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Evolution of Life Cycles
in Early Amphibians
Rainer R. Schoch
Staatliches Museum für Naturkunde, D-70191 Stuttgart, Germany;
email: schoch.smns@naturkundemuseum-bw.de
Annu. Rev. Earth Planet. Sci. 2009. 37:135–62
Key Words
First published online as a Review in Advance on
January 20, 2009
larvae, metamorphosis, neoteny, Paleozoic, plasticity, Triassic
The Annual Review of Earth and Planetary Sciences is
online at earth.annualreviews.org
Abstract
This article’s doi:
10.1146/annurev.earth.031208.100113
c 2009 by Annual Reviews.
Copyright All rights reserved
0084-6597/09/0530-0135$20.00
Many modern amphibians have biphasic life cycles with aquatic larvae and
terrestrial adults. The central questions are how and when this complicated
ontogeny was established, and what is known about the lives of amphibians
in the Paleozoic. Fossil evidence has accumulated that sheds light on the life
histories of early amphibians, the origin of metamorphosis, and the transition
to a fully terrestrial existence. The majority of early amphibians were aquatic
or amphibious and underwent only gradual ontogenetic changes. Developmental plasticity played a major role in some taxa but was restricted to minor
modification of ontogeny. In the Permo-Carboniferous dissorophoids, a condensation of crucial ontogenetic steps into a short phase (metamorphosis) is
observed. It is likely that the origin of both metamorphosis and neoteny falls
within these taxa. Fossil evidence also reveals the sequence of evolutionary
changes: apparently, the ontogenetic change in feeding, not the transition to
a terrestrial existence per se, made a drastic metamorphosis necessary.
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INTRODUCTION
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Amphibians:
salamanders, frogs,
and caecilians plus
their extinct relatives,
Lower Carboniferous
to Recent
Tetrapods: the
four-legged land
vertebrates
(amphibians, reptiles
and birds, mammals)
and their extinct
relatives, Upper
Devonian to Recent
Metamorphosis: in
amphibians, a short
phase of rapid changes,
in which a water-living
larva (e.g., a tadpole)
transforms into a
(typically) land-living
adult
Neoteny: a life
history strategy only
known in amphibians,
in which sexual
maturity is reached in
the larval stage,
permitting a species to
abandon
metamorphosis
Deceleration: an
evolutionary change in
ontogeny, resulting in
a slowdown of the
developmental rate
with respect to the
ancestor (formerly
sometimes called
neoteny)
The origin of land vertebrates is traditionally considered to have involved some transition from
fish-like animals to ones resembling modern amphibians (Romer 1958, Schmalhausen 1968).
Among the surviving tetrapods, salamanders are generally believed to come closest to that primitive condition. Many modern salamanders have aquatic larvae that transform, through a process
referred to as metamorphosis, into a terrestrial adult during a relatively short period of time.
In frogs and toads, the transition is even more drastic, and unlike salamanders, they are unable
to abandon metamorphosis because sexual maturity is reached late. Abandonment of the adult
terrestrial phase is a frequent evolutionary strategy in salamanders, referred to as neoteny. This
may result from a deceleration of development or from the truncation of ontogeny, omitting all
stages within and after metamorphosis. In this concept, neoteny is a life history strategy of taxa
that have larval stages; it differs from an old definition of neoteny (Alberch et al. 1979) as a simple
reduction in the rate of development (of any organism), an evolutionary process that is referred
to as deceleration today (see Reilly et al. 1997). In the limbless caecilians, metamorphosis is not
as dramatic an event as in living salamanders, but still involves numerous fast changes throughout
the body (Reiss 1996). Although these facts suggest that metamorphosis is a shared character of
all modern amphibians (the lissamphibians) (Reiss 2002), many extant species have no need to
metamorphose at all (Duellman & Trueb 1986). However, this mode of reproduction is believed
to be evolutionarily derived and apparently has been acquired independently in numerous lineages
of modern amphibians (Wake 1982).
Hence, the general consensus is that early tetrapods should have metamorphosed as well,
although this view is often not formulated explicitly (Schmalhausen 1968). However, when the
available evidence in the fossil record is carefully analyzed, the phenomena of metamorphosis
and neoteny are elusive (Schoch 2001). Instead, most Paleozoic tetrapods, and especially the vast
majority of early amphibians, underwent only gradual changes in ontogeny (Boy 1974). Although
a few of the larger taxa such as Eryops were probably capable of effective locomotion on land, they
reached the adult morphology only after a long phase of incremental transformation (Schoch
2002a). Moreover, their skulls and dentition do not differ from their more common aquatic
relatives, which were evidently fish eaters according to preserved gut contents.
The central questions to be addressed in this review are how and when the complicated life cycles of modern amphibians evolved. Here, I focus on (a) the evolution of the ontogeny in Paleozoic
and early Mesozoic amphibians and (b) our current knowledge of their paleoecology inferred from
the analysis of the sedimentary deposits from which these fossil tetrapods are recovered. There is
now substantial evidence for a broad range of life cycles in early amphibians, and we know a great
deal about how these relate to the environments in which these taxa lived. This is the first time
that developmental data are analyzed in an evolutionary context for such a wide range of early
tetrapods. The present synopsis reports the emerging picture from numerous paleontological,
developmental, and paleoecological studies carried out in the past decades (Boy 1972, 1974, 1977,
1988, 1990; Schoch 1992, 2002b, 2003; Warren & Schroeder 1992; Boy & Sues 2000; Schoch &
Fröbisch 2006; Witzmann 2006; Witzmann & Schoch 2006).
EARLY AMPHIBIAN DIVERSITY
The knowledge of early tetrapod evolution is still cast with major uncertainties, and the phylogenetic debate is in a state of flux (Laurin & Reisz 1997, Clack 2002, Ruta et al. 2003b). Although
it is widely accepted that modern amphibians form a natural group with resepct to all other living groups (Lissamphibia), their origin among the vast range of Paleozoic taxa remains debated
(Laurin & Reisz 1997, Ruta et al. 2003a, Vallin & Laurin 2004, Anderson 2007). Recent finds
136
Schoch
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Temnospondyli
50 cm
Eryops
Seymouriamorpha
20 cm
E ARL Y
Microsauria
Pantylus
Nectridia
10 cm
Diplocaulus
A M P H I B I A N S
5 cm
L E POSPONDYL I
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Seymouria
Aistopoda
2 cm
Phlegethontia
Lysorophia
1 cm
Lysorophus
Figure 1
The major groups of Paleozoic and early Mesozoic amphibians. The most speciose clade (Temnospondyli) includes many large-sized
taxa (1–6 m) and probably gave rise to lissamphibians. The seymouriamorphs were 1–2-m-long Permian upland dwellers. The
lepospondyls were diverse but generally of tiny size, and they disappeared after the Permian period. Skeletons drawn to different scales.
have supported the hypothesis that at least frogs and salamanders (Batrachia) arose from a group
of dwarfed temnospondyls, the amphibamids (Anderson et al. 2008). Yet the origin of the modern
limbless amphibians (caecilians) is still controversial (Ruta & Coates 2007, Anderson 2007).
Phylogenetically speaking, the term amphibians should be restricted to the Lissamphibia and
their stem group. However, as the origin(s) of the lissamphibians is still not satisfactorily resolved,
it is fair to refer to all those groups that have been recently considered potential stem-group taxa
as early amphibians. These fall into the following major clades (Figure 1):
1. Temnospondyli: a speciose natural group (160 genera, 300 species) of mostly aquatic
tetrapods known from the Viséan (middle Lower Carboniferous) through the Aptian (upper
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WHY STUDY ONTOGENY?
Ontogenetic data can provide deep insights into morphology. Instead of the static view, focused on adult anatomy,
larval and juvenile morphologies offer the option to study growth trajectories of body parts. Although adult morphology may differ between taxa, the ontogenetic pathways can still be similar. For instance, recent salamanders and
Paleozoic amphibians differ in many aspects of skull morphology. However, some bones went through remarkably
similar morphogenetic stages in both groups. Yet because in salamanders the differentiation of most bones ended
at an earlier stage than in branchiosaurids, their adult morphology differs substantially. Hence, ontogenetic studies
may sometimes detect hidden similarity, such as shared spatial or temporal patterns of skeleton formation.
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Lower Cretaceous). They formed the majority of medium-sized (1–2 m) to large (2–6 m)
tetrapods in stream, lake, and swamp environments (Schoch & Milner 2000). At least
frogs, but probably salamanders as well, originated from temnospondyls, probably in the
Stephanian (Upper Carboniferous)-Lower Permian interval (Ruta & Coates 2007, Anderson
et al. 2008, see Vallin & Laurin 2004 for disagreement). Most temnospondyls resemble giant
salamanders and were predominantly fish eaters.
2. Seymouriamorpha: a small clade of tetrapods, falling into two distinct groups, the aquatic
discosauriscids and the terrestrial seymouriids (Klembara et al. 2006). Although they
are probably not closely related to lissamphibians, they share numerous plesiomorphic
features of modern amphibians (e.g., aquatic larval stage and external gills). They are
generally believed to be closely related to modern amniotes (Laurin & Reisz 1997,
Clack 2002).
