Adaptations to Underground Nesting in Birds and Reptiles 1

AMER. ZOOL., 20:437-447 (1980) Adaptations to Underground Nesting in Birds and Reptiles 1 ROGER S. SEYMOUR Department of Zoology, University of Adelaide, Adelaide, South Australia 5000 AND RALPH A. ACKERMAN Physiological Research Laboratory, Scripps Institution of Oceanography, La folia, California 92093 SYNOPSIS. Most bird eggs have evolved a suite of remarkably consistent adaptations for appropriate exchanges of respiratory gases and water vapor during incubation in nests above ground. However, underground incubation is associated with selective forces different from those operating at the surface. New information from mound-building birds, living reptiles and extinct dinosaurs shows convergent adaptations to nest atmospheres that are high in CO 2, low in O> and nearly saturated with water vapor. High humidity eliminates the danger of excessive dehydration, so gas conductance of the eggshell may be higher than normal, as a compensation for the unusual nest gases. In contrast with embryos of birds that next above ground and initiate breathing inside the shell, those of megapode birds lack an aircell and can breathe only after the shell is broken. Extreme precocity of megapode chicks is related to long incubation time and large energy stores in the egg. Because the material around a buried nest restricts diffusion, the size of the nest must be limited to prevent intolerable gas tensions adjacent to the eggs. This effect may have forced certain large reptiles to separate their layings into several clutches and some megapodes to actively ventilate their mounds. INTRODUCTION Natural selection of birds nesting on or above ground has resulted in a remarkably consistent suite of adaptations that provide appropriate exchanges of respiratory gases and water vapor across the shell (Ar and Rahn, 1978). Because there is a large body of information on gas exchange in eggs laid in an aerial environment, we can now appreciate the adaptive compensations to unusual nesting conditions. Birds of the family, Megapodiidae, incubate their eggs in mounds or simple excavations beneath the ground. They share this behavior with certain reptiles, chiefly crocodilians and chelonians, that also construct incubation mounds or subterranean chambers. Isolated from the free atmosphere, the embryos must develop under conditions that depart from those experienced by most bird eggs above ground. The gaseous environment of buried eggs 1 From the Symposium on Physiology of the Avian Egg presented at the Annual Meeting of the American Society of Zoologists, 27-30 December 1979, at Tampa, Florida. is characterized by high humidity as well as high CO 2 and low O 2 tensions. The nest atmosphere depends not only on the rates of respiration of the eggs, but also on the decomposition of organic matter and the resistance to diffusion in the material surrounding the eggs. In this report, we examine the behavior and physiology of underground nesting in birds and reptiles, considering the conditions experienced by the developing embryos and some of the adaptations to subterranean life. MEGAPODE BIRDS The nests There are 13 species of I ndo-pacific megapodes, but only two Australian species have produced significant information on incubation biology. This is regrettable because of the extreme variability of nest environments, ranging from excavations in sand heated by the sun or geothermal activity to mounds of forest litter heated by organic decomposition (Frith, 1962). Fortunately, there is information about the

