Life in the "Fast" Lane: Adélie penguins and the coordination of nest relief
It is 10:22 on 6 December. Stiff southerly gusts swat the penguin as it crouches low over its eggs, face into the wind. Overhead, the sky is puffed and bruised by dark clouds. Impending snow chills the air. It's a bleak day which, for this penguin, is about to get bleaker.
Without ceremony, the penguin stands to one side of its nest. Its weak legs struggle to keep balance in the swirling wind. In a last, pathetic bid to fulfil its fatherly duties, the bird steals a stone from a nearby nest and uses it to secure the walls of its own nest. Then he staggers down the slope towards the sea, leaving his embryoes to die in the freezing cold.
Death comes quickly. A honey-breasted skua hovers above the outstretched pecks of incubating penguins, before plucking one of the eggs from the abandoned nest with practised deftness. A similar fate awaits the other.
Two days later, breast glinting in the late evening sun, feathers still wet from the sea, a female penguin walks up to the colony. She moves directly to the abandoned nest, uttering a loud call and moving her head rhythmically from side to side as she does so. She stands first in the nest, then beside it. Then, in it again. In a little while she will head back to the sea. For she, like her mate, had become a failed breeder two days earlier.
Leopard seals can break their bodies, south polar skuas can crunch their young, but, as I have observed, the major cause of breeding failure in Adélie penguins results from a failure of pairs to coordinate nest relief. Adélie penguins are their own worst enemies.
In late October to early November each year, some sixty thousand Adélie penguins leap from Antarctica's Ross Sea and attempt to breed at the Northern Rookery, Cape Bird, on Ross Island. Penguins are aquatic birds. They spend most of their lives at sea. And though they have been able to adapt to their watery domain with streamlined torsoes, wings modified as paddles, and feathers that lock together to provide insulation from the heat-stealing waters: they are not fish, because they are constrained by their past to be air breathers; and they are not whales, because their history, again, dictates that they must lay eggs. And eggs cannot be laid at sea. So each year the penguins must separate themselves from their source of sustenance in order to breed. While on land penguins fast. Hence, the breeding season for an Adélie penguin consists of alternating periods of fasting on land and feeding at sea.
Initially, male and female fast together during a courtship that takes about 12 days. Males return to nests they occupied in previous seasons; their nests being little more than scraped depressions in the frozen earth which they line with stones. Returning females choose a partner from those males occupying nests. Females show a preference for their former partners, but as more than a quarter will have died during the dark days of winter, and perhaps as many again will arrive at the rookery after them, most often female Adélie penguins must choose new partners. Time for breeding in the short Antarctic summer is extremely limited: it does not pay females to wait for late lovers, no matter how good they might have been. Few chicks fledge from late eggs.
Courting pairs copulate frequently, and at the end of the courtship period a clutch of two eggs is laid (young breeders may lay only a single egg). Females, their energy reserves sapped by fasting and the cost of producing eggs, leave their males to incubate while they go to sea. This First Foraging Trip, as it is known, lasts for upwards of two weeks. Including the period of courtship, males are without food for about one month. When relieved by their females, and relief is the word, males do not tarry long before departing on the Second Foraging Trip. They, too, are away about a fortnight. If time allows before their chicks hatch, females may get to take the Third Foraging Trip, which can last from one to seven days. The chicks hatch after being incubated for 34 days. Thereafter, parents must fetch frequent dinners for their demanding youngsters, and they switch to taking short foraging trips that rarely last for much more than a day at a time.
Coordination of nest reliefs after hatching is not a problem. During the guard stage, when parents take turns remaining with the chicks to protect them from the cold and skuas, there is little risk that the attending parent or the chicks will not have enough energy reserves to cope easily with the absence of the foraging parent for a day or so. Foraging birds return, not to thwart desertion or starvation, but in a bid to fatten their chicks as quickly as possible. Chicks of Adélie penguins must fledge in half the time that can be taken by penguins at lower latitudes, like, say, yellow-eyed penguins breeding on New Zealand's Otago Peninsula. When the chicks are about three weeks old, they no longer need protection from the cold and they can find protection from skuas in crèches. At this point both parents will absent themselves from the nest in a bid to stuff their chicks fuller still. This is the crèche stage and there is no longer any need to coordinate nest relief: the parents return to the nest only long enough to regurgitate their latest gastronomic delights to their chicks. There is little chance of starvation for the chicks (even should one parent die at this stage, the other can usually keep the chicks alive in its absence); what matters is the growth rate of the chicks. Those that fledge earliest and biggest have a much greater likelihood of surviving to breed. And for parents, a chick that dies at 10 months might just as well have died at 10 days for all the good it will have done them in an evolutionary sense. The timing of foraging trips after hatching, then, is unlikely to provoke desertions or starvation.
