Thermal Physiology and the Origin of Terrestriality in Vertebrates

Home , Panderichthys

Blackwell Science, LtdOxford, UKZOJZoological Journal of the Linnean Society0024-4082The Lin- nean Society of London, 2005? 2005 1433 345358 Original Article

ORIGIN OF TETRAPODSR. L. CARROLL ET AL.

Zoological Journal of the Linnean Society, 2005, 143, 345–358. With 11 figures

Thermal physiology and the origin of terrestriality in vertebrates

ROBERT L. CARROLL FLS1*, JASON IRWIN2† and DAVID M. GREEN1

1Redpath Museum, McGill University, 859 Sherbrooke St. West, Montreal, Quebec, Canada, H3A 2K6 2Biology Department, Bucknell University, Lewisburg, Pennsylvania, PA 17837, USA

Received January 2004; accepted for publication September 2004

The adaptive reasons for the evolutionary transition between obligatorily aquatic lobe-finned fish and facultatively terrestrial early tetrapods have long been debated. The oldest adequately known amphibians, Acanthostega and Ich- thyostega, from the final stage in the Upper Devonian (Famennian), can be clearly distinguished from the most advanced choanate sarcopterygian fish from the next older stage (Frasnian) by the presence of large pectoral and pelvic girdles, limbs generally resembling those of later Palaeozoic land vertebrates, and the absence of bones linking the back of the skull with the shoulder girdle. Upper Devonian and most Lower Carboniferous amphibians, like their aquatic predecessors, differed significantly from modern amphibians in their much larger size, up to a metre or more in length. Animals of this size, resembling modern crocodiles and the marine iguana, could have raised their body temperatures by basking in the sun and sustained them upon re-entry into the water. It is hypothesized that the physiological advantages of thermoregulation were a major selective force that resulted in the increasing capacity for the ancestors of tetrapods to move into shallow water, and later to support their bodies against the force of gravity and increase the size and locomotor capacities of the limbs. © 2005 The Linnean Society of London, Zoological Jour- nal of the Linnean Society, 2005, 143, 345–358.

ADDITIONAL KEYWORDS: Acanthostega – basking – Carboniferous – Devonian – Eusthenopteron – footprints – Ichthyostega – Panderichthys – tetrapods – thermoregulation.

INTRODUCTION erable morphological gap between the typical fish fins in Eusthenopteron and the tetrapod limbs of Acan- One of the most significant events in the history of ver- thostega (Fig. 1). Based on the presence of a fish-like tebrates was the attainment of a terrestrial way of life. tail and the apparent retention of internal gills, Clack The phylogenetic sequence from choanate sarcoptery- & Coates (1995) suggested that Acanthostega and Ich- gian fish such as Eusthenopteron to primitive tetra- thyostega were primarily aquatic, and that ‘tetrapod’ pods is documented by the fossil record of the Late limbs might have evolved for aquatic locomotion. Devonian to Early Carboniferous, but the adaptive or selective advantage of the transition between life in the water and life on land has remained difficult to GIRDLES AND LIMBS explain. To investigate the initiation of terrestriality, it is nec- Numerous hypotheses to explain this transition essary to know the specific sequence of structural (Table 1) were discussed in the recent book, Gaining change. The broad outline of the phylogenetic relation- Ground (Clack, 2002a). Clack hesitated to chose ships of the best known genera involved in this among these hypotheses, citing the still incomplete sequence (Fig. 2) is generally agreed upon at present knowledge of the fossil record. There is still a consid- (Coates, 1996; Ahlberg & Johanson, 1998; Coates, Jef- fery & Ruta, 2002; Ruta, Coates & Quicke, 2003). Attention has long been focused on the hands and feet as being unique characters of tetrapods, but *Corresponding author. E-mail: [email protected] †Current address: Biology Department, Okanagan University the known Upper Devonian fossils retain distinctly College, 3333 University Way, Kelowna, BC Canada VIV 1V7 archaic characteristics relative to Carboniferous

