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Biological Research

versión impresa ISSN 0716-9760

Biol. Res. v.33 n.3-4 Santiago  2000 

Reduced oxygen diffusion across the shell of Gray gull
(Larus modestus) eggs


1 Departamento de Transporte de Oxígeno, Universidad Peruana Cayetano Heredia, Lima, Perú
2 Clinicum Laboratorio Automatizado, Iquique, Chile
3 Universidad de Antofagasta, Antofagasta, Chile
4 Universidad Arturo Prat, Iquique, Chile


Gray gulls, Larus modestus, nest 1500 m above sea level in northern Chile's Atacama Desert, one of the driest in the world. Their eggshell gas permeability, one third of that found in other Larus species, is an adaptation that reduces water loss, but at the expense of oxygen diffusion into the air cell with resultant hypoxia and reduced metabolic rate. This contrasts with characteristics found in birds nesting at very high altitudes where oxygen diffusion across the egg shell is maximized at the expense of water conservation.

The oxygen consumption (MO2) of Larus modestus is 66% that of Larus argentatus; the oxygen conductance (GO2) is equivalent to 48% of that obtained in 5 other bird species. The oxygen partial pressure (PAO2) in the air chamber of Larus modestus (84 Torr) is lower than that of 10 other bird species whose average (PAO2) is 106 Torr. The CO2 partial pressure (PACO2) in the air chamber of Larus modestus is 68 Torr, a higher value than that found in 9 other bird species whose average (PACO2) is 39 Torr.

Key words: Atacama; eggshell; oxygen conductance; oxygen consumption; Gray gull (Larus modestus)


Gray gulls (Larus modestus) nest in the Atacama desert of northern Chile, one of the driest and most barren deserts in the world. Extensive studies of their adaptations to desert nesting have been conducted by Howell et al. 1974; Fitzpatrick et al. 1988; 1989; Guerra et al. 1989; 1988, including the water vapor conductance of their eggs. Guerra et al. (1988) report the water vapor conductance to be just 33% of that predicted for eggs of the mass of Gray gull eggs, using an equation based on values for other species of gulls. They interpreted the reduction in water vapor conductance as an adaptation for conserving water and postulated that the long incubation period of Gray gulls is a consequence of a concomitant reduction in the diffusion of the metabolic gases O2 and CO2. In this article we report on a study designed to measure O2 diffusion across Gray gull egg shells and test the hypothesis that their embryos have lower O2 consumption rates (MO2) than predicted for their masses. We based our hypothesis on Fick's Principle of gas diffusion for O2, using the equation:

MO2 = GO2 (PiO2 - PAO2) (1)

where MO2 is the oxygen consumption per unit time, GO2 is the oxygen conductance of the shell, PiO2 is the atmospheric PO2,, and PAO2 is the egg air cell PO2. A decrease in the GO2 could be compensated for by a reduction of MO2 by the embryo or in PAO2 or both.


Eighteen eggs were collected on the same day during Chilean summer from El Tigre (the location and description of this site is given by Fitzpatrick et al. (1989) and Guerra et al. (1988)), a nesting site approximately 35 kilometers from the coast. This location was at 1500 m. altitude. The ages of the eggs were estimated by means of a flotation technique (Aguilar et al, 1994), which consisted of placing the egg into a container with water and determining its inclination relative to the container bottom. The eggs were transported in a portable incubator at 37ºC to the Clinicum Laboratory of Iquique (at sea level) within approximately 7 hours. We began experimental work immediately upon arrival.

Embryonic MO2 and air cell PAO2 and PACO2 tensions were measured following the methods outlined in Carey et al. (1989) for each of 9 eggs. Each egg was placed in a 10 x 6 cm lucite chamber connected to an similarly sized chamber by a water-filled manometer. The two chambers were submerged in a water bath maintained at 37º±1ºC. After a 0.5-1 h equilibration period, during which the chamber containing the egg was continuously flushed with air, the system was closed, and 1 ml of oxygen was injected with a syringe into the chamber displacing the fluid in the manometer.

The calculation of MO2 was based on the time needed for the embryo to consume that volume of oxygen and for the fluid to return to its original position. Results on each egg were converted to STPD and averaged. After obtaining the air cell gases, the air cell was filled with water and the egg was weighed to obtain its weight at the onset of incubation. Each embryo was separated from the yolk and membranes, blotted dry and weighed using a precision balance. One had pipped the air cell. The shell thickness was measured with a thickness micrometer gauge (Mitutoyo, Japan) from dried eggshell fragments after removal of the outer membrane. Pore counts were made for seven eggs. Fragments of each shell were boiled in 5% NaOH solution, washed and dried. A film of methylene blue was applied to the inner surface of the fragment, and after drying, the pores were visible on the outer side of the shell. Using a dissecting microscope and calibrated screen, the number of pores was counted.