438 R. S. SEYMOUR AND R. A. ACKERMAN TABLE 1. Respiratory parameters of buried megapode eggs compared to predictions from other bird eggs incubated above ground. Parameter Incubation temperature, C Nest Po 2, torr Nest Pco 2, torr Egg weight, g Shell thickness, mm Water vapor conductance, mg/day torr Functional pore area, mm 2 Incubation time, days Pre-hatching O 2 consumption, ml/day Mean Brush Turkey {AUctura tathami) 37.3 100 62 203 0.34 47.3 6.87' 49 h 1433 Predicted 35.7 a 136" 8" 60 c 0.58 d 21.3 e 7.41* 38' 1106 k Mean 34 126 29 170 0. 21 62 1 1350 Mallee Fowl I[Leipoa oceluua) Predicted 35.7" 136" 8" 60 c.27 0.53 d.4 15.9 2..47' 5.94" 1 37' 732 k Data from Seymour and Rahn (1978) and Seymour, Vleck and Vleck (unpublished) unless otherwise noted: a Drent(1975). b Calculated from nest ventilation and gas exchange data of Rahn el al. (1974, 1976). c 1800 g Galliform bird, Lack (1968). d Equation 7, Ar el al. (1974). e Equation 4, Ar and Rahn (1978). ' Equation 5, Ar el al. (1974). 8 Equation 9, Ar and Rahn (1978). h Baltin (1969). 'Frith (1959). 1 Equation 1, Rahn and Ar (1974). k Equation 4, Rahn et al. (1974). mounds and eggs of the Brush Turkey (Alectura lathami) which uses organic decomposition only (Fleay, 1937; Baltin, 1969; Seymour and Rahn, 1978), and the Species Sea Turtles Dermochelys coriacea Chelonia mydas Caretta caretta Eretmochelys imbricata Lepidochelys olivacea Crocodilians Alligator mississippiensu Crocodylus porosus Crocodylus niloticus Crocodylus novaeguineae Crocodylus aculus Crocodylw, palustris Mallee Fowl (Leipoa ocellata) which supplements solar radiation with organic heat (Frith, 1955, 19566, 1957, 1959, 1962; Seymour, Vleck, and Vleck, unpublished). Megapode nests vary in size and shape from simple pits in sand containing a single egg of the Maleo Bird (Megacephalon maleo) to the mounds of Scrub Fowl (Megapodius freycinet) which may exceed 10 m in diameter and 4 m in height (Frith, 1962). The size of the mound is related to the degree of reliance on organic decomposition as a heat source. Mounds are not normally formed by species employing solar radiation or vulcanism as the sole source of heat. TABLE 2. Collected nesting data for large underground or mound nesting reptiles. Approx. mass (kg) 400 150 136 34 30 62 200 200 50 127 100 Clutch size # eggs 88 113 120 160 111 40 50 60 29 56 41 Clutch mass kg 7.1 5.5 4.5 5.2 3.7 2.6 5.6 13.1 2.0 5.2 4.9 Nest temp, c 28-30 27-30 28-30 27-31 28-30 36-38 Incubation time (days) 65 58 55 62 51 64 85 Reference Ackerman, 1980 Ackerman, 1980 Ackerman, 1980 Ackerman, 1980 Ackerman, 1980 Seymour, 1979; Neil, Joanen, 1969 Seymour, 1979; Xeil, Seymour, 1979; Xeil, Neil, 1971 Seymour, 1979; Rand Seymour, 1979 1971; 1971 1971, 1968ft

ADAPTATIONS TO UNDERGROUND NESTING 439 u 2 150 144 140 138 134 21 124 30 122 32 128 29 20 FIG. 1. The incubation mound of a Mallee Fowl (Leipoa ocellata) on 15 October 1979, approximately six weeks after the first egg was laid. Gas tensions are presented at selected depths in the center of the mound. Unpublished data were collected by Seymour, Vleck, and Vleck. Despite the various sources of heat, megapode eggs are incubated at temperatures surprisingly close to those of other bird eggs (Table 1). Whereas reptile eggs are usually incubated at about 30 C (Table 2), incubation temperatures of five megapode species average about 35.8 C (range = 31-39 C) (Frith, 1956a). In Brush Turkey and Mallee Fowl mounds, the central temperature is maintained remarkably constant by the industrious activities of the males which periodically dig down to the egg layer, test the temperature with the head or beak and then open or close the mound as appropriate. Aside from regulation by the birds, the large mass of many mounds is important for thermal stability. Baltin (1969) estimated that a Brush Turkey mound consists of about 3.6 metric tons of leaf litter and soil, a mixture with good insulative properties. Birds that rely on organic heat for incubation must incorporate fresh material in a mound each year. Brush Turkeys usually accomplish this by constructing a new mound each breeding season while Mallee Fowl often open previously used mounds and add fresh litter. Scrub Fowl may continually add new material to the outside of an old mound which causes the mounds to grow through the years (Frith, 1956a). The rate of decomposition clearly depends on adequate moisture in the litter. The onset of egg laying in Mallee Fowl is delayed until the gathered material is sufficiently moistened by winter and spring rains (Frith, 1956a). Breeding in Brush Turkeys is also dependent on sufficient rain, and these birds are reported to form a funnel in the top of the mound prior to rain so that the water soaks into it (Fleay, 1937). Organic decomposition in megapode mounds is totally aerobic and occurs through the action of microorganisms, respiration by the plant material itself and spontaneous oxidation of organic material. No location is anoxic (Seymour, Vleck, and