346 R. L. CARROLL ET AL.

Table 1. Hypotheses to explain the origin of tetrapods, 5 more clearly resemble distal tarsals, although they based largely on Clack (2002a) are in line with a bone identified as a fibulare because of its articulation with the fibula. However, this ‘fibu- 1To get back into the water under arid conditions (Romer) lare’ articulates distally with bones resembling the 2 ‘Limbs’ initially for burrowing in the mud (Orton) metatarsals of digits 3–5, without the interposition of 3 Competition and/or predation with other aquatic forms bones resembling distal tarsals. If the bones proximal (McNamera, Shelden) to digits 2–4 are distal tarsals, the phalangeal counts 4To escape oxygen-depleted water of these digits are 3, 3, 3. The more lateral digits are 5Feeding on terrestrial or semiterrestrial food sources incomplete distally. The tarsus of Ichthyostega appears 6 Increase in body temperature (Clack) nearly completely ossified, but there remains the ques- a. Increase in rate of digestion tion of homology in the area of the distal tarsals and b. Speed development metatarsals. In Tulerpeton, the 5th digit of the manus 7 Spawning on land 8 Limbs evolved originally for amplexus in the water appears to correspond with that of some Carboniferous (Martin, 2002) labyrinthodonts in having a phalangeal count of 4, a discrete metacarpal, and being separated from the ulnare by a squarish distal carpal. In contrast, the bone that has the appearance of the metacarpal of the 4th digit articulates directly with the ulnare, without the amphibians (Fig. 3). The autopodia (the bones distal to intervention of a typical, squarish distal carpal. In the the ulna and radius in the forelimb and the tibia and foot, there appear to be typical distal tarsals proximal fibula in the hind limb) of Acanthostega, Ichthyostega to most if not all metatarsals, but with no more than and Tulerpeton (Coates et al., 2002) are comparable two rows of tarsals medially. with those of later tetrapods in the presence of the The structure of the autopod, especially in Acan- mesopodium (the carpals and tarsals), metapodium thostega, suggests that the movements across the (metacarpals and metatarsals) and digits, but the wrist and ankle joints were significantly different number and arrangement of these bones are more from those of later tetrapods. Clack (2002a) illustrated variable and distinctly more primitive than those of Acanthostega in association with the reputed foot- well-known Carboniferous and Permian tetrapods, prints of a Devonian tetrapod, suggesting lateral ori- suggesting a period of ‘experimentation’, during which entation of the digits, as might be appropriate for the more effective joints of the wrist and ankle of later aquatic locomotion (Fig. 4). tetrapods had not yet evolved (Carroll & Holmes, It is only later, in the Lower Carboniferous (Tour- 2005). naisian) Horton Bluff Formation in Nova Scotia that In Acanthostega, the ulna extends well beyond the typical footprints with forward-facing digits have been radius, precluding an effective wrist joint, and most of documented (Matthew, 1905; Sarjeant & Mossman, the carpus remains unossified. The number of digits 1978). In a more recently collected trackway (Fig. 5), varies from eight in both the hand and the foot of Acan- the stride and pace are comparable with those of thostega, to seven in the foot of Ichthyostega (no fossil Upper Carboniferous and Permian amphibians. Other is yet known that shows the full structure of the manus; trackways represent animals walking in shallow Clack, Blom & Ahlberg, 2003), and six in Tulerpeton water, and record the movement of the digits in an (Lebedev & Coates, 1995). As emphasized by Coates anterior to posterior direction. Many newly discovered et al. (2002), the feet of Acanthostega and Tulerpeton footprints and trackways from the Horton Bluff For- appear to have evolved more rapidly than the hands. mation are now under study at Redpath Museum, Acanthostega is notable in ossifying only one element McGill University. of the carpus (the intermedium). The ossification of the Clack (2002b) emphasized the asymmetrical shape tarsus is also limited. Coates et al. (2002) state that of the metatarsals in the Tournaisian whatcheerid there appear to be fewer than the three rows of carpals Pederpes that indicates forwardly directed digits, as in and tarsals common to later Palaeozoic tetrapods, but later tetrapods. By the Viséan and Namurian A, a rel- the number is difficult to specify because of the problem atively consistent pattern of three rows of carpals and of establishing the homology of the elements between tarsals had been established, as exemplified by the the proximal row of carpals and the digits. In the hand putative stem amniote Westlothiana (Smithson et al., of Acanthostega, the proximal elements of the digits are 1994), the colosteid Greererpeton (Godfrey, 1989) and elongate bones that might be identified as metacarpals, the temnospondyl Balanerpeton (in which the number indicating a phalangeal count of 4, 4, 4, 4, 5, 5, 5, 4. Or of digits in the manus is reduced to four) (Milner & (as indicated by Coates, 1996) they may be distal car- Sequeira, 1994) (Fig. 3F–I). pals, giving a count of 3, 3, 3, 3, 4, 4, 4, 3. In the foot, Although the fossil record is still very inadequately the more squarish bones proximal to digits 2, 3, 4 and known and marked by large gaps, the information

