Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

Seasonal decline of offspring quality in the European starling Sturnus vulgaris: an immune challenge experiment

In seasonally fluctuating environments, timing of reproduction is a crucial determinant of fitness. Studies of birds show that late breeding attempts generally result in offspring of lower reproductive value, with lower recruitment and long-term survival prospects. Several proximate mechanisms, including a seasonal decline of immune system functioning, may lead to a seasonal decline of offspring fitness. We investigated seasonal variation in offspring quality by subjecting first- and second-brood chicks of a sexually size dimorphic species, the European starling Sturnus vulgaris, to an immune challenge with a bacterial endotoxin (LPS), and evaluated their growth and physiological response in terms of total plasma antioxidant capacity (TAC), concentration of reactive oxygen metabolites and hematocrit. LPS challenge did not affect chick growth or oxidative status. However, hematocrit of second-brood chicks was higher in LPS chicks compared to controls. Body mass halfway through the rearing period (days?8–9 post-hatching), TAC and hematocrit were lower among second- vs. first-brood chicks. Interestingly, sexual dimorphism in body mass at days?8–9 post-hatching markedly differed between broods, first-brood males being 4.7% and second-brood males 22.7% heavier than their sisters, respectively. Pre-fledging mortality occurred among second-brood chicks only and was strongly female-biased. Our findings suggest that starling chicks, even if in poor conditions, are little affected by a bacterial challenge, at least in the short-term. Moreover, our study indicates that sex differences in body size, possibly mediated by sex-specific maternal investment in egg size, may heavily impact on pre-fledging survival in a different way in the course of the breeding season, resulting in sex-specific seasonal decline of offspring fitness. Finally, we suggest that levels of circulating antioxidants should be regarded among the proximate causes of the association between timing of fledging and long-term survival in avian species.     

Evidence for sexy sons in European starlings (Sturnus vulgaris)

The sexy son hypothesis suggests that females obtain future fitness benefits from mating with polygynous males through the inheritance by their sons of traits contributing to mating success. We tested this hypothesis in the facultatively polygynous European starling (Sturnus vulgaris) in two ways. We first compared sons of monogynous and polygynous free-living males for their abilities in nest site acquisition and female-directed behaviors in controlled aviary tests. We then investigated eggs laid in monogynous and polygynous matings for concentrations of maternal steroid hormones that could affect behavioral differentiation of sons. Sons of polygynous fathers defended more nest boxes and produced more courtship song than sons of monogynous fathers. Mean concentrations of maternal androstenedione (A4), 5-dihydrotestosterone (DHT), testosterone (T), and 17-estradiol (E) in yolks were not affected by mating status. However, the within-clutch pattern of A₄ depended on mating status, with higher concentrations in last than in first eggs of clutches of monogynous but not polygynous matings. These results suggest that (1) sons may inherit from their fathers behavioral qualities for the successful acquisition of nest sites and attraction of mates; (2) differential exposure to maternal steroid hormones during development in the egg is unlikely the cause of the behavioral differences between adult sons of monogynous and polygynous fathers; and (3) females adjust the within-clutch pattern of androgen to mating status, possibly in response to the expected contribution of their mate to nestling care.     

Responses to sugars and their behavioural mechanisms in the starling (Sturnus vulgaris L.)

Summary The response of the starling to sugar solutions was investigated as this species, which eats sweet fruits, does not prefer sugar solutions according to the literature.In choice tests using two identical fountains, moderate preference for higher concentrations (0.5 M and 1 M) of glucose and fructose to water was demonstrated. The same concentrations of sucrose were rejected. Lower concentrations (0.25 M and less) of all three sugars were neither preferred nor rejected. In choice tests using two differently coloured fountains the subjects did not generally respond more sensitively to sugar solutions. In learning experiments with differently coloured fountains the starlings developed very marked preferences for 0.5 M glucose and 0.5 M fructose and a corresponding rejection of 0.5 M sucrose in the course of 1–2 days. In a learning experiment with dentical fountains they also developed a pronounced preference; the preference values obtained, however, are higher if secondary cues such as the colour of the fountain or its position are available. In short time tests immediate responses to sugar solutions could not be demonstrated.The rejection of sucrose is attributed to illness-induced aversion learning, the learned preference for glucose and fructose to the preference according to gain in energy per unit of time as postulated by the optimal foraging theory. Taste sensations play, if any, only a minor role. The learning mechanisms operating in the experiments could be employed by the starling for the selection of fruits.     

