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.     

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     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Infanticidal and anti-infanticidal strategies in the swallow Hirundo rustica

Summary Five definite and nine suspected cases of infanticide were documented in the swallow Hirundo rustica. Unmated males visited neighbouring nests and removed entire broods during the first days of the nestling period, preferentially from nests owned by young late-breeding individuals. Infanticide followed the disappearance of the male nest owner in 11 of the 14 cases. The unmated infanticidal male later mated with the female victim although renesting during the same season only took place in 12 of the 14 cases. The fraction of unmated males increased with colony size, and infanticide was relatively more common if unmated males were abundant. Females did not engage in extra-pair copulations in order to avoid infanticide. Intense guarding of the nest and its contents prevented infanticide. Nest guarding intensity was higher in colonial compared with solitarily breeding swallows, and guarding intensity increased with colony size. Experimental removal of male swallows during the early nestling period reduced the nest guarding intensity and increased frequency of visits from unmated males in colonies, but not among solitarily breeding swallows. Colonial nests from which the male was removed suffered from infanticide more often than solitary nests, and nests where infanticide was recorded were guarded significantly less intensely than other nests before the infanticidal incidents.     

Egg removal and intraspecific brood parasitism in the European starling (Sturnus vulgaris)

Summary From 1983 to 1986 we monitored 284 European starling (Sturnus vulgaris) nests in New Jersey for evidence of intraspecific brood parasitism and egg removal during the laying period. Egg removal occurred significantly more often at nests where intraspecific brood parasitism was detected (12 of 35 nests, 34%) than at unparasitized nests (23 of 249 nests, 9%). Brood parasitism (92% of parasitized nests) and egg removal (74% of nests with egg removal) were most common at nests where egg laying began in April of each year (i.e., early nests). Egg removal occurred at 26 (19%) and brood parasitism at 32 (23%) of 138 early nests. Both brood parasitism and egg removal were concentrated during the first four days in the laying period when brood parasitism is most likely to be successful and when host nests are most vulnerable to parasitism (Romagnano 1987). Both parasitism and removal usually involved a single egg at each nest. We detected brood parasitism and egg removal on the same day at five of 12 nests (42%) where both were observed. Because starlings do not remove foreign eggs from their nests once they begin laying (Stouffer et al. 1987) we hypothesize that parasite females sometimes removed host eggs while parasitizing nests.     

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     

Differential parasitism of least flycatchers and yellow warblers by the brown-headed cowbird

Summary Brown-headed cowbirds (Molothrus ater) parasitized yellow warblers (Dendroica petechia) six times more frequently than least flycatchers (Empidonax minimus) nesting in the same riparian habitat in southern Manitoba. This difference was surprising because least flycatchers were higher quality hosts; flycatchers always accepted cowbird eggs while warblers did so on only about half the occasions. Both hosts were equally good foster parents, at least until fledging; thus, once an egg was accepted there was probably no further advantage in parasitizing one species over the other. The probability that a nest was parasitized decreased with increasing nest height, perhaps as a consequence of the cowbird's habit of searching for nests close to the ground. Since least flycatchers nested higher in the canopy than yellow warblers, a greater proportion of flycatcher nests probably were not detected by cowbirds. Nevertheless, nest height alone could not account fully for the lower incidence of parasitism on flycatchers. Clutch initiation in flycatchers peaked 6 days after warbler clutch initiations and 5 days after that of cowbirds. Despite the later peak in initiations, flycatcher nests were always available as potential hosts over the entire cowbird laying season and it was not until new clutch initiations by warblers declined in late summer that flycatchers were actually used as hosts. Because least flycatchers responded more aggressively than yellow warblers to a model female cowbird at the nest, we concluded that greater nest defense by flycatchers may have also reduced the rate of brood parasitism in this host. Together, our results suggest the large difference in the frequency of parasitism between these two hosts was primarily a product of nest location but that differences in host nest-defense and breeding season asynchrony may have contributed to preferential host selection.Offprint requests to: J.V. Briskie     