ORIGIN OF TETRAPODS 347

Figure 1. Structural changes between ﬁsh and tetrapods. A, Eusthenopteron, the most thoroughly known Upper Devonian choanate sarcopterygian (from Andrews & Westoll, 1970). B, Panderichthys, an Upper Devonian ﬁsh intermediate between Eusthenopteron and the Upper Devonian amphibians (from Vorobyeva & Schultze, 1991). C, the Upper Devonian amphibian Acanthostega (Coates & Clack, 1995). D, the Upper Devonian amphibian Ichthyostega (from Coates & Clack, 1995). More details of the forelimb have since been discovered (Clack, Blom & Ahlberg, 2003). Animals are reproduced at approximately equal head/trunk lengths.

available indicates a long period of progressive change function of advanced Carboniferous species by the in distal limb structure. The conﬁguration that is Late Devonian. The timing of change is most readily characteristic of most later Carboniferous and Per- seen in the pelvis (Fig. 6). That of Eusthenopteron is mian tetrapods was not achieved until the mid-Tour- much smaller than in Acanthostega, far below the ver- naisian, approximately 10 million years after the tebral column, and the two halves have no more than evolution of attachment of the pelvic girdle to the ver- a cartilaginous attachment at the symphysis. The ace- tebral column via a sacral rib. This indicates that sup- tabulum faces posteriorly, and neither a puboischiadic port of the body above the ground in early tetrapods plate nor a dorsal expansion of the ilium is evident. was achieved prior to a fully effective foot structure. On the other hand, the relative size and general con- In contrast with the autopodia, the pectoral and pel- ﬁguration of the pelves of Acanthostega and Ichthy- vic girdles of Ichthyostega and Acanthostega had ostega indicate a supporting role comparable with already achieved the basic structure and probable those of Carboniferous tetrapods, with the dorsally

348 R. L. CARROLL ET AL.

Coelacanths tetrapods that have become highly adapted to an anguilliform mode of swimming, such as early ichthy- Lungfish osaurs, mosasaurs and primitive whales (Carroll, 1988). On the other hand, Clack & Coates’s (1995) Porolepiforms argument that Acanthostega and Ichthyostega were Kenichthys primarily aquatic is certainly true both phylogeneti- cally and ontogenetically in that they evolved from Rhizodontids obligatorily aquatic animals, and almost certainly Eusthenopteron reproduced via eggs that developed in the water (Cote et al., 2002). They retained a fish-like tail and appar- Panderichthys ently had internal gills, at least as juveniles, although both the gular plates and the bones of the operculum, Elginerpeton which cover the gills in fish, are lost. In contrast, the Acanthostega structure of the girdles, and to a lesser extent the elaboration of the autopodium, indicate capacity for sup- Ichthyostega port and locomotion on land. This combination of Tulerpeton characters is exactly what would be expected of animals intermediate between fish and later tetrapods. Proterogyrinus That is, they had the typically biphasic life history of amphibians – initially obligatorily aquatic at hatch- Seymouria ing, but capable of leaving the water as adults. Eryops Similar changes to support the body and move it forward are also evident in the pectoral girdle (Fig. 7). In Figure 2. A simplified phylogeny of sarcopterygians Eusthenopteron, the ventral surface of the shoulder including stem tetrapods and the base of the tetrapod girdle consists entirely of dermal bone, greatly limit- crown group (from Coates et al., 2002). ing ventral elaboration of muscles originating from the endochondral girdle and inserting on the humerus. Superficially, this appears to be the case in Panderich- thys as well, but Vorobyeva & Kuznetsov (1992) and Vorobyeva (1995) showed that the scapulocoracoid of elaborated iliac blade linked to the vertebral column this genus was much expanded ventrally, to a degree via a sacral rib, and ventrally, an extensive puboischi- roughly intermediate between Eusthenopteron and adic plate. The centrally placed acetabulum faces the late Devonian tetrapods. Vorobyeva & Kuznetsov directly laterally (Coates, 1996). The pelves of Acan- (1992) suggested that the expansion of the coracoid thostega and Ichthyostega have most of the structural plate was related to the elaboration of proximal ven- features common to later tetrapods, including early tral fin muscles. However, the glenoid is still orien- amniotes, that are associated with support of the tated posteriorly and the ‘shoulder’ joint is interpreted trunk above the substrate, against the force of gravity. as operating as a hinge, rather than serving as a site The great elaboration of the puboischiadic plate, in of rotation. A similar pattern of articulation may be common with basal diapsids and synapsids, indicates retained in an early tetrapod from the Upper Devo- attachment of an extensive musculature that could nian of Pennsylvania designated ANSP 21350 (Shu- have acted to raise the body off the ground and push it bin, Daeschler & Coates, 2004). In Acanthostega and forward. An isolated bone from slightly earlier in the Ichthyostega the endochondral portion of the girdle is Upper Devonian (late Frasnian) raises the possibility widely exposed ventrally, as in later tetrapods, in of a still earlier stage in the evolution of the pelvic gir- which it serves for the origin of extensive muscles, dle. Ahlberg (1998) described a piece of weathered including the coracobrachialis brevis and longus, the bone, attributed to the genus Elginerpeton, that biceps, pectoralis and the supracorocoideus, that pull resembles the base of the dorsal process of the ilium in the forelimb medially and raise the trunk (Holmes, Ichthyostega in having an opening termed the iliac 1977). The shoulder girdle is also decoupled from the canal. skull by the loss of the dermal elements of the oper- It is difficult to imagine any reason for the evolution culum and the suprascapular bones that link the back of the pelvic structure of Acanthostega and Ichthy- of the skull table to the dorsal portion of the shoulder ostega except as a means to support the trunk against girdle. The early appearance of highly advanced, the force of gravity. This interpretation is re-reinforced weight-bearing girdles can only be explained on the by the rapid reduction in the size of the pelvic girdle assumption of a selective advantage for terrestriality and loss of connection with the vertebral column in per se.

