Intraspecific Brood Parasitism Research Articles

Alternative mating strategies in Eurasian Reed Warblers: extra-pair paternity and egg dumping

Alternative mating strategies, involving mating outside a social pair bond, have been studied intensively during the last few decades. However, we are still far from understanding what factors affect their frequencies in wild bird populations. In 2006–2011 we studied Eurasian Reed Warblers breeding in the nature reserve “Stawy Milickie” in SW Poland, and analysed the frequency of extra-pair paternity (EPP) and intra-specific brood parasitism (IBP). We genotyped a total of 786 nestlings from 259 nests. EPP offspring constituted 13.40% of all young (from 7.63% to 22.82% in different study years), and they were found in 21.62% of the broods (from 14.6% to 32.7% annually). The mean proportion of females with EPP young was 24.2% (from 16.2 to 41.7% annually). The proportion of EPP young in nests containing any EPP offspring ranged from 25% to 100% (on average 60%) and was not related to brood size. EPP young in one nest were sired usually by one or two males (92% of all cases), but we recorded one brood with three EPP fathers and one brood of four, where each young was sired by a different EPP male, and none by a social male. We found only one case of intra-specific brood parasitism (IBP). The brood with IBP constituted 0.39% of all examined broods, while the nestling that hatched from the dumped egg constituted 0.13% of all young whose parents were genotyped. We conclude that extra-pair paternity is a relatively common and regularly occurring alternative mating strategy in our study population of Reed Warblers, while intra-specific brood parasitism is extremely rare.

High within-clutch repeatability of eggshell phenotype in Barn Swallows despite less maculated last-laid eggs

Abstract Ecological and life-history variation and both interspecific and intraspecific brood parasitism contribute to diversity in egg phenotype within the same species. In this study, Barn Swallows (Hirundo rustica erythrogaster) laid eggs with high intraclutch repeatability in egg size, shape, and maculation. Despite this high intraclutch repeatability, last-laid eggs had consistently less of the eggshell covered in spots and fewer spots than earlier-laid eggs in the clutch. We examined sources of interclutch and intraclutch variation using both direct measurements and custom software (SpotEgg, NaturePatternMatch) that provide detailed information on egg characteristics, especially maculation measures. In addition to our main findings, maculation on different sides of the egg was highly repeatable; however, only shape, proportion of the eggshell maculated, and average spot size were repeatable between first and replacement clutches. Low intraclutch variation in maculation could allow females to recognize their clutch and this may be adaptive for colonial nesting species, such as the Barn Swallow. Characterizing intraspecific variation in egg size, shape, and maculation is the first step in understanding whether intraclutch variation is low enough—and interclutch variation high enough—such that eggs could serve as identity signals.

Extra-pair paternity in a species with frequent extra-pair courtship feedings, few extra-pair copulations, and male-biased parental care

Patterns of extra pair paternity (EPP) and intraspecific brood parasitism (IBP) were studied in a Whiskered Tern Chlidonias hybrida population characterized by female brood desertion, a high level of extra pair courtship feedings (10%) and a low level of extra pair copulation (EPC; 0.6%). In this study, we used a set of microsatellite loci to analyse parentage in 56 Whiskered Tern families from southern Poland. Depending on the method, we detected that 1.4%–3.6% of chicks were sired by an extra-pair male, and extra-pair chicks were present in 3.6%–8.9% of broods. IBP was observed in 8.9%–14.3% of broods, corresponding to 3.6%–6.4% of the chicks. The low rate of EPP is in agreement with the hypothesis that in species with high male parental investment, females should avoid EPC. The low level of IBP indicates that intraspecific egg dumping is not a common female strategy in Whiskered Tern, similar to many other colonial waterbird species.

Adjustment of egg laying by both hosts and intraspecific brood parasites in a beetle

AbstractBrood parasites lay their eggs in the nests of other females, thereby shifting the costs of offspring care onto others. Given that care is costly, potential hosts should evolve mechanisms to avoid brood parasitism. Meanwhile, brood parasites should evolve mechanisms to circumvent host defences. Here we investigate whether hosts or intraspecific brood parasites adjust their egg laying behaviour as a mechanism to reduce or increase the effectiveness of brood parasitism. We use the burying beetle Nicrophorus vespilloides as our study system, in which hosts and brood parasites lay their eggs in the soil around a carcass controlled by the host. To test whether females adjust their egg laying behaviour when breeding as a host or brood parasite, we used an experimental design with three treatments: hosts, where focal females bred alongside a smaller female; brood parasites, where focal females bred alongside a larger female; and controls, where focal females bred alone. We used focal females from a narrowly defined size range to control for potential effects of body size. We found that hosts delayed the start of egg laying, which may allow them to recognise brood parasitic offspring that arrive too early. Meanwhile, brood parasites laid their eggs over an extended period, which may increase the chances that their egg laying overlapped with the host. Our results suggest that adjusting egg laying behaviour is a mechanism used by both hosts and brood parasites that may contribute to the differences in reproductive success shown in prior studies.