Genetic evidence of multiple parentage in broods of cliff swallows

Summary Parental exclusion analyses based on allozyme data were performed on 105 families of cliff swallows (Hirundo pyrrhonota) from southwestern Nebraska, USA. The protein products of seve polymorphic loci were resolved from blood, and at least one parental exclusion occurred at six of these loci. One or both putative parents were excluded for 35 nestlings from 22 different families. The mean number of non-kin nestlings in these families was 1.59. Non-kin nestlings were found in families with brood sizes ranging from two to five. A greater percentage of families in an 1100-nest colony had non-kin offspring than in two smaller colonics, although the difference was not statistically significant. Application of genetic models to these data and the observed distribution of parental exclusions suggested that multiple parentage in cliff swallows results more often from intraspecific brood parasitism than from forced extra-pair copulations. Based on the calculated probabilities of detecting non-kin, we estimate that 23.7% of all nestlings in our population are not the offspring of one or both of their putative parents. We estimate that about 43% of all cliff swallow nests in Nebraska contain at least one offspring resulting from intraspecific brood parasitism, and that about 6% of nests might contain offspring resulting from extra-pair copulations.     

Age,experience, and enemy recognition by wild song sparrows

Summary Older female Song Sparrows (Melospiza melodia) breeding on Mandarte Island, B.C., Canada, are more often parasitized by a brood parasite, the Brown-headed Cowbird (Molothrus ater), than yearling females breeding for the first time. This may be explained if older Song Sparrows behave differently than yearlings towards searching female cowbirds, and are thus more readily recognized as potential hosts. We tested this hypothesis by measuring the responses of Song Sparrows to a stuffed mount of a female cowbird in 1982, when no cowbirds frequented the island. This mount, and a control (a female junco) were presented near the nests of wild female sparrows of known age. As predicted, adult female sparrows behaved differently towards the cowbird model from yearlings (Table 1). They did not differ in their responses to the junco. Adult males also responded differently to the cowbird and junco (Table 2), but adult males did not differ significantly from yearlings in their response to either model. When birds that responded weakly as yearlings in the absence of cowbirds were retested as 2-year-olds after the recolonization of the island by cowbirds, they responded strongly to cowbird models. Two-year-old birds not exposed to cowbirds as yearlings, were parasitized at a rate intermediate between the rate for experienced adults and that for yearlings. Yearling females were parasitized less often at the beginning of the period of breeding activity by cowbirds than at the end. All these results are consistent with our hypothesis that age-selective parasitism results from differences among age classes in the mobbing responses of Song Sparrows to cowbirds. The greater response of adult sparrows to cowbirds seems non-adaptive, because it apparently results in a loss of reproductive output through selective parasitism. We suggest that this paradox can be resolved if the response to cowbirds near the nest is an instance of a more general acquired response to all potential enemies that approach a nest.     

The effect of resource holding potential,nest size and information about resource quality on the outcome of intruder-owner conflicts in the sand goby

Summary Sand goby, Pomatoschistus minutus Pallas, males need a nest site for successful breeding. The value of the nest increases with size, as larger nests can hold more eggs. In the field using artificial nest sites, takeovers occurred in 29.0% of the cases. The winning intruders were on average 16.3% larger than the owners. These, in turn, were significantly smaller than the nonreplaced males. Replacement probability increased with nest size. Prior ownership was of no importance in experimental situations, but might have affected takeover probabilities in the field. Males assessed the size of a potential nest site on the basis of its external appearance. When intruders and owners were given opposite information about nest size the experiments resulted in takeover rates of around 50% in situations where takeover rates were expected to be extreme. This suggested that intruders might update their information about a site's true value during the fight. The continuous assessment, in turn, might affect their motivation to continue fighting. On average, larger males were more active in initiating displays. However, smaller opponents challenged their larger opponents more actively when they were defending a large nest than when they were defending a small nest. The greater willingness to defend might provide the intruder with more information about the real value of the nest.     