ORIGIN OF TETRAPODS 349

Figure 3. Fore and hind limbs of Upper Devonian and Lower Carboniferous tetrapods. A, B, Acanthostega, from the Famen- nian (Uppermost Devonian). C, Ichthyostega, from the Famennian. D, E, Tulerpeton, Famennian. F, G, the temnospondyl Balenerpeton, Lower Carboniferous (Viséan). H, the stem amniote Westlothiana, Viséan. I, the colosteid Greererpeton, Lower Carboniferous (Namurian A). A, B, from Coates (1996); C–E, from Coates et al. (2002); F, G, from Milner & Sequeira (1994); H, from Smithson et al. (1994); I, from Godfrey (1989). Anatomical abbreviations are given in Appendix 1.

350 R. L. CARROLL ET AL.

VERTEBRAE AND RIBS The structure of the vertebrae and ribs of Acan- thostega and Ichthyostega provides less conspicuous evidence for support on land, but these bones are closer to their appearance in later tetrapods than to Eusthenopteron. Coates (1996) refers to the configura- tion of the vertebrae in Acanthostega as ‘rhachito- mous’, the pattern common to primitive members of the two major groups of Palaeozoic labyrinthodonts, the temnospondyls and anthracosaurs (all three of these groups may prove to be paraphyletic, but until specific affinities can be established between them and more derived amphibians and amniotes, these remain convenient terms for referring to readily distinguish- able assemblages of Palaeozoic amphibians). The vertebrae are distinct from those of Eusthenopteron in the presence of zygapophyses, although these structures remain small in Acanthostega. The first two arches are comparable with those of the atlas and axis of later tetrapods, and the anterior zygapophyses of the atlas indicate the presence of a proatlas. This pattern is in strong contrast to that of Eusthenopteron (Hitchcock, 1995), in which there is no evidence of bony contact between the occiput and the anterior vertebrae. The importance of structural support in Acanthostega is indicated by the medial fusion of the atlas and sacral intercentra, in contrast with their paired nature in the rest of the column (Coates, 1996). The ribs of Eusthenopteron are very short bones, linking the arches and intercentra. They may have helped to connect the elements of the vertebral column, but did not extend ventrally around the viscera. Ribs are omitted in the directly lateral view of Acan- thostega (Fig. 1), but in the obliquely dorsal view (Fig. 8) they are seen to be elongated to about the degree observed in Carboniferous and Permian temnospondyl amphibians and would have served to provide a degree of support to the flanks to prevent collapse of the lungs and other viscera when the body was not supported by the buoyancy of the water. The sacral and anterior caudal ribs are more elongate than those just anterior to the sacrum, as in later tetrapods. The sacral rib (Fig. 9) is more elongate than those of the anthracosaurs Archeria and Eogyrinus, but more closely resembles those of Greererpeton and Eryops, with the distal extremity of the shaft flat- tened and spatulate where it attached to the mesial surface of the dorsal process of the ilium (Coates, 1996).

