The Lilliput Effect in The Aftermath of The End-Permian Extinction Event
The Lilliput Effect in The Aftermath of The End-Permian Extinction Event
The Lilliput Effect in The Aftermath of The End-Permian Extinction Event
www.elsevier.com/locate/palaeo
Abstract
Early Triassic animal body fossils and trace fossils are small relative to those in older and younger intervals. Size decreases
sharply through the end-Permian extinction event and Permian/Triassic boundary, and the smallest sizes are encountered in the
parvus and isarcica Zones of the earliest Induan. Animals appearing within these two zones are also exceedingly small,
compared to younger congenerics and conspecifics. Temporary, dramatic size decrease of surviving taxa in the immediate aftermath
of the extinction event is an example of the Lilliput effect (coined by [Urbanek, A., 1993. Biotic crises in the history of Upper
Silurian graptoloids: a palaeobiological model. Historical Biology 7, 29–50.]). Body size increases somewhat from the carinata
Zone (mid-Induan) but remains depressed for the duration of the Early Triassic, and pre-extinction sizes are not commonly
recorded until at least the Middle Triassic. Marine and terrestrial faunas appear to be similarly affected. The Lilliput effect and
longer term size reduction could be the result of several factors. Environmental parameters such as marine anoxia, due to low
atmospheric concentrations of oxygen at this time coupled with sluggish ocean circulation in a greenhouse world, and food
shortage are the likely proximal causes for the Early Triassic Lilliput effect. No single cause can explain all the observations, and a
combination of factors are likely to be involved.
© 2007 Elsevier B.V. All rights reserved.
aftermath, or Survival Interval (sensu Kauffman and occurs after other biotic crises as well (e.g. in several
Erwin, 1995), of many extinction events, although molluscan taxa during the Pliensbachian–Toarcian event
Urbanek's (1993) terminology has rarely been specif- of the Early Jurassic; personal observation). It appears,
ically used in descriptions of such fossil assemblages. therefore, to be one factor that is common to all known
The Lilliput effect apparently occurred in the aftermath extinction crises and has important implications for our
of most of the major Phanerozoic extinction episodes, and understanding of the response of organisms to ecological
has been documented in a variety of animal groups, such as disturbance at both global and local scale. It may even
Early Silurian corals (Kaljo, 1996), Late Devonian allow us to predict the future response of the biosphere to
conodonts (Girard and Renaud, 1996; Renaud and Girard, present-day environmental change.
1999), and Early Danian echinoids (Jeffery, 2001), The mass extinction event that occurred in the latest
although the term “Lilliput effect” was not used by these Permian was the most severe event of the Phanerozoic
authors. There is growing evidence that the phenomenon (e.g. Erwin, 1993, 1994; Benton, 1995). It is ranked first
for both the magnitude of the diversity loss as well as for
the severity of the ecological impact on the marine and
terrestrial ecosystems of the Earth (McGhee et al., 2004).
It has long been recognised that the low diversity
assemblages of the Early Triassic aftermath are predom-
inantly composed of abundant, small-sized organisms
(e.g. Newell, 1952; Schubert and Bottjer, 1995), which are
typical attributes of Urbanek's (1993) “post-event syn-
drome”. Previous data have been a mixture of largely
qualitative or semi-quantitative studies. The aims of this
study are to assess the evidence for size decrease during
the Permian–Triassic extinction event, to document the
duration of the Lilliput effect, and to discuss some of the
potential causes of this phenomenon.
Table 1
Geometric sizes of bivalve and gastropod specimens through the Permian–Triassic interval
Permian Triassic
Cissuralian Guadalupian Lopingian Early Middle Late
Gastropods
Mean (mm) – 33.0 17.9 4.9 10.5 29.9
s.d. (mm) – 13.0 6.9 2.6 7.4 20.2
Maximum (mm) – 49.1 48.7 17.0 39.0 83.5
n – 30 54 153 83 47
Bivalves
Mean (mm) 31.2 – 21.3 12.1 22.3 23.4
s.d. (mm) 11.2 – 7.3 0.9 13.0 17.3
Maximum (mm) 58.8 – 42.4 80 47 75.2
n 14 – 108 1166 27 137
Permian/Triassic (P/Tr) boundary, as was claimed in a Similar patterns are seen in all other benthic groups
previous publication (Hayami, 1997), and Late Permian studied thus far. For example, Early Triassic ophiuroids are
genera are smaller (mean size 23.7 mm) than Early much smaller (maximum disk diameter of 10 mm) than
Triassic taxa. However, the proportion of very large-sized Middle Triassic (20 mm), modern temperate (30 mm), or
genera (i.e. those in excess of 64 mm) does appear to modern tropical (45 mm) taxa (Twitchett et al., 2005).