Cowbird removals unexpectedly increase productivity of a brood parasite and the songbird host

Generalist brood parasites reduce productivity and population growth of avian hosts and have been implicated in population declines of several songbirds of conservation concern. To estimate the demographic effects of brood parasitism on Bell's Vireos (Vireo bellii), we removed Brown-headed Cowbirds (Molothrus ater) in a replicated switchback experimental design. Cowbird removals decreased parasitism frequency from 77% and 85% at unmanipulated plots to 58% and 47% at removal plots in 2004 and 2005, respectively. Vireo productivity per pair was higher at cowbird removal plots when years were pooled (mean = 2.6 +/- 0.2 [SE] young per pair) compared to unmanipulated plots (1.2 +/- 0.1). Nest desertion frequency was lower at cowbird removal plots (35% of parasitized nests) compared to unmanipulated plots (69%) because removal of host eggs was the proximate cue for nest desertion, and vireos experienced lower rates of egg loss at cowbird removal plots. Nest success was higher among unparasitized than parasitized nests, and parasitized nests at cowbird removal plots had a higher probability of success than parasitized nests at unmanipulated plots. Unexpectedly, cowbird productivity from vireo pairs was higher at cowbird removal plots (mean = 0.3 +/- 0.06 young per pair) than at unmanipulated plots (0.1 +/- 0.03) because fewer parasitized nests were deserted and the probability of nest success was higher. Our study provides the first evidence that increases in cowbird productivity may be an unintended consequence of cowbird control programs, especially during the initial years of trapping when parasitism may only be moderately reduced. Thus, understanding the demographic impacts of cowbird removals requires an informed understanding of the behavioral ecology of host-parasite interactions.     

Equality of feeding roles and the maintenance of monogamy in tree swallows

Summary We investigated the division of labor in male and female tree swallows by measuring the rate of food delivery to nestlings at 36 nests. By observing natural nests and performing brood manipulations we found that males and females divided the feeding duties about equally and responded similarly to changes in brood size and age. Feeding rate was most highly correlated with brood mass. Manipulation and removal experiments showed that increased feeding rates could be elicited, but only for limited periods of time. Male and female tree swallows could only partially compensate in feeding nestlings when mates were removed. This, along with the higher mortality in enlarged broods and in those raised by single parents, indicates that both male and female are required to raise an entire brood to fledging. We argue that this requirement contributes to the absence of mate guarding and the maintenance of monogamy in the tree swallow.     

Post-ejection nest-desertion of common cuckoo hosts: a second defense mechanism or avoiding reduced reproductive success?

Hosts of the common cuckoo (Cuculus canorus), an avian brood parasite, develop antiparasite defense mechanisms to increase their reproductive success. Ejection of the parasite egg and desertion of the parasitized nest are the most typical adaptations in response to brood parasitism, but nest desertion may also occur in response to partial clutch reduction, independently from parasitism. Some great reed warblers (Acrocephalus arundinaceus) showed both mechanisms in the same incidence of cuckoo parasitism: in 18% of successful ejections of the parasite eggs, they deserted their nests. We studied if such cases of post-ejection nest-desertion are caused by brood parasitism or reduced clutch value. We experimentally parasitized clutches consisting of five or three host eggs with two painted conspecific eggs to mimic parasitic eggs, as multiple parasitism is frequent in the area. Although hosts ejected these parasitic eggs in both clutch categories (100% and 67% for the larger and smaller inital clutch sizes, respectively), we found that after manipulation, post-ejection nest-desertion frequently occurred at small (3-egg) clutches (40%), but rarely at large (5-egg) clutches (17%). The same phenomenon also occurred when unparasitized 3-egg clutches were reduced by two eggs, but not when 5-egg clutches were reduced in the same way. A logistic regression model revealed that only initial clutch size affected nest desertion of parasitized nests in our experiments. Therefore, we conclude that post-ejection nest-desertion is not a second antiparasite mechanism, which might serve as a redundant antiparasite defense, but a reaction to typically small and further decreased clutch size.     

Northern harriers on feeding territories respond more aggressively to neighbors than to floaters

Summary Territory owners often respond less aggressively towards intruding neighbors than towards intruding floaters, an observation termed the dear enemy phenomenon. Comparisons of territory owners' responses to intruding neighbors versus their responses to intruding floaters usually have been made for owners of multi-purpose and/or breeding territories. Here, I describe responses of female northern harriers Circus cyaneus (owners) on winter feeding territories towards three types of intruders (female neighbors, female floaters, and male floaters) and show that the dear enemy phenomenon does not occur. Owners' responses towards neighbors were more intense (mostly flights rather than calls) than responses towards female floaters, which in turn were more intense than responses towards male floaters. The greater intensity of owners' responses towards neighbors compared to owners' responses towards male and female floaters may be related to differences in the threat posed by each of the three intruder types in terms of fighting ability (RHP) and potential losses from intrusion. Hence, whether owners respond more aggressively towards neighbors or floaters, and whether the dear enemy phenomenon is observed, may depend upon the relative magnitude of threat presented by neighbors and floaters to owners in terms of fighting ability and potential losses from intrusion.     