In contrast, associated with the longer foraging trips taken during the incubation period there is a high risk of desertion or starvation. Penguin pairs must coordinate two (sometimes three) nest reliefs between laying and hatching. My research has shown that up to a third of those breeding at Cape Bird may fail to do so. The consequences of being late are quite different, depending upon whether it is the First or Second (and Third) Foraging Trip.
Desertion in Adélie penguins is largely a male phenomenon. It occurs when a female does not arrive back from the First Foraging Trip before the fat reserves of her partner are too exhausted to fast any more. Desertions had been noted before in Adélie penguins and other species of penguins, particularly those species where one partner must fast for long periods in the absence of the foraging bird, such as emperor, magellanic, and chinstrap penguins. Usually such desertions had been put down to the foraging partner dying at sea. Indeed, leopard seals are renowned killers of Adélie penguins, and there have even been unconfirmed reports of killer whales taking them. Add to this the Antarctic's reputation for being more hostile than hospitable, and it seemed not unreasonable that when birds failed to relieve their partners, it was because they had succumbed to the biting cold or biting seal.
With the help of four field assistants, I kept a colony of Adélie penguins under continuous round-the-clock surveillance for over 1500 hours: in only one instance did a late mate not return at all. As with the forlorn father I observed on 6 December, for the vast majority of deserting males, their females come back to the colony anything from a few hours to a few days after they have left. It is not the flex of a leopard seal's jaw, but the timing of the female's return that is so fatal: a little sooner and breeding failure would have been averted.
At the beginning of courtship males are a bloated and puffy 5 kilograms or more. A quarter of that body mass is fat, most of it concentrated in a layer just under the skin. Fat is their fuel, the fire that keeps them warm through those cold days spent fasting on Antarctica's shores. They burn the fat to provide the energy to make their muscles move. We know from studies on emperor penguins, that fasting penguins get over 96% of their daily energy from their fat reserves, and that they utilize this energy source first. For, the alternative to burning fat is to burn protein. And the source of protein is their muscles. One doesn't need to be an economist to realize the limitations of breaking down muscle tissue in order to maintain functioning muscle tissue. A bird that has started to seriously consume its own muscles to stay alive, has little time before it will be immobilized, little time before it will die. Such a bird must replenish its energy stores immediately. Hence, the size of the fat reserves of a penguin place a definite limitation on the time it can spend fasting.
At the beginning of the courtship period a male has just over 51,500 kilojoules of energy tied up as fat. Work on the energetics of fasting males by my colleague, Brian Green, and I has shown that they chew through around 1270 kilojoules of energy per day. If 96% of their daily energy requirements are derived from fat (most of the rest comes from protein), then males have enough fuel to fast for an absolute maximum of 42 days. In fact, as the fat reserves near depletion, there is a threshold at which the penguins shift to mobilizing increasing quantities of protein. In emperor penguins this occurs when about 20% of the initial fat reserves are left. If the same is true for Adélie penguins, then the males would have only enough fat reserves to fast for 34 days before they started to rapidly break down their proteins (this occurs mainly by breaking down the tissue that forms the large pectoralis muscles: those muscles responsible for moving their flippers and, ultimately, their ability to forage). It is not just coincidence that I found that the peak for desertions occurred when the males had been incubating unrelieved for 22 days. Add to that the 12 days spent fasting during courtship, and it comes to 34 days: males were deserting when they had to start burning their muscles!
In emperor penguins, the body mass at which the shift to high protein usage occurs is the point at which the males desert. Fasting male Adélie penguins lose 50 grams of body mass per day, and after 34 days they weigh about 3.5 kg. This is the body mass at which 20% of their initial fat reserves remain. It is also the body mass at which they desert.
Brian and I found that the metabolic rate (i.e. rate of energy consumption) for fasting females was higher than that for males. But even allowing for the faster utilization of fat reserves that this implies, because the female has only just replenished those fat depots when she begins her incubation spell, she can fast for approximately 20 days or so. Since very few males would typically take longer than this on the Second Foraging Trip, incubating females are much less likely than their male counterparts to desert the nest. The big risk for a foraging male is not that his female will desert, but that if he is too long the eggs will hatch; and the female, with nothing to regurgitate but her voice, will not be able to prevent their chicks from starving to death. Adélie penguin chicks hatch with an insurance policy against tardy dads: the remnants of their yolk sac can sustain them for 6-8 days. Even with this leeway, the greatest risk of starvation for chicks occurs when thay are 6-8 days old. Half of all chicks that die of starvation do so because they have never been given a meal from the time they enter the world outside their shell. They starve because the foraging parent has not returned to the nest in time to give them their first feed, and very often that foraging penguin is their father overdue from the Second Foraging Trip.
So, if being late from these long foraging trips is going to precipitate eggs being deserted and chicks starving to death, where are the penguins going and why don't they come back?