3. Lepospondyli: a heterogenous but probably monophyletic group (62 genera, 84 species) of
mostly tiny (5–10 cm) tetrapods, which includes many superficially salamander-like species,
but also numerous aberrant aquatic forms as well as limbless animals (Carroll et al. 1998).
Modern caecilians have been referred to as lepospondyls by some authors (Anderson 2007),
although others hold that all lissamphibians might have originated from them (Laurin &
Reisz 1997, Vallin & Laurin 2004).
In this review, the basal most tetrapods are not considered, because their life cycles are unknown
and their relationships to lissamphibians unclear. These groups include the baphetids, colosteids,
anthracosaurs, and various stem tetrapods (Acanthostega, Ichthyostega, Tulerpeton, Pederpes), which
have been summarized by Clack (2002, 2009).
FOSSIL ONTOGENIES
Larval Life in Early Amphibians
Monophyletic group:
a group of taxa with a
common ancestor,
including all
descendants of that
ancestor (synonym:
clade)
138
Juvenile and larval specimens have been described from numerous Paleozoic amphibians (Boy
1974, Carroll & Gaskill 1978, Schoch 1992, 2002a, Warren & Schroeder 1992, Klembara 1995,
Boy & Sues 2000, Anderson 2002, Klembara & Ruta 2005). These cases show that ontogeny was
quite diverse in early amphibians, highlighting differences in larval ecology and growth between
clades. Typical features of most or all early amphibian larvae are as follows (Figure 2):
1. Many temnospondyls, microsaurs, and aistopods (see Figure 1) share hyobranchial skeletons, which formed a series of interconnected rods arranged like a basket behind and below
the skull (Figure 2). By analogy with bony fishes and lissamphibians, the hyobranchium supports the external gills in larvae, but may be retained in adults to form the floor of the tongue.
Schoch
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a
b
Lateral line
groove
Lateral line
grooves absent
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Larval
ornament
Polygonal
adult
ornament
Braincase bones
present
c
d
e
Cartilage
Palate
Bony gill skeleton
Gill slit
Skull roof
Body outline
Massive
girdle
Hyobranchial
apparatus
Short
trunk
Ceratobranchial
External gills
Bony
tarsals
Gill
Branchial
clefts dentition
Long swimming tail
Short tail
Figure 2
Features of early amphibians correlating with their life habits. (a) Larval morphs (temnospondyl Micromelerpeton) possessed lateral line
sensory organs (found only in aquatic vertebrates). (b) Adult morphs (Micromelerpeton) lacked lateral lines and had a different bone
ornament. (c) Aquatic taxa had a gill skeleton (hyobranchial apparatus: cartilage in blue, bone in orange) with gill teeth (branchial
dentition) and external gills (larval Micromelerpeton). (d ) Aquatic taxa had long trunks and swimming tails and poorly ossified skeletons
(Micromelerpeton). (e) Terrestrial taxa were more robust, with massive shoulder and pelvic girdles, a foreshortened trunk, and an
abbreviated tail (Micropholis).
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2.
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3.
4.
5.
11:16
Hyobranchia differ substantially between early amphibians, and some well-preserved cases
suggest differences in the feeding mechanism used (Boy & Sues 2000).
Some exceptionally well-preserved taxa show traces of external gills similar to those of
modern salamanders (the temnospondyls: Isodectes, Apateon, Micromelerpeton, Sclerocephalus,
and Archegosaurus; the seymouriamorph: Discosauriscus). These gills were associated with
typical hyobranchia; on the basis of this correlation, many more early amphibians probably
bore such external respiratory organs even though they are not seen in the fossil specimens.
Witzmann (2004) showed that the primitive condition of tetrapod larvae is to have three
pairs of external gills on each side.
In modern salamander larvae, the rods of the hyobranchium (ceratobranchials) support the
walls of the gill clefts, which open between the bases of external gills, permitting swallowed
water to leave the body. Salamanders have spike-like projections (gill rakers) on all three ceratobranchials, forming a zipper-like apparatus to close the gill clefts. Ceratobranchials were
mostly cartilaginous and thus not preserved in early amphibians, but in a few temnospondyls
they were bony (Dvinosaurus, Onchiodon, Acanthostomatops). Gill rakers have never been found
in any early amphibians. However, in many temnospondyls and the microsaur Microbrachis,
the ceratobranchials bore small bony plates with a battery of teeth. By analogy with bony
fishes, this is called the branchial dentition. Specimens possessing branchial dentitions are
likely to have lived in the water because the dentitions are only of use when the gill slits are
open, permitting water to flow through this region.
Most temnospondyls, the microsaur Microbrachis, and the aquatic seymouriamorphs have
impressions of the lateral line sensory organ on the external side of the skull bones. In contrast
to bony fishes and some early tetrapods (Acanthostega, Ichthyostega, early temnospondyls), the
lateral lines were housed in grooves on top of the bones instead of in completely closed canals.
In many temnospondyls, these grooves were retained in adults.
Larvae of early amphibians all share poorly ossified skeletons: the skull bones were thinlayered and often not fully sutured; the ends of limb bones and ribs were still cartilage capped;
limb elements were undifferentiated and short; and, in many taxa, the vertebrae were not
yet fully formed.
The available data suggest that many early amphibians raised their young in the water, irrespective of what their adult life was like. The environments, however, in which these early larvae
lived were diverse. For instance, there is evidence that some groups preferred or tolerated brackish
or even salt water (e.g., plagiosaurid and trematosaurid temnospondyls), and others are found only
in freshwater lake deposits (dissorophoid and seymouriamorph larvae). Some fast-growing larvae
evidently focused on fish, and therefore preferred lakes and ponds with sufficient palaeonisciform
fish available (large temnospondyls Sclerocephalus, Archegosaurus), whereas others either preyed on
smaller amphibians (Micromelerpeton, Mastodonsaurus) or were microphagous (branchiosaurids).
An overview of the most significant life-history correlates is given in Figure 3.
Metamorphosis
In modern salamanders, frogs and toads, and caecilians, land-living adults either hatch from eggs
laid in the water or are born on land. In species spending their first phase of life in the water,
the change to the terrestrial existence requires profound changes in respiration, locomotion, and
feeding. In modern amphibians, these changes come fast and in close succession, most impressively
in frogs. Accordingly, in this review, metamorphosis is understood as a drastic morphological
transformation that happens in a short period of time. Alberch (1989) referred to metamorphosis
as a “condensation of developmental events.”
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Terrestrial
Aquatic
Ambiguous
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TE M N O SP O N DYL I
S EY M O U R I A M O R PH A
Dissorophoidea
DiscoSeysauriscids mouriids
Micro- BranchioAmphi- melerpesaurid
bamids tontids metamorph
Stereospondylomorpha
Archegosaurids
Zatracheids
ScleroEryopids cephalids
Stereospondyls
Key features:
Locomotion
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Bony limb joints
Pelvis complete
Carpals, tarsals
Shoulder girdle
Vertebral centra
Feeding (land)
Tongue skeleton
Aquatic adults
Branchial dentition
Gill skeleton
Lateral line
Aquatic larvae
Larvae preserved
Gills preserved
Figure 3
Key features indicating the life habits of early amphibians and their presence (circles) in various Paleozoic groups. Unfilled circles
indicate incipient formation of bone; filled circles indicate fully formed bones. Locomotion on land correlates with fully formed bones
in the postcranial skeleton, whereas aquatic habits are indicated by gills, branchial skeletons, and lateral line grooves.
In the literature, metamorphosis in Palaeozoic amphibians was mostly defined on a formal basis,
following a checklist of criteria developed by Boy (1974, 1988) based on a temnospondyl model.
These involved features such as changes in the dermal ornament, the hyobranchial apparatus, and
the formation of braincase bones and the jaw joint. A detailed survey of these features indicated
that many of them cannot be used as universal indicators of metamorphosis (Schoch 2001). It
seems more appropriate to compare ontogenetic trajectories between taxa rather than define
developmental stages, an approach that has been shown to be laden with problems (Alberch
1985).
LIFE CYCLES OF EARLY AMPHIBIANS
Lepospondyls: Successful Dwarfism
Most early amphibians were small, a fact that is often overlooked when the giant amphibians of
the Permian and Triassic are considered. From this perspective, the lepospondyls constitute the
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stereotypical early amphibians, dominated by taxa in the 5 to 20 cm size range. However, the
anatomical diversity of the group is enormous, and its monophyly has sometimes been questioned
(Milner 1993, Ahlberg & Clack 1998) but is also frequently supported by others (Carroll 1995,
Laurin & Reisz 1997, Vallin & Laurin 2004). Recently, both Anderson (2001) and Ruta et al.
(2003a) found lepospondyls to be a natural group, which is followed herein.