Behavioral tactics of subadult female floaters in the tree swallow

Summary There are large numbers of reproductively mature female tree swallows (Tachycineta bicolor) which do not breed due to limits of suitable nesting cavities. Many of these floaters are one-year-old females that have a distinctive subadult plumage. This study examines the behavioral tactics that these subadult female floaters use to obtain breeding opportunities. Early in the season, subadult floaters tended to intrude briefly (Fig. 4) on many nest sites in succession (Figs. 2, 3), although they rarely gained close access to nest sites (Fig. 5). Subadults responded very quickly to vacant nest sites, where the resident female had been experimentally removed, by entering the nest cavity and defending it from conspecifics. We argue that the early season exploratory behavior increases a subadult's chances of discovering a vacant nest site, rather than increasing its success in evicting resident females or laying eggs in other females' nests. During the nestling period, subadult females intruded on fewer nest sites for longer periods, and often gained close access to the nest site. Late in the season, subadult floaters may be gathering information on the quality of nest sites for the next breeding season, rather than searching for current breeding opportunities. The reproductive tactics of subadult female tree swallows are consistent with the breeding threshold model for the evolution of delayed plumage maturation in passerines.     

Hovering guards of the stingless bee <Emphasis Type="Italic">Tetragonisca angustula</Emphasis> increase colony defensive perimeter as shown by intra- and inter-specific comparisons

Social insects need to defend their nest against robbery, parasitism and predation. The stingless bee Tetragonisca angustula is unique in that it has guards that hover near the nest entrance in addition to guards that stand at the entrance. We tested both the general hypothesis that hovering guards increase the effectiveness with which flying intruders are detected and the specific hypothesis that hovering guards improve the detection of workers of the obligate robber bee, Lestrimellita limao. In an intraspecific study comparing colonies, we found a strong positive relationship between the number of hovering guards and the distance at which a dummy robber bee or L. limao worker, experimentally moved towards the nest entrance, was detected. These results were mirrored in an interspecific study showing that four species of stingless bees with similar population colonies but which lacked hovering guards, detected L. limao only at the nest entrance, in contrast to T. angustula. In addition, we found that a greater number of attacks by guards occurred when dummies were impregnated with citral, a major component of L. limao mandibular gland odour. Our results support the hypothesis that T. angustula hovering guards increase the detection perimeter for flying intruders, especially L. limao.     

Do male tree swallows guard their mates?

Summary We monitored the time spent at the nest and following behavior of mated tree swallows to determine if males were guarding their mates. The proportion of time spent together at the nest did not decrease significantly between fertile and postfertile periods, and the tendency of males to follow females was not significantly different from that of females to follow males. Following by either sex was infrequent. We suggest that the lack of mate guarding in tree swallows is related to an apparently low probability of extra-pair copulations, which in turn is likely to be due to two factors. Nesting opportunities are limited, perhaps more so for females than males. If the operational sex ratio is skewed towards females, this would not only reduce the risk of extra-pair copulations, but would also select against promiscuous females which would risk being abandoned by their mates. Secondly, under natural conditions, the limited availability of nest sites has selected for territorial defense by both males and females, which may decrease the occurrence of extra-pair copulation. Both factors would lead to relaxed selection for mate guarding behavior.     