decrease across the P/Tr boundary (Hayami, 1998, p. 39). Small body size is also characteristic of Early Triassic
Other molluscan taxa are also smaller in the Early marine and terrestrial vertebrates (e.g. Smith, 1995;
Triassic. “Microgastropods”, which are defined as being Tverdokhlebov et al., 2002), although quantitative data of
gastropods that are less than 10 mm in height (Fraiser and size change are currently lacking. Early Triassic terrestrial
Bottjer, 2004), are so common in Lower Triassic rocks ecosystems are typically described as being dominated by
that they may reach rock-building densities (Fraiser et al., small organisms, at least in the very earliest Triassic. In
2005). Early Triassic gastropod assemblages in all known Russia, small temnospondyls characterise the beginning of
marine environments are dominated by microgastropod the Triassic, and the ecological niches for large herbivores
species, whereas Permian, Middle Triassic, or modern and predators were unoccupied (Tverdokhlebov et al.,
gastropod assemblages tend to be dominated by larger 2002). Similarly, in South Africa it appears that the
gastropods (Fraiser and Bottjer, 2004). In a parallel study terrestrial ecosystems of the Early Triassic were dominated
based on literature review, Payne (2005) also demonstrat- by small sized tetrapods (Smith, 1995).
ed a similar pattern of size change in Permian–Triassic These qualitative and quantitative data give a first order
(P–Tr) gastropods: namely, size decrease into the Early understanding of P–Tr size change at the stage or series
Triassic followed by size increase in the Middle Triassic. level. All animal groups apparently record identical
As a complementary study to the literature-based changes, with size minima in the Early Triassic. However,
compilations by Payne (2005) and Hayami (1998), I am a few studies have also documented size changes at a much
compiling data from measurements based on actual higher resolution (i.e. sub-stage or zonal scale). The
fossil specimens from field studies and museum earliest such study involved analyses of the diameter of
collections. Preliminary results are shown here plotted trace fossil burrows from the Bellerophon and Werfen
at series scale (Fig. 1, Table 1) and the patterns of size formations of northern Italy (Twitchett, 1999). From the
change through the Permian and Triassic are very Late Permian Bellerophon Formation into the parvus and
similar to those found in previous studies. Both the isarcica conodont zones (i.e. early–mid Griesbachian,
mean and maximum body sizes of gastropods decrease earliest Induan) of the Werfen Formation, burrow diameter
through the Permian to reach a minimum in the Early decreased by an order of magnitude. As burrow diameter is
Triassic, before increasing during the subsequent a good proxy of the size of the organism that made the
Triassic (Fig. 1A). The mean body size of bivalves burrow (e.g. Savrda et al., 1984; Savrda and Bottjer, 1986),
also reaches a minimum in the Early Triassic, although these data imply a dramatic reduction in the body sizes of
the maximum size (e.g. specimens of Claraia from the the infaunal, soft-bodied, trace-making community.
