Cunning cuckoos
Cuckoos are notorious for duping other species into raising their offspring, but this may provide some foster families with surprising benefits, too.
Crows enjoy a surprising side-effect of having their nests intruded by great spotted cuckoos
It’s a sunny spring day in the Sobarriba, a plateau 950m above sea level in northern Spain, and a warm breeze is carrying a faint smell of wild thyme and lavender, which grow in the hedgerows and meadows of this low-intensity agricultural landscape. For nearly 10 minutes, we have been observing a great spotted cuckoo female perching on a branch of a tall poplar tree, just a couple of meters away from a carrion crow nest that we need to check for new eggs. The crow female is sitting on the nest, in an incubating posture, ignoring the cuckoo, though she must have seen it.
We have never witnessed an active defence by breeding crows against great spotted cuckoos – literature has never described it either – but we are nevertheless surprised by the absolute lack of reaction to such a conspicuous threat.
The cuckoo female will spend the spring laying up to 26 eggs in various nests.
Great spotted cuckoos, like the more famous common cuckoos, are brood parasites that lay their eggs in the nests of other species and then abandon their progeny to be cared for by the foster parents. Because host parents generally lose part or all of their brood due to the presence of a voracious cuckoo chick, they clearly benefit from evolving defensive strategies against these uninvited guests – attacking adult cuckoos that loiter nearby or ejecting alien eggs from their nests. But the persistent parasites have counter-evolved more and more sophisticated tricks – such as producing eggs that better resemble those of their target species – in a continuous ‘evolutionary arms race’ that has fascinated scientists for decades.
However, our crow female sits placidly on her nest while being closely observed by the great spotted cuckoo. When the crow finally flies away to forage, the cuckoo immediately seizes her chance. She flies to the unattended nest, sits in it for few seconds then makes a swift getaway. We run over and check the contents of the nest – three crow eggs and one, considerably smaller, cuckoo egg.
Making themselves at home
The cuckoo female will spend the rest of the spring laying up to 26 eggs, distributed among various nests – which is remarkable, compared to the ‘normal’ clutch of five or six eggs of the main host species. Then, in late June to early July, she (and all her conspecifics) will start the long journey towards Africa, where she will spend the winter, before returning in the spring.
The great spotted cuckoo’s main host is usually the magpie, but crow nests in our study area are heavily parasitised, too – up to 70 per cent in some years. While the young of common cuckoos will evict all other eggs and chicks from the nest shortly after hatching, great spotted cuckoo chicks don’t. Instead, they throw themselves into begging behaviour, to make sure they hold the attention of their foster parents at mealtimes. They also tend to hatch a few days earlier than their nest-mates, gaining an age advantage that makes them far more competitive in obtaining food. In fact, the majority of magpie chicks starve to death when forced to compete with these cuckoos.
It is therefore not surprising that magpie adults use a range of defensive strategies against these freeloaders. Crows, however, seem to completely lack such animosity. Though some crow chicks (larger than the parasite) can make it to fledgling, brood reduction due to the presence of the
parasite is common, and therefore some reaction towards the great spotted cuckoos should be expected.
The fact the crows are, generally, secondary hosts that suffer relatively low parasitism rates, and that the costs in terms of brood loss are not so dramatic, have been, so far, considered sufficient reasons to explain why defences have not yet evolved. However, an intriguing phenomenon, which may provide an alternative explanation for the peaceful convivence between host and parasite, came to light a few years ago…
Accidental hero
Examining the breeding performance of crow nests, monitored over 16 years, revealed that parasitised and non-parasitised nests produced, on average, the same number of crow chicks every year.
On the one hand, nests with cuckoos present were more likely than non-parasitised ones to fledge at least one crow chick, while non-parasitised nests suffered complete brood loss (usually attributed to depredation) at higher rates. On the other hand, however, nests that were successful produced significantly fewer crow chicks when they were parasitised, because, as expected, the cuckoo chick usually outcompeted some crow nest-mates for food.
Why on earth parasitised nests were more likely to be successful was a mystery that needed to be solved. A simple explanation could be that great spotted cuckoos were able to target the nests of high-quality crow parents that were more skilled in defending their nest against predators, so their young would be more likely to survive.
Unconvinced by this, we performed an authorised translocation experiment where we swapped cuckoo hatchlings from parasitised nests into non-parasitised ones. We then compared the reproductive success of these nests with a set of unmanipulated ones (half parasitised, half non-parasitised). We found that the nests where we had introduced cuckoo chicks were less likely to fail than the ones from which we removed the chicks – mirroring the patterns observed in the unmanipulated control nests. These results demonstrated that the presence of the cuckoo chick itself was causing the higher success of nests… but how?
As anyone who’s worked with great spotted cuckoos will know all too well, young chicks expel a conspicuous quantity of a dark, fetid, liquid secretion from the cloacal (a common cavity for faeces, urine and reproduction), as a self-defence strategy, as soon as they are manipulated. Could this substance repel predators, saving crow chicks from attack in the process?
We collected samples of the secretion and analysed their composition. They appeared to be a caustic mixture of acid, indoles, phenols and sulphur compounds already known to repel mammals and birds. We then performed an experiment where we presented bait (some treated with the cuckoo secretion, others untreated) to mammalian carnivores and raptors – they were clearly repelled by the substance, strongly avoiding the food that was spread with it, and therefore supporting the theory.
Altogether, these findings reveal an incredible scenario where the definition
In years of very low predator density, great spotted cuckoos are true parasites for crows.
of parasitism itself appears inadequate to describe the connection between the great spotted cuckoo and its crow hosts, which may have more of a mutually beneficial relationship than previously thought.
However, in years of very low predator density, great spotted cuckoos are true parasites for the crows – begging vigorously so as to outcompete their nest-mates, leading to considerable brood reduction and loss of reproductive success for crows. But in years when nest predators are abundant, and up to 70 per cent of crow nests can lose all their chicks, the presence of a cuckoo chick means nests are more likely to be spared and at least one crow chick is likely to fledge alongside the parasite.
The outcome of the relationship fluctuates between parasitism (when the parasite gains and the host pays a net cost) and mutualism (when both partners benefit), according to the environmental conditions. This may have prevented the evolution of defences against the brood parasite in this species.
Though great spotted cuckoos also parasite magpies, and other cuckoo species are known to expel an unpleasant substance when molested, a protective effect towards their host is unlikely to be general. In magpies, host chicks starve to death in their very first days of life, due to cuckoo chicks monopolising all provisioning effort of the parents. Common cuckoos, which also produce an anti-depredatory substance, actively kill all host nest-mates – ejecting them from the nest as soon as they hatch. The larger size of crow chicks, which allows them to better cope with the presence of a voracious cuckoo, also enables them to benefit indirectly from its self-defensive behaviour, a situation that is probably quite uncommon among all brood parasite-host relationships.