Physiological Contraints: Asphyxia
Loss of oxygen during a dive is probably the most widely studied physiological phenomenon faced by penguins and other diving birds.
Oxygen-saving mechanisms include:
Principle oxygen stores in the body of a penguin are 1) hemoglobin, 2) myoglobin and 3) lungs and air sacs (Stonehouse 1975, Muller-Schwarze, 1984). Hemoglobin and myoglobin have an interesting relationship; they are functionally related and structurally similar. Myoglobin is a protein that contains a heme group, an organic structure that contains iron. Oxygen binds to the iron in this heme group. Hemoglobin contains four protein subunits, each of which carries a heme group. The iron of hemoglobin's heme group is also the site of oxygen-binding. Myoglobin has a higher affinity for oxygen than hemoglobin (Kooyman and Ponganis 2004) (see Fig. 1). These oxygen stores can be enhanced by increasing oxygen carrying capacity of the blood, meaning a greater concentration of hemoglobin and red blood cells (since hemoglobin is contained in red blood cells). The blood volume of the body might also be enlarged. Oxygen carrying capacity of blood and perhaps also blood volume does appear to be greater in diving birds, though there is few comparative data (Stonehouse 1975, Muller-Schwarze 1984).
Figure 1. Oxygen binding to myoglobin and hemoglobin. (Adapted from stingray.bio.cmu.edu/ ~web/bc/Lec/Lec12/lec12.html).
Myoglobin is much more concentrated in terrestrial birds than aquatic, based on muscle color. However, the oxygen bound by myoglobin represents only a small part of the total oxygen store and it is likely that in the penguin this supply exhausts much sooner than the actual breath-holding limit. Oxygen reserves in the myoglobin are the first to be exhausted during a dive, and once this oxygen is gone the muscles switch to less efficient anaerobic metabolic pathways (Muller-Schwarze 1984). Since myoglobin has a much greater affinity for oxygen than hemoglobin, if any of the remaining blood oxygen stores were exposed to muscle, the oxygen would move from the blood to the myoglobin. Therefore the muscles have to be shut off from other oxygen stores in the body since they would deprive obligate aerobic tissues such as the brain of sufficient oxygen (Muller-Schwarze 1984, Stonehouse 1975).
The lung and air sac contribution to total body oxygen stores in the penguin is very significant (they contain about 50% of the total oxygen), as opposed to seals that exhale about 50-60% of inspiratory lung volume before diving. Penguins dive right after an inspiration; therefore the diving gas volume relative to body weight of penguins (about 160 cm 3/kg) is much greater than seals which is about 22 cm 3/kg (Stonehouse 1975).
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A 5 kg penguin has an estimated oxygen reserve of about 250 ml; this would last for 2.5 minutes at resting metabolism. However, penguins have adapted various oxygen-saving mechanisms that allow oxygen in the body to last longer.
Though the majority of penguin dives are essentially aerobic, anaerobic metabolism may be used in some circumstances (Green et al. 2003). Many tissues such as muscle have a capacity to continue anaerobically whereas other tissues, such as the brain, must have a continuous oxygen supply. Accordingly, there are major changes in blood flow during a dive, most importantly being a slowed heart rate and the reduced circulation to muscles (Stonehouse 1975). Ponganis et al. (1999) found that cardiac output was restricted in diving King penguins and blood flow was predominantly reduced to the brain, heart and lungs. A reduction in respiratory O 2 stores and a relative increase in muscle O 2 stores appear to be adaptations for deep-diving in King penguins (Ponganis et al. 1999).
As the dive begins, the penguins heart rate slows. In Adelie and Gentoo penguins, the diving heart rate is about 20 beats per minute. This is independent of the pre-dive rate of about 80-100 beats per minute (Stonehouse 1975). Muscles such as the gastrocnemius and pectoralis obtain less blood, while the heart receives a maximum (Muller-Schwarze 1984). It was shown in Gentoo penguins that pectoral muscles and toe vessels bleed much more slowly during submersion than when the bird is breathing normally (Stonehouse 1975). Heart rates during diving have also been recorded for Humbolt penguins. In this study, no significant reduction in heart rate below resting levels was seen even up to the longest voluntary dives recorded at 50 s (mean dive length was 36.4 s). However, when voluntary dives were forcibly extended by waving hands over the water surface, at 60 s heart rates had fallen dramatically to 78 beats per minute from 119-135 beats/min in shorter dives (Butler and Woakes 1984).
In Macaroni penguins, heart rate was higher than resting before and after dives, falling to a level close to or lower than resting level during dives (Figure 2, Green et al. 2003). According to Green et al. (2003), this response appears to be a trade-off between a classic dive response, which conserves oxygen stores while the animal is deprived of access to air, and the exercise response, which prioritizes blood flow and oxygen uptake to active muscles when exercising. Adjustments in heart rate allow the dive duration to be extended by ensuring full loading of oxygen stores before the dive, then by reducing aerobic metabolism during the dive and ensuring the full and effective use of oxygen stores while submerged (Green et al. 2003).