Nestmate recognition in three species of stenogastrine wasps (Hymenoptera,Vespidae)

The capacity to recognise a conspecific intruder was investigated in Parischnogaster jacobsoni, Liostenogaster flavolineata and L. vechti, three species of primitively social wasps of the subfamily Stenogastrinae. Results of behavioural experiments carried out in the field showed that females of all three species react pacifically if presented with female nestmates, but aggressively reject an intruder from a conspecific colony. As L. flavolineata and L. vechti both build large clusters of nests, often very close to each other, the recognition capacity among females from different nests, but in the same conspecific cluster, was also investigated. Females of both species were more aggressive towards females from a different colony in the same cluster than towards their female nestmates. Additional experiments on L. flavolineata showed that there was no difference in reaction towards females from colonies nearer or further from the tested colony but within the same cluster, nor towards females from a different cluster. The capacity to recognise an alien conspecific nest containing immature brood was investigated in P. jacobsoni. Adult females of this species, invited to land on an alien nest which had experimentally been exchanged for their own, accepted the new nest and partially destroyed the immature brood. The behaviour of the females when they land on an alien nest, however, suggests that they do recognise the nest as foreign. Acceptance of foreign nests coupled with low immature brood destruction is probably due to the high energetic costs of egg-deposition and larval rearing in stenogastrine wasps. These results suggest that nestmate recognition in these wasps is very efficient, even though they belong to the most primitive subfamily of social wasps. Received: 16 April 1996/Accepted after revision: 9 August 1996     

The superseded female's dilemma: ultimate and proximate factors that influence guarding behaviour of the carpenter bee Xylocopa pubescens

Both solitary and primitively social nests of the facultatively social carpenter bee Xylocopa pubescens can be found throughout most of the breeding season. In social nests there is reproductive division of labour between a dominant forager and a guarding female. Two types of guarding females can be discerned: the young pre-reproductive guards, and older, formerly reproductive guards. The latter type of guard is found when, after a take-over of reproductive dominance either by a nestmate (mostly a daughter) or an intruder, the defeated female stays in the nest instead of leaving to try and found or usurp another nest. She is then manipulated into the role of a guard. The dominant female profits from the presence of the guard since she protects the nest against pollen robbery by conspecifics (Hogendoorn and Velthuis 1993). We have studied why superseded females might prefer to remain as a guard, rather than try their luck somewhere else. The hypotheses investigated pertain to (1) the difficulty for the defeated female of finding a new nest and of restarting reproductive activities due to (a) ecological constraints (nest and pollen shortage) and (b) the effect of age and wear on the defeated female; (2) the effects of guarding in terms of inclusive fitness. We found that superseded females remained as guards significantly more often when a nestmate (not necessarily close kin) took over reproductive dominance than when an intruder did so. Other factors associated with the decision of the defeated female to stay or leave were her age and the number of her own young still present after the supersedure. The probability of finding or constructing a new nest was lower for old than for young females. After finding a nest, old females produced less brood than young foundresses. As a result of these two factors old superseded females gained, in terms of inclusive fitness, by staying as guards, whereas young females profited from leaving the nest. We interpret these results as an indication that guarding behaviour has evolved due to kin selection. However, kin discrimination apparently did not occur. Therefore we conclude that in this species kin selection is not, in the proximate frame of reference, based on kin recognition and preference for helping kin. Correspondence to: K. Hogendoorn     

Does the great spotted cuckoo choose magpie hosts according to their parenting ability?

When brood parasites are about to lay an egg, they have to decide which nest to parasitize. The best nest in which to lay will depend on the parenting ability of the host. We have studied selection of magpie (Pica pica) hosts by great spotted cuckoos (Clamator glandarius). Great spotted cuckoos preferentially parasitize large host nests. Nest volume in magpies is a good indicator of territory quality, since there is a negative relationship between magpie nest size and breeding date, and timing of breeding in magpies is known to be positively related to territory quality. Moreover, magpies occupying high-quality territories have high breeding success. Therefore, nest size is positively related to the quality of magpies. Parasitized magpie nests were of greater volume than the nearest neighbouring nest not parasitized by the great spotted cuckoo. In order to test whether the great spotted cuckoos might select high-quality magpie hosts, we manipulated pairs of parasitized and non-parasitized nests with identical laying dates and habitats, introducing into each of the nests the same number of parasitic and non-parasitic eggs. The number of fledglings reared (magpie plus great spotted cuckoo chicks) in naturally parasitized nests was higher than in experimentally parasitized nests. Thus, the probability of survival of the parasite chicks increased if cuckoo eggs were laid in the nests of high-quality hosts originally chosen by the parasite.