440 R. S. SEYMOUR AND R. A. ACKERMAN Vleck, unpublished). Temperature increases with depth into the mound, and Po 2 and Pco 2 depart from atmospheric levels in a similar fashion (Fig. 1). This suggests that both heat and gas move through the mound primarily by diffusion. The correlation between gas tensions and temperature in Brush Turkey mounds led Drent (1975) to wonder whether the bird regulated temperature or gas tensions, but experiments of Frith (1957) showed that temperature is the stimulus in Mallee Fowl. Measurements have been made of O 2 consumption and CO 2 production by the decomposing plant material in megapode mounds, and we know the pattern of O 2 consumption during embryonic development (Vleck, Vleck, and Seymour, unpublished). It is therefore possible to make an assessment of the relative effects of egg and mound metabolism on the gas tensions in the mound. The mean O 2 consumption of a Brush Turkey egg throughout incubation is about 20 ml O 2 /hr. With a 49 day incubation period and laying interval of 2-5 days (Baltin, 1969), there are up to 20 eggs in the mound at once. Therefore the total O 2 consumption by the eggs is about 400 ml O 2 /hr. This is about 3% of the O 2 consumption (13.7 liters/hr) by the mound itself. Hence mound metabolism appears to be the major determinant of mound gases and temperature in the Brush Turkey mound. The eggs Water loss and the aircell. Because Mallee Fowl and Brush Turkey eggs are incubated in a gaseous environment that is virtually saturated with water vapor, the only water loss occurs by virtue of small vapor pressure differences across the shell that develop as a consequence of the embryo's heat production (Packard et al., 1977). Mallee Fowl eggs, incubated in their own mound material in the laboratory, lost only about 2 3% of their original mass during the course of development (Vleck, Vleck, and Seymour, unpublished). As water is lost, a small bubble appears beneath the shell membranes and moves around in the albumen, always remaining uppermost. In this regard, it is distinct from the aircell that forms in most bird eggs between the inner and outer shell membranes and remains fixed at one end of the egg. An aircell is also lacking in the eggs of Brush Turkeys (Baltin, 1969) and Scrub Fowl (Meyer, 1930), but Baltin reported seeing small gas bubbles under the membranes in even freshly laid eggs. The aircell in most birds plays an important role in the slow transition from chorioallantoic to pulmonary respiration (Visschedijk, 1968). Because the small bubble under the membranes is insufficient to permit pulmonary respiration within the shell, the megapodes do not pip internally and cannot breathe until the shell and membranes are broken and the fluids are drained from around the head. From the moment this occurs, the chick requires only 30 min or so to completely free itself from the shell. During this time, breathing is evident but we do not know the extent of perfusion of the chorioallantois. However, the explosive nature of hatching suggests that perfusion is stopped much more quickly in megapodes than in other birds. Because rapid circulatory changes are well known for mammals at birth, a rapid shift in gas exchange organs is not surprising, and we are forced to wonder why the transition takes so long in other birds. Respiratory gas exchange. In eggs incubated above ground, there is a selective pressure on eggshell conductance and excessive evaporation