by Tim Birkhead
Willughby and Ray made a point of dissecting as many bird (and fish) species as possible, noting the state of their internal organs and the gonads, in particular. They were quick to comment on whether a male’s testicles (testes) were relatively large (as in the quail, house sparrow, dunnock and turtle dove) or small (as in the shrike they killed near Augsburg). Exceptionally large testes tell us something interesting; small testes don’t necessarily indicate much because in all birds that breed in temperate regions, such as Europe, the testes shrink away to almost nothing outside the breeding season and this means that a bird with tiny testes may simply be out of breeding condition. A bird with big testes, however, is one in which the females of that species are promiscuous.
Allow me to explain the logic here. As a result of molecular paternity studies conducted during the 1980s and 1990s, it is now well known that, despite the fact that most birds (but not ruffs or jungle fowl) breed as pairs, infidelity is common and results in broods of mixed paternity. In species where females are unfaithful, males attempt to minimise their loss of paternity by transferring more sperm, and they do this by evolving larger testes. Willughby and Ray naturally knew nothing of evolution, nor the concept of what is known as ‘sperm competition’, but they were on the right track when they said that the quail had ‘Great testicles for the bigness of its body, whence we may infer that it is a salacious bird’ – as indeed it is. Frequent copulation with his partner is the male quail’s best chance of being the biological father of her offspring.17
Like the testes, the reproductive organs of female birds – the ovary and the oviduct – also show profound changes in size through the year, and are at their maximum, of course, during the breeding season. The autumnal reduction in size may be an adaptation for flight – why carry all that additional anatomical baggage outside the breeding season when it isn’t needed? A further weight-saving adaptation in female birds is achieved by having – in most species – only a single functional ovary and oviduct. In comparison, most mammals and reptiles have two – a paired system. The existence of just one, and it is usually the left ovary and oviduct, has been known for as long as people have been butchering chickens. But as Willughby’s question suggests, this might not always be true. He asks: ‘Whether some birds have a double cluster of eggs, as viviparous animals have two ovaria?’
Double ovaries have been recorded in two groups of birds: in raptors, such as the Eurasian sparrowhawk and harriers, and in kiwis – routinely.18 It is possible that Willughby found double ovaries in some of the raptors he and Ray dissected. Kiwis weren’t discovered until the nineteenth century, so he couldn’t have known about them. On reading through the raptor accounts in the Ornithology, I was disappointed to find not a single instance where Willughby had discovered a double ovary. It is possible that one of the earlier ornithologists, such as Gessner, Belon or Aldrovandi, had noted an example, but I had no luck there either. It is not known why some female raptors occasionally have a double reproductive system, but in kiwis (which of course are flightless and so do not benefit in the same way as flying birds from saving weight) it is thought that the two ovaries and oviducts alternate in producing eggs. But of course this still does not explain their existence.19
Willughby’s final question about reproduction asks whether female birds that are ready to lay eggs are able to hold on to them if, for example, their nest is destroyed, or ‘whether they [their eggs] sometimes fall from them against their wills’.
The only thing I can think of that might have prompted this question was that Willughby, or someone he knew, had encountered isolated eggs in unlikely locations – such as an intact starling egg lying conspicuously in the middle of a lawn. As a boy, when starlings were much more common than they are today, I came across several such eggs, and like Francis Willughby I wondered whether the female had been ‘caught short’ and forced to lay away from her nest. I couldn’t think of any other explanation. However, in the 1970s, careful field studies showed that starlings are unusual in sometimes behaving like a cuckoo, laying eggs in the nests of other females, but of their own species. Some female starlings attempt to exploit the parental care of other starlings by dumping one or more eggs in their nest. As they do so, the parasitic individual removes one of the host’s eggs (presumably to minimise the chances of her egg being detected) and then flies off with it and drops it somewhere.20 Eggs dropped onto a hard surface smash and quickly disappear; those dropped onto a grassy lawn are more likely to survive intact.
Another example of eggs turning up in unlikely places is guillemot eggs dredged up from the seabed by fishing boats many miles from any breeding colony. Such eggs were greatly prized by nineteenth-century egg collectors who, of course, were desperately vulnerable to being duped. However, there were enough records to show that guillemots must occasionally – for whatever reason – lay their eggs far out at sea, exactly as if they have been ‘caught short’.21
Experiments on chickens have shown that if a hen is deprived of somewhere to lay, she can hold on to her egg for several hours beyond her normal laying time.22 So, this answers Willughby’s question: birds can hold on to an egg for a while, but after a certain time, if they are unable to lay in their nest, they are forced to deposit their egg more or less at random.
There is one bird, however, that routinely holds on to its egg for longer than most others, the European cuckoo. As Willughby and Ray knew, this species is a brood parasite, depositing its eggs in the nests of other species so that the young cuckoo is reared by foster parents such as the dunnock. Whether Willughby and Ray knew that Aristotle had commented on the cuckoo’s parasitic habit isn’t clear, but they were, nevertheless, shocked by it because, as one of them – probably John Ray – writes, it ‘seems so strange, monstrous and absurd, that for my part I cannot sufficiently wonder there should be such an example in nature; nor could I have been induced to believe such a thing had been done by nature’s instinct, had I not with my own eyes seen it.’
