Begging behavior and food acquisition by brown-headed cowbird nestlings

Understanding the selective forces that limit the exaggeration of begging signals is a critical issue in understanding the evolution of begging behavior. I studied the begging behavior of nestlings of the brown-headed cowbird (Molothrus ater), a brood parasite. In the nests of indigo buntings (Passerina cyanea), brown-headed cowbird nestlings received approximately twice as much food per hour than their host nestmates. I tested three hypotheses for the mechanism by which cowbirds acquired more food than their bunting nestmates: the size advantage hypothesis, the signal exaggeration hypothesis, and the novel begging behavior hypothesis. I found support for the hypotheses that cowbirds acquire more food as a result of their larger body size, and due to the exaggeration of begging signals that are not dependent on body size. I did not find support for the role of novel begging behaviors in cowbird food acquisition. These results suggest that food acquisition by host chicks in unparasitized nests could be increased by the exaggeration of begging signals. Recent work suggests that such exaggeration may be limited by the risk of nest predation, but further studies are needed. Received: 12 December 1997 / Accepted after revision: 29 December 1997     

Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds

Field observations and model-presentation experiments have shown that yellow warblers (Dendroica petechia) produce seet calls preferentially in response to brood-parasitic brown-headed cowbirds (Molothrus ater). In this study, we investigated whether seet calls are functionally referential alarm calls denoting cowbirds by determining whether female warblers responded appropriately to seet calls in the absence of a cowbird, whether alarm calling by warblers varied with response urgency, and how warblers in a population allopatric with cowbirds responded to cowbird and avian predator models and seet playbacks. As a control, we presented chip calls, which are elicited by nest predators as well as by non-threatening intruders, but are not strongly associated with cowbirds. Yellow warblers responded differently to playbacks of seet than chip calls. To seet playbacks, almost 60% of females gave seet calls and rushed to sit in their nests, responses typically elicited by cowbirds, whereas these responses were given infrequently in response to chip calls. Yellow warblers seet called equally in situations that simulated low, medium and high risk of parasitism, which suggests that these calls did not vary with response urgency. In a population allopatric with cowbirds, seet calls were rarely produced in response to cowbird or avian nest predator models and never to seet playbacks. These results suggest that seet calls are functionally referential signals denoting cowbirds and that cowbird parasitism was a strong selective pressure in the evolution of functional referentiality in the seet call of yellow warblers.Communicated by W.A. Searcy     

Differential allocation of reproductive effort to territorial establishment and maintenance by male yellow warblers (Dendroica petechia)

Summary We tested the hypothesis that the basis of the variation in reproductive strategy among male yellow warblers (Dendroica petechia) is a tradeoff in the allocation of reproductive effort to intrasexual competition (territorial effort) and to parental care (parental effort). Since a negative correlation between level of parental effort and amount of brown streaking on the breast (plumage score) has already been demonstrated in this species, this study looked for evidence of a positive correlation of territorial effort with plumage score and a negative correlation with parental effort. Analysis of the spatial and temporal use of territories, prior to egg-laying, by males with different plumage scores supported the prediction that brighter (higher plumage score) males allocate more effort to territorial establishment and maintenance (Fig. 1). Male plumage score was positively and highly significantly correlated with six different measures of the relative amount of time spent, rate of energy expended, and risk of injury assumed by each male during territorial activities. The level of territorial effort was also found to be negatively correlated with the level of parental effort expended by the same males later in the season, confirming that there is a tradeoff in allocation of reproductive effort to these two major components. Further analysis revealed that territory quality was positively correlated with male plumage score (Figs. 3 and 4), while average nestling growth rate and other indices of reproductive success were not (Fig. 6). These results suggest that increased territorial effort by brighter males enables them to occupy higher quality territories where high levels of parental effort are not necessary to maintain high levels of reproductive success. Since reproductive success was not correlated with plumage score, this study further supports the differential allocation hypothesis that different males are using alternative strategies for the allocation of reproductive effort.     