Figure 4. Diagram from Clack (2002a) showing how an THE SELECTIVE ADVANTAGE OF Acanthostega-like tetrapod might produce tracks like TERRESTRIALITY those known from the Upper Devonian Genoa Locality in Australia. What then was the selective advantage for Acan- thostega and Ichthyostega to be on land? Or, to put it

Figure 5. On the left, amphibian trackway from the Lower Carboniferous (Tournaisian) of the Horton Bluff Formation, Hantsport, Nova Scotia, Redpath Museum, McGill University RM 20.6777. Tail drag indicates that the trackway was made on land. Note similarity with diagram of a trackway from the Upper Carboniferous on the right (from Baird, 1952). another way: ‘What would have been the result of stem In these and other aspects of their anatomy and phys- tetrapods being on land, rather than in the water?’ iology, frogs, salamanders and caecilians are very Here we leave the area of ecological speculation, and highly divergent from ancestral tetrapods. The earli- turn to the more testable realm of physics. As is well est land vertebrates, by contrast, reached lengths of a known from the debate on warm-blooded dinosaurs, metre or more as adults. The scalation of most Car- terrestrial ectothermic animals can raise their body boniferous tetrapods covered the entire body, possibly temperature by basking in the sun (Thomas & Olson, suggesting a relatively impervious integument, 1980). The closest thermal analogues to ancestral tet- although only the ventral scales are preserved in rapods are provided by living reptiles, especially croc- Acanthostega and Ichthyostega. odiles and lizards, which are ectothermic and highly The modes of heat gain and loss in modern terres- dependent on the radiant energy of the sun for main- trial vertebrates (Fig. 10) provide a model for ances- taining a high metabolic rate (Avery, 1982; Pianka & tral tetrapods. The probable rates of heat gain and loss Vitt, 2003). In contrast, modern amphibians have lit- in primitive land vertebrates can be calculated on the tle capacity to make use of radiant heat to achieve or basis of formulae derived from study of living reptiles maintain a high body temperature because of their and amphibians (Spotila, O’Connor & Bakken, 1992). small size and moist body surface, both associated To facilitate computation, the animals were treated with cutaneous respiration (Feder & Burggren, 1992). as though cylindrical in shape. The body width, based

Figure 6. Pelvic girdles of Eusthenopteron and Upper Devonian and Permo-Carboniferous tetrapods. A, B, lateral and dorsal views of the pelvic girdle of Eusthenopteron (from Andrews & Westoll, 1970). C–E, lateral, ventral and anterior views of the pelvic girdle of Acanthostega (from Coates, 1996). E is a composite of his ﬁgures 9c and 20a, with rib proportions from ﬁgure 11. F, lateral view of the pelvis of Ichthyostega from Jarvik (1980). G, lateral view of the pelvis of the Lower Car- boniferous whatcheerid Whatcheeria (after Lombard & Bolt, 1995). H, lateral view of the pelvis of the Lower Carboniferous anthracosaur Proterogyrinus from Holmes (1984). I, lateral and ventral views of the pelvis of the Upper Carboniferous temnospondyl Dendrerpeton (from Holmes, Carroll & Reisz, 1998). J, lateral and ventral views of the Lower Permian amniote Captorhinus (from Holmes, 2003). Anatomical abbreviations are given in Appendix 1.