is avoided. This selective pressure is relaxed below ground where humidity is nearly saturated. Here, in a hypercapnic and hypoxic environment, there appears to be selection for increased shell conductance so that tissue gas concentrations are not intolerable (Table 1). The extent of increase, moreover, is related to the deviation of the mound gases from the free atmosphere. For example, the Mallee Fowl shell conductance is about 35% higher than predicted (by egg mass and incubation time) and the mound Pco 2 reaches about 30 torr whereas the Brush Turkey's conductance is about 120% above predicted and the mound Pco 2 reaches about 70 torr. The increased conductance results from an abnormally thin shell; the

ADAPTATIONS TO UNDERGROUND NESTING 441 functional pore area is actually lower than predicted by other bird eggs (Table 1). Perhaps it is significant that conductance is increased this way. A thin shell is not a liability in the protective mound environment and it is an advantage to the adult, because it reduces the energy and materials required for shell formation, and to the hatchling, because it facilitates quick emergence. Energetics of the embryo. The failure of megapode eggs to lose much water during incubation may be connected with the energy budgets for the developing embryo. Most bird eggs lose about 14-18% of their mass by evaporation (Rahn and Ar, 1974; Rahn et ai, 1976; Drent, 1970). This volume potentially represents an increased energy store for megapode development. The yolk of Scrub Fowl accounts for 67% of the egg volume (Meyer, 1930). In Brush Turkey eggs, it averages about 49% of initial egg volume (Vleck, Vleck, and Seymour, unpublished). Both of these values are higher than data from other precocial (35.2%) and altricial (19.8%) species (Romanoff and Romanoff, 1949). These energy stores could ultimately appear as a heavier hatchling (relative to the fresh egg weight) a high metabolic rate or a long development time. But hatchling Brush Turkeys weigh 64-70% of the fresh egg and Mallee Fowl about 67.5% (Seymour, Vleck, and Vleck, unpublished; Baltin, 1969); this is about the same as the average of 68% for many birds (Romanoff, 1944). Therefore it seems that the additional energy supports the higher than predicted metabolism of the embryo during a long incubation period (Table 1). The result is an extremely precocial hatchling which is capable of flight 24 hr after leaving the egg (Frith, 1962). The precocity of megapode chicks is also related to the relatively large eggs. Adult female Brush Turkeys and Mallee Fowl weigh about 1800 g (Baltin, 1969; Frith, 1959) which, according to Lack's (1968) data for the Galliformes, predicts a weight of about 60 g in eggs laid every 1-2 days. Brush Turkeys require about 2 5 days (Baltin, 1969) and Mallee Fowl about 5-9 days (Frith, 1959) to produce eggs weighing about 200 and 170 g respectively. Therefore the rate of egg tissue formation appears similar among the Galliformes. THE EGYPTIAN PLOVER Besides megapodes, the Egyptian Plover (Pluvianus aegyptius) is one of the few bird species reported to bury their eggs (Howell, 1979). The adults lay 2-3 eggs of about 9 g each in shallow scrape nests in sandy areas near rivers. The eggs are covered by 2-3 mm of sand during the day and the adults incubate over the sand. At night the eggs are uncovered and incubated in contact with the brood patch to maintain about 38 C. During the day when ambient temperatures may rise well above 40 C, the adults soak their belly feathers in the nearby river and return to wet the sand surrounding the eggs. Evaporative cooling keeps egg temperatures at 38-41 C. The belly soaking behavior results in high nest humidities and the eggs lose only 11% of their initial mass. This is slightly lower than predicted for other birds (Rahn and Ar, 1974) and occurs despite a longer incubation period and greater eggshell gas conductance than predicted from egg mass (Rahn and Ar, 1974). The incubation period of the Egyptian Plover is