Red-winged blackbird parental investment following brood parasitism by brown-headed cowbirds: is parentage important?

Parental investment by red-winged blackbirds (Agelaius phoeniceus) in response to natural and experi‐mental parasitism by brown-headed cowbirds (Molothrus ater), and in response to freeze-dried, female cowbird mounts presented near redwing nests during the egg-laying period was measured. Two measures of redwing parental investment were used: nest defense effort toward a model predator, and rate of feeding nestlings. There were no significant differences in levels of parental investment among unparasitized nests, naturally parasitized nests, or experimentally parasitized nests. Similarly, parental investment did not differ between redwings that were exposed to the cowbird mount and those that were not exposed to the mount, or among redwings exposed to the cowbird mount at different distances from the nest. This suggests that red-winged blackbirds do not recognize when they have been parasitized, and hence do not associate parasitism with a decrease in their parentage, or that parentage is not an important predictor of parental investment in this species. Received: 24 January 1997 / Accepted after revision: 7 June 1997     

Costs of brood parasitism and the lack of defenses on the yellow-winged blackbird - shiny cowbird system

The shiny cowbird (Molothrus bonariensis) is a generalist brood parasite that lays either white-immaculate or spotted egg morphs in eastern Argentina and Uruguay. Some hosts accept both morphs, others accept spotted eggs and reject the white morph, but no host has been found to accept white eggs and reject spotted ones. It has been suggested that the yellow-winged blackbird (Agelaius thilius) may be that type of host. The finding of a white acceptor-spotted rejector species would help to explain the occurrence and maintenance of the parasite egg polymorphism. We studied the incidence of shiny cowbird parasitism on this host, its costs for their reproductive success and the presence of antiparasitic defenses in the yellow-winged blackbird - shiny cowbird system. The parasite affected the reproductive success of the host in two ways. Cowbirds punctured host eggs causing a reduction in clutch size, and yellow-winged blackbirds deserted their nests whenever they suffered high egg loss. In addition, parasitized nests suffered higher predation during the nestling stage, but not during egg stages, indicating that the difference found was related to the presence of the cowbird chick, and not to higher exposure of parasitized nests to both parasites␣and predators. Despite the costs imposed by the parasite, yellow-winged blackbirds have not evolved antiparasitic defenses. This host did not reject any egg morph of the shiny cowbird nor desert parasitized nests unless it had suffered high egg loss. Current explanations for the host lack of defenses, the “time lag” and the “equilibrium” hypothesis, are discussed. Received: 29 August 1997 / Accepted after revision: 10 January 1998     

Food abundance and parental care in yellow warblers (Dendroica petechia)

Emlen and Oring (1977) suggested that monogamy in birds is maintained because of the need for strict biparental care. A corollary of their suggestion is that paternal care should decrease under conditions of high food abundance. An alternative is that paternal care would increase if males take advantage of the higher food abundance by trying to reduce the length of the nestling feeding period. We tested these two ideas using yellow warblers (Dendroica petechia) by providing some pairs with supplemental food, thereby reducing the importance of biparental care. However, the extra food did not decrease paternal effort, nor did it increase it (Fig. 2). Early in the nestling period experimental females brooded more but visited their nestlings less than did control females, but later, when brooding times decreased, experimental females fed their nestlings more than did control females (Fig. 3). There were no significant differences in nestling survival (Fig. 5), but nestlings in the control treatment were larger and heavier up to 6 days old (Fig. 6). The main effect of supplemental food was on maternal, not paternal behaviour. Models of biparental care assume interdependence between the parental effort of both parents. In this species, however, males and females provide for their brood independently from each other.     