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1. The most speciose group are the microsaurs, which were overall salamander-like, with fully
ossified skeletons, strong jaws, and large, often bulbous teeth. Microsaurs seem to have
inhabited the full range of biotopes, from lakes, swamps, ponds, and riverbanks to the terrestrial realm (Carroll et al. 1998). The only well-known ontogeny among microsaurs is that
of Microbrachis pelikani, a long-bodied newt-like animal that lived in the small swamp-lake
of Nýřany in the Czech Republic (Carroll & Gaskill 1978). Microbrachis had well-impressed
lateral lines on the dorsal skull bones, the trunk was elongated to approximately five times
the length of the skull, and the limbs and girdles were minute. Most other microsaurs fall
into two groups: terrestrial salamander-like morphs with short trunks and strong limbs
(Asaphestera, Batropetes, Pantylus, Tuditanus) and caecilian-like forms with elongated trunks,
small limbs, and skulls designed for burrowing (Cardiocephalus, Micraroter, Rhynchonkos). A
range of taxa was even miniaturized; that is, they had reached such a tiny size that their
skeletal structure was affected by scaling effects (Carroll 1990). Microsaurs range from the
late Viséan (middle Lower Carboniferous) (Brigantian of East Kirkton in Scotland) to the
Artinskian (lower Lower Permian) (Carroll et al. 1998).
2. The lysorophians form a small clade that has recently been suggested to be closely related
to some microsaurs, probably deriving from them (Laurin & Reisz 1997). Lysorophians
were extremely elongated, snake-like animals with tiny skulls and rudimentary limbs. Although their ontogeny is largely unknown, adult Lysorophus was found in burrows along with
lungfishes in the Texas Red Beds, which indicates that the animal hibernated in the ground
during the dry season (Olson 1971). Lysorophians probably lived in aquatic environments
during the rainy seasons, which is suggested by their extensive branchial skeletons (Carroll
et al. 1998) and the deposits of tiny ponds in which they occur (Olson 1971, Boy 1977).
Lysorophians range from the Moscovian (Westphalian C) to the Artinskian (upper Lower
Permian) (Carroll et al. 1998).
3. Nectrideans are a peculiar group best known by their largest representative, “napoleon-head”
Diplocaulus magnicornis. They had vertebrae formed by membrane bone (which lacked a cartilaginous precursor), neural arches with unique articulations, and tail vertebrae with massive
hemal arches (Bossy & Milner 1998). The laterally compressed swimming tail measured
two-thirds the length of the animal. Most nectrideans were apparently aquatic, although
they lack lateral line impressions; their feeble limbs and extremely long tails resemble those
of modern newts. Diplocaulus is the only nectridean known sufficiently well that its ontogeny
can be described: Rinehart & Lucas (2001) studied a large sample of specimens and found
that Diplocaulus went through a biphasic life cycle. However, in contrast to lissamphibians,
this was not connected with a change in habitat, but possibly involved a change in the mode
of feeding. Nectrideans range from the Bashkirian (Melekesskian of Jarrow, England) to the
Artinskian (upper Lower Permian) (Carroll et al. 1998).
4. The aistopods are unique in several ways: they lack limbs and the pelvic girdle, and their
extremely elongated trunks reach vertebral counts between 78 (mid-Viséan) and 230 (Lower
Permian). Their skulls are fenestrate and their jaws have very wide gapes and long, recurved
teeth. Anderson (2002) described the ontogeny of the triangular-skulled Phlegethontia, which
has feebly ossified skull elements.
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Lepospondyls were successful both in their large taxonomic diversity and their abundance
in Carboniferous and early Permian habitats. Their dwarfism—compared with most other early
tetrapods—was probably key to their success. By analogy with modern salamanders, small size
offers the possibility of using cutaneous respiration (skin breathing), both along the body and
within the mouth epithelium, and this can be done both in the water and on land (Wake 1966).
The large amount of bone in these tiny skeletons, with carpals and tarsals largely ossified and
extensive pelvic girdles, indicates that terrestrial locomotion was an option for almost all microsaurs
(except Microbrachis and Hyloplesion). Further, the heavy ossification was reached very early, at
developmental stages in which temnospondyls had many fewer elements of the skeleton formed
(Carroll et al. 1998). As a consequence, metamorphosis probably did not occur. Instead, even
tiny specimens looked like adults in the presence and proportions of their bones. Miniaturization
meant that scaling effects came into play, such as large surface-to-volume ratios making cutaneous
respiration an attractive option. Although skin breathing is common in modern salamanders, their
larvae are usually quite different from the adults, refelecting profound differences in feeding and
ecology. Hence, despite their superficial resemblance to modern salamanders, lepospondyls must
have had quite different life histories.
Amniotes: all land
vertebrates lacking an
aquatic larval stage
that lay eggs on land
or bear live young
Seymouriamorphs: Either Water or Land
Seymouriamorphs form a small clade known from the Permian of Eurasia and North America.
They were long conceived as a stem amniote clade, but this view was challenged by phylogenetic
analyses in which they nested much more basally (Laurin & Reisz 1997, Anderson 2001, Clack
2002). Recently, in turn, Ruta et al. (2003a) found seymouriamorphs to be stem-amniotes again,
showing that the issue is far from settled. Seymouriamorphs fall into two groups: the seymouriids,
which had terrestrial adults known from floodplain deposits such as Tambach (Germany) and the
Red Beds of Texas and New Mexico; and discosauriscids, which were aquatic forms inhabiting lakes
in Central Europe (Czech Republic, Germany) and Asia (Tadzhikistan, Kazakhstan). Seymouria
had a fully ossified skeleton with large and robust limbs and a massive axial skeleton (Berman
et al. 2000). Both from its anatomy and the habitats in which it was found, we infer that this
genus was capable of locomotion on land and probably had a fully terrestrial existence (Eberth
et al. 2000). Discosauriscus is only known from lake deposits and appears like a larva compared
with Seymouria, with a poorly ossified skeleton and weakly built limbs (Klembara & Bartı́k 2000).
Even external gills were present, as exquisitely preserved in lake mudstones (Klembara 1995).
Therefore, Discosauriscus was sometimes regarded the juvenile of Seymouria. However, although
new finds from Tambach yielded juveniles of Seymouria sanjuanensis that fall into the size range of
adult Discosauriscus austriacus, a detailed comparison of the two genera reveals profound differences
For example, Seymouria grew some adult features at a faster rate than Discosauriscus, and each taxon
has its own set of unique (apomorphic) characters (Klembara et al. 2006). Thus, Discosauriscus and
other aquatic seymouriamorphs were not simply larvae of terrestrial taxa but formed a clade of their
own, similar to the situation of the branchiosaurid temnospondyls (see below). However, unlike
branchiosaurids, there is no evidence for either metamorphosis or neoteny in seymouriamorphs.
Early Temnospondyls: Increasing the Size Range
In temnospondyls, numerous ontogenetic trajectories have been described, providing rich data on
their life histories (Figure 4). In contrast to other Paleozoic amphibians, temnospondyls could
reach a relatively large size, with Edops and Nigerpeton probably falling in the 2.5–3 m range.
Some of the most primitive taxa are preserved together with a terrestrial amniote fauna inside
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Terrestrial
Aquatic
Ambiguous
Eryopid
Amphibamid
Zatracheid
Branchiosaurid
Pelvis
complete
Ontogenetic events
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Limb joints
fully formed
Sclerocephalus
Carpals,
tarsals,
complete
Archegosaurus
Shoulder
girdle
complete
Terrestrial
Mastodonsaurus
Aquatic
Braincase
bones form
Last skull
bones form
First skull
bones form
2
4
6
8
10
12
14
16
18
20
40
60
80
100
120
Skull length (cm)
Figure 4
Developmental trajectories (ontogenies) of some of the temnospondyl taxa known from numerous size classes. The plot illustrates the
sequence of key developmental events and the trajectories of the skull sizes and shapes. Advanced ontogenetic events (upper part)
correlate roughly with the capability of leaving the water (some features are listed); these events were never reached by fully aquatic
taxa, in which development ceased at a certain point (lower right).
tree trunks (Dendrerpeton, Cochleosaurus), which suggests they were probably capable of land excursions (Holmes 2000). In an alternative interpretation, these temnospondyls were washed into
the tree trunks during flooding events. In any case, this evidence does not imply that they were
fully terrestrial: Although some taxa lack lateral line grooves, the lateral line in others was partly
enclosed in the bones, making it difficult to detect (Steyer et al. 2006). Most finds are either
from lakes and swamp sediments, such as Cochleosaurus from Nýřany (Czech Republic) (Sequeira
2004) and Balanerpeton from East Kirkton (Scotland) (Milner & Sequeira 1993), or from the
fluvial Red Bed deposits of Texas like Edops (Romer & Witter 1942). All available data indicate
that development was gradual, and there was no transformation typical of modern amphibians
(Schoch 2002a). In Cochleosaurus, which reached larger adult size, larvae had shorter snouts and
poorly ossified limbs, and morphological change through ontogeny progressed very slowly (Steen
1938). The dvinosaurians, a clade of mostly Permian temnospondyls with short faces and feeble
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skeletons, formed a fully aquatic branch. Unlike the earliest forms, they had deeply impressed lateral line grooves throughout their lives, and most of them retained bony hyobranchial skeletons as
adults; adult Trimerorhachis even retained the juvenile branchial dentition. Olson (1979) discussed
evidence that Trimerorhachis either practiced mouth breeding or was cannibalistic.