long and may have the adaptive benefit of extreme precocity at hatching. The fresh chick weighs about 75% of initial egg mass which is somewhat greater than that reported for other birds (Romanoff, 1944). Howell (1979) suggests that the initial evolutionary advantage of egg burying was concealment and that the combination of burying and wetting behavior ultimately permitted egg survival in what otherwise would be a lethal environment. REPTILES The nests Most reptiles deposit their eggs in the ground or in litter at ground surface. Small reptiles may scatter their egg clutches (1-2 eggs) in suitable sites in the ground litter (Rand, 1967). Large reptiles, however, may bury their large clutches (10-200 eggs) in holes excavated in the ground (hole nesters) or in raised mounds (mound nesters). These reptiles include all of the

442 R. S. SEYMOUR AND R. A. ACKERMAN 10 20 30 40 TIME (days) FIG. 2. Oxygen and carbon dioxide tensions in Green Turtle (Chelonin mydas) and Loggerhead Turtle (Caretta caretta) nests during incubation. Data are summarized from Ackerman (1977) for three, 100 egg nests of each species. Hatching occurred near 60 days for Chelonia and 50 days for Caretta. Curves were drawn by eye. 6O marine, and most of the semi-aquatic and terrestrial turtles (Carr, 1952, 1967; Ernst and Barbour, 1972), some larger lizards (Hirth, 1963; Bartholomew, 1966; Rand, 1968a, 1972) and all the alligators and crocodiles (Greer, 1970, 1971; Neil, 1971). Hole nests may be shallow scrapes or laboriously constructed holes or tunnels often in a sand substrate. The clutch is deposited, covered and left to develop. Crocodilians are probably the only reptilian mound nesters but many species dig holes (Greer, 1971). The mounds are constructed of soil and vegetation raised up to about 1 m above ground level, often in a shady location (Neil, 1971). The egg clutch is deposited inside and completely covered with material from the mound. The temperatures of most clutches are around 30 C (Table 2), but there may be notable exceptions to this generalization. For example, characteristic mound temperatures are in excess of 35 C for Crocodylus novaeguineae (Neil, 1971). Hole nest temperatures are chiefly determined by the temperature of the nesting medium, which may influence the timing of egg laying (Rand, 1972). Egg temperatures in the hole nest may rise above the temperature of the nesting beach (Hendrickson, 1958; Carr and Hirth, 1961; Bustard, 1972) and a temperature gradient of this magnitude may exist between the center and periphery of the nest toward the end of incubation (Bustard, 1972). As in megapode mounds, temperatures in crocodilian mound nests may be heated by organic decomposition (Chabreck, 1973; Webb et ai, 1977; Goodwin and Marion, 1978) but there are no measurements of mound metabolism. Neil (1971) suggested that, among mound building crocodilians, the prevention of egg overheating is a major factor in the selection of the nesting site. Perhaps in some cases, a mound is constructed for temperature stability only and the heat production by decomposition in the mound may be a disadvantage. The eggs Thermal relations. There is very little information on the thermal requirements for incubation of eggs of underground nesters although there is more for other reptiles. Some crocodile eggs do best around 30 C (Bustard, 1971a). Sea turtle eggs can be successfully incubated between about 26 C and 35 C (Bustard, 19716), but appear to have greatest hatching success between 28 C and 32 C (Bustard and Greenham, 1968; Simon, 1975). Water exchange. In contrast with most avian eggs which must lose water, many reptilian eggs increase in mass during incubation by taking up water from the substrate. However, water may be exchanged in both directions by diffusion of water vapor or by liquid flow (Tracy et at, 1978; Packard et ai, 1979a). This occurs through fibrous membranes or discrete pores in the shell. Shell pores may occur in some hard and soft shelled eggs but not in others (Young, 1950; Packard and Packard, 1979; Sexton et ai, 1979). Hard shelled