Figure 2. (A) Changes in depth during dives of 102-110s and (B) associated changes in heart rate (filled circles) with overall heart rate during diving bouts (open circles), recorded from 13 breeding female macaroni penguins. Values are means +/- S.E.M. Figure from Green et al. (2003).
It is also shown that while oxygen concentration drops during a dive, CO2 levels increase correspondingly. Generally, diving birds and mammals are less sensitive to CO2 than land animals, probably due to greater buffering ability of the blood (Muller-Schwarze 1984). Reduced sensitivity to CO2 is beneficial in extending the breath hold since CO2 is one of the principle stimuli to terminating an apnoeic episode (Stonehouse 1975).
A surge of lactic acid concentration usually occurs after a dive, reflecting and increased flow to tissues previously functioning anaerobically (Muller-Schwarze 1984, Croll et al. 1992). As blood passes through the tissue, mainly muscle, it picks up large quantities of lactic acid accumulated gradually during the dive. The gradual increase of lactic acid during a dive indicates anaerobic processes in the muscles which are supplied with little blood during the dive but are generously suffused after emerging (Muller-Schwarze 1984). However, some increase in blood lactic acid occurs during the dive, which suggests that a small amount of flow continues to the muscle. In fact, this leakage may be considerable compared to the grey seal, Halichoerus grypus. In the penguin during a 5 minute dive the lactate concentration of arterial blood doubles, but in the grey seal there is hardly a noticeable change within the first 5 minutes of submersion (Stonehouse 1975).
The aerobic dive limit (ADL) is the diving duration beyond which post-dive blood lactate levels increase above resting values. ADL has been calculated (cADL) for several penguin species by dividing an estimate of usable body oxygen stores by an estimate of the rate of oxygen consumption (V O 2) while submerged. Many studies have found that 2-50% of observed penguin dives exceeded the cADL. However, the dive:pause ratio in these studies suggests that it is unlikely that so many dives use predominantly anaerobic metabolism. In order for a large proportion of natural dives to be aerobic, the cADL must be greater. If estimates of the usable oxygen stores for penguins are correct, then V O 2 during diving needs to be as low as that recorded from penguins at rest on the water surface for most dives to be within the cADL (Green et al. 2003).
In a study done by Green et al. (2003), heart rate was used to estimate V O 2 in Macaroni penguins. A suite of physiological and behavior adaptations were found to contribute to the maximizing of cADL while penguins were submerged, including 1) variation of heart rate and circulation, 2) regional hypothermia, and 3) the use of passive gliding during the ascent and descent of dives. This study found that if heart rate is averaged over complete dive cycles, it is an accurate and reliable predictor of V O 2 for the dive cycle. As observed dive durations increased, V O 2 decreased, and hence cADL increased. For all dive durations of up to 138 s (95.3% of all dives), the cADL was greater than the observed dive duration. These results imply that most natural dives within diving bouts by Macaroni penguins are aerobic (Figure 3, Green et al. 2003).
cADL was calculated using V O 2 while resting on water for three other penguins species, though V O 2 was measured using respirometry rather than estimated in the field. In emperor penguins, 96% of dives would be within the cADL, whereas in king penguins and gentoo penguins only 80% of the dives would be within the cADL. Oxygen stores are assumed to be the same for all four species of penguin, so there must be a difference in diving behavior or V O 2 while submerged between species. Food density, distribution and location fluctuate for each species, and are more likely to be the cause of variability in diving performance between species than differences in physiology. Breeding success of gentoo penguins is far more vulnerable than in macaroni penguins to variations in food availability, so it may be that gentoo penguins are under greater pressure to gather enough food to feed their two chicks, leading to a higher proportion of anaerobic dives. Emperor penguins are much bigger than king penguins (and so have greater oxygen stores that allow them to dive to greater depths and for longer durations), and yet their diving performance is similar. A large proportion of foraging dives for both species are to 100-200 m in depth and last up to 5-6 minutes. This indicates that emperor penguins operate well within their physiological limits, whereas king penguins dive to depths and durations that are close to the maximum of their capabilities (Green et al. 2003).
Figure 3. Change in observed calculated aerobic dive limit (cADL, open diamonds, with 95% confidence limits) with increasing dive duration (grouped into 10 s bins). The line marked by filled diamonds represents the line of equality where cADL equals dive duration. Dive durations (on the line of equality) above the observed cADLs probably involve an anaerobic component. Also shown are the cumulative percentage frequency of dive durations (grey bars) (Figure from Green et al. 2003).