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Sclerocephalus: Flexible Response to the Environment
One of the most abundant and well-preserved temnospondyls is Sclerocephalus haeuseri from the
Lower Permian of Germany (Figures 4 and 5). This species is known from several hundred
specimens, and a large number of these speciments are now on display in public collections. Its
ontogeny is well known and is believed to represent the condition in primitive temnospondyls
rather well (Boy 1988). As in Cochleosaurus, larvae resembled adults closely, and there was no metamorphosis (Schoch 2003). Sclerocephalus inhabited freshwater lakes, where it was usually the top
TEMNOSPONDYLI
Sclerocephalus
Dendrerpeton
Cochleosaurus
Dendrerpeton
Eryops
Dissorophoidea
Edopoidea
? Fish eater
Zatracheidae
Feeding
on land
Stereospondylomorpha
Eryopidae
?
Fish eater
!
Land excursions
probable/evident
? Diet indicated
only by dentition
! Diet confirmed by
stomach contents
Figure 5
Phylogeny of temnospondyls, with probable life habits mapped onto cladogram. The most primitive taxa (left) probably preyed in the
water but were also present in forest habitats. Dissorophoids and zatracheids (center) specialized in evolving a terrestrial existence for
adults, whereas stereospondylomorphs (right) produced large aquatic predators.
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Ontogenetic
trajectory: linear
coordinate plot of
ontogeny, in which
(a) the sequence of
developmental events
and (b) the rate of
development are
described
Developmental
plasticity: phenotypic
responsiveness of a
species to external
parameters, resulting
in an altered ontogeny
as a response to
environmental
variation
11:16
predator (Boy & Sues 2000). Ossification of the braincase and postcranial elements progressed
very slowly, with some bones and bony joints appearing only in large adults. Most of these bones
were required for support in land locomotion, such as carpals, tarsals, and the joints of limb elements. Fossil trackways suggest that, although large adults made excursions on land (Voigt 2007),
their preferred habitat was lakes. Intestinal contents revealed that Sclerocephalus almost exclusively
fed underwater, focusing on fish (dominated by the actinopterygians Paramblypterus or Aeduella).
Examination of samples from different lakes suggests that Sclerocephalus was able to respond to
environmental parameters by modification of its ontogenetic trajectory. Development could be
truncated, extended, or the rate could be changed. As a consequence, the resulting morphologies and adult sizes are quite variable. Paleoecological studies indicate that the Odernheim Lake
in Germany was large and shallow but seasonally instable and not so rich in nutrition, and the
branchiosaurid populations show signs of stress (Boy 2003). In that environment, Sclerocephalus
truncated development to produce small adults that focused on smaller prey. Instead, the Jeckenbach Lake [near the Saar-Nahe-Lorraine Basin (SNLB) in southwest Germany] was richer and
more diverse, with a complex ecosystem (Boy & Sues 2000). There, Sclerocephalus grew to large
size by extending the trajectory beyond the points reported from other localities and horizons. It
is conceivable that Jeckenbach Sclerocephalus left the lake occasionally, but its regular occurrence
in the lake and proven piscivory (fish eating) indicate it was still predominantly aquatic. In cases
where larger predators were also present (e.g., Niederkirchen Lake, with a 2-m-long shark Orthacanthus), Sclerocephalus was present only with its larvae, whereas adults must have lived elsewhere.
These patterns indicate a high level of developmental plasticity in Sclerocephalus that enabled ready
adjustment to variable lake ecosystems.
Triassic Gigantism: Slow Development, Aquatic Adults
The most impressive early amphibians were the Triassic stereospondyls, which reached a body
length well beyond 3 m, in some cases approaching even 6 m (Schoch & Milner 2000). This vast
clade appears to have been predominantly aquatic (Figure 6), which was confirmed by recent histological analysis (Steyer et al. 2004). Stereospondyls had large parabolic skulls with lateral lines
throughout, a long swimming tail, but rather weak and smallish limbs. The group arose in the
Lower Permian, but reached its maximum diversity in the Lower Triassic. The slender-snouted
genus Archegosaurus forms a plausible stem-stereospondyl. Its ontogeny is well known (Witzmann
2006) and differs from that of Sclerocephalus by having a slower development, resulting in a stretching of the ontogenetic trajectory. Several bones typical of other temnospondyls (pubis, coracoid,
carpals, tarsals) were not formed (Witzmann 2006). Archegosaurus inhabited the same lake systems
as Sclerocephalus but preyed on acanthodian fish instead of actinopterygians (ray-finned fish) and
preferred the center of deep lakes (Boy & Sues 2000). The Middle Triassic Mastodonsaurus giganteus
is the largest known temnospondyl, reaching a snout-to-tail length well beyond 5 m (Schoch &
Milner 2000). Studies of its ontogeny (Figure 4) reveal an even flatter, stretched-out version of the
trajectory exemplified by Archegosaurus. Even though the rate of development of Mastodonasaurus
was very slow, it was not truncated compared with other members of its clade. Thus, the last developmental events in Mastodonsaurus were the same as in Sclerocephalus and Micromelerpeton, including
the formation of the coracoid, pubis, carpals, and tarsals. Like Archegosaurus, Mastodonsaurus was
a fully aquatic animal that retained lateral line sulci on the dermal bones even in the largest adults
and had poorly established limbs hardly capable of any locomotion outside the water. The ontogeny of Mastodonsaurus did not involve any drastic changes, and unlike Sclerocephalus or Onchiodon,
even tiny specimens are remarkably similar to the adult morphology. Similar observations were
recently made on trematosaurid ontogeny (Schoch 2006). The general stereospondyl condition
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TEMNOSPONDYLI
Stereo spo nd y li
T
Mastodonsaurus
Trematolestes
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Eryops
Capitosauria
Trematosauria
Gerrothorax
Eryopidae
Sclerocephalus
Gigantism
Plagiosauridae
Bottom
dweller
Sclerocephalidae
Slow transformation
into land-living adult
Increased developmental
plasticity
Fully aquatic,
large predators
Figure 6
The large temnospondyls include amphibious taxa that transformed slowly into 2-m-long adults such as Eryops, aquatic taxa with high
developmental plasticity (1.5-m-long Sclerocephalus), and a diverse clade of aquatic taxa inhabiting streams, lakes, and even the sea
(2–6-m-long Stereospondyli).
must have involved numerous changes in early life (probably a steep first part of the trajectory)
and the early establishment of adult features; the longest part of the trajectory encompassed very
slow changes with almost no morphological change or metamorphosis. Despite the large numbers
of specimens from different localities and sedimentary facies, the best-studied stereospondyls all
had stable, well-constrained ontogenies (Rhinesuchus, Trematolestes, Metoposaurus, Mastodonsaurus).
Stereospondyls were the dominant top predators in late Permian and early Mesozoic ecosystems,
and their gigantism and presence in the same habitat all of their life reflects stable living conditions. They reached a worldwide distribution and are known from the Upper Permian (Ufimian
of South Africa) through the Lower Cretaceous (Aptian of Australia).
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Plagiosaurids: Life Bound to the Water Bottom
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The most bizarre clade of aquatic amphibians are the plagiosaurids. They evolved extremely
flattened skulls and bodies, paralleling modern flatfishes in some features (Hellrung 2003). Unlike
almost all other aquatic temnospondyls, plagiosaurids probably developed at a faster rate and
had fully ossified skeletons with complete bony braincases and all postcranial elements wellestablished except for carpals (wrist bones) and tarsals (ankle bones). Thus, whereas the trajectory
of plagiosaurids involved similar events as in other stereospondyls, these occurred at a faster pace,
with the final morphology (a carapace-bearing water-bottom dweller) established relatively early.
The inherited stereospondyl trajectory (Archegosaurus, Mastodonsaurus) was apparently modified
to meet the selective pressure for a protection against predators in these nearly immobile animals.
Although complete larval skeletons are still unknown, drastic morphological changes are unlikely,
because small single bones are identical to those of adults. Like in neotenic branchiosaurids, the
last part of the plagiosaurid trajectory was flat, with no identified skeletal changes occurring in
adult life. Plagiosaurids are known from the Middle to Upper Triassic from Central Europe and
the Urals.
Eryopids: Land Excursions Probable, but Slow Transformation
One of the stereotypical lower tetrapods is Eryops, the 2–3-m-long temnospondyl from the Red
Beds of Texas (Romer 1947). Despite its humble appearance, this genus must have been capable
of land excursions as it had fully ossified shoulder blades, pelvis, joints, carpals (wrists), and tarsals
(ankles). In this respect, Eryops was not unlike Seymouria, but it reached a substantially larger size.