Extra-pair paternity and intraspecific brood parasitism in wild zebra finches Taeniopygia guttata,revealed by DNA fingerprinting

Summary The frequency of extra-pair parentage in a wild population of zebra finches Taeniopygia guttata was examined by DNA fingerprinting. A total of 25 families, comprising 16 pairs of parents and 92 offspring (in broods of 1 to 6) were examined. Ten cases of extra-pair parentage, presumed to constitute intraspecific brood parasitism, were detected (10.9% of offspring or 36% of broods), including one possible instance of quasi-parasitism (parasitism by a female fertilized by the male nest owner). The average number of parasitic eggs per clutch detected by fingerprinting was 1.10±0.32 SD, very similar to the one egg difference in average clutch size between parasitised (6.0±0.82) and unparasitised nests (5.0±0.95). Two cases of extra-pair paternity (EPP) were detected among 82 offspring whose maternity was confirmed: 2.4% of offspring, or 8% of broods. In both cases EPP accounted for only a single offspring within a brood. Behavioural observations show that EPP occurs through extra-pair copulation rather than rapid mate switching. The results are discussed in the light of what is known about the fertile period and sperm precedence patterns in this species. Offprint requests to: T.R. Birkhead     

Exogenous testosterone increases female aggression in the European starling (<Emphasis Type="Italic">Sturnus vulgaris</Emphasis>)

In the European starling, Sturnus vulgaris, optimal mating systems differ between males and females. Males gain from polygyny, whereas monogamy increases female fitness. The cost of polygyny to females lead to intense female–female competition, and it has previously been shown that the intensity of female aggression during the pre-breeding period can predict the realised mating system. The physiological regulation of such female aggression in starlings is not yet known. This study examines the role of testosterone in mediating aggressive behaviours involved in intra-specific reproductive competition in female starlings. Testosterone levels were experimentally elevated with testosterone implants in females during the pre-laying period. To simulate a situation in which an additional female tried to mate with the focal female’s mate, a caged female was presented close to a nest-site to which the male could attract a secondary female. Testosterone was significantly related to several behaviours involved in female–female interactions. Females with testosterone implants spent significantly more time close to the caged female and produced more song bouts than control females. In contrast, male behaviour was unrelated to the experimental status of the mate. Females mated to males that attracted a secondary female were less aggressive towards the caged female than those that remained monogamously mated. The effect of exogenous testosterone in this study indicates that androgens may mediate social behaviours in female starlings during the breeding season.     

Egg pigmentation reflects female and egg quality in the spotless starling <Emphasis Type="Italic">Sturnus unicolor</Emphasis>

It has been proposed that blue colouration in eggs has evolved as a signal of female quality that males can use to modulate their parental investment. This hypothesis is based in the antioxidant properties of biliverdin whose costly deposition in the eggshell is expected to signal female antioxidant capacity and egg quality. Since maternally derived androgens are costly to produce and may adaptively affect offspring phenotype, high-quality females may benefit by signalling their androgen investment through egg colouration. Our aim was to investigate whether egg colour variation in the spotless starling reflected the amount of pigments on the eggshell and whether egg pigmentation was related to female and egg quality. Chromatography analyses revealed that spotless starling eggshells contained two different pigments: biliverdin and protoporphyrin IX with no correlation between them. Biliverdin contents correlated positively with egg colouration indicating that darker eggs with a higher peak in the blue–green segment of the spectrum contained higher amounts of biliverdin. Eggs containing more biliverdin were laid by high-quality females and contained higher yolk testosterone levels. However, despite the strong correlation between biliverdin and colorimetric variables, egg colouration did not reflect accurately female and egg quality. Our results provide evidence that eggshell pigmentation in the spotless starling is related to female and egg quality as shown by the yolk testosterone levels. However, the lack of relation between egg colour and female condition and egg quality do not provide evidence to support the signalling function of egg colouration.     