Table I contains the basic data and the derived data relevant to oxygen transport evaluation. We selected eggs 5 through 8 to be representatives of embryos near term before pipping in accordance with Aguilar et al, (1994). The mean values were used to calculate the transport parameters. To convert the water-vapor permeability to O2 permeability of the 12 different values for Larus published by Guerra et al. (1989), we used conversion factors for the gas diffusion coefficients and for the correction of the temperatures (26ºC for water vapor permeability and 37ºC for oxygen conductance measurements). The conversion factors were validated in our laboratories by direct comparison of oxygen conductance calculated from water vapor permeability and the direct measurement of MO2 and (PiO2 -PAO2) with excellent agreement (Copernik-Bitterman, 1984).

Table I

Respiratory parameter used to evaluate diffusion in Larus modestus

PIO2= 149 Torr


W embryo W egg MO2 PAO2 PACO2 GO2 PL
  g g ml gr-1 hr-1 Torr Torr ml h-1Torr-1 mm


  6,71     48,9 0,972 122,8 24,2 0,249 0,224
2 12,21     52,1 1,122 - - - 0,234
3 14,5 2802 1,121   88,9 64,9 0,27 0,24
4 15,82     51,3 0,964 116 20 0,462 0,212
5 17,61     47,3 0,918    96,9 56,4 0,31 0,227
6 17,78     54,7 0,858    70,6 86,1 0,195 0,287
7 20,67     50,8 1,151    81,4 67,4 0,352 0,215
8 24,85     56 0,658    83,6 61,6 0,25 0,238
9 27,02     56,3 0,764 - - - 0,231

Table 1: W egg = egg mass; W embryo = embryo mass; PL = pore length

Table II compares values of L. modestus with relevant data from the literature. Because gas conductance is proportional to the functional pore area of the eggshell as well as to the gas diffusion coefficient and is inversely proportional to the pore length, the Fick equation can be written as follows:

MO2 = (D/RT)(Ap/PL)(PiO2 -PAO2) (2)

D = gas diffusion coefficient
R = gas constant
T = absolute temperature
Ap = functional pore area
PL = pore length

Table II shows that the oxygen consumption of L. modestus embryos is 66% the rate of L. argentatus and seven species of birds having an egg mass close to that of L. modestus (Hoyt and Rahn, 1980). Oxygen conductance is 48% of the value for the same seven species of birds (Hoyt and Rahn, 1980). If the values for water vapor conductance predicted for Larus are converted to oxygen conductance, the value for L. modestus is 56% that the other species (Paganelli et al. 1974, 1978).

Table II

Comparison of respiratory parameters in Larus modestus, species of same genus and other bird species.(mean values)

(ml · g-1 · h-1)

L. modestus
L. argentatus
1 (n=2)
A / B

(ml · h-1 · Torr-1)
L. modestus
*5 bird species 1, 2
A / C

Pore area
L. modestus
Larus 2 (n=9)
A / D


L. modestus
Larus 2 (n=9)
A / D

L. modestus
**8 bird species3
A / E

L. modestus

***9 bird species4

A / F

RQ L. modestus   0,78


1 Hoyt and Rahn (1980) Larus ridibundis (Black-headed gull)
2 Rahn and Dawson (1974) Larus tridactyla (Black-legged kittiwake)
3 Ar and Rahn (1978) Larus fuscus (Lesser Black-backed gull)
4 Rahn et al (1974) Larus canus (common gull)
* Gallus gallus (chicken)
Dendrocygna autumnalis (Red-billed whistling Duck) *** Coturnix coturnix (Japanese quail)
Dendrocygna bicolor (Fulvous Whistling Duck) Sterna hirundo (common tern)
Aythya fuligula (Tufted Duck) Columba livia (pigeon)
Netta rufina (Red-crested Pochard) Phasianus colchicus (ring-necked pheasant)
Gallus gallus (hen)
** Larus glauceseaus (Glaucous-winged Gull) Anas boscas (Pekin duck)
Larus marinus (Great Black-backed gull) Meleagris gallopavo (turkey)
Larus heermanni (Heermann's gull) Larus argentatus (herring gull)
Larus occidentalis (Western gull) Anser domesticus (embden goose)

The functional pore area of L. modestus eggs is 34% and the pore length 88% of the value reported for nine other species of Larus (Ar and Rahn, 1978). The PO2 of the air cell in L. modestus eggs is reduced to 84 Torr, substantially lower than that of the other 10 bird species, the mean value of which is 106 Torr (Rahn et al. 1974). The PCO2 of the air cell was 80% (68 Torr) above the values reported for the other 10 species of birds (Rahn et al. 1974). The RQ of L. modestus embryos falls within the expected range for birds. Theory predicts 0.7 for an embryo metabolizing fat, but this parameter is usually higher in bird embryos (Rahn et al. 1974).