Unlike upland dwelling Seymouria, eryopids inhabited lowland pond and stream environments,
where they probably fed on aquatic animals. The ontogeny of eryopids is most interesting: the
European genus Onchiodon underwent similar morphological changes as Sclerocephalus but within
a much shorter time. In this sense, the eryopid ontogenetic trajectory—modified from that of
Sclerocephalus in the opposite way from that of Archegosaurus—became steeper. However, there
was still no period of drastic changes comparable to that in modern lissamphibians. Instead, the
transformation from an aquatic juvenile into a terrestrial animal progressed gradually and must
have spanned a considerable time (Boy 1990, Schoch 2002a). Starting with a larva almost identical
to that of Sclerocephalus, Onchiodon developed a very broad skull, large internal narial openings
(choanae)—presumably required for intensified aerial respiration—and stout limb bones with
numerous attachments for muscles required in limb-driven locomotion (Boy 1990). Unlike aquatic
amphibians swimming by undulations of trunk and tail, eryopids had abbreviated and stiffened
trunks and much larger arms and legs, which propelled the body on land. After all, Eryops and
Onchiodon still appear somewhat paradoxical in that they probably spent a considerable time outside
the water, but most likely still preyed on fish and aquatic tetrapods. The discovery of lateral line
canals inside the skull bones highlights this (Warren 2007).
Zatracheids: Adults Feeding on Land
The zatracheids form a tiny clade of short-bodied and big-headed animals resembling the modern
horned frog genus Ceratophrys. Their larvae, which again closely resemble those of Sclerocephalus,
were aquatic with larval gill skeletons. After a rather short phase of transformation, the skull became wider and the trunk and tail proportionally much shorter, as exemplified by Acanthostomatops
vorax (Witzmann & Schoch 2006). In that species, the larval gill-cleft supporting hyobranchium
was resorbed during some kind of metamorphosis, and a much different, adult tongue-supporting
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skeleton formed. This recalls the situation in many salamanders, where a similar remodeling of the
hyobranchium marks the change from underwater to terrestrial feeding (Wake & Deban 2000). In
further analogy with salamanders and frogs, Acanthostomatops probably housed a large intermaxillary gland, which in modern batrachians produces a sticky seceretion for the capture of prey on
land. Zatracheids are exclusively known from the Lower Permian of North America and Europe.
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Dissorophoids: Increased Developmental Plasticity
The dissorophoids were small, often miniaturized temnospondyls that probably gave rise to lissamphibians (Bolt 1969, Anderson et al. 2008) (Figure 7). Although they have various juvenile features
that make them appear paedomorphic, most known species were probably terrestrial as adults.
Immature specimens are known from three groups: the Micromelerpetontidae, Branchiosauridae, and Amphibamidae (Milner 1982, Boy 1974, Schoch 1992, Witzmann & Pfretzschner 2003).
As exemplified by Micromelerpeton credneri, the first of these clades to appear was largely aquatic
but had reached an increased level of plasticity. Adult size and morphology differ conspicuously
DISSOROPHOIDEA
O l s on i f or mes
Trematopidae
Dissorophidae
Dwarfed tax a
Branchiosauridae
Neoteny
Amphibamidae
Micromelerpetontidae
Pedicely
Fully aquatic
Drastic metamorphosis
Aquatic adaptation
Terrestrial adaptation
Filter-feeding larva
Figure 7
The most terrestrial Paleozoic amphibians were the dissorophoids, which were generally smaller than one meter. They include the
aquatic micromelerpetontids, the dwarfed amphibamids and branchiosaurids, and the larger, armor-plated olsoniforms. A
lissamphibian-like metamorphosis evolved within the dissorophoid clade, and the origin of specialized larvae enabled the evolution of
adults with larval morphologies (neotenes).
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between three different populations that inhabited different lakes (Boy & Sues 2000). Unlike
Sclerocephalus, Micromelerpeton was not only variable regarding adult size, but also produced different morphotypes, ranging from small to large predators with different tooth morphologies (Boy
& Sues 2000). Dissorophoids (sensu stricto) are known from the Pennsylvanian (North America
and Europe) through the Lower Triassic (South Africa), and if the temnospondyl hypothesis of
lissamphibian origin is correct, modern salamanders and frogs are surviving dissorophoids.
Branchiosaurids: Neoteny as Life History Strategy
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The monophyletic Branchiosauridae form a clade of 5–15-cm-long aquatic dissorophoids with
a larval appearance (Boy & Sues 2000). Most species seem to have been exclusively aquatic and
therefore have been interpreted as neotenes (Boy 1972), and it was long believed that they were
all neotenic. However, a drastic metamorphosis was recently reported in one species (Schoch &
Fröbisch 2006). The ontogenetic trajectories of all the aquatic branchiosaurids stagnate at some
point in development, beyond which only their sizes change. This point is seen as an indication of
the onset of neoteny (Figure 8). Unlike all other temnospondyls, neotenic branchiosaurids simply
BRANCHIOSAURIDAE
Apateon
Metamorphosis
Number of studied ontogenetic events
60
Terrestrial
50
A. gracilis
Bifurcation
Stagnation
40
Neoteny
30
20
Aquatic
10
A. caducus
LARVA
0
2
4
6
8
10
ADULT
12
14
16
18
20
30
Skull length (mm)
Figure 8
In the Permo-Carboniferous branchiosaurids, the ontogenetic trajectory was significantly modified
compared with that of other temnospondyls; it either stagnated beyond a certain point, which led to the life
history strategy of neoteny (adult life in water, paedomorphic morphology), or it went through a fast
sequence of major changes (drastic metamorphosis), after which the adult was capable of a fully terrestrial
existence.
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failed to form numerous bones, independent of the adult size they reached. Moreover, immature
specimens of all branchiosaurid species share a range of larval adaptations, such as specialized
brush-like branchial dentition (interpreted as a device for filter feeding), needle-shaped larval teeth,
and an open cheek that might have permitted a greater mobility of the skull during suction feeding.
The evolution of cranial kinesis (a skull in which the single elements were moveable against each
other) was most likely made possible by the concommitant slowdown in the ontogenetic formation
of the skull roof (Schoch & Milner 2008).
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Amphibamids: Miniaturization and Metamorphosis
The most readily overlooked temnospondyl fossils are those of amphibamids, which were dwarfs
in the 5–12 cm size range inhabiting upland environments. The smallest taxa, Amphibamus and
Doleserpeton, had thin skeletal elements, including the bones surrounding the eye opening, the
back of the skull roof, and the elements in the shoulder girdle. In Amphibamus and its probable
close relative Platyrhinops, the early ontogeny is known, and their larvae hardly differ from branchiosaurids (Milner 1982, Clack & Milner 2007). Similar to the metamorphosing branchiosaurid,
metamorphosis was profound and brought drastic changes, including in ornamentation, extreme
widening of the skull and palatal vacuities, and change in the shape of teeth: like lissamphibians,
both Amphibamus and Doleserpeton had pedicellate teeth, characterized by a moveable crown with
two tips (Bolt 1969). Hyobranchial skeletons are known from both Amphibamus and Doleserpeton
larvae (which look similar to those of branchiosaurs) and adults (where they look like those of
adult salamanders), indicating that the change of habitat correlated with a change in feeding. Our
knowledge of this group has been greatly augmented by the fascinating find of the amphibamid
Gerobatrachus from the Lower Permian of Texas (Anderson et al. 2008), which bridges the gap
between Paleozoic amphibians and modern salamanders and frogs.
Dissorophids and Trematopids: Armored Upland Dwellers
Unlike earlier temnospondyls, dissorophoids include several clades that specialized in different,
well-defined life history strategies. The mostly neotenic branchiosaurids and the metamorphosing, dwarfed amphibamids were probably closely related (Milner 1988, Schoch & Milner 2008).
Their probable sister taxon is formed by two clades of larger, more robust animals, the olsoniforms (dissorophids plus trematopids). These reached a maximum body length of approximately one meter, with oversized heads, abbreviated trunks, and short tails (Williston 1910).
Their limbs were stout and fully ossified, and the back was often covered with numerous bony
plates or “armor” (DeMar 1968). These animals were probably upland dwellers (Carroll 1964),
the only larger temnospondyls that lived in the same environments as the terrestrial seymouriamorphs and amniotes. In one of the most fascinating discoveries, Milner (2007) reported an
ontogenetic sequence of the trematopid Mordex, starting from branchiosaurid-like larvae (including a filter feeding branchial dentition) and ending up with fully terrestrial adults. This confirms that branchiosaurids were not the stereotypical temnospondyl larvae—as Romer (1939) had
suggested and Boy (1972) was able to reject—but that they had a highly derived larval morphotype that evolved within dissorophoids and was probably shared among the amphibamids,
branchiosauirds proper, and olsoniforms. The basal dissorophoids Micromelerpeton and Branchierpeton were neither metamorphosing in the sense defined here, nor did they evolve neotenic
taxa; instead, they closely resembled the larvae of Sclerocephalus (Werneburg 1991, Boy & Sues
2000).