Effects of paternal care on reproductive success in the polygynous spotless starling Sturnus unicolor

For males of socially polygynous avian species like the spotless starling, there may exist a trade-off between investing in paternal care and controlling several nests. To determine how the intensity of paternal care affects reproductive success per brood sired or expressed as the total number of young raised in all nests controlled by the same male, it is necessary to manipulate paternal care. Testosterone (T) has been shown to depress the tendency for males to care for their young, and induces them to acquire more mates. The effects of paternal care on reproductive success were studied by treating certain male starlings with exogenous T and others with the antiandrogen cyproterone acetate (CA), and comparing the parental behavior of T- and CA-males throughout the breeding season with that of controls. CA-males fed their chicks more during the first week after hatching than T-males, with controls feeding at intermediate rates, both on a per nest basis and as total effort for all nests controlled by the same male. Paternal feeding rates during the first week of chick life had a significant positive effect on the number of fledged young. The hormone treatment significantly affected the number of chicks raised per nest, CA-males having a higher breeding success per nest than T-males, and controls showing intermediate levels of success. There was no significant effect of treatment on total reproductive success attained by males throughout the season. In the polygonous spotless starling, the intensity of paternal care of young affects reproductive success per nest positively but not on a seasonal basis. Received: 6 February 1999 / Received in revised form: 30 June 1999 / Accepted: 11 July 1999     

A field test of the intraspecific brood parasitism hypothesis in the golden egg bug (<Emphasis Type="Italic"> Phyllomorpha laciniata</Emphasis>)

In natural populations of golden egg bugs ( Phyllomorpha laciniata), females lay eggs on plants where they develop unattended, or on conspecifics, where they remain firmly glued until the nymphs hatch and start an independent life. Mortality rates among eggs laid on plants are higher than among eggs carried by adults. Because females cannot lay eggs on themselves, in order to improve offspring survival, they have to lay eggs on other individuals. Two hypotheses have been proposed to explain egg carrying: (1) the mating pair intraspecific brood parasitism hypothesis suggests that females dump eggs on copulating pairs, and (2) the paternal care hypothesis suggests that the system is driven mainly by males accepting eggs to improve the survival rates of their own offspring. Our data from the field show that 77% of the eggs are carried by males, because more males than females carry eggs, and because males carry a greater number of eggs. In addition, we show that mating males carry more recently laid eggs than single males. These results support the view that egg carrying is performed predominantly by males and that eggs are laid on males by their current mating partner, probably between repeated copulations. Males are likely to accept eggs, despite intermediate levels of paternity, because they cannot discriminate in favour of their own eggs, because rejected eggs will face 97% mortality rates on plants, and because they do not suffer mating costs when they carry eggs. However, females carry 23% of the eggs, but no differences in egg carrying have been found between mating and single females, suggesting that this is not the result of egg dumping while females are copulating. Egg carrying by females could reflect low levels of intraspecific parasitism, which is likely to reflect the low rate of successful attempts by egg-laying females who try to oviposit on other conspecifics rather indiscriminately, in an effort to improve the survival of their offspring.     

Electrophoretic variants of egg white transferrin indicate a low rate of intraspecific brood parasitism in colonial cliff swallows in the Sierra Nevada,California

Summary The frequency of intraspecific brood parasitism in two colonies of cliff swallows (Hirundo pyrrhonota) nesting in the eastern Sierra Nevada in California was assessed through an electrophoretic analysis of egg white (albumin) proteins. Albumin proteins are maternally derived and are presumed to directly reflect maternal genotype. Thus, a comparison of protein banding patterns produced by eggs collected from a single clutch allows any egg laid by a female other than the putative mother to be detected. Eggs were collected from 13 cliff swallow nests in 1984 and 41 nests in 1987, a total of 54 nests. Of the clutches collected in 1984, one showed evidence of intraspecific brood parasitism, giving a nest parasitism rate of 7.6%. In 1987, one of 41 nests contained a parasitic egg, for a parasitism rate of 2.4%. Over both years combined the rate of intraspecific brood parasitism was 2 of 54 nests, or 3.7%. These parasitism rates are much lower than those estimated for Nebraskan cliff swallows (22–43%) and 2nd-year purple martins (36%). Possible explanations for the discrepancy between parasitism rates in Sierran cliff swallows and other groups of swallows are discussed.Correspondence to: A.P. Smyth     