Following penguins around the ice-encrusted seas of Antarctica to answer this was never going to be straight forward. Ice can prevent the passage of ships, open water, the passage of helicopters (the US Navy helicopters that provide logistic support for our Antarctic operations are not permitted to fly over open water). If the penguins could travel, then, where I could not wander, I reasoned that satellites provided the only feasible means of tracking them.
With another colleague, Gary Miller, I glued small transmitters to the backs of four females before they departed on their First Foraging Trips. The transmitters sent coded signals to three polar-orbiting satellites which passed overhead every 90 minutes. From the signals, the satellites could compute the location of the penguins to within a few hundred metres.
One female, at her furtherest point, was 270 kilometres from the rookery: the equivalent of going from New York to Boston for dinner! But because of the erratic path she took, the distance she actually covered was much greater. Despite the large distances each penguin may travel on their foraging trips, the satellites revealed that they foraged mostly within a zone about 50-250 kilometres from the rookery. For a bird capable of swimming at sustained speeds of 5 km/hour or more, potentially then, the penguins are never more than 1-2 days from the rookery. This begs the question: why don't they come back to the rookery a little earlier and avoid any risk of desertions or starvation?
One clue came from the tracked birds themselves: they took longer on their foraging trips than did birds without transmitters. The cross-sectional area of the transmitters was kept as small as possible. Even so, aerodynamic drag associated with any alteration to the streamlined penguin's torso reduces its swimming speed and probably its foraging efficiency also.
Adélie penguins feed almost exclusively on krill, small shrimp-like crustaceans that form part of the zooplankton. These occur in dense swarms that are scattered throughout the southern seas. The penguins must swim to find them, and dive to depths of tens of metres to catch them. Slow a penguin's swimming speed or reduce its catch rate and you will lower the rate at which it can assimilate energy, lower the pace at which it can lay down fat.
Females on the First Foraging Trip eat, it seems, until they reach some threshold in terms of replenishment of their energy reserves, some level of fat deposition, before they will return to the rookery and their incubating males. Females return only when they have put on around 1 kilogram of body weight (most of which is fat). Birds with transmitters had slower rates of fat deposition and had to spend longer at sea to put on that kilogram. Other females, induced to lay a third egg, used more of their energy reserves than normal before departing on the First Forgaing Trip, and so had to compensate by putting on more than a kilogram before returning to the rookery.
The success of a female will depend on how long she takes to reach this critical level of fat deposition, and how long her male can fast in her absence.
Fat males make better lovers. Fat males can fast longer. My research shows that females choose fat males either by mating with males that have already proved their fasting abilities (males that endured their female's absence the year before will be reunited but deserters are unlikely to be given a second chance) or by assessing males on the basis of their call characteristics. Favoured males have the deepest voices. Falsettos are not for females, probably because the pitch of the voice is influenced by the size of the calling bird.
Males foraging on the Second Foraging Trip may also forage until they reach a certain threshold of fat deposition; but not if the chicks are about to hatch. If time available until hatching is less than the time males need to replenish their fat reserves (this will occur if females take a long time on the First Foraging Trip), they cut short their foraging. Males that have gone without food for the longest time, therefore, feed for the shortest time.
The cue to tell them when to come back is not derived from the eggs. Birds given eggs that would hatch either five days before or after their own eggs, made no adjustments to their foraging trips in response to the substitute eggs. Therefore, males, at least, must have an internal timer capable of assessing the incubation period of their eggs. Such a timer is likely to have a hormonal basis, as virtually all biological clocks are manifested by patterns of hormone release. Much like an oven timer, there must be something to set the timer, and there must be a warning that the cake is cooked, or the egg is done.
The sudden stop in sexual activity at the time of egg laying may set the timer relative to the start of the incubation period as this results in a dramatic fall in testosterone levels. But, a hormonal message is needed to anticipate the hatching of the eggs and warn the male to return to the nest. Working in collaboration with endocrinologist John Cockrem, we have found that progesterone levels in males rise before hatching. High progesterone levels mean that the eggs will hatch soon, and a male can presumably respond to this hormonal bell by returning to the nest.
This alarm clock is either not accurate enough to prevent some males from being late, or perhaps, if energy reserves of the males are too low, it's ignored - the males putting protein before progeny, survival before reproductive success. If so, it is just another example of that constant compromise for a penguin: balancing its need for food against the abilities of others to fast, replenishing its fat reserves before the fat reserves of its mate or chicks run out.
Sitting on the push ice, that icy margin which forms an interface between the watery world of the Adélie penguin's food supply and the land on which it must breed, I still struggle to understand why the penguins should go away for so long to feed during the incubation period. However, as I watch a group of penguins leap ashore from a calm blue sea, a sea scattered with ice floes and the sun's reflections - while beyond, there is every mountain that you should ever hope to see - I begin to understand why they come back.
– Lloyd Spencer Davis
– From: Natural History, 91/1: 46-55