Perth Basin of western Australia) exceeds that of the Since this initial study, further field measurements have
Lopingian. been made through the same succession – the data set now
R.J. Twitchett / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 132–144 135
Fig. 2. Burrow diameters of trace fossils through the Late Permian to Middle Triassic of the Dolomites, northern Italy. A: all burrow types; B: vertical
domichnia of suspension feeders (i.e. Arenicolites, Skolithos, Diplocraterion); C: fodinichnia of deposit feeders (i.e. Planolites). Circles indicate
mean value; vertical lines indicate one standard deviation above, and below, the mean; shaded region indicates total burrow range between the
maximum and minimum recorded sizes. Measurements recorded in the field to the nearest 0.5 mm. TOH = Tesero Oolite Horizon; AzH = Andraz
Horizon; GOM = Gastropod Oolite Member.
comprises some 1257 samples – yet the patterns remain San Lucano Member, but it is not until the Anisian that
robust (Fig. 2). The initial decrease in both maximum and burrow size commonly exceeds 10–15 mm, with
mean burrow size from the Bellerophon Formation into the Thalassinoides reaching 30 mm and Rhizocorallium
Mazzin Member of the Werfen Formation remains the reaching 20 mm in diameter.
most severe decline. Following this there is a gradual Recent work on the shelly body fossils of the Late
increase in mean burrow size through the Early Triassic, Permian and Early Triassic record of northern Italy has
interrupted by temporary decreases in the upper Siusi revealed similar patterns of size change (Price-Lloyd
Member and Campil Member. Similar patterns are and Twitchett, 2002) (Fig. 3). The taxa Bellerophon and
observed when the domichnia of suspension feeders (e.g. Lingula show statistically significant reductions in body
Arenicolites, Skolithos) and the fodinichnia (e.g. Planolites) size from the Bellerophon Formation through the
are considered separately (Fig. 2). One or two rare, large extinction event into the Mazzin Member of the Werfen
burrows are encountered in the lower Siusi Member and Formation. In addition, taxa which appear in the
136 R.J. Twitchett / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 132–144
immediate aftermath of the event, namely Claraia and Event. The taxon P. dubius spans the entire extinction–
Unionites, are also smallest in the Mazzin Member. recovery interval, although the Lilliput forms are assigned
All taxa show significant increases in body size in the to the subspecies P. dubius parvus, whereas the ‘normal’
lower Siusi Member. pre-extinction, and later recovery, forms are assigned to the
subspecies P. dubius frequens.
3. The Early Triassic Lilliput effect Adhering to Urbanek's original definition of the
Lilliput effect, it is clear that the only Permian–Triassic
Urbanek's (1993) definition of the Lilliput effect data described above that could fit with this definition are
describes it as “the occurrence of diminuative forms the statistically significant, short-term size changes within
among some of the species in the relic assemblages” of the the surviving taxa Lingula and Bellerophon during the
immediate post-extinction aftermath. In other words, the Griesbachian (early Induan), which were first described
Lilliput effect, as originally defined, describes size by Price-Lloyd and Twitchett (2002). Poor preservation
reduction within specific taxa (species) that survive the and dramatic size change mean that the Lilliput forms of
extinction event and is a temporary phenomenon confined these taxa in the Dolomites sections are typically not
to the Survival Interval (sensu Kauffman and Erwin, 1995). assigned to species, but are usually referred to as Lingula
The classic example of the Lilliput effect described by sp. or Bellerophon sp. Until further taxonomic study is
Urbanek (1993) is the mass occurrence of short and slim undertaken, it is not possible to be certain that size
Pristiograptus dubius in the aftermath of the lundgreni reduction is happening at the specific or generic level.
