Equivocal Responses of Feeding Parents to Experimental Brood Sizes in a Hawk–Cuckoo Host: Brood Size as a Reference for Parental Provisioning Decisions?

The number of offspring surviving until independence is the fundamental drive in the evolution of parental care. Because of the related costs, parental investment must be balanced with essential resources for parents themselves, among the resources available in the environment under the current parental condition. It is advantageous for parents to adjust their level of investment to the number of offspring; however, there is little evidence that parents employ numerical competence in adjusting their investment level. We investigated how parents respond to experimentally manipulated brood sizes in a passerine species, known as a host of a brood parasitic cuckoo whose chicks presumably deceive their hosts numerically. Parents reduced their provisioning to broods of reduced sizes, whereas parents did not increase provisioning to enlarged broods compared to that in the control condition. These parental responses can be attributed to the response of chicks to the experimental treatments compared to that in the control: chicks lowered begging intensity in the reduced condition, while they did not intensify being in the enlarged condition. Further analyses revealed that eagerness of parents to respond to chick begging intensity differed between the experimental treatments: strong parental response was detected toward begging chicks only in the reduced condition. We propose that the detected equivocality of parental responses might be related to the difference in the number of chicks between the unmanipulated and experimentally manipulated broods, the former reflecting the initial parental decision on the amount of resources to allocate to the brood.     

The adaptive value of parental responsiveness to nestling begging

Despite extensive theoretical and empirical research into offspring food solicitation behaviour as a model for parent-offspring conflict and communication, the adaptive value of parental responsiveness to begging has never been tested experimentally. Game theory models, as well as empirical studies, suggest that begging conveys information on offspring state, which implies that parental investment can be better translated to fitness by responding to begging when allocating resources rather than by ignoring it. However, this assumption and its underlying mechanisms have received little or no attention. Here we show by experiments with hand-raised house sparrow (Passer domesticus) nestlings that a 'responsive parent' will do better than a hypothetical 'non-responsive' mutant (that provides similar food amounts, but irrespective of begging). This is neither because food-deprived nestlings convert food to mass more efficiently, however, nor because responsiveness reduces costly begging. Rather, responsiveness to begging is adaptive because it reduces two opposing risks: one is wasting time when returning too soon to feed already satiated nestlings and the other is repeatedly overlooking some nestlings as a result of the stochastic nature of a random, non-responsive strategy. This study provides the first experimental evidence for the adaptive value of parental responsiveness to offspring begging.     

An offspring signal of quality affects the timing of future parental reproduction

Solicitation signals by offspring are well known to influence parental behaviour, and it is commonly assumed that this behavioural effect translates into an effect on residual reproduction of parents. However, this equivalence assumption concerning behavioural and reproductive effects caused by offspring signals remains largely untested. Here, we tested the effect of a chemical offspring signal of quality on the relative timing and amount of future reproduction in the European earwig (Forficula auricularia). We manipulated the nutritional condition of earwig nymphs and exposed females to their extract, or to solvent as a control. There were no significant main effects of exposure treatment on 2nd clutch production, but exposure to extracts of well-fed nymphs induced predictable timing of the 2nd relative to the 1st clutch. This result demonstrates for the first time that an offspring signal per se, in the absence of any maternal behaviour, affects maternal reproductive timing, possibly through an effect on maternal reproductive physiology.     

Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent-offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent-offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent-offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent-offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.     

Parents and offspring in an evolutionary game: the effect of supply on demand when costs of care vary

Current models of parent-offspring communication do not explicitly predict the effect of parental food supply on offspring demand (ESD). However, existing theory is frequently interpreted as predicting a negative ESD, such that offspring beg less when parental supply is high. While empirical evidence largely supports this interpretation, several studies have identified the opposite case, with well-fed offspring begging more than those in poorer condition. Here, we show that signalling theory can give rise to either a negative or a positive ESD depending on the precise form of costs and benefits. Introducing variation among parents in the cost of care, we show that the ESD may change sign depending upon the quantitative relation between two effects: (i) decreased supply leads to increased begging because of an increase in marginal fitness benefit of additional resources to offspring, (ii) decreased supply leads to reduced begging because it is associated with a decrease in parental responsiveness, rendering begging less effective. To illustrate the interplay between these two effects, we show that Godfray's seminal model of begging yields a negative ESD when care is generally cheap, because the impact of supply on the marginal benefits of additional resources then outweighs the associated changes in parental responsiveness to begging. By contrast, the same model predicts a positive ESD when care is generally costly, because the impact of care costs on parental responsiveness then outweighs the change in marginal benefits.     

Families on the spot: sexual signals influence parent–offspring interactions

In 1950, Tinbergen described the elicitation of offspring begging by the red spot on the bill of parent gulls, and this became a model system for behavioural studies. Current knowledge on colour traits suggests they can act as sexual signals revealing individual quality. However, sexual signals have never been studied simultaneously in relationship to parent–offspring and sexual conflicts. We manipulated the red-spot size in one member of yellow-legged gull pairs and observed their partners'' feeding efforts in relationship to offspring begging. In the enlarged-spot group, partners doubled their effort compared with the other groups. Furthermore, in the reduced-spot group, partners provided food in relationship to offspring begging, contrasting with the fixed effort of the partners of enlarged-spot gulls. Manipulated gulls, independently of treatment, provided food in relationship to chicks begging only when the partner''s investment was low, and performed a fixed effort when the partner''s contribution was high. Results demonstrate that the red spot in yellow-legged gulls functions as a sexual signal and indicate that parental rules are plastic, depending on the information on offer. Previous evidence and this study indicate that this signal is used by all family members to adjust decision rules. The incorporation of sexual signals in parent–offspring interactions can be crucial in understanding intra-familial conflicts.     