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     

Tests of landscape influence: nest predation and brood parasitism in fragmented ecosystems

The effects of landscape fragmentation on nest predation and brood parasitism, the two primary causes of avian reproductive failure, have been difficult to generalize across landscapes, yet few studies have clearly considered the context and spatial scale of fragmentation. Working in two river systems fragmented by agricultural and rural-housing development, we tracked nesting success and brood parasitism in > 2500 bird nests in 38 patches of deciduous riparian woodland. Patches on both river systems were embedded in one of two local contexts (buffered from agriculture by coniferous forest, or adjacent to agriculture), but the abundance of agriculture and human habitation within 1 km of each patch was highly variable. We examined evidence for three models of landscape effects on nest predation based on (1) the relative importance of generalist agricultural nest predators, (2) predators associated with the natural habitats typically removed by agricultural development, or (3) an additive combination of these two predator communities. We found strong support for an additive predation model in which landscape features affect nest predation differently at different spatial scales. Riparian habitat with forest buffers had higher nest predation rates than sites adjacent to agriculture, but nest predation also increased with increasing agriculture in the larger landscape surrounding each site. These results suggest that predators living in remnant woodland buffers, as well as generalist nest predators associated with agriculture, affect nest predation rates, but they appear to respond at different spatial scales. Brood parasitism, in contrast, was unrelated to agricultural abundance on the landscape, but showed a strong nonlinear relationship with farm and house density, indicating a critical point at which increased human habitat causes increased brood parasitism. Accurate predictions regarding landscape effects on nest predation and brood parasitism will require an increased appreciation of the multiple scales at which landscape components influence predator and parasite behavior.     

Adoption or infanticide: options of replacement males in the European starling

The behaviour of a male bird towards a potential mate and her clutch may depend both on his expected paternity and on the likelihood that she will produce a replacement clutch if he commits infanticide. In this study we evaluate the choices made by replacement male European starlings Sturnus vulgaris. By removing males before and during laying, we induced other males, mainly neighbours, to mate with the reproductively active females. When the original male was removed before laying, a new male adopted the subsequent clutch in 14 out of 15 cases. When ten females were widowed during their laying period, replacement males never adopted their clutches. The paternity of replacement males was a function of when they replaced the former male. When replacement occurred more than 3 days before egglaying, the new male fathered nearly all offspring; when it occurred the day before laying, the new male still fathered more than every second young. When the original male was removed during his mate’s laying period, in five out of ten cases a replacement male committed infanticide by throwing out the eggs, but this only occurred in one out of 15 cases when removal took place before laying. The evidence for infanticide actually being committed by the replacement male was circumstantial. Four out of six of the females affected by apparent infanticide produced replacement clutches in which the male presumably had higher paternity than in the original clutch. In all cases, the male adopted the replacement clutch. In five cases when the original male was removed during laying, the neighbours neither adopted the brood nor committed infanticide, although they sometimes were seen courting the widowed female and copulating with her. These cases occurred later during laying than those were males comitted infanticide. The time from infanticide to the laying of the replacement clutch tended to increase as infanticide was committed later in the laying sequence. We conclude that strategies of potential replacement males are influenced by their expected paternity in the current brood and the probability that the female will produce an early replacement clutch. Received: 10 March 1995 / Accepted after revision: 28 October 1995     

Female choice for complex song in the European starling: a field experiment

Male European starlings Sturnus vulgaris sing long complex songs that appear to be important in the courtship of females but which also influence competitive interactions between males. We tested the hypothesis that females choose mates on the basis of the complexity of their songs, rather than on the quality of the territories the males defended. In order to determine whether certain territories were preferred over others, the first set of birds to settle in the experimental nest-boxes was removed and a second set allowed to settle. Consistent preferences for certain nest-boxes were indicated by correlations between the settlement patterns of the first and second sets of birds. However, males with the most complex song did not necessarily occupy the most preferred nest sites. Males with more complex song acquired mates faster. This relationship remained significant when nest-site preference was statistically controlled, indicating that female starlings chose males with complex song rather than those that defended preferred nest sites. A number of morphological variables were also found to be uncorrelated with female choice. Song complexity in European starlings increases with age, and the evolution of song complexity in this species is consistent with an age-indicator model of sexual selection. Males with larger repertoires were also in better condition, indicating that females obtain high-quality mates by choosing on the basis of male song. Received: 29 April 1995/Accepted after revision: 9 September 1995     

Habitat edge, land management, and rates of brood parasitism in tallgrass prairie.