ADAPTATIONS TO UNDERGROUND NESTING 443 alligator eggs do have pores (Packard et al., 19796) while soft shelled sea turtle eggs do not (Ackerman, unpublished). Consistent with high nest humidity, the water vapor conductance in reptilian eggs is generally greater than predicted by most birds (Packard et al, 1979«, b\ Harrison et al., 1978; Ackerman and Rahn, unpublished). Typical values range from 2 to 60 times the avian predictions. Respiratory gas exchange. The O 2 consumption of reptilian eggs increases continuously through incubation (Clark, 1953; Lynn and Von Brand, 1945; Dmi'el, 1970; Prange and Ackerman, 1974) reaching its maximum level just prior to hatching. Oxygen uptake increases during hatching and returns afterwards to prehatching levels (Lynn and Von Brand, 1945; Prange and Ackerman, 1974). Although the values for individual reptilian eggs are low compared to avian eggs (Seymour, 1979), the metabolic rate of a large clutch may be appreciable. Because most crocodilians and sea turtles produce clutches ranging from 30 to 200 eggs and hatchlings range in mass from 10 to 60 g, the O 2 consumption of these clutches can exceed 10 liters/ day. Sea turtle (Chelonia mydas, Caretta caretta) embryos consume about 5 ml O 2 / g-day (Ackerman, 1975; Prange and Ackerman, 1974) just prior to hatching. Near hatching, a clutch of 100 Green Sea Turtle eggs producing 22 g hatchlings would consume about 11 liters O 2 /day (Ackerman, 1977). As in buried avian eggs, this high metabolic rate occurs in an environment which impedes the movement of gases. In the nests of the Green (Chelonia mydas) and Loggerhead (Caretta caretta) Turtles, Po 2 falls to about 80-110 torr and Pco 2 rises to 30-50 torr during incubation (Fig. 2). The description of gas exchange by sea turtle nests is simplified by the fact that there is little or no metabolism occurring in the surrounding sand and by the spherical symmetry of the nest gas exchange process (Ackerman, 1977). This process is sensitive to such physical parameters as the grain size and water content of the sand which varies from beach to beach. Gradients in gas tension develop not only between the egg clutch and beach but also within the clutch. Ackerman (1977) suggested that the characteristic nesting behavior of sea turtles which resulted in the interior of the egg clutch being free of sand (Carr, 1967) was related to the gas exchange requirements of the eggs. Simon (1975) reported that sea turtle egg mortality increased when the spaces between the eggs were filled with sand. This may be due to impeded gas exchange by the eggs (Ackerman, 1980). DINOSAURS Most values of shell gas conductance in avian eggs have been obtained by measuring water loss with a known gradient of water vapor pressure across the shell (Ar et al., 1974). Conductance can also be estimated by direct morphometric analysis of the pore structure. In eggs with simple straight pores such as hens' eggs, there is good correlation between the values obtained by the gravimetric method and the direct method (Wangensteen et al., 1970/ 71; Hoyt, et al., 1979). In several species of fossil dinosaur eggs, the hard, calcareous shell structure remains intact and reveals simple pores. Thus we can assess shell gas conductance in animals which have been extinct for over 65 million years (Seymour, 1979). Furthermore, the conductance may correlate with the humidity in dinosaur nests and suggest something about dinosaur incubation behavior. Shell structure has been analyzed in three species of Upper Cretaceous dinosaurs: a sauropod from southern France (Hypselosaurus priscus), an unnamed sauropod from the Gobi Desert and a small ceratopsian also from the Gobi (Protoceratops andrewsi). The best data come from the 2100 g eggs of Hypselosaurus which show a shell conductance over seven times higher than predicted by similarly sized bird eggs. Protoceratops eggs (360 g) are over 4 times, and the "multi-canalicular" eggs (1800 g) of the Gobi sauropod are over 100 times higher. This is evidence that the eggs were incubated in high humidity environments, possibly underground or in incubation mounds. It is clear that the conditions in many living birds'