One key to the cuckoo chick’s success is hatching before those of its host. This allows the young cuckoo to eject the host’s eggs or chicks, and to monopolise the food brought by the parents. Early hatching is arranged by the cuckoo in several ways: by laying early in the host’s laying sequence; by producing a relatively small egg that requires fewer days incubation; and partly by giving her egg a head start by retaining and incubating it within her body for an additional twenty-four hours. Laying early in the host’s sequence and producing a small egg are both adaptations that have evolved through natural selection as part of the cuckoo’s brood parasitic repertoire. Retaining the egg in the oviduct for an extra twenty-four hours is a fortuitous accident (for non-parasitic species of cuckoo also do it), which may nevertheless have predisposed cuckoos to become brood parasites.
In most birds, including the domestic fowl and songbirds such as thrushes, wagtails and pipits, females lay their eggs at intervals of twenty-four hours. That’s how long it takes for an ovum to be released from the ovary, be fertilised, to have the albumen and shell added to form the egg and to pass through the oviduct and into the nest. The ovum (essentially what we think of as the yolk) is fertilised within minutes of being released from the ovary and the embryo’s development starts a little bit further down the oviduct about five hours later. By the time the completed egg is laid, the embryo consists of a few thousand cells that appear as no more than a pale speck on the yolk’s surface. Things are different in the cuckoo; its eggs are laid at intervals of forty-eight hours. Each egg takes twenty-four hours to form, just as in other birds, but the female cuckoo retains the fully formed, shelled egg inside her for a further twenty-four hours. During this time the embryo continues to develop, so that when the egg is laid the embryo has a head start. An additional twenty-four hours in the oviduct might be expected to provide the chick with a twenty-four-hour advantage, but because the body temperature (40°C) of the female cuckoo is several degrees warmer than eggs experience during incubation (36°C), the youn
g cuckoo ends up with a thirty-hour hatching advantage over the host chicks.23
Willughby’s final three questions are about how birds survive the cold of winter conditions; which of them migrate or hide; and what would become of migrant birds if they were kept in captivity over the winter?
For small birds that don’t migrate, the way they cope with cold winter nights is truly remarkable, and I think Willughby would have been astonished at what ornithologists have since discovered. This is how Willughby phrased his question: ‘How cometh it to pass that the most vehement cold in winter-time, if they have but food enough, doth not congeal or mortifie the tender body of small birds?’
Before we answer this, let us consider what our smallest European bird, the goldcrest, has to endure. Weighing just five grams – little more than a teaspoon of sugar – a goldcrest typically has to survive sixteen hours of winter darkness each night at temperatures as low as minus 20°C. How does it do that?
Superficially, we might imagine the answer to be: fat and feathers. Even Willughby might have realised this, but in fact the way small birds make it through the long winter nights depends on an extraordinary combination of anatomical, physiological and behavioural tactics.
Birds have to possess sufficient fuel in the form of fat to keep their engines generating heat overnight. Many small birds forage strategically during the winter day, subconsciously deciding on the basis of the ambient temperature how much food to convert to fat for their overnight survival. It is a delicate balance: too little fat and you don’t make it through the night; too much and you are too heavy when flying and vulnerable to being caught by a hawk.
Feathers provide extraordinary insulation, and birds typically fluff themselves up into a ball when they go to roost. This is most easily seen if you have a camera nest box used by a roosting great tit or blue tit during the winter. That spherical shape minimises the bird’s surface area, and hence its heat loss. The colder it is the more the feathers are erected and the more air is trapped and the less heat lost. It is often said that birds put their head under their wing when they sleep, but that’s not true: rather, they turn their neck and place their head under the feathers on the back. With the rest of the plumage fluffed up, the head becomes invisible, and there’s a good reason for this. More heat is lost from the head, and especially around the eyes and beak, than from anywhere else on the bird’s body, so keeping the head warm is a priority.
Roosting in a nest box isn’t a bad idea, for the microclimate at the roost site obviously has a huge effect on the temperature to which a sleeping bird is exposed. Many small birds roost in cavities and some – such as tree creepers and wrens – do so in huddling groups, benefiting from each other’s body heat and insulation. Sometimes goldcrests roost in the open, but usually with others in a huddle, for the same reason.
We know from our own experience of trying to stay warm in bed that food and feathers (an insulating eiderdown or down-filled duvet) are essential. Willughby would have understood this, but he would also have recognised that our problem isn’t as acute as that of a goldcrest because our greater body size means that we lose heat more slowly. There must be something else going on, and indeed there is, but I doubt that Francis Willughby could have anticipated what it is.
Studies of the North American black-capped chickadee by Susan Budd Chaplin in the 1970s revealed that although they went to roost with some 7 per cent of their body mass as fat, this was insufficient to maintain their body temperature (42°C) and survival through the entire night, despite their wonderful insulating feathers.