Bird populations in North America's grasslands have declined sharply in recent decades. These declines are traceable, in large part, to habitat loss, but management of tallgrass prairie also has an impact. An indirect source of decline potentially associated with management is brood parasitism by the Brown-headed Cowbird (Molothrus ater), which has had substantial negative impacts on many passerine hosts. Using a novel application of regression trees, we analyzed an extensive five-year set of nest data to test how management of tallgrass prairie affected rates of brood parasitism. We examined seven landscape features that may have been associated with parasitism: presence of edge, burning, or grazing, and distance of the nest from woody vegetation, water, roads, or fences. All five grassland passerines that we included in the analyses exhibited evidence of an edge effect: the Grasshopper Sparrow (Ammodramus savannarum), Henslow's Sparrow (A. henslowii), Dickcissel (Spiza americana), Red-winged Blackbird (Agelaius phoeniceus), and Eastern Meadowlark (Sturnella magna). The edge was represented by narrow strips of woody vegetation occurring along roadsides cut through tallgrass prairie. The sparrows avoided nesting along these woody edges, whereas the other three species experienced significantly higher (1.9-5.3x) rates of parasitism along edges than in prairie. The edge effect could be related directly to increase in parasitism rate with decreased distance from woody vegetation. After accounting for edge effect in these three species, we found evidence for significantly higher (2.5-10.5x) rates of parasitism in grazed plots, particularly those burned in spring to increase forage, than in undisturbed prairie. Regression tree analysis proved to be an important tool for hierarchically parsing various landscape features that affect parasitism rates. We conclude that, on the Great Plains, rates of brood parasitism are strongly associated with relatively recent road cuts, in that edge effects manifest themselves through the presence of trees, a novel habitat component in much of the tallgrass prairie. Grazing is also a key associate of increased parasitism. Areas managed with prescribed fire, used frequently to increase forage for grazing cattle, may experience higher rates of brood parasitism. Regardless, removing trees and shrubs along roadsides and refraining from planting them along new roads may benefit grassland birds.     

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     

Inter-sexual conflicts over copulations in the European starling: evidence for the female mate-guarding hypothesis

Recent studies have suggested that conflicts of interests between the sexes may lead to variation in copulation behavior among pairs. We examined differences in the rate and timing of copulation solicitations and copulations among females of different mating status in the facultatively polygynous starling in an attempt to explain why females copulate repeatedly with their mate. All within-pair copulations were female-solicited indicating that females control copulations in the starling. Before egg laying, females solicited copulations at a high rate (usually more than 2 per hour). In contrast to most other species studied so far, females continued to solicit copulations throughout the egg laying period, and also solicited after egg laying (the latest solicitation occurred when the nestlings were 4 days old). Primary females solicited more copulations than monogamous females both during and after the fertile period. Many copulation solicitations of primary females occurred at the nestbox where their male was singing to obtain an extra female. Both primary and secondary females solicited more copulations after the egg-laying period than monogamous females. A large proportion of female copulation solicitations was refused by the male partner: female solicitation resulted in more male refusals in primary females than in monogamous females. Primary females were more likely to be chased aggressively when they solicited a copulation than monogamous females; most aggressive chases occurred when primary females flew towards their male to solicit copulation when he was singing at another nestbox. Overall, our results demonstrate that there is a conflict over copulation between males and females in polygynous pairs. The conflict presumably relates to the cost of sharing male parental investment: females use copulation solicitation behavior to interrupt their singing males apparently in an attempt to prevent them from becoming polygynous. We present the first empirical evidence that female songbirds use copulation solicitation behavior as a form of mate guarding, often in a non-reproductive context. We did not find a positive relationship between copulation rate during the fertile period and the amount of male parental care as is predicted by the paternity confidence hypothesis.