444 R. S. SEYMOUR AND R. A. ACKERMAN Cetalopsian Dinosaui ADULT BODY WEIGHT <Kg> FIG. 3. Calculated maximum rates of oxygen consumption of entire clutches of buried eggs shortly before hatching. The least squares regression line is based on the data from turtles and crocodilians only. The data are from Seymour (1979) and Ackerman (1980) except for the megapode data which are derived from unpublished work of Vleck, Vleck, and Seymour. nests (Table 1) would have fatally dehydrated the dinosaur embryos if their tolerances to water loss and their incubation times were at all similar to modern birds and reptiles (Seymour, 1979). The fossil sites of Protoceratops show that the clutches were deposited in three layers, with the eggs separated by sand (Brown and Schlaikjer, 1940), a conformation indicating hole nesting. Fossil nests of Hypselosaurus, on the other hand, suggest that an incubation mound was constructed. There is evidence that the adult did not excavate a hole, and the clutches are associated with fossilized rushes similar to those incorporated into some crocodilian mounds (Dughi and Sirugue, 1966). LIMITS ON CLUTCH SIZE Gas transfer between the atmosphere and a clutch of buried eggs occurs by diffusion through the soil or mound material. The rate of diffusion depends on gas pressure gradients developed by egg metabolism and organic decomposition in the soil. The increased shell conductance in buried eggs may be viewed as an adaptive compensation for the soil's resistance to diffusion. Nevertheless, there is a limit to this compensation and the limit is evident in dinosaur eggshells that have conductances so high that the differences in O 2 tension across them would have been less than 2 torr (Seymour, 1979). Thus the conductance of the matrix surrounding a buried clutch is of primary importance in determining the gas tensions inside the eggshell. Another important factor determining gas tensions in the nest is the metabolic rate of the eggs. It is possible for a buried nest to be so large that in late development, diffusion would fail to supply the gas exchange requirements of the embryos. Ackerman (1975, 1980) proposed that the requirement for optimal gas tensions in the nest might limit clutch size in marine turtles and account for i) the remarkable selectivity of the females for certain nesting beaches with suitable gas transport properties, ii) the similarity of clutch mass between species of very different body weights, and iii) the requirement for multiple layings within a year. He found that the gaseous environment of natural nests resulted in the shortest incubation time and greatest hatching success of Chelonia mydas and Caretta caretta. Deviations from this optimum, as would occur if more or fewer eggs were deposited in a nest, resulted in longer incubation time and poorer hatch, both results being evolutionarily disadvantageous. This is reason to believe that the maximum metabolic rate of a buried sea turtle clutch is less than about 800 ml O 2 /hr. The Po 2 would be about 100 torr and the Pco 2 about 40 torr in the center of a nest metabolising at that rate in clean beach sand (Ackerman, 1977). Nest gas tensions will be more extreme if decomposing material is incorporated around the eggs. It is therefore significant that the largest clutch mass (13.1 kg, Table 2) with a calculated maximum O 2 consumption of 775 ml O 2 /hr (Seymour, 1979) occurs in Crocodylus niloticus which does not include organic material in its hole nest (Cott, 1961). Crocodylus porosus, on the other hand, is a similarly sized animal but it incubates its eggs in a mound of almost pure vegetation (Webb et ah, 1977). This behavior may limit its clutch size to 5.6 kg with a calculated O, consumption of only 395 ml O.,/hr.