Figure 7. Pectoral girdles. A, B, lateral and ventral views of the pectoral girdle of Eusthenopteron (from Jarvik, 1980). C, D, lateral and composite dorsal and ventral views of Acanthostega (from Coates, 1996). on reconstructions of Devonian fish and amphibians, as follows (abbreviations used in the formulae are was taken as 15% of the skull–trunk length. When at explained in Appendix 2): rest on land, one-quarter of the body surface area was Insolation: Qabs = (aSASS + asAss + arArr)/A assumed to be in contact with the substrate. Body 4 4 4 4 Thermal radiation: R = se[As(Tr - Tsk ) + Ar(Tr - Tg )] water content was taken as 75% and the specific heat Convective heatloss: C = Ahc(Tr - Ta), where of the water-free tissue was assumed to match that of 0.6 -0.04 hc = 6.77·V ·D a modern anuran (0.29 cal. g-1 ∞C-1; Layne & Lee, Evaporative cooling: Ec = A(1/re)(rs - RHra) 1989). Taken together, these values produce an overall Conduction: G = Kf Ag[(Tb - Tg)/df] specific heat of 3.438 J g-1 ∞C-1, similar to the generally applicable 3.430 J g-1 ∞C-1 suggested by Gates These equations and their unfamiliar abbreviations (1980). The skin was assumed to have similar charac- may appear daunting, but all are related to the simple teristics to modern amphibians with a thermal con- phenomena of the rates of heat gain and loss associ- ductivity of 0.45 W m-1 ∞C-1, a resistance to water ated with differing ratios of body volume and surface vapour transfer similar to that of Iguana iguana, area. Specifically, heat loss decreases with increased 10 000 s m-1 (Lillywhite & Maderson, 1982), and a volume-to-surface ratio, whether this be the size of long-wave emissivity of 0.96. Because of their large individual cells, entire organisms or inanimate size, the Devonian animals were assumed to have skin objects. Doubling of linear measures results in squar- 5 mm thick. The specific components of the model are ing the surface area, while the volume increases by a

Figure 9. A, posterior trunk through anterior caudal ribs of A, the Permian seymouriamorph Kotlassia, and B, the Upper Devonian Acanthostega, showing the clear distinc- tion of the sacral ribs for attachment with the dorsal process of the ilium (from Coates, 1996).

Figure 10. Modes of heat gain and loss for a basking liz- ard (from Pianka & Vitt, 2003).

mals of different sizes and under different environmental conditions can be measured by temperature- sensitive devices. Hundreds of experiments have been conducted in the ﬁeld and laboratory on both reptiles and amphibians to determine response to varying conditions. Differences in some features used in this Figure 8. Dorsal view of the skeleton of Acanthostega model, including wind velocity, nature of the sub- (from Coates, 1996). strate, thickness of the skin and relative humidity, cannot be determined for animals that lived in the Devonian, but, as under modern conditions, the main power of three (Schmidt-Nielsen, 1989). Hence, the factor that controls the rates of heat gain and heat loss larger the amphibian or reptile, the longer it retains is the volume of the animal. heat, such as that provided by the radiant energy of Certain physical conditions of the environment need the sun (Gans & Pough, 1982; Feder & Burggren, to be included in this model. The water temperature 1992). The speciﬁc rates of heat gain and loss in ani- was set at 20 ∞C, air temperature at 30 ∞C and soil

34 Panderichthys and Upper Devonian amphibians would not have heated up as rapidly as smaller indi- 32 viduals, but could have attained a higher temperature

C) and retained it signiﬁcantly longer after they ceased

° 30 1.0 m long to bask. But what were the selective advantages of 28 0.2 m long warming up? 26