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HABITATS AND PALEOECOLOGY
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Like only a few other vertebrates, many Paleozoic and early Mesozoic amphibians are known
from a range of localities which preserve essential components of the paleoecosystems these taxa
occupied. In addition to cases of exceptional preservation (such as stains of skin, gill skeletons,
and even shadows of external gills), these lagerstätten provide rich information on normal populations (large time-averaged samples of specimens) as well as their paleocommunities and even their
interspecific interactions (through gut contents, coprolites, and evidence of scavenging). These
data are complementary to the ontogenetic and morphological studies reported above, and together these provide a more complete picture of early amphibian life and evolution. The preserved
habitats range from coastal lagoons, salt marshes, and brackish lakes to large intermontane longterm lakes, small ponds, and oxbow lakes, as well as to floodplains with streams and ephemeral
ponds and even cave systems. This wide range of environments seems to have been inhabited by
early amphibians from at least the Pennsylvanian through the Permian. By the Lower Triassic,
most terrestrial amphibians had disappeared, whereas the aquatic stereospondyls now populated
numerous rivers, swamps, and even marine environments.
Coastal Rain Forest and Floodplain: Joggins
One of the earliest well-preserved faunal assemblages is the Joggins Formation of Nova Scotia,
Canada. This upper Pennyslvanian deposit (Westphalian A) preserves three different environments
and their ecosystems (Falcon-Lang et al. 2006). Joggins was located within the continent, but
was reached by a distal extension of the European marine band, which formed a brackish sea
in Nova Scotia. In the open water, numerous shark and bony fish species co-occurred with early
tetrapods (baphetids). On the coastal plains, tropical rain forests spread and housed a rich tetrapod
fauna composed of terrestrial temnospondyls (Dendrerpeton), four genera of terrestrial microsaurs
(Asaphestera, Hylerpeton, Leiocephalikon, Ricnodon), and three amniotes (a captorhinomorph and
two synapsids). Dendrerpeton and the other tetrapods have been found in tree stumps of large
lycopods, where they probably became trapped. Scavenging dissolved and dissociated most of
their skeletons. The tetrapods coexisted with a wide range of arthropods, including myriapods
(e.g., 2-m-long Arthropleura), eurypterids, arachnids, and insects (Carroll et al. 1972), and the
forest consisted of lycopods, calamiteans, ferns, pteridosperms, and cordaitaleans (Falcon-Lang
et al. 2006). Unfortunately, larvae of amphibians (temnospondyls, microsaurs) are unknown from
Joggins. The third type of ecosystem formed on well-drained alluvial plains and included rather
rare microsaurs and anthracosaurs. Another tree stump locality with tetrapods is Florence, in Nova
Scotia, which produced the temnospondyl Cochleosaurus (Godfrey & Holmes 1995).
Swamps and Lakes: Nýřany
One of the richest Paleozoic lake deposits with an autochthonous fauna is the Gaskohle (gas
coal) of Nýřany, southwest of Plzen, Czech Republic. The fauna was described in 15 detailed
monographs by Fritsch (1879–1901), the sedimentary facies were described by Pešek (1974), and
the paleocommunity was analyzed by Milner (1980). Situated within the Upper Pennsylvanian
Plzen Basin, the Nýřany Member (Westphalian D) consists of flood-plain deposits and alluvial
fans, with swamp and lake deposits restricted to a small area of a few kilometers in cross section.
The Gaskohle formed in a perennial lake that was intermittently overgrown. The tetrapod-rich
layers are found at the local transition from a swamp to a stratified lake in which no currents
existed. Apparently, the Nýřany swamp-lake was less than 1 km in diameter, poorly aerated, and
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impoverished in fish. Instead, small aquatic amphibians predominated, which were obviously also
breeding in the lake: the temnospondyls Branchiosaurus, Limnogyrinus, and Cochleosaurus; and the
lepospondyls Sauropleura, Microbrachis, and Ophiderpeton. The terrestrial trematopid Mordex was
also breeding in the lake, and its larvae are preserved in substantial numbers along with the similar
branchiosaurids (Milner 2007). After metamorphosis, Mordex apparently left the lake and returned
only in the breeding seasons. The rare temnospondyl Capetus was probably not autochthonous
but was assigned to the marginal terrestrial fauna by Milner (1980). The assemblage at Linton, in
Ohio, is larger than that of Nýřany, and the fauna was more diverse, representing an oxbow lake
within a general swamp environment (Milner 1980).
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Large Intermontane Lakes: Saar-Nahe-Lorraine
In the Stephanian (upper Pennsylvanian)-Permian interval, Central Europe formed the core part
of the Variscian mountain range, which housed numerous intermontane basins (Autun, SaarNahe-Lorraine, Saale-Thüringen, Döhlen, Boskovice, Podkrkonoše). The largest was the SNLB
in southwest Germany, which measured some 80 km in the long axis and in which a continuous series of fluvial to lacustrine sediments were deposited (Rotliegend facies), ranging from the
Gzhelian (upper Pennsylvanian) well into the Sakmarian (lower lower Permian). Most larger lakes
were inhabited by palaeonisciform fishes, whereas in some small lakes the gill-breathing branchiosaurid Apateon was the only vertebrate. In contrast to Nýřany, the diversity was low, with 1 to
3 branchiosaurid species (Apateon, Melanerpeton), a slightly larger dissorophoid (Micromelerpeton),
and the 1.5-m-long top predator Sclerocephalus being the only tetrapods. Lepospondyls are only
known from a few small lakes but were absent in the larger water bodies. In contrast to other
regions, the temnospondyls were exclusively aquatic. Despite thousands of specimens, there is no
evidence that any temnospondyl taxon permanently left the water as an adult. Even the large adults
of Sclerocephalus, which resemble Texas Red Bed Eryops in their excessive bone growth, preyed exclusively on the palaeonisciforms in the lake. Boy (2003) has studied the paleoecology of many
lakes in the SNLB and reported numerous different paleocommunities. The Variscian mountain
lakes all have in common a low taxonomic diversity. This has been attributed to the probable high
altitude of the basin within the vast orogen (Boy & Sues 2000), and this could also explain why
the temnospondyls did not become more fully terrestrial, because low oxygen pressures might not
have permitted the change to a fully terrestrial existence.
Small Lakes: Niederhäslich
The Döhlen basin was only 22 km long and housed small lakes in the region southwest of Dresden in eastern Germany. The Niederhäslich locality was discovered by miners in the nineteenth
century, who quarried the thin Lower Permian limestone beds. Three of these beds are locally
extremely rich in tetrapods, but none contain a single fish (Schneider 1994). The lake deposits preserved calcareous algae, bivalves, and crustaceans (Schneider 1994). The tetrapods fall into three
groups: (a) fully aquatic temnospondyls that lived in the lake throughout their life (Branchierpeton),
(b) larvae of temnospondyls that left the lake as adults and returned only in the breeding season
(tiny Apateon gracilis, Acanthostomatops, and large Onchiodon), and (c) terrestrial tetrapods that were
washed in by a river (microsaurs, seymouriamorphs, diadectids, pelycosaurs, and diapsids).
Floodplain Ponds, Streams, and Oxbow Lakes: Texas Red Beds
The Texas Red Beds form a thick Stephanian-Permian continental sequence deposited on floodplains. In Archer County, thin meander-belt sandstones and fine-grained overbank deposits have
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preserved rich tetrapod assemblages (Sander 1989). Among these, the pond bone beds produce
fish and temnospondyl faunas (Olson 1977). In alternating periods of drought and monsoonal
rains, seasonally drying mudflat ponds and marshes were dissected by channels that formed during floods (Parrish 1978). In this environment, the ponds were inhabited by sharks (Xenacanthus),
fully aquatic amphibians (gill-bearing Trimerorhachis, Diplocaulus), and the anthracosaur Archeria
(Bakker 1982). In some ponds, mass assemblages of Trimerorhachis probably formed when the
water body was drying out, often indicated by abundant desiccation cracks (Case 1935). Another
bone bed, at Thrift, is again rich in Trimerorhachis and probably formed by the inland incursion of
a major tropical storm (Parrish 1978). The large temnospondyl Eryops is found in most deposits,
but is most abundant in mixed floodplain and stream localities (Bakker 1982). As one of the largest
predators, Eryops probably preyed on larger fish and tetrapods of the ponds and rivers: young
adults appear to have preferred swamp habitats, which might have been safer environments for
juveniles (Bakker 1982). In the floodplain deposits, smaller and more fully terrestrial amphibians
(dissorophids, trematopids) also occur, but are less frequent.