Regardless, it is clear that the remaining data
concerning size reduction in the Early Triassic (documen-
ted above) do not comfortably fit within Urbanek's (1993)
definition of the Lilliput effect: small size is recorded in
newly originating taxa as well as surviving taxa; in the
relative proportions of ‘small’ and ‘large’ species within
higher taxa; and through the whole of the Early Triassic,
not just the immediate post-extinction aftermath. This
represents a larger-scale, longer-term depression of body
size, affecting the entire fauna (survivors as well as newly
originating taxa) and lasting through the Survival Interval
and well into the Recovery Interval. This is not the Lilliput
effect in the sense of Urbanek (1993) and may or may not
be related to the extinction event. The apparent long-term
decline in body size through the Permian (e.g. Fig. 1) may
be related to long term environmental changes (see below)
or successive extinction events (end-Guadalupian, end-
Permian). Typically, studies based largely on literature
review and/or semi-quantitative analyses of taxa at the
generic or family level (e.g. Payne, 2005) will highlight
this longer term depression of body size, whereas
measurements of individual, well-dated specimens from
field or museum collections are necessary to document the
Fig. 3. Size change in benthic marine invertebrates in the aftermath of shorter term Lilliput effect. Regarding trace fossils: size
the end-Permian extinction event. Black square = Bellerophon (n = 42); reduction within specific ichnogenera or ichnospecies in
grey circle = Lingula (n = 195); black diamond = Claraia (n = 721); grey the immediate aftermath of an extinction event is herein
triangle = Unionites (n = 258). Symbols show mean size; horizontal
lines indicate maximum and minimum recorded sizes. Size calculated considered to also represent the Lilliput effect, although it
as the geometric mean of length and height. All within-taxon size is recognised that a single ichnotaxon may have been
changes are significant at the 5% level (Kolmogorov–Smirnov test). produced by more than one animal species. Studies
Data collected in the field from localities in northern Italy showing a size reduction of the entire ichnofauna, without
(Bellerophon and Werfen formations). The Griesbachian is divided identifying the individual ichnotaxa (e.g. Twitchett, 1999;
into three conodont zones: parvus, isarcica, and carinata. Arrow
indicates approximate position of extinction event. Data from Price-
Fig. 1), do not demonstrate the Lilliput effect in the strict
Lloyd and Twitchett (2002). Bell Fm = Bellerophon Formation; sense, but do record this longer term depression of body
To = Tesero Oolite Horizon; Mb = Member; Az = Andraz Horizon. size.
R.J. Twitchett / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 132–144 137
4.2. Environmental controls on body size this is most often demonstrated by measuring the size of
burrows that these animals leave behind (e.g. Savrda and
Stanley (1973) hypothesised that for any given set of Bottjer, 1986). Finally, experimental data generally show
environmental parameters there is an optimal body size that animals reach smaller maximum adult size, and/or
for animals, and that size trends result from the process of mature at smaller size, under conditions of sub-lethal
attaining optimal size in the face of changing environ- hypoxia (e.g. in copepods; Richmond et al., 2006).
mental conditions. If the aftermaths of mass extinction Regarding the data from northern Italy (Figs. 2 and 3),
events represent times when environmental conditions are the smallest burrow diameters and smallest shelly
such that small size is the optimum, then this would invertebrates are found in the Mazzin Member of the
explain both within-lineage size decrease and the small Werfen Formation. This unit was deposited under very
sizes of newly appearing taxa. While many environmental low, but fluctuating, oxygen conditions as indicated by
factors may result in size decrease (Hallam, 1965), two are facies analysis and geochemistry (Wignall and Twitchett,
considered most important with regards to explaining the 1996, 2002). In localities of identical age, but where facies
Lilliput effect in the aftermath of the end-Permian indicate well oxygenated conditions, such as in Oman
extinction event: anoxia and food shortage. (Krystyn et al., 2003), diversity is much higher and the
sizes of shelly taxa (e.g. gastropods) are also slightly
4.2.1. Anoxia larger (Twitchett et al., 2004; Wheeley and Twitchett,
A substantial body of evidence has accumulated that 2005). Thus, from these preliminary data, the correspon-
demonstrates that anoxic, and even euxinic, conditions dence between body size decrease and anoxia is good,
were widespread in most marine environments and suggesting that it may be a possible cause of the Lilliput
regions through most of the Early Triassic (e.g. Wignall effect in the parvus and isarcica zones of the Induan. The
and Twitchett, 1996, 2002; Grice et al., 2005). In the deep very low atmospheric oxygen levels that apparently
ocean, oxygen restriction lasted from the Lopingian to characterised the entire Early Triassic (Berner, 2005) may
Middle Triassic (e.g. Isozaki, 1997), whereas in some be a cause of the longer-term depression of body sizes
shallow shelves marine anoxia is only recorded in the observed in all animal groups studied to date.