24 THE ADVANTAGES OF WARMING UP Study of modern amphibians and reptiles show that Body temperature ( 22 they have a Q10 of ~2 (Gatten, Miller & Full, 1992). 20 That is, all metabolic processes roughly double with a 10 C increase in body temperature – double the rate 18 ∞ 0 100 200 300 400 500 of digestion, elaboration of reproductive tissue, respi- Time (minutes) ration and increased capacity for locomotion. This, in turn, implies increased requirements for food and Figure 11. Rate and amount of heat gain and loss in ani- raises the question of what stem tetrapods ate. Judg- mals the size of adults of Eusthenopteron, Panderichthys, ing by their dentition, with large palatal fangs and rel- Acanthostega and Ichthyostega (~1 m), and smaller tetra- atively large marginal teeth, and the known stomach pods. Ambient water temperature is 20 ∞C, and ambient air contents of Eusthenopteron, it is probable that adults temperature is 30 ∞C. On the left, time of emergence from of the earliest land vertebrates relied primarily on the water, on the right, return to the water. fish. Little is known of large animal prey available on land in the Late Devonian, other than other amphibians. The fossil record of terrestrial non-vertebrate temperature at 35 ∞C. Direct solar radiation was esti- animals is very poorly known for the Frasnian– mated as 800 W m-2 and indirect sunlight as 100 W Viséan, the critical period for the emergence of terres- m-2. Wind speed was set at 1 m s-1 and relative humid- trial vertebrates (DiMichele & Hook, 1992). What is ity at 85%. It was assumed that the effective radiant known of terrestrial invertebrates from the Upper Sil- temperature of the atmosphere (required to estimate urian and Lower to Middle Devonian consists prima- radiative heat gains from the sky) was 20 ∞C below rily of small arthropods, most of which were soil and ambient (Gates, 1980). The time constant for heating detritus feeders, e.g. fungus-eating microarthropods, and cooling (t) was calculated as the time required to mites, spiders, millipedes, centipedes, scorpions and achieve 63% of the total change between the initial pseudoscorpions (Grey & Shear, 1992). Collembolans temperature and the final equilibrium temperature appear in the Early Devonian. Wingless and perhaps (Gates, 1980). even flying insects are known by the Lower Devonian Although the girdles and limbs were clearly differ- (Engel & Grimaldi, 2004), but were of small size. ent on the two sides of the evolutionary transition, the Arthropleurids, which reached up to 2 m in length by adult body size and proportions of these animals were the Upper Carboniferous, were known from only closely comparable, so they would respond to about the minute forms in the Middle Devonian. None of these same degree to changes in the thermal environment. animals appears as probable food for the early tetra- However, to test the significance of size, animals of two pods, all of which were of large body size, with a den- sizes were modelled: an adult length of 1 m and a juve- tition suited for much larger prey. nile length of 0.2 m. Modern crocodiles, many of which rely heavily on The results of the model showed that a 0.2-m-long aquatic prey, provide a good model for Upper Devo- animal equilibrates at a maximum body temperature nian tetrapods (Cogger & Zweifel, 1998). Raising the of nearly 30 ∞C (about 10 ∞C above that of the water) body temperature by basking is extremely important, within about 40 min of basking (Fig. 11). However, because they can operate at a much higher metabolic this difference is completely lost within about 25 min rate for short periods of time in the water than their of returning to the water. The 1-m-long animal raises aquatic prey. The marine iguana uses a similar strat- its body temperature to the ambient 30 ∞C within egy for feeding on plants in the cold, up-welling waters about an hour, but its temperature continues to rise surrounding the Galápagos islands. Heat gained by slowly until, after about 5 h, it reaches more than basking is retained for a long enough time for a fast 32 ∞C, significantly above ambient. On returning to sprint after food, or to escape from marine predators. the water, some appreciable retention of this elevated Our model, based on a cylindrical body shape, cir- temperature is maintained for about 20 min. There- cumvents additional assumptions that are difficult to fore, animals the size of adults of Eusthenopteron, quantify. However, the evolution of tetrapod limbs