Sexual selection and variation in reproductive strategy in male yellow warblers (Dendroica petechia)

Summary Male yellow warblers (Dendroica petechia) exhibit extensive variation in the amount and conspicuousness of the sexually distinctive brown streaking on the breast. We investigated this intraspecific variation in degree of sexual dichromatism to see if male plumage rank (essentially the amount of brown streaking) is correlated with the amount of reproductive effort allocated to parental investment, as sexual selection theory would predict. As predicted, the average rate of feeding visits to the nest by males was negatively correlated with the plumage rank of the male in 1982 (Fig. 1) and 1983 (Fig. 2), and varied little between years or among study areas. Within one study area, the higher nest visit rate of dull (low plumage rank) males was correlated with higher nestling growth rates. But in the other two study areas, where bright (high plumage rank) males predominated, nestlings of bright males tended to have the highest growth rates despite minimal nest visit rates. Thus, overall there was no correlation between male plumage rank and nestling growth rate, a potential index of relative reproductive success, in either year (Figs. 3 and 4). This overall equal nest success likely helps to maintain the behavioral and plumage polymorphism. Since we could find no evidence that the high nestling growth rates of bright males were due to an adjustment of female parental effort to compensate for low male parental effort, there must be some other benefit of being bright which contributes to nest success. To address this, we used the relationship between parental feeding rates and nestling growth rates for each nest as an index of relative territory quality. This analysis suggests that bright males generally occupy the best territories available, possibly because they are more aggressive in obtaining and defending them than dull males. Dull males appear to be relegated to poorer territories, where an increase in male parental contribution would be necessary to achieve high nestling growth rates. We propose that different males are using alternative but evolutionarily stable reproductive strategies, in a way that is consistent with the predictions of sexual selection theory. Allocation of limited reproductive effort to parental investment decreases as sexual dichromatism increases, which probably reflects an increased investment in intermale competition for the best territories.     

Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs

Brood parasitism is costly to hosts, and, therefore, a number of anti-parasite defenses have evolved. Surprisingly, several high-quality hosts such as martins and swallows are rarely parasitized, raising the question why that is the case. We hypothesize that martins and swallows may avoid parasitism by breeding in close association with humans, and by building nests that are inaccessible for common cuckoos Cuculus canorus and other brood parasites. Here we show using egg rejection experiments that red-rumped swallows Hirundo daurica, house martins Delichon urbica, and barn swallows Hirundo rustica in Europe do not reject foreign eggs placed in their nests, while barn swallows in China often reject foreign eggs. The frequency of parasitism of barn swallows in Europe was significantly higher than in house martins relative to the expectation based on the abundance of the two species. Barn swallows in Europe that were parasitized by cuckoos more often placed their nests outdoors than expected by chance, suggesting that avoidance of cuckoo parasitism can be achieved by breeding indoors. These findings suggest that barn swallows in China have gained egg rejection behavior because they cannot avoid parasitism when breeding outdoors.     

An experimental investigation of the bioacoustics of cowbird song

Summary Female cowbirds (Molothrus ater ater), maintained in isolation from males during the breeding season, respond to the playback of male song with copulatory postures. They respond to some songs more than to others. Cowbird song potency can thus be operationally defined by the proportion of copulatory postures a song elicits across multiple playbacks. The purpose of the present study was to explore whether song potency changes with distance in the field. No field recordings elicited high levels of responding by the females. When songs of known high potency are systematically degraded, the results indicate that female cowbirds are sensitive to small changes in signal to noise ratio and to atmospheric attenuation. The data suggest that cowbird song potency degrades very rapidly with transmission distance in the field.     

Response of American redstarts (suborder Passeri) and least flycatchers (suborder Tyranni) to heterospecific playback: the role of song in aggressive interactions and interference competition