The extreme environmental conditions where the Larus modestus nests were described by Fitzpatrick et al. 1989. The distance from the coast restricts adults to foraging only once a day. Incubating and brooding adults, as well as unnattended young, experience extreme diurnal environmental conditions (the air temperature ranges between 2.5º and 38ºC, ground temperature between 2º and 61ºC, wind velocity from 0 to 833 ms-1 and relative humidity from 6% to 99%). Studies done on the adult birds include thermoregulatory behavior and metabolic rate (Guerra et al. 1988), the energetics of reproduction (Fitzpatrick et al. 1988), and the time and temperature of incubation (Aguilar et al. 1994). Eggs of this species have shown water vapor conductance is only 33% that of 12 other Larus species (Guerra et al. 1989). Our results place the metabolic rate of L. modestus embryos at 66% that of the other birds. The oxygen conductance is 48% of that found in seven species of birds with a mass similar to that of Larus modestus. The functional pore area was reduced to 34% when compared with nine other Laras species. This is perhaps the most important finding of this investigation, and is in agreement with the reduction of water vapor conductance to 33%, as described (Guerra et al. 1989).

The pore length did not play a prominent role in adaptation, as seems to be the case in many other studies of adaptation of eggs to extreme environments. The pore radius of 1.3 m can be compared with that in L. heermanni of similar mass where it was found to be 8.6m (Rahn and Dawson, 1979). Because the total number of pores (4,758) was close to that of L. argentatus (5,720), it seems that the total pore area adaptation is primarily due to a reduction in individual pore size, not in pore number. The significant drop in the PAO2 is a unique finding. The air cell equilibrates with atmospheric air pressure over a short period of time (less than an hour) (Carey et al. 1989, 1994), and the eggs were exposed to sea level conditions for a period of approximately 7 - 10 hours. A PAO2 of 84 Torr is well below the expected average of 104 Torr at sea level, and PAO2 will necessarily be lower at the altitude of 1500 m. The increase of the gas diffusion coefficient at altitude will attenuate the drop in PO2, but will not correct it (León-Velarde et al. 1984).

Despite the low metabolic rate, the marked reduction of the gas permeability must be the cause of a significant elevation of the PCO2. In the case of PO2 at an altitude of 500 m, this elevation will be attenuated by a factor of 640/760, due to the increase of the gas diffusion coefficient in inverse proportion to the fall in barometric pressure (PB). The PAO2 corresponding to the altitude of 1500 m can be calculated by introducing the factor PB/760 into the Fick equation:

PAO2 = PiO2 - (MO2 / GO2) (PB / 760) (3)

Assuming that MO2 does not change between sea level and 1500 m, this equation predicts a PAO2 of 69 Torr at Gray gull nesting sites, a 33% reduction in the average sea level value of 104 Torr. The corresponding PCO2 at the nesting site (1500 m) would be 57 Torr, which is still significantly higher than the maximum of 43 Torr for 10 bird species (Table II). The increase in PCO2 must be buffered if the blood pH is to be protected. This finding suggests the need to explore the acid-base equilibrium of L. modestus embryos.

Our results contribute to the integrative ecological physiology of birds in extreme desert conditions. We have previously shown that the high altitude environment can lead to a reduction of water vapor conductance of eggs at altitudes up to approximately 2500 m, whereas at higher altitudes water conservation is sacrificed in favor of higher oxygen conductance. It is important, however, to point out that the high altitude eggs studied were nesting near aquatic environments (Monge-C. et al. 1988). There is another ecological situation in which water vapor permeability is compromised, and this occurs in sea birds with markedly prolonged incubation times. Whittow (1980) defined prolonged incubation time as that exceeding the upper 95% confidence limit of the regression line relating incubation time and egg weight for birds in general. Rahn and Ar (1974) published an extensive list of prolonged incubation times that included the orders Procellariformes (22 species), Pelecaniformes (11 species) and Charadriiformes (3 species). In this latter group, only two terns, both tropical species, and one alcid were included. No gulls were included. Using the allometric equation relating the incubation time and egg mass in L. modestus, we obtained a figure of 28 days. The alue reported is 29 days, which is not long enough to explain the Gray gull's low eggshell permeability (Aguilar et al. 1994). The present work presents evidence that selection for water conservation can have consequences for the PO2 of egg air cell in the extremely arid conditions of the Atacama Desert. As in a previous paper (Ostojic et al, 2000), this publication compares species in an altitudinal point of view, showing another example of the perpetual competition of oxygen and water, two of the most important biological molecules in bird eggs (Monge-C. et al. 1991).

Corresponding Author: Hrvoj Ostojic P. Clinicum Laboratorio Automatizado, Casilla 169, Iquique, Chile. Telephone: (56-57) 420599. Fax: (56-57) 427683. e-mail:

Received: July 11, 2000. Accepted: August 22, 2000


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