early Induan (e.g. Wignall and Twitchett, 1996). Taking a However, while there is some correspondence between
global view, peak anoxia (i.e. the widest geographic low oxygen levels and small size in these data, it also
spread of oxygen-poor waters) occurred in the parvus and seems apparent that anoxia alone cannot account for all
isarcica zones of the early Induan (Wignall and Twitchett, the data thus far collected. In northern Italy, the Lilliput
2002). At this time, only shallow seamounts and offshore effect lasts until the latest Griesbachian and sizes begin to
highs were free of evidence of marine anoxia (e.g. increase in the lower Siusi Member of the Werfen
Krystyn et al., 2003). Low oxygen conditions were Formation (Figs. 2 and 3). The lower Siusi Member,
probably the direct result of global warming and a however, is still affected by low oxygen conditions to
subsequent sluggishness in oceanic circulation, and have some extent (e.g. Wignall and Twitchett, 1996). Also,
been recreated in computer simulation models (Hotinski there are significant regional differences in the sizes of
et al., 2001). High temperatures would have also have some taxa that cannot be explained by differences in
caused a decrease in the amount of dissolved oxygen in oxygen levels. Measurements of the sizes of individual
the oceans, exacerbated by the relatively low concentra- Claraia specimens from the basal Wordie Creek Forma-
tion of oxygen within the atmosphere (Berner, 2005). tion of East Greenland and the Hovea Member of the
A large number of published data, from both modern Kockatea Shale Formation of Western Australia show that
experimental studies and analyses of the fossil record, the Australian specimens are significantly larger (Fig. 8).
have demonstrated the link between oxygen concentra- Yet, all of these specimens, from both regions, derive from
tion and body size. Episodes of surprisingly large body typical Griesbachian oxygen-restricted facies, charac-
size in terrestrial animals correlate with times of high terised by dark grey, parallel-laminated mudstones with
atmospheric oxygen and the inferred cause–effect link has rare, bioturbated horizons that were formed under similar,
been strengthened by modern experiments, such as in fluctuating low oxygen conditions (e.g. Wignall and
regard to Carboniferous dragonflies (Graham et al., 1995; Twitchett, 2002; Grice et al., 2005). Thus, the size
Harrison and Lighton, 1998). Likewise, in marine settings differences in this instance cannot be attributed to
Rhoads and Morse (1971) and Savrda et al. (1984) differences in environmental parameters that can be
demonstrated that as the oxygen concentration in bottom assessed from the rock record (such as relative oxygen-
waters decreases so does the size of marine animals ation), but must be due to other factors that are more
inhabiting the substrate. In fossil and modern examples difficult to measure/observe from geochemical and facies
142 R.J. Twitchett / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 132–144
that all animal groups suffered a size reduction after the Erwin, D.H., 1993. The great Paleozoic crisis: life and death in the
Late Permian extinction event and that body sizes Permian. Columbia University Press, New York. 327 pp.
Erwin, D.H., 1994. The Permo-Triassic extinction. Nature 367, 231–236.
remained low, relative to earlier Permian or later Triassic Erwin, D.H., 1996. Understanding biotic recoveries: extinction, survival,
times, for the duration of the Early Triassic. In addition to and preservation during the end-Permian Mass Extinction. In:
this longer-term depression of body sizes, a shorter Jablonski, D., Erwin, D.H., Lipps, J.H. (Eds.), Evolutionary
duration, more severe body size reduction is observed in Paleobiology. University of Chicago Press, Chicago, pp. 398–418.
Fara, E., 2001. What are Lazarus taxa? Geological Journal 36, 291–303.
the immediate aftermath of the extinction event affecting
Flessa, K.W., Jablonski, D., 1983. Extinction is here to stay.
both survivors (i.e. the Lilliput effect) and newly Paleobiology 9, 315–321.
originating taxa. This phenomenon is only observed in Fraiser, M.L., Bottjer, D.J., 2004. The non-actualistic Early Triassic
high resolution data, and spans the parvus and isarcica gastropod fauna: a case study of the Lower Triassic Sinbad
zones of the Griesbachian (early Induan). From the cari- Limestone Member. Palaios 19, 259–275.
nata Zone onwards body size recovers somewhat, but Fraiser, M.L., Twitchett, R.J., Bottjer, D.J., 2005. Unique microgastropod
biofacies in the Early Triassic: indicator of long-term biotic stress and
remains lower than expected until the Middle Triassic. A the pattern of biotic recovery after the end-Permian mass extinction.