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Upland Ecosystems: Tambach and Fort Sill
In contrast to the aforementioned deposits, the central German Bromacker locality at Tambach
formed in a dry upland environment (Eberth et al. 2000). This deposit, which was long famous
for its tetrapod track fauna, also preserves a unique Lower Permian ecosystem with numerous
terrestrial vertebrates (Martens 1989). Aquatic or amphibious tetrapods are absent, and the large
plant-eating amniote Diadectes is unusually common. The amphibian fauna is dominated by seymouriamorphs (Seymouria) and dissorophoids (trematopid Tambachia, amphibamid Georgenthalia)
(Berman et al. 2000). A second, very different upland deposit is preserved in the Dolese Quarry at
Fort Sill, Oklahoma (Olson 1967). For seven decades, continued quarrying unearthed a Permian
cave system with its autochthonous vertebrate fauna that includes remains of 36 fully terrestrial
tetrapods (Reisz 2007). The amphibian fauna is much richer than at Tambach, probably indicating abundant water and more favorable living conditions. The largest predator was a trematopid
(Acheloma), accompanied by a dissorophid (Cacops) and several amphibamids, although microsaurs
and seymouriamorphs are also present (Reisz 2007).
Brackish Swamps and Lakes: Kupferzell
In the Triassic, microsaurs and seymouriamorphs were already extinct, whereas temnospondyls
became extremely diverse and reached worldwide distribution. In numerous sedimentary basins
throughout Pangaea, aquatic stereospondyls are among the most common finds. One of the richest deposits are the swamp and lake horizons of Kupferzell and neighboring localities in southern
Germany (Wild 1980). These Middle Triassic mudstones and carbonates preserve numerous temnospondyls, such as 1–2-m-long plagiosaurids (Gerrothorax, Plagiosuchus), 5–6-m-long Mastodonsaurus, 2-m-long Kupferzellia, 1-m-long newt-like Trematolestes, and 1.5-m-long metoposaurid
Callistomordax. In a lake deposit near Schwäbisch Hall, the mentioned amphibians form an autochthonous fauna (R. Schoch, unpublished work). The freshwater lake must have been rich in
resources because, besides the six predatory temnospondyl species, up to 12 bony fish taxa and
two sharks lived in the water body. None of the temnospondyls left the water, and the terrestrial
fauna was composed of small diapsid reptiles and archosaurs of various sizes. This is quite typical
of Triassic ecosystems, with temnospondyls restricted to rivers, deltas, lakes, and even shallow marine environments, where they formed the largest aquatic predators. Terrestrial temnospondyls
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Primitive life cycle
Derived life cycle
T ER R ES T R I A L A D U L T S
Eryopids
Zatracheids
M E T AM O RP H O S IS
a
Branchiosaurids
Ontogenetic events
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c
Sclerocephalus
Plagiosaurids
b
A Q U A TI C A DU L TS
Capitosaurs
NEOTENY
Age/size
Figure 9
The three different life history strategies employed by Paleozoic and Mesozoic amphibians. (a) slow morphological transformation of
an aquatic larva into an amphibious adult capable of land excursions. (b) stagnating trajectory producing a perennibranchiate adult.
(c) fast transformation (drastic metamorphosis).
or other early amphibians had completely vanished, except for the early lissamphibians whose
habitats are still largely unknown.
AMPHIBIAN LIFE HISTORY STRATEGIES
The ontogenetic and paleoecological data reported in the last sections shed some light on the
evolution of life histories in early amphibians. Apparently, lepospondyls, seymouriamorphs, and
temnospondyls explored different strategies to cope with life around the water-land interface
(Figure 9).
Perennibranchiates
Some taxa of the three earliest amphibian clades share a strategy by which they remain in the
breeding pond as adults (Microbrachis, nectrideans, discosauriscids, many temnospondyls), a perennibranchiate life history strategy. In modern salamanders, this is often practiced by suppressing
metamorphosis, which initiates neoteny; among Paleozoic amphibians, the salamander strategy
evolved only in branchiosaurid temnospondyls. In other groups, in which a drastic metamorphosis
was not established, larvae transformed into adults gradually. If such groups evolved the perennibranchiate condition, they did so by truncating development, with the result that adult features
associated with a terrestrial mode of life did not appear. By definition, this truncation involved
paedomorphosis in some way, but the exact process (rate change, delayed onset, or premature
www.annualreviews.org • Life Cycles in Early Amphibians
Paedomorphosis:
special case of
heterochrony, in which
the ontogenetic
trajectory is truncated,
resulting in an adult
descendant resembling
a juvenile ancestor
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Neotenic morph: a
specific morphology
developed only in
amphibians that fail to
metamorphose,
resulting in aquatic
adults with their own
set of specific features
11:16
offset) was probably different in each case. Branchiosaurids also truncated development to become perennibranchiates, but they employed two additional strategies: (a) they evolved specific
larval morphs, permitting exploitation of the larval niche (filter feeding = microvory), and (b) they
evolved neotenic morphs, allowing them to exploit a different food source form those employing
the first strategy after completing the larval phase (with a focus on crustaceans, fish, and amphibian
larvae = macrovory) Both morphs are typical of branchiosaurids, and intestinal fillings confirm
this (Boy 2003). This novel strategy permitted branchiosaurids to invade lakes that were otherwise
not inhabited by vertebrates (Boy & Sues 2000), and the larval adaptations probably formed a key
innovation that led to an increase in species diversity for this group (Schoch & Milner 2008). This
strategy is here called neoteny, in a more restricted and very specific use of the term (see below).
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Terrestrial Morphs
The alternative strategy to staying in the breeding pond was to produce adults able to leave the
water for at least a short period of time. Tracks indicate that most of these amphibians were not
very elegant creepers, probably using trunk and tail undulations. Such land excursions required
skeletal development and growth to proceed until the body trunk, shoulder and pelvic girdles, and
limbs were strong enough to support locomotion on land. In lepospondyls, these features were
established early in ontogeny and were probably predisplaced (occurring earlier) with respect to
the ontogeny of other groups. This is opposite to the pattern of paedomorphosis and is called
peramorphosis (Reilly et al. 1997). In contrast, temnospondyls and seymouriamorphs developed
these features late in ontogeny (Boy 1974, Klembara & Ruta 2005). Hence, for a species to create
a terrestrial morphology, either the rate of development had to increase (leading to a small adult
size), or the life span had to be extended (leading to an enlarged size). The existence of both
types of peramorphic change is seen in the early onset of strong positive allometry of the limbs
in dissorophoids as compared with their very slow development in the eryopid Onchiodon (Boy
1990). Among peramorphic terrestrial forms, variations in their terrestrial morpholgies—from
amphibious taxa to inhabitants of dry uplands—were readily produced by slight modification of
the ontogenetic trajectory. It is trivial to say that this involved peramorphosis, but extremely hard
to say by which underlying process the peramorphosis was achieved. In other clades (Sclerocephalus,
Micromelerpeton), enhanced developmental plasticity became the strategy for adjusting to variable
environments or stress. Some temnospondyls appear to have been extreme generalists, made
possible by this increased developmental plasticity. This was probably key to the success of Permian
and Triassic temnospondyls, which populated so many different environments.
Metamorphosis
A different strategy for enabling a change in habitat during the life span of an individual evolved
in a peculiar group of terrestrial temnospondyls, the dissorophoids. In addition to changing the
rate and timing of events in their ontogeny, they evolved a short phase in which crucial events
were all coupled: this was the origin of metamorphosis as it is known in lissamphibians (Schoch
& Fröbisch 2006). The origin of the drastic metamorphosis seen in branchiosaurids was a major
turning point in amphibian life history evolution. Whereas the relatively flexible ontogenies of
other temnospondyls permitted many different kinds of change in order to adjust to fluctuating
parameters, branchiosaurids could employ one of two well-constrained alternatives, each canalized
from one path of their group’s bifurcating trajectory (Figure 9). It is very likely that amphibamids,
the probable stem-group of modern batrachian lissamphibians, had the same life history strategy,
as their larvae are hardly distinguishable from those of branchiosaurids.
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In salamanders and frogs, metamorphosis forms a developmental bottleneck that usually must
be passed through as quickly as possible. The crucial evolutionary question here is not what
maintains this bottleneck today (although this is an interesting question) but how it was established
in the first place. The evolutionary trajectory of ever more terrestrial adults may be best exemplified
by two different temnospondyls, Onchiodon and Acanthostomatops. Both genera underwent major
morphological changes throughout their ontogenies, in contrast to the uniform ontogenies of
Cochleosaurus, Sclerocephalus, and stereospondyls. However, this transition was not the dramatic
event it was in branchiosaurids or many lissamphibians. Onchiodon (and Eryops) may have spent
more time out of the water than Sclerocephalus but most likely still preyed on fish: their dentition
differs in no way from that of their aquatic relatives. Morphological transformation proceeded
at a slow rate. Acanthostomatops reached a much smaller adult size than Onchiodon, and its limbs
developed fast with respect to the rest of the postcranium (Witzmann & Schoch 2006). Unlike
Onchiodon, it had small teeth, an intermaxillary gland, and a specialized adult tongue-supporting
skeleton. These features indicate a focus on different prey and a new mechanism to catch it:
the dentition was not well suited for the capture of fish but may have been favorable to secure
arthropods or snails by tongue manipulation. In dissorophoids, most of which were smaller than
Acanthostomatops, the same morphological correlates of feeding are found.
