José M. Marcos

Effect of parentage and relatedness on the individual contribution to cooperative chick care in carrion crows Corvus corone corone

Carrion crows Corvus corone corone in northern Spain form complex cooperative groups that contain non-dispersing offspring and immigrants. Reproduction is often shared among group members, with polyandry prevalent over joint egg laying. However, due to incest avoidance or sexual immaturity, reproduction is potentially available only to a fraction of group members (“potential breeders”), while others do not breed (“non-breeders”). We combined molecular data with video-recorded observations at nests in order to investigate whether potential breeders and non-breeders adjust their individual effort in nestling feeding respectively to their level of parentage and the relatedness with the chicks. Overall, parents of at least one chick in the brood showed the highest feeding rates. Among potential breeders, genetic mothers and fathers fed chicks at significantly higher rates than individuals with no parentage, but they did not adjust their effort according to the proportion of offspring generated. Current direct fitness benefits are therefore important in determining a high provisioning effort, but crows may lack a mechanism to finely assess their share of parentage. Among non-breeders, males contributed more than females to chick feeding, but we found no significant correlation between feeding rate and relatedness to the nestling. We discuss how the latter result can be reconciled with the fact that kin selection has been shown to be important in shaping the crow cooperative society.

Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows.

Kin-based societies, where families represent the basic social unit, occur in a relatively small number of vertebrate species. In the majority of avian kin societies, families form when offspring prolong their association with the parents on the natal territory. Therefore, the key to understanding the evolution of families in birds is to understand natal philopatry (i.e. the tendency to remain on the natal territory). It has been shown that, within populations, the strength of the association between parents and offspring (i.e. family stability) increases when offspring dispersal is constrained by external environmental factors, but it is unclear whether and how family wealth influences juvenile dispersal decisions. Here, we show that young carrion crows (Corvus corone corone) from territories that were food-supplemented year-round were more philopatric and more likely to help at their familys nest than the unfed ones. The results suggest that offspring philopatry and helping behaviour are influenced by the quality of ‘home’ and that the availability of food resources positively affects the cohesion of the family.

COOPERATIVELY BREEDING GROUPS OF CARRION CROW(CORVUS CORONE CORONE) IN NORTHERN SPAIN

Abstract The Carrion Crow (Corvus corone) is almost invariably reported as a species breeding as unassisted pairs, but a population of Carrion Crows (Corvus c. corone) from northern Spain that we have been studying since 1995 regularly exhibits cooperative breeding. The Spanish population thus demonstrates that cooperative breeding can vary greatly across populations. Most of the breeding territories (73.3%) in Spain were held by cohesive groups, which consisted of up to nine birds (mode = 3 birds). The proportion of fledglings that delayed dispersal for one year varied between 12.2 and 47.5% for different cohorts. The corresponding values for juveniles postponing dispersal for two years were 4.9 and 19.2%. Philopatry was skewed toward males. Some social groups contained immigrants. Therefore, delayed juvenile dispersal was not the only route towards sociality. Up to three helpers provided food to the nestling and at least one helper was found in all the groups surveyed. However, some group members refrained from visiting nests and thus the contribution to nestling care was highly variable among individuals.

Cooperative breeding in carrion crows reduces the rate of brood parasitism by great spotted cuckoos

Interactions between brood parasites and hosts can lead to coevolutionary arms races, whereby hosts evolve defences such as ejection of alien eggs and nest defence, and parasites respond with mimetic eggs and shorter laying times. However, little is known about interactions between brood parasites and cooperatively breeding hosts. The presence of several caregivers may either benefit the brood parasite by increasing reproductive success or be a disadvantage, if helpers improve nest defence. We addressed these hypotheses in cooperative carrion crows, Corvus corone corone, and their brood parasite, the great spotted cuckoo, Clamator glandarius, whose chicks are raised together. Parasitism rate by great spotted cuckoos was inversely correlated with crow group size and unassisted pairs were most likely be parasitized, in spite of being relatively rare. Moreover, in the nests of unassisted pairs, cuckoo chicks enjoyed a greater age advantage with respect to crow chicks compared to nests of larger groups, suggesting that parasitic females could not optimize laying date in nests with helpers. Although multiple caregivers increased cuckoo chick survival, this merely compensated for the smaller age advantage that parasitic chicks enjoyed in nests with helpers compared to those of unassisted pairs. Our results indicate that the presence of helpers reduces the cuckoos laying performance, providing the first indication that cooperative breeding may protect against brood parasitism. This might occur in crows because the presence of helpers allowed incubating females to increase the time spent at the nest, reducing the parasites opportunities to lay eggs.

Reproductive success increases with group size in cooperative carrion crows, Corvus corone corone

The effect of group size and the number of helpers on reproductive success is crucial to understand the evolution and maintenance of cooperative breeding. In northern Spain, carrion crows form kin-groups (three to nine individuals) where up to five individuals contribute to rearing the young. Using data from 99 different territories, followed over 10 years, we showed that group size was positively correlated with the annual number of fledglings produced, after controlling for the potential confounding effect of territory quality. This occurred through: (1) an increased probability for larger groups of renesting after early nest failure; (2) a higher probability of nest success; and (3) a higher number of fledglings produced in successful attempts. Video-recorded observations at the nests showed that chicks received more food in larger groups during the first 10 days of life, when the risk of starvation is highest, suggesting a role of allofeeding by additional carers in augmenting the reproductive success of a group. In crows, indirect and direct benefits through increased production of young are therefore available to nonbreeding group members.