© 2005 The Linnean Society of London, Zoological Journal of the Linnean Society, 2005, 143, 345–358 356 R. L. CARROLL ET AL. that were much larger than the fins of choanate fish water level, but would have enabled this genus to would also have had the result of increasing the sur- make use of the radiant heat of the sun to raise body face for absorbing radiant heat. In addition, blood cir- temperature and so metabolic rate. This would have culation to and from the limbs could have been subject increased its effectiveness as an aquatic predator. An to control (as in modern tetrapods) to increase flow to increase in the surface area of the paired fins would and from the rest of the body while basking, but have raised the capacity to absorb radiant heat, restricting heat loss from the body core when they and may have set the stage for the origin of an entered cold water (Dzialowski & O’Connor, 1999). autopodium. Cooling rates are only one half of the heating rates in Even very rudimentary hands and feet would have the marine iguana (Bartholomew & Lasiewski, 1965). facilitated lifting and moving the body on land, but Whatever other selective advantages there may effective terrestrial locomotion would have required have been for stem tetrapods to have come on land, improved support by the axial skeleton, evidenced by increased control over their body temperature must the elaboration of the zygapophyses and ribs, and have been a major factor. The structure of the earliest decoupling the skull from the trunk. This was accom- tetrapods indicates that they were primarily aquatic panied in Upper Devonian amphibians by the elabo- animals, most likely preying upon fish and other ration of a firm attachment between the vertebral aquatic organisms. Their attainment of primitive column and the pelvis, and the great increase in the limbs does not imply, necessarily, that they were as yet amount of limb musculature and its areas of attach- highly adapted to life on land. Rather, we suggest that ment to the ventral surfaces of the pectoral and pelvic stem tetrapods emerged from the water in order to girdles, to support the trunk on the limbs. The final take advantage of an abundant but previously unex- stage in the origin of efficient terrestrial locomotion ploited resource – the radiant heat of the sun – which was the evolution of effective wrist and ankle joints by enabled them to function better as shallow-water, the Early Carboniferous. predatory fish. The thermal advantage of basking would have given them faster reaction times while in ACKNOWLEDGEMENTS the water, higher metabolic and assimilation rates leading to faster growth, earlier attainment of sexual We thank Neal Cody and Ray Stazko for donations to maturity and, ultimately, enhanced reproductive rates Redpath Museum of footprints they collected from the compared with other fish. This set the stage for the Horton Bluff Formation, Mary-Ann Lacey for prepa- attainment of truly terrestrial life. ration of line drawings used in the text, and Guy L’Heureux and Carole Smith for photographic work. This research was supported by grants to R.L.C. and THE ATTAINMENT OF TERRESTRIALITY D.M.G. from the Natural Sciences and Engineering Lobe-finned fish were common and diverse throughout Research Council of Canada. the Devonian and Carboniferous. 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Shubin NH, Daeschler EB, Coates MI. 2004. The early evo- APPENDIX 2 lution of the tetrapod humerus. Science 304: 90–93. Smithson TR, Carroll RL, Panchen AL, Andrews SM. ABBREVIATIONS USED IN FORMULAE FOR CALCULATING 1994. Westlothiana lizziae from the Viséan of East Kirkton, HEAT GAIN AND LOSS West Lothian, Scotland, and the amniote stem. Transactions Insolation: of the Royal Society of Edinburgh: Earth Sciences 84: 383– Qabs = energy gained from solar radiation 412. aS, as, ar = absorptance to solar radiation (direct, Spotila JR, O’Connor MP, Bakken GS. 1992. Biophysics of indirect, reflected, respectively) heat and mass transfer. In: Feder ME, Burggren WW, eds. A surface area of animal exposed to direct solar Environmental physiology of the amphibians. Chicago: Uni- S = versity of Chicago Press, 59–80. radiation Thomas RDK, Olson EC, eds. 1980. A cold look at the warm- As = surface area of animal exposed to indirect solar blooded dinosaurs. AAAS Selected Symposium, 28. Colorado: radiation Westview Press. A = total surface area -2 Vorobyeva EI. 1995. The shoulder girdle of Panderichthys S = intensity of direct solar radiation, 800 W m -2 rhombolepis (Gross) (Crossopterygii), Upper Devonian, s = intensity of indirect solar radiation, 100 W m Latvia. Geobios 19: 285–288. r = intensity of reflected solar radiation, assumed to be Vorobyeva E, Kuznetsov A. 1992. The locomotor apparatus negligible of Panderichthys rhombolepis (Gross), a supplement to the problem of fish-tetrapod transition. In: Mark-Kurik M, ed. Thermal radiation: Fossil fishes as living animals. Tallin: Academy of Sciences of s = Stefan–Boltzmann constant Estonia, Institute of Geology, 131–140. e = longwave emissivity of skin Vorobyeva EI, Schultze H-P. 1991. Description and system- As = Surface area exposed to thermal radiation atics of panderichthyid fishes with comments on their rela- Ar = Surface area exposed to reflected thermal tionship to tetrapods. In: Schultze H-P, Trueb L, eds. Origins radiation of the higher groups of tetrapods. Ithaca: Cornell University Tr = Body surface temperature Press, 68–109. Tsk = effective temperature of the sky (20 ∞C below air temperature) APPENDIX 1 Convective heat loss: ANATOMICAL ABBREVIATIONS hc = convection coefficient -1 ace acetabulum V = wind speed (1 m s ) c centrale D = Characteristic dimension of animal (m) dc distal carpal Ta = air temperature (∞K) do pr dorsal process of ilium Other parameters as listed above dt distal tarsal ent entepicondylar foramen Evaporative cooling: F femur re = external resistance to water loss Fi fibula rs = saturation vapour density of water at body surface fib fibulare temperature H humerus ra = saturation vapour density of water at air i intermedium temperature il ilium RH = relative humidity il pr iliac process isch ischium Conduction: mc metacarpal Kf = conductivity of the skin mt metatarsal Ag = area in contract with ground (one-quarter of ob f obturator foramen surface area in our model) pos pr posterior process of ilium Tb = body temperature (∞K) pu pubis Tg = ground temperature pub pr pubic process df = thickness of skin R radius Ti tibia tib tibiale U ulna ul ulnare