What Chaplin discovered was extraordinary: the chickadees drop their night-time body temperature to around 30°C, entering a state of hypothermia and reducing their fuel consumption so that there is sufficient fat to see them through the night. Hummingbirds, which are even smaller, and are especially vulnerable to losing heat at night (even in the tropics, and especially at high altitudes), do something similar and drop their body temperature to below 10°C, becoming torpid as a result. The energetic saving of torpor is enormous. Torpor also occurs in both the European nightjar and the common poorwill of North America, which in the latter case can remain in a state of suspended animation for several days on end – a mini-hibernation. Even birds such as tits and finches reduce their roosting body temperature – usually by only five degrees – to enjoy the benefits of this overnight energy saving.24
What about migrants? In Willughby’s day the whole issue of bird migration was still up in the air, so to speak. Doubt about migration had been cast centuries before by Aristotle, who suggested that some birds metamorphosed into others between summer and winter – thereby accounting for why some species disappear and others appear in winter. But he also thought that some hibernated, hiding themselves away in holes during the winter months. He was fairly confident that others, such as white storks, migrated to warmer climes, because he could see them leaving in the autumn and returning again in the spring. Willughby agreed, saying in the Ornithology: ‘it is most certain, that storks before the approach of winter fly out of Germany into more temperate and hot countries’. There were a few other convincing instances of migration, including the ornithologist Pierre Belon’s observations of common quail made in the mid-1500s: ‘When we sailed from Rhodes to Alexandria of Egypt many quails flying from the north towards the south were taken into our ship, whence I am verily persuaded that they shift places.’25 The real problem was small birds such as warblers and swallows. It was obvious that they disappeared in the autumn, but they seemed too fragile to fly across vast tracts of ocean, and – because they typically migrate at night – their seasonal movements remained unobserved. It was precisely for this reason that doubts about migration in such species persisted for so long. It wasn’t until the 1800s that most naturalists eventually agreed that migration was the only plausible explanation for their seasonal appearance and disappearance.
The answer, therefore, to Willughby’s question – ‘What birds hide themselves or change places, whether in summer or winter?’ – is that no birds hide themselves or hibernate; those like warblers, nightingales and flycatchers migrate, while others such as finches and tits stick it out and are resident all year round.
The next part of Willughby’s question is a revealing one: ‘What would become of nightingales, cuckoos etc., in winter, and old fieldfares &c. in summer if they were kept in cages, and carefully tended, fed and cherished?’ I should first point out that – as Willughby was well aware – the fieldfare is a winter visitor from northern Europe to Britain, which is why he asks what would happen to it in summer. Willughby’s question is revealing because it confirms a suspicion I have from reading the Ornithology, that neither he nor Ray had very much to do with those people who trapped or kept small birds as cage birds. Keeping songbirds – including canaries imported from Spain – was increasingly popular from the Middle Ages onwards, and a huge variety of species was kept. Most of them probably didn’t survive very well, but some – including a few migratory species – occasionally found themselves in the care of an expert and lived long and lusty lives. This means of course that had Willughby been more familiar with this aspect of ornithology he might have been able to answer his own question.
Of all the small birds kept as pets in the seventeenth century, the nightingale – a migratory species – was the most popular, because of its lovely song. Also, as Willughby and Ray knew, Valli da Todi and Olina had already written extensively about the habits of this species. And although they do not say so explicitly, my guess is that both these authors – and probably other individuals too – will have kept nightingales over winter.26 Cuckoos would have been a different matter, because everyone that has tried it has found them to be impossible to maintain in captivity.
The first details of what captive nightingales do during the winter came from Nicolas Venette, a French physician and professor of anatomy at La Rochelle, whose account appeared in 1697 while John Ray was still alive. Venette was a polymath and publi
shed on a wide range of topics including pruning trees, poetry and the treatment of scurvy. He was best known, however, for a work entitled De la génération de l’homme, ou tableau de l’amour conjugal, popularly known as Conjugal Love, a book that dealt with genital anatomy, sexual gratification, pregnancy and embryo development. Most references to it criticised the book for its lewdness, but the English translation I obtained revealed it to be anything but lewd. Instead Conjugal Love is a wide-ranging sex manual that includes genuine attempts to solve problems associated with pregnancy and sexual dysfunction – something with which Ray, given that he had his own period of impotence after his marriage in 1673, should have been able to identify.
When Venette retired from medical practice, he was evidently not very mobile and decided to study captive nightingales. Among the many things he noticed was their agitated behaviour in autumn and spring at exactly the time when wild nightingales were migrating. Perceptively, he correctly deduced that the birds’ frantic hopping was sublimated migration and, indeed, this behaviour later came to be known as ‘migratory restlessness’. However, because it was assumed to have been discovered by German bird-keepers in the 1700s, it was termed ‘Zugunruhe’, but in fact our French physician seems to have been the first to document it towards the end of the preceding century. Subsequently, many of those writing about cage birds, such as quail and the golden oriole, commented on their agitated behaviour at the time of migration. Venette himself was convinced that small birds migrated and that an internal clock controlled their seasonal restlessness. He also made some ingenious suggestions regarding the cues that birds use to find their way on migration.27