Park area of New South Wales led
in time to the only known case of a graptolite relict fauna of
Wenlock types within an early Ludlow assemblage.
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Received 17 April 2001; revised typescript accepted 6 August 2001.
Scientific editing by Duncan Pirrie.