ADAPTATIONS TO UNDERGROUND NESTING 445 Of course, small reptiles cannot lay very large clutches, so we would expect to see a limit on clutch mass only in large reptiles. Indeed, the limit becomes obvious only if we include the data from the largest living reptiles and dinosaurs (Fig. 3). Not only do dinosaur fossils provide eggshell morphology, but three species also indicate egg weight and clutch size. Whereas the clutch represents 1-10% of the adult body weight in living large reptiles, it is only 0.1% in the 10 ton sauropod, Hypselosaurus (Seymour, 1979). With an allometric relationship between egg weight and maximum egg metabolism in reptiles as a guide, Seymour (1979) calculates that the clutch O 2 consumption reached only 300-400 ml O 2 / hr, a value similar to those of living reptile clutches. Had this sauropod's clutch conformed to a prediction based on adult weight (Fig. 3), there would have been about 116 eggs totalling about 250 kg. The clutch would have consumed 7500 ml O 2 / hr and reduced the Po 2 in the center of the egg mass to zero. However, there is little doubt that the fossil sites of these sauropods contain complete clutches of 4-6 eggs totalling only 10 kg (Dughi and Sirugue, 1966). Is it possible that the nest environment severely restricted the reproductive effort of dinosaurs? The fossil beds in southern France suggest not. They provide evidence that a single female sauropod, Hypselosaurus, actually divided up her eggs into separate clutches. The clutches were evenly spaced in up to five parallel lines, each line containing 15-20 eggs. A total of about 50 eggs was deposited a reasonable reproductive effort for a 10-ton reptile. The considerations of gas exchange in the nest provide a plausible explanation for the necessity of this dinosaur's behavior. The Brush Turkey has an alternate solution to the problem of clutch size. Because the mound can contain 20 eggs which consume O 2 at a total rate of about 400 ml O 2 /hr, and the mound consumes O 2 at about 30 times this rate, the nest gas tensions tend to become extreme (Table 1). Were it not for the continual attention of the male bird, which regularly turns over the mound material and constructs tunnels down to the egg level, it is doubtful whether the eggs would survive either the buildup of heat or the severe gaseous environment that could develop in the mound (Baltin, 1969). It appears, therefore, that these underground nesters cansurvive total nest metabolic rates considerably above the suggested limit of 800 ml O 2 /hr, but the survival depends on behavioral control of the mound environment. ACKNOWLEDGMENTS We thank C. M. Vleck and D. Vleck for helping to collect new data on megapode respiration and commenting on the manuscript. We appreciate the assistance of J. Price, R. Altmann, P. Kempster and J. Thompson in preparation of the manuscript and figures. This work was supported by the Australian Research Grants Committee (RSS), an NSF grant, PCM79-05052 (RAA), and an NSF grant, DEB7903847 to the American Society of Zoologists. REFERENCES Ackerman, R. A. 1975. Diffusion and the gas exchange of sea turtle eggs. Ph.D. Diss., University of Florida, Gainesville, Florida. Ackerman, R. A. 1977. The respiratory gas exchange of sea turtle nests (Chelonia, Caretta). Respir. Physiol. 31:19-38. Ackerman, R. A. 1980. Physiological and ecological aspects of gas exchange by sea turtle eggs. Amer. Zool. 20. (In press) Ar, A., C. V. Paganelli, R. B. Reeves, D. G. Greene, and H. Rahn. 1974. The avian egg: Water vapor conductance, shell thickness, and functional pore area. Condor 76:153-158. Ar, A. and H. Rahn. 1978. Interdependence of gas conductance, incubation length, and weight of the avian egg. In J. Piiper (ed.), Respiratory function in birds, adult and embryonic, pp. 227 236. Springer-Verlag, Berlin, Heidelberg, New York. Baltin, S. 1969. Zur Biologie und Ethologie des Talegalla-Huhns (Alectura lathami Gray) unter besonderer Beriicksichtigung des Verhaltens wahrend der Brutperiode. Z. Tierpsychol. 26:524-572. Bartholomew, G. A. 1966. A field study of temperature relations in the Galapagos marine iguana. Copeia 1966: 241-250. Brown, B. and E. M. Schlaikjer. 1940. The structure and relationships of Protoceratops. Ann. N.Y. Acad. Sci. 40:133-265. Bustard, H. R. 1971a. Temperature and water tolerances of incubating crocodile eggs. Br. J. Herpet. 4:198-200.

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