number of potential causes of the observed size changes Comptes Rendus Palevol 4, 543–552.
have been proposed and these can be tested from Girard, C., Renaud, S., 1996. Size variations in conodonts in response to
geological data. It is likely that a combination of factors the upper Kellwasser crisis (upper Devonian of the Montagne Noire,
was involved. Environmental parameters such as low France). Comptes Rendus de l'Academie des Sciences, Serie IIa 323,
435–442.
atmospheric and dissolved oxygen concentrations and Graham, J.B., Dudley, R., Aguilar, N.M., Gans, C., 1995. Implications of
food shortage caused by primary productivity collapse the Late Palaeozoic oxygen pulse for physiology and evolution.
may all have played a role. Nature 375, 117–120.
Grice, K., Cao, C., Love, G.D., Böttcher, M.E., Twitchett, R.J.,
Acknowledgements Grosjean, E., Summons, R.E., Turgeon, S.C., William Dunning,
W., Jin, Y., 2005. Photic zone euxinia during the Permian–
Triassic Superanoxic Event. Science 307, 706–709.
Caroline Hensley (Natural History Museum, London) is Hallam, A., 1965. Environmental causes of stunting in living and fossil
thanked for her help in accessing specimens in her care. marine benthonic invertebrates. Palaeontology 8, 132–155.
Rob Willink (Origin Energy) is thanked for inviting me to Hallam, A., 1975. Evolutionary size increase and longevity in Jurassic
study the Permian-Triassic Hovea-3 core in Perth. I have bivalves and ammonites. Nature 258, 493–496.
Harries, P.J., Kauffman, E.G., Hansen, T.A., 1996. Models for biotic
received encouragement and useful input over the years survival following mass extinction. In: Hart, M.B. (Ed.), Biotic
from numerous people, including Margaret Fraiser and Recovery from Mass Extinction Events. Geological Society of
Dave Bottjer (USC), and members of the Palaeo Discussion London Special Publications, vol. 102, pp. 41–60.
Group at Bristol (2002), particularly Mike Benton, Paul Harrison, J.F., Lighton, J.R.B., 1998. Oxygen-sensitive flight
metabolism in the dragonfly Erythemis simplicicollis. Journal of
Pearson (now Cardiff), and former students James Wheeley
Experimental Biology 201, 1739–1744.
and Nathan Price-Lloyd. P. Wignall and an anonymous Hayami, I., 1997. Size changes of bivalves and a hypothesis about the
reviewer are thanked for comments on an earlier draft. cause of mass extinction. Fossils 62, 24–36 (in Japanese).
Hayami, I., 1998. Ecology of mass extinctions: the diversity and shell
size of bivalves through time. Iden 52, 38–44 (in Japanese).
References
Hotinski, R.M., Bice, K.L., Kump, L.R., Najjar, R.G., Arthur, M.A.,
2001. Ocean stagnation and end-Permian anoxia. Geology 29, 7–10.
Barbault, R., 1988. Body size, ecological constraints and the evolution Isozaki, Y., 1997. Permo-Triassic boundary superanoxia and stratified
of life-history strategies. Evolutionary Biology 22, 261–286. superocean: records from lost deep sea. Science 276, 235–238.
Benton, M.J., 1995. Diversification and extinction in the history of life. Jablonski, D., 1996. Body size and macroevolution. In: Jablonski, D.,
Science 268, 52–58. Erwin, D.H., Lipps, J.H. (Eds.), Evolutionary Paleobiology. Chicago
Berner, R.A., 2002. Examination of hypotheses for the Permo-Triassic University Press, Chicago, pp. 256–289.
boundary extinction by carbon cycle modelling. Proceedings of the Jablonski, D., Raup, D.M., 1995. Selectivity of end-Cretaceous marine
National Academy of Sciences 99, 4172–4177. bivalve extinctions. Science 268, 389–391.