Least flycatchers (Empidonax minimus) and American redstarts (Setophaga ruticilla) overlap in the use of food resources on their breeding grounds, promoting high levels of interspecific aggression by the socially dominant flycatcher. We examined the role of song in this interspecific aggression by using repeated-measures-designed playback experiments and observational data on induced aggressive interactions. Flycatchers were more likely to approach the speaker during presentation of redstart song than during intervals of no song or presentation of control song. Approach was close enough to enable visual contact with a singing redstart. In contrast, redstarts made significantly fewer flights following presentation of flycatcher song, when risk of flycatcher attack may be greatest. Reducing the number of flights likely reduces the risk of flycatcher attack on the redstart, as flycatchers do not attack stationary redstart models and are apparently dependent on cues from redstart flight for visual heterospecific recognition. Flycatcher-specific responses of redstarts and marked differences in song morphology rule out misdirected intraspecific aggression as a proximate or ultimate cause of interspecific response to song. Results indicate that song is an important component in aggressive interactions between these two species, and reflect the dominant role of the flycatcher in such interactions. Our results also illustrate the capacity for interspecific interference competition to influence behavior and heterospecific song recognition in two distant avian taxa. Received: 10 January 1995/Accepted after revision: 8 June 1996     

Singing and the establishment and maintenance of dominance hierarchies in captive brown-headed cowbirds

Summary The importance of singing in the establishment and maintenance of dominance rank was investigated in captive flocks of brown-headed cowbirds (Molothrus ater). Each flock consisted of 3 males and 1 female. In one experiment the two largest males in each of 4 flocks were temporarily devocalized by puncturing the interclavicular air sac just before group formation. The third male in each group was sham-operated. There was a significant tendency for the non-devocalized birds to become the dominant member of their group. Only sham-operated males sang immediately after the operation. In a second experiment, dominant males from flocks with established hierarchies were temporarily devocalized. None of these males lost their dominant positions, despite their inability to sing. These results suggest that song is important in the establishment of dominance rank; however, once established, social hierarchies may be maintained by non-vocal means, such as social inertia or individual recognition.     

Identification of sex and parasitism via pheromones by the Ozark zigzag salamander

Chemical communication appears to be the primary mode of information transfer among woodland salamanders of the genus Plethodon. These pheromones have been shown to convey a wide variety of information, and are used to establish territorial boundaries. Responses to pheromones can include changes in both behavior and energy consumption. The ability of Ozark zigzag salamanders, Plethodon angusticlavius, to detect the sex of a conspecific through chemical substrate markings has not been assessed. In addition, some populations of P. angusticlavius are naturally infected with the ectoparasitic mite Hannemania eltoni. Parasitism can impact both the behavior and metabolism of the host as well as the behavior of others towards the parasitized individual. We examined whether sex and parasitism of the pheromone donor and receiver influenced behavioral and metabolic responses in P. angusticlavius. In laboratory trials, behavior of P. angusticlavius was influenced by the sex and parasite load of the pheromone donors and receivers. Behavioral responses were also influenced by whether the receiver was in its own territory or in the territory of the pheromone donor. Metabolic responses were not affected by the sex or parasite load of the pheromone donor, but males had higher metabolic rates than females, even after adjusting for differences in body size. Overall, our study indicates that both sex and parasitism can be detected via pheromones in this species, and the nature of the response depends on residency status, sex, and parasite load of the receiver.     

Adaptations of meadow pipits to parasitism by the common cuckoo

Summary The meadow pipit Anthus pratensis is one of the most frequent hosts in Europe parasitized by the common cuckoo Cuculus canorus. The cuckoo normally removes one or more of the host eggs and replaces them with one of its own. The aim of the present study, which was conducted in an upland area of Central Norway, was to test the following question: assuming the cuckoo has laid a mimetic egg (which is slightly larger than and slightly different in color from that of a meadow pipit egg), under what circumstances are the parent meadow pipits able to detect such parasitism? The reaction of the meadow pipits to artificial parasitism was tested. Plastic model cuckoo eggs were used that bore a striking resemblance to real cuckoo eggs found in other meadow pipit nests in the same area. In addition, in some experiments a stuffed cuckoo dummy was used. The meadow pipits tolerated the experimental procedures and remained in their nests when given an artificial cuckoo egg, with or without removal of one of the host's eggs. However, when a host egg was removed and replaced with an artificial cuckoo egg, and at the same time a stuffed cuckoo dummy was presente, 50% of the birds deserted their nests. The difference between this result and the results of the other experiments was statistically significant. When only the stuffed cuckoo was presented, without any egg manipulations, the meadow pipits reacted in the same way as in the egg experiments. We conclude that the meadow pipit is capable of detecting whether or not its nest has been parasitized, provided it has observed the cuckoo near the nest site. Furthermore, because of the results of our experiments, we reject the hypothesis that the cuckoo has evolved egg removal behavior in order to prevent the host from assessing an increase in egg numbers.     