From Parasitism to Mutualism: Unexpected Interactions Between a Cuckoo and Its Host

Predation Favors Parasitism Parasitism in birds often results in ejection or starvation of the hosts nestlings. Consequently, many host bird species have evolved protective behavior such as mobbing and parasite egg rejection. Curiously, some host species show no parasite avoidance behaviors; for example, the crow Corvus corone corone tolerates cuckoo chicks among its own brood. In a long-term study, Canestrari et al. (p. 1350) found that crow nests containing a cuckoo chick had lower rates of predation because the parasites chicks secrete a noxious repellent substance. Overall, in years of high predation pressure, the presence of cuckoos improves the crows breeding success, but when there are fewer predators around, parasitism reduces crow fitness. The carrion crow Corvus corone corone can benefit from parasitism by the great spotted cuckoo Clamator glandarius. Avian brood parasites lay eggs in the nests of other birds, which raise the unrelated chicks and typically suffer partial or complete loss of their own brood. However, carrion crows Corvus corone corone can benefit from parasitism by the great spotted cuckoo Clamator glandarius. Parasitized nests have lower rates of predation-induced failure due to production of a repellent secretion by cuckoo chicks, but among nests that are successful, those with cuckoo chicks fledge fewer crows. The outcome of these counterbalancing effects fluctuates between parasitism and mutualism each season, depending on the intensity of predation pressure.

History, environment and social behaviour: experimentally induced cooperative breeding in the carrion crow

Kin–based cooperative breeding, where grown offspring delay natal dispersal and help their parents to rear new young, has a long history in some avian lineages. Family formation and helping behaviour in extant populations may therefore simply represent the retention of ancestral features, tolerated under current conditions, rather than a current adaptive process driven by environmental factors. Separating these two possibilities challenges evolutionary biologists because of the tight coupling that normally exists between phylogeny and the environmental distribution of species and populations. The carrion crow Corvus corone corone, which exhibits extreme interpopulational variation in the extent of cooperative breeding, with populations showing no delayed dispersal and helping at all, provides a unique opportunity for an experimental approach. Here we show that offspring of non–cooperative carrion crows from Switzerland will remain on the natal territory and express helping behaviour when raised in a cooperative population in Spain. When we transferred carrion crow eggs from Switzerland to Spain, five out of six transplanted juveniles delayed dispersal, and two of those became helpers in the following breeding season. Our results provide compelling experimental evidence of the causal relationship between current environmental conditions and expression of cooperative behaviour.

Costs of chick provisioning in cooperatively breeding crows : an experimental study

The costs of providing care to offspring and how these costs influence individual allocation of resources to current and future reproduction are likely to be important in the evolution of cooperative breeding. We reduced the costs of offspring care experimentally in 12 groups of cooperatively breeding carrion crows, Corvus corone corone, by providing supplementary food throughout the breeding season. Neither nonbreeders nor breeders from supplemented territories significantly increased their levels of provisioning effort. However, unfed crows lost more weight than fed crows and, in contrast to fed crows, lost weight in relation to provisioning effort. Furthermore, breeders decreased their provisioning rates in groups with more than three caregivers, supporting both the idea that provisioning chicks is costly and the conclusion that crows invest in self-maintenance rather than in the current brood when costs are reduced.

Helpers at the nest compensate for reduced maternal investment in egg size in carrion crows

Life history theory predicts that mothers should trade off current and future reproductive attempts to maximize lifetime fitness. When breeding conditions are favourable, mothers may either increase investment in the eggs to improve the quality of the offspring or save resources for future reproduction as the good raising environment is likely to compensate for a ‘bad start’. In cooperatively breeding birds, the presence of helpers improves breeding conditions so that mothers may vary the number, size and quality of the eggs in response to the composition of the group. Here, we show that in cooperatively breeding carrion crows Corvus corone corone, where nonbreeding males are more philopatric and more helpful at the nest than females, breeding females decreased egg size as the number of subordinate males in the group increased. However, despite the smaller investment in egg size, fledglings’ weight increased in groups with more male subordinates, improving post‐fledging survival and indicating that helpers fully compensated for the initial ‘bad start’. These results highlight a ‘hidden effect’ of helpers that bears profound implications for understanding the ultimate function of helping.

Helpers but not breeders adjust provisioning effort to year-round territory resource availability in carrion crows

In most cooperatively breeding bird species, individuals live year round in all-purpose territories that may vary greatly in quality. Territory resource availability is likely to influence the investment in provisioning the brood, and different group members may respond in different ways, according to individual strategies of investment in self-maintenance or current reproduction. Although this may be important for understanding division of labour within the group, few studies have investigated how individuals respond to changing conditions ‘at home’. In cooperatively breeding carrion crows, Corvus corone, chick provisioning is costly and both breeders and helpers allocate additional resources to self-maintenance, rather than the current brood, when food availability is temporarily augmented during the breeding season. However, here we show that helpers, but not breeders, increased their chick-feeding rate when territory resources were experimentally enhanced throughout the year. These results indicate a role of year-round territory quality in shaping cooperation at the nest in this species. We suggest that the probabilities of reproducing in the following breeding season, which are higher for breeders than for helpers, modulate the effect of long-term resource abundance on individual provisioning decisions, leading to a higher investment in the current brood by helpers only.