Berner, R.A., 2005. The carbon and sulfur cycles and atmospheric Jeffery, C.H., 2001. Heart urchins at the Cretaceous/Tertiary boundary:
oxygen from Middle Permian to Middle Triassic. Geochimica et a tale of two clades. Paleobiology 27, 140–158.
Cosmochimica Acta 69, 3211–3217. Kaljo, D., 1996. Diachronous recovery patterns in Early Silurian corals,
Brasier, M.D., 1995. Fossil indicators of nutrient levels. 2: evolution and graptolites and acritarchs. In: Hart, M.B. (Ed.), Biotic Recovery from
extinction in relation to oligotrophy. In: Bosence, D.W.J., Allison, P.A. Mass Extinction Events. Geological Society, London, Special
(Eds.), Marine Palaeoenvironmental Analysis From Fossils. Geolog- Publications, vol. 102, pp. 127–134.
ical Society Special Publication, vol. 83, pp. 133–150. Kauffman, E.G., Erwin, D.H., 1995. Surviving mass extinctions.
Cotgreave, P., 1993. The relationship between body size and Geotimes 14, 14–17.
population abundance in animals. Trends in Ecology and Kauffman, E.G., Harries, P.J., 1996. The importance of crisis progenitors
Evolution 8, 244–248. in recovery from mass extinction. In: Hart, M.B. (Ed.), Biotic
144 R.J. Twitchett / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 132–144
Recovery from Mass Extinction Events. Geological Society, London, Schubert, J.K., Bottjer, D.J., 1995. Aftermath of the Permian–Triassic mass
Special Publications, vol. 102, pp. 15–39. extinction event: palaeoecology of Lower Triassic carbonates in the
Keller, G., 2003. Biotic effects of impacts and volcanism. Earth and western USA. Palaeogeography, Palaeoclimatology, Palaeoecology
Planetary Science Letters 215, 249–264. 116, 1–39.
Kingsford, M.J., Hughes, J.M., 2005. Patterns of growth, mortality and Smith, R.M.H., 1995. Changing fluvial environments across the
size of the tropical damselfish Acanthochromis polacanthus across Permian–Triassic boundary in the Karoo Basin, South Africa, and
the continental shelf of the Great Barrier Reef. Fishery Bulletin possible causes of tetrapod extinctions. Palaeogeography, Palaeo-
103, 561–573. climatology, Palaeoecology 117, 81–104.
Krystyn, L., Baud, A., Richoz, S., Twitchett, R.J., 2003. A unique Smith, A.B., 2001. Large-scale heterogeneity of the fossil record:
Permian–Triassic boundary section from Oman. Palaeogeography, implications for Phanerozoic biodiversity studies. Philosophical
Palaeoclimatology, Palaeoecology 191, 329–344. Transactions of the Royal Society of London. Series B 356, 351–367.
Labarbera, M., 1986. The evolution and ecology of body size. In: Smith, A.B., Jeffrey, C.H., 1998. Selectivity of extinction among sea
Raup, D.M., Jablonski, D. (Eds.), Patterns and Processes in the urchins at the end of the Cretaceous period. Nature 392, 69–71.
History of Life. Springer-Verlag, Berlin, pp. 69–98. Stanley, S.M., 1973. An explanation for Cope's Rule. Evolution 27,
Lockwood, R., 2005. Body size, extinction events, and the early 1–26.
Cenozoic record of veneroid bivalves: a new role for recoveries? Tverdokhlebov, V.P., Tverdokhlebov, G.I., Surkov, M.V., Benton, M.J.,
Paleobiology 31, 578–590. 2002. Tetrapod localities from the Triassic of the SE of European
Marshall, C.R., 1998. Determining stratigraphic ranges. In: Donovan, Russia. Earth Science Reviews 60, 1–66.
S.K., Paul, C.R.C. (Eds.), The Adequacy of the Fossil Record. Twitchett, R.J., 1999. Palaeoenvironments and faunal recovery after the
John Wiley and Sons, Chichester, pp. 23–54. end-Permian mass extinction. Palaeogeography, Palaeoclimatology,
McGhee, G.R., Sheehan, P.M., Bottjer, D.J., Droser, M.L., 2004. Palaeoecology 154, 27–37.