These findings indicate that those taxa in which transformation became more profound (and
increasingly rapid) (i.e., those that evolved metamorphosis) used a different feeding strategy and
prey preference compared with aquatic-feeding (the most common mode) taxa. In other words,
terrestrial prey was the focus instead of aquatic prey. Moreover, their heavily ossified skeletons
and overall morphology suggest that their adults were terrestrial. The initial morphological innovations enabled the establishment of a specific adult feeding mechanism that involved tongue
manipulation (adult hyobranchium) and secretion of sticky liquids in the palate (intermaxillary
gland). Both of these innovations assisted feeding on prey outside the water. To accomplish maximum coherence and integration of these new structures, it appears that their components were
formed within a short period of time. This was best achieved by a condensation of ontogenetic
events; these crucial changes to the feeding apparatus were packed into a metamorphic event
(posterior shift of jaw hinge, enlargement of adductor chamber, transformation of hyobranchial
apparatus, and enlargement of intermaxillary vacuity).
The transition from water to land, per se, was probably not the crucial factor in the evolution
of metamorphosis. Based on fossil trackways, evidently eryopids, edopoids, microsaurs, and seymouriids could all leave the water occasionally without undergoing metamorphosis (Voigt 2007).
Rather, the change from feeding under water to feeding on land and the concomitant shift in prey
preference imposed the critical changes to ontogeny. The crucial factor in the establishment of a
lissamphibian-like metamorphosis was probably not a reduction in adult body size per se, but the
evolution of an ever more complicated and fine-tuned adult feeding apparatus. In amphibamids,
this is highlighted by the invention of a specialized dentition with bicuspidity and pedicely (Bolt
1969, Anderson et al. 2008).
Neoteny
Metamorphosis and neoteny travel together. Once a drastic metamorphosis was established within
dissorophoids, the conventional way to produce a perennibranchiate (slow down the rate of metamorphosis or truncate development to produce an imperfect or juvenilized adult) was not an option
any more. Too many crucial events were already packed into the short period of metamorphosis. Instead, a “neotenic program” appears to have been initiated, which led to the establishment
of specific neotenic features (e.g., a different kind of ornamentation, more robust teeth to grasp
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larger prey under water) and the transformation of the larval traits into adult neotenic traits in an
otherwise frozen larval form. Such morphs are currently known only from branchiosaurids but
may have been more widespread among dissorophoids. A crucial point here is that metamorphosis
and neoteny were present in different species of the same clade (Schoch & Fröbisch 2006). Branchiosaurids were either metamorphosing or obligate neotenes, according to our present knowledge
(Fröbisch & Schoch 2009). We do not yet know at which evolutionary stage the bifurcating developmental pathways evolved within one species, i.e., the option to initiate neoteny as a facultative
strategy, under conditions when metamorphosis was not favorable. Although facultative neoteny
is common in modern salamanders, it is very difficult to prove in fossil taxa.
It would be premature to state which of the two life history strategies—perennibranchiate or
terrestrial—is the primitive, original one for early amphibians and tetrapods in general. Perhaps
this question is the wrong one, because both strategies were always present as an option, and
their frequent parallel evolution supports this. However, regardless of the answer to this specific
question, it is clear that metamorphosis was obviously not a primitive feature of early amphibians.
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SUMMARY POINTS
1. Most early amphibians (especially temnospondyls) were aquatic in the sense that they
(a) bred in lakes or other water bodies in which their young grew up, (b) focused on an
aquatic diet (mostly fish), and (c) retained lateral line organs throughout their lives.
2. Various other early amphibians (especially microsaurs) were capable of a terrestrial existence but did not undergo metamorphosis and were of small size (5–20 cm range).
3. For the vast majority of early amphibians, their larvae and juveniles did not differ substantially from the adults, but some taxa had external gills that were eventually resorbed in
the adults, although the larval branchial dentition and open gill slits were often retained.
4. Most of the better known Paleozoic and Triassic amphibians did not move from their
aquatic habitats as adults, but fossil trackways indicated that they were nevertheless able
to leave the water for extended periods of time.
5. Some Paleozoic temnospondyls were able to adapt to the challenge of fluctuating environments by increasing their developmental plasticity via the ability to fine-tune certain
developmental parameters (rate of development, formation of crucial bones).
6. Metamorphosis as known in modern amphibians evolved tens of millions of years after
the first tetrapods had gained ground.
7. Neoteny (sexual maturity reached in a larval stage) probably evolved as an alternative life
history strategy in species that underwent a drastic metamorphosis.
8. Paleozoic and Mesozoic amphibians occupied a wide range of positions in the trophic
web of paleoecosystems, from tiny filter feeders to giant aquatic top predators; in modern
lissamphibians this range is markedly reduced.
FUTURE ISSUES
1. Histology and skeletochronology are promising fields by which additional data on life
histories (e.g., growth strategies, absolute age data) may be derived in the future.
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2. The study of ontogeny in early amphibians requires more taxa to be sampled, which needs
intensified collecting at deposits where different size classes of the same taxa are found.
3. More paleoecological studies of rich deposits will help to understand the full range of
life history strategies and the structure of the trophic systems.
4. A detailed comparison and calibration of tracks and skeletons might shed light on the
locomotory abilities of terrestrial amphibians.
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DISCLOSURE STATEMENT
The author is not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
I thank Jason Anderson, Jürgen Boy, Robert Carroll, Jenny Clack, Nadia Fröbisch, Hanna
Hellrung, Michel Laurin, Andrew Milner, John Reiss, Armand de Ricqlès, Marcello Ruta, Sophie Sanchez, Thomas Schindler, Dieter Seegis, David Wake, Anne Warren, Ralf Werneburg,
and Florian Witzmann for numerous fruitful discussions, and the Deutsche Forschungsgemeinschaft for supporting a related project on temnospondyl metamorphosis.
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Contents
Volume 37, 2009
Where Are You From? Why Are You Here? An African Perspective
on Global Warming
S. George Philander p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Stagnant Slab: A Review
Yoshio Fukao, Masayuki Obayashi, Tomoeki Nakakuki,
and the Deep Slab Project Group p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p19
Radiocarbon and Soil Carbon Dynamics
Susan Trumbore p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p47
Evolution of the Genus Homo
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Feedbacks, Timescales, and Seeing Red
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Atmospheric Lifetime of Fossil Fuel Carbon Dioxide
David Archer, Michael Eby, Victor Brovkin, Andy Ridgwell, Long Cao,
Uwe Mikolajewicz, Ken Caldeira, Katsumi Matsumoto, Guy Munhoven,
Alvaro Montenegro, and Kathy Tokos p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 117
Evolution of Life Cycles in Early Amphibians
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The Fin to Limb Transition: New Data, Interpretations, and
Hypotheses from Paleontology and Developmental Biology
Jennifer A. Clack p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 163
Mammalian Response to Cenozoic Climatic Change
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Forensic Seismology and the Comprehensive Nuclear-Test-Ban Treaty
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How the Continents Deform: The Evidence from Tectonic Geodesy
Wayne Thatcher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 237
The Tropics in Paleoclimate
John C.H. Chiang p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 263
vii
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Rivers, Lakes, Dunes, and Rain: Crustal Processes in Titan’s
Methane Cycle
Jonathan I. Lunine and Ralph D. Lorenz p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 299
Planetary Migration: What Does it Mean for Planet Formation?
John E. Chambers p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 321
The Tectonic Framework of the Sumatran Subduction Zone
Robert McCaffrey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 345
Annu. Rev. Earth Planet. Sci. 2009.37:135-162. Downloaded from www.annualreviews.org
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Microbial Transformations of Minerals and Metals: Recent Advances
in Geomicrobiology Derived from Synchrotron-Based X-Ray
Spectroscopy and X-Ray Microscopy
Alexis Templeton and Emily Knowles p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 367
The Channeled Scabland: A Retrospective
Victor R. Baker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 393
Growth and Evolution of Asteroids
Erik Asphaug p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 413
Thermodynamics and Mass Transport in Multicomponent, Multiphase
H2 O Systems of Planetary Interest
Xinli Lu and Susan W. Kieffer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 449
The Hadean Crust: Evidence from >4 Ga Zircons
T. Mark Harrison p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 479
Tracking Euxinia in the Ancient Ocean: A Multiproxy Perspective
and Proterozoic Case Study
Timothy W. Lyons, Ariel D. Anbar, Silke Severmann, Clint Scott,
and Benjamin C. Gill p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 507
The Polar Deposits of Mars
Shane Byrne p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 535
Shearing Melt Out of the Earth: An Experimentalist’s Perspective on
the Influence of Deformation on Melt Extraction
David L. Kohlstedt and Benjamin K. Holtzman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 561
Indexes
Cumulative Index of Contributing Authors, Volumes 27–37 p p p p p p p p p p p p p p p p p p p p p p p p p p p 595
Cumulative Index of Chapter Titles, Volumes 27–37 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 599
Errata
An online log of corrections to Annual Review of Earth and Planetary Sciences articles
may be found at http://earth.annualreviews.org
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Contents