Low frequency of extra-pair paternity in pied flycatchers revealed by DNA fingerprinting

Summary Genetic parentage of 135 nestlings from 27 broods of polygynous and monogamous pied flycatchers Ficedula hypoleuca was analyzed by means of multilocus DNA fingerprinting. The minisatellite probe alpha-globin 3HVR detected approximately 12 scorable bands per fingerprint, and the proportion of bands shared between presumably unrelated adults averaged 0.22+0.08 SD. The fingerprints of 125 of the 135 nestlings made a complete match to those of their putative parents. In 4 nestlings a single mismatched band occurred, but since band sharing with both putative parents was high, the single mismatches were assumed to be caused by mutation. The 6 remaining nestlings had 5 or more mismatched bands each, low band-sharing proportions with their putative father and high band-sharing proportions with their putative mother. We thus conclude that they were all sired through extra-pair copulations (EPCs). Hence, only 4% of nestlings were sired through EPCs, and none resulted from intraspecific brood parasitism. One of the cuckolding males was identified, explaining all 5 mismatched bands in the nestling's fingerprint. Three of the illegitimate nestlings were from primary nests of polygynous males; 3 were from nests of monogamous males. The fact that many males in this study started to advertise for a second female in a distant territory several days before their first mate began egglaying, and still managed to secure almost exclusive paternity in their first brood, suggests that male polyterritoriality is not costly in terms of lost paternity. Common anti-cuckoddry tactics performed by male birds, like high rate of within-pair copulation and continuous mate-guarding thoughout the female's fertilizable period, do not seem to be important in pied flycatchers.Offprint requests to: J.T. Lifjeld     

Territory choice during the breeding tenure of male sedge warblers

A territorial male can shift the location of its territory from year to year in order to increase its quality. The male can base its decision on environmental cues or else on its breeding experiences (when territory shift is caused by breeding failure in previous seasons). We tested these possible mechanisms of territory choice in the sedge warbler (Acrocephalus schoenobaenus), a territorial migrating passerine that occupies wetlands. This species bases its territory choices on an environmental cue: tall wetland vegetation cover. We found that the magnitude of territory quality improvement between seasons (measured as the area of tall wetland vegetation) increased throughout the early stages of a male's breeding career as a result of territory shifts dependent on the earliness of arrival. The distance the territory was shifted between seasons depended negatively on the previous year's territory quality and, less clearly, on the previous year's mating success. On the other hand, previous mating or nesting success had no influence on territory quality improvement between seasons as measured in terms of vegetation. The results imply that tall wetland vegetation is a long-term, effective environmental cue and that a preference for territories in which this type of landcover prevails has evolved into a rigid behavioral mechanism, supplemented by short-term individual experiences of breeding failure.     

High frequency of extra-pair paternity in Swedish pied flycatchers revealed by allozyme electrophoresis and DNA fingerprinting

Summary We used two genetic techniques to study multiple parentage in the pied flycatcher (Ficedula hypoleuca). Allozyme electrophoresis of 131 nestlings from 22 clutches sampled in 1982 and 1987 showed that one nestling had a mismatched allele compared with its putative parents. In one additional nest the devitation from Mendelian inheritance of parental genotypes suggested extra-pair paternity. The calculated probability of detecting multiple paternity from the genetic variation at four loci was 0.115. The estimated population frequency of extra-pair fertilization (EPF) was 13%, based on two mismatches and the probability of detecting multiple paternity. The seven families (n = 38 nestlings) in the 1987 sample were also analyzed by DNA fingerprinting using the M13 and Jeffrey's 33.15 probes. Overall, 24% (n = 9) of the nestlings analyzed were genetically inconsistent with their putative father, with EPF occurring in three (43%) of the seven clutches. One nestling originated by intraspecific brood parasitism. Comparison of the two techniques using the same samples showed that allozyme electrophoresis has a resolution only 11% of that of DNA fingerprinting, close to the calculated probability of detecting multiple paternity (0.115). Both techniques suggest that extra-pair fertilization is relatively common in the Swedish populations investigated compared to the low frequency reported from a Norwegian population. Correspondence to: H.P. Gelter at the present address     

Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting

Parasitic female moorhens (Gallinula chloropus) lay from one to six eggs in the nests of conspecific neighbours. DNA fingerprinting was used to show that parasitic eggs could be correctly identified when they appeared in addition to or outside the host’s laying sequence. Moorhen hosts accept all parasitic eggs laid after the 2nd day of their laying period. To understand why moorhen hosts tolerate parasitic eggs, we tested two hypotheses. (1) The quasi-parasitism hypothesis: females lay their eggs in the evening when the host males are normally in attendance at the nest, so host males may allow parasitic females to lay in their nests in exchange for fertilizing their eggs. However, DNA fingerprinting showed that all the parasitic eggs were sired by the parasites’ mates. Parasitic moorhens frequently continue laying a clutch in their own nest, without a break in the laying sequence after a parasitic laying bout. The eggs laid by brood parasites in their own nests were also sired by their own mates. Therefore this hypothesis was rejected. (2) The kin selection hypothesis: if one or both members of the host pair are close relatives of the parasite, the costs of rearing parasitic chicks will be to some degree offset by inclusive fitness benefits. We examined the genetic relationships between parasites and their hosts using DNA fingerprinting and genealogical data. Natal philopatry by both sexes was relatively common in this population, and the probability that a neighbour of either sex was a first-order relative (parent-offspring) was calculated as 0.18. Although first-order relatives were not preferentially chosen as hosts over individuals that were not first-order relatives, even through random host selection there is almost a one-in-five chance that brood parasites in this population are closely related to their hosts. This may facilitate host tolerance of parasitic eggs. Other hypotheses are also discussed. Received: 3 February 1995/Accepted after revision: 27 August 1995     

Reproductive success of monogamous and polygynous pied flycatchers (Ficedula hypoleuca)

One of the most interesting aspects of the mating system of pied flycatchers is the regular occurrence of polygyny. Here we present data on the reproductive success of polygynously paired pied flycatcher males compared to monogamous males based on paternity analyses through DNA fingerprinting. Males paired with two females suffered a higher loss in reproductive output per female compared to monogamous males due to (1) a greater proportion of unhatched eggs in their broods, (2) greater nestling mortality and (3) a greater probability of being cuckolded. Nevertheless, the number of fledglings was significantly greater for polygynous males. Based on the number of nestlings that returned for subsequent breeding seasons, however, the reproductive success of monogamous and polygynous males did not differ significantly. These data raise the question as to why males attempt polygyny. Received: 16 August 1999 / Received in revised form: 15 March 2000 / Accepted: 18 March 2000     

Female siskins choose mates by the size of the yellow wing stripe

Commonly, female birds use the brightly coloured patches on males to choose the best-quality mates. Coloured wing patches, however, have received little attention or have been previously related to social behaviour (as a signal to recruit conspecific individuals at feeding patches) or foraging (to flush prey) contexts, rather than to sexual selection. Here we provide evidence that in siskins (Carduelis spinus), wing patches function in mate choice. Mate-choice experiments showed that females were attracted by the size of the yellow wing stripe of the male, but not by the size of its black bib, body size, general plumage brightness or age. Experiments on birds with manipulated yellow wing stripes showed that females were sensitive to the size of this colour patch, irrespective of other male qualities. The preference of female siskins for males with larger wing patches when searching for a mate may be explained by the relationship of this trait to foraging ability, which would ensure females good parental investment from the chosen male.Communicated by W.A. Searcy