Ecological ranking of Phanerozoic biodiversity crises: ecological Twitchett, R.J., 2001. Incompleteness of the Permian–Triassic fossil
and taxonomic severities are decoupled. Palaeogeography, Palaeo- record: a consequence of productivity decline? Geological Journal
climatology, Palaeoecology 211, 289–297. 36, 341–353.
Newell, N.D., 1952. Periodicity in invertebrate evolution. Journal of Twitchett, R.J., 2006. The palaeoclimatology, palaeoecology and
Paleontology 26, 371–385. palaeoenvironmental analysis of mass extinction events. Palaeo-
Paul, C.R.C., Donovan, S.K., 1998. An overview of the completeness of geography, Palaeoclimatology, Palaeoecology 232, 190–213.
the fossil record. In: Donovan, S.K., Paul, C.R.C. (Eds.), The Adequacy Twitchett, R.J., Krystyn, L., Baud, A., Wheeley, J.R., Richoz, S., 2004.
of the Fossil Record. John Wiley and Sons, Chichester, pp. 111–132. Rapid marine recovery after the end-Permian mass extinction event
Payne, J.L., 2005. Evolutionary dynamics of gastropod size across the in the absence of marine anoxia. Geology 32, 805–808.
end-Permian extinction and through the Triassic recovery interval. Twitchett, R.J., Feinberg, J.M., O'Connor, D.D., Alvarez, W., McCollum, L.,
Paleobiology 31, 269–290. 2005. Early Triassic Ophiuroids: their paleoecology, taphonomy and
Price-Lloyd, N., Twitchett, R.J., 2002. The Lilliput effect in the aftermath distribution. Palaios 20, 213–223.
of the end-Permian mass extinction event. GSA Abstracts with Urbanek, A., 1993. Biotic crises in the history of Upper Silurian
Programs 34 (6), 355. graptoloids: a palaeobiological model. Historical Biology 7, 29–50.
Renaud, S., Girard, C., 1999. Strategies of survival during extreme Wheeley, J.R., Twitchett, R.J., 2005. Palaeoecological significance of
environmental perturbations: evolution of conodonts in response to a new Griesbachian (Early Triassic) gastropod assemblage from
the Kellwasser crisis (Upper Devonian). Palaeogeography, Palaeo- Oman. Lethaia 38, 37–45.
climatology, Palaeoecology 146, 19–32. Wignall, P.B., Benton, M.J., 1999. Lazarus taxa and fossil abundance
Rhoads, D.C., Morse, J.W., 1971. Evolutionary and ecologic significance at times of biotic crisis. Journal of the Geological Society of
of oxygen-deficient marine basins. Lethaia 4, 413–428. London 156, 453–456.
Richmond, C., Marcus, N.H., Sedlacek, C., Miller, G.A., Oppert, C., Wignall, P.B., Twitchett, R.J., 1996. Oceanic anoxia and the end
2006. Hypoxia and seasonal temperature: short-term effects and long Permian mass extinction. Science 272, 1155–1158.
term implications for Acartia tonsa dana. Journal of Experimental Wignall, P.B., Twitchett, R.J., 2002. Extent, duration and nature of the
Marine Biology and Ecology 328, 177–196. Permian–Triassic superanoxic event. In: Koeberl, C., MacLeod, K.G.
Savrda, C.E., Bottjer, D.J., 1986. Trace-fossil model for reconstruction (Eds.), Catastrophic Events and Mass Extinctions: Impacts and
of paleo-oxygenation in bottom waters. Geology 14, 3–6. Beyond. Geological Society of America Special Paper, vol. 356,
Savrda, C.E., Bottjer, D.J., Gorsline, D.S., 1984. Development of a pp. 395–413.
comprehensive oxygen-deficient marine biofacies model: evidence Zachos, J.C., Arthur, M.A., Dean, W.E., 1989. Geochemical evidence
from Santa Monica, San Pedro and Santa Barbara Basins, California for suppression of pelagic marine productivity at the Cretaceous–
continental borderland. American Association of Petroleum Geolo- Tertiary boundary. Nature 337, 61–64.
gists Bulletin 68, 1179–1192.