Sex differences in provisioning rules: responses of Manx shearwaters to supplementary chick feeding

Sex differences in food provisioning have been found in a numberof socially monogamous birds with biparental care, but the reasonsremain unclear. In Manx shearwaters, males provide 40–50%more food for chicks than do females, and previous empiricaldata have suggested that this difference could arise becausefemales are able to regulate food delivery by reducing the provisioningof well-nourished chicks, whereas males are not (hypothesis1). Alternatively, however, males may be as capable as femalesof assessing and responding to the variation in the nutritionalrequirements of their chick but have a higher threshold forreducing food delivery to well-nourished chicks (hypothesis2). To test these two hypotheses, we used supplementary feedingto manipulate the nutritional status of chicks and then examinedthe responses of male and female parents and their offspring.Supplementary feeding significantly reduced both the beggingbehavior of chicks and the frequency and sizes of meals deliveredby parents. Males and females reduced their overall provisioningrates to a similar extent (males by 38%, females by 42%), somaintaining the same difference in contributions to provisioningin the control group (males 58%, females 42%) and the experimentaltreatment (males 59%, females 41%). These data strongly supporthypothesis 2. Supplementary feeding of chicks resulted in fewervisits by parents and a higher proportion of long trips in bothsexes (4 days for males, 5–7 days for females). However,maximum trip durations were unchanged, suggesting that supplementaryfeeding of chicks had no effect on the foraging ranges or overallfood-provisioning strategies of parents.     

Sex differences in responsiveness to begging in a cooperative mammal

In species where young are provisioned by both parents, males commonly contribute less to parental care than females, and are less responsive to variation in begging rates. Similar differences in the care of young occur among adults in cooperative breeders, but fewer studies have investigated whether these are associated with differences in responsiveness. Here, we present results from a playback experiment investigating responsiveness to begging in the meerkat (Suricata suricatta), a cooperatively breeding mammal. Although increased begging rate raised the feeding rate of adults of both sexes, there was no consistent tendency for females to be more responsive than males. However, when we examined changes in the proportion of food items found that were fed to pups (generosity), we found that females were more responsive than males to increased begging rate. These results can be explained in terms of sex differences in dispersal: in meerkats, females are philopatric and receive considerable benefits from investing in young, both directly, by increasing group size, and indirectly, by recruiting helpers if they inherit the breeding position. In addition, they emphasize that generosity provides a more sensitive measure of responsiveness to begging than feeding rate, as it accounts for variation in foraging success.     

Detectability matters: conspicuous nestling mouth colours make prey transfer easier for parents in a cavity nesting bird

An often underappreciated function of signals is to notify receivers of the presence and position of senders. The colours that ornament the mouthparts of nestling birds, for example, have been hypothesized to evolve via selective pressure generated by parents'' inability to efficiently detect and feed nestlings without such visually conspicuous targets. This proposed mechanism has primarily been evaluated with comparative studies and experimental tests for parental allocation bias, leaving untested the central assumption of this detectability hypothesis, that provisioning offspring is a visually challenging task for avian parents and conspicuous mouths help. To test this assumption, I manipulated the mouths of nestling house sparrows to appear minimally and maximally conspicuous, and quantified prey transfer difficulty as the total duration of a feeding event and the number of transfer attempts required. Prey transfer to inconspicuous nestlings was, as predicted, more difficult. While this suggests that detectability constraints could shape nestling mouth colour evolution, even minimally conspicuous nestlings were not prohibitively difficult for parents to feed, indicating that a more nuanced explanation for interspecific diversity in this trait is needed.     

Hurry-up and hatch: selective filial cannibalism of slower developing eggs

Filial cannibalism (the consumption of one's own offspring) is thought to represent an adaptive strategy in many animals. However, little is known about the details of which offspring are consumed when a parent cannibalizes. Here, we examined patterns of within-brood filial cannibalism in the sand goby (Pomatoschistus minutus). Males spawned sequentially with two females, and we asked whether males cannibalized selectively with regard to egg size or the order in which eggs were received. Males preferentially consumed the larger eggs of the second female they spawned with. Because larger eggs took longer to hatch, and because female 2's eggs were up to 1 day behind those of female 1, such preferential cannibalism might allow males to decrease the time spent caring for the current brood and re-enter the mating pool sooner. More work is needed to understand the fitness consequences of such selective cannibalism.     

Stability and value of male care for offspring: is it worth only half the trouble?

Models of parental investment often assume a trade-off for males between providing care and seeking additional mating opportunities. It is not obvious, however, how such additional matings should be accounted for in a consistent population model, because deserting males might increase their fertilization success at the cost of either caring males, other deserting males or both. Here, we present a game theory model that addresses all of these possibilities in a general way. In contrast to earlier work, we find that the source of deserting males' additional matings is irrelevant to the evolutionary stability of male care. We reject the claim that fitness gains through male care are intrinsically less valuable than those through desertion, and that the former must therefore be down-weighted by 1/2 when compared with the latter.