Reproductive Strategies Change With Time in a Newly Founded Colony of Spotless Starlings (Sturnus unicolor)

Variation in avian reproductive strategies is often studied from a comparative perspective, since even closely-related taxa differ greatly in the degree of polygyny, extra-pair paternity (EPP) or intra-specific brood-parasitism. However, substantial variation at the species level suggests that ecological factors are important in shaping these patterns. In this study, we examined the temporal plasticity of these strategies, following a population from the year of colony formation to 2 years after this. Parentage data from these years shows that polygyny decreased with time, likely as a consequence of increased competition for nesting sites and mates by new recruits, and immigrants of higher quality arriving to the colony as time passed. In parallel to this temporal change, we found an increase in intra-specific brood-parasitism and quasi-parasitism (QP). We interpret these patterns as a consequence of an increase of floaters with time; these birds pursue a mixture of alternative mating strategies to succeed in the population. We also found evidence of conspecific brood parasitism (CBP), by nesting females that laid part of the clutch in another nest or that after losing a partially laid clutch resorted to lay the last eggs in another nest. Analyses of the distance between the main nest and nests containing the secondary polygynous brood or extra-pair or parasitic young showed an avoidance of contiguous nests for conducting these alternative reproductive tactics. At the same time, these secondary nests were closer to the main nest than random distances within the colony, suggesting that access to public information was restricted to a narrow area around the main nest. Our study emphasizes how behavioral patterns are plastic traits that vary not only with individual circumstances, but also with time, tracking changes in density and social structure.

Extra‐pair paternity, intraspecific brood parasitism, quasi‐parasitism and polygamy in the Red‐footed Falcon (Falco vespertinus)

Based on the genotyping of 97 chicks and 74 adults from 37 families we describe extra‐pair paternity (EPP), intraspecific brood parasitism (IBP), quasi‐parasitism (QP) and polygamy in the Red‐footed Falcon Falco vespertinus. The frequency of chicks resulting from EPP was 2.06% affecting 2.70% of families (two chicks, one nest), the values for IBP were 1.03% and 2.70% for offspring and families, and the same values were detected for QP (each one chick in one nest). Altogether, 4.12% of offspring and 8.11% of families were affected by some of the alternative reproductive strategies. As far as we know, this is the first described case of QP in the genus Falco.

Extra food provisioning reduces extra‐pair paternity in the lesser kestrel Falco naumanni

Female promiscuity can function to acquire both direct and indirect benefits from their social mate and extra‐pair males. In many raptor species, intense mate‐feeding significantly contributes to female energy requirements before and during egg laying. Moreover, females may use mate‐feeding effort to assess male quality. In this study of the lesser kestrel Falco naumanni, we aimed at experimentally manipulating the female's perception of mate quality by providing females with extra food during egg laying, and evaluated the occurrence of extra‐pair paternity in food‐supplemented and control broods by parentage analyses. No extra‐pair offspring (EPO) was found among 19 food‐supplemented broods, whereas EPO occurred in five out of 17 control broods. No significant differences in morphological traits, body condition and reproductive success were found between faithful and unfaithful females. However, clutches containing EPO were laid later in the breeding season. Moreover, un‐cuckolded males had longer tarsi than cuckolded ones, indicating larger body size. Hence, extra food provisioning and early breeding reduced the occurrence of EPO in lesser kestrels. In addition, we confirmed the occurrence of intraspecific brood parasitism, as five nestlings were not the offspring of the brooding female. The results of our food‐provisioning experiment support the idea that mate‐feeding ability is a reliable indicator of male quality, and are in accordance with the hypothesis that male mate‐feeding behaviour is a sexually selected trait.

Reproductive and brood-rearing strategies in Alchisme grossa (Hemiptera: Membracidae): genetic analyses of kinship relationships

Alchisme grossa is a treehopper species showing maternal care until at least the third nymphal instar. A secondary female treehopper has frequently been observed near a family (primary female guarding its egg clutch). Intraspecific brood parasitism, communal breeding or alloparental care may be suggested as possible mechanisms to explain secondary female presence. To distinguish between these phenomena, we performed relatedness analyses of genetic samples of groups including one A. grossa primary female, a secondary female and the associated offspring using polymorphic microsatellites. Furthermore, we characterized the behavioral interaction between both females during maternal care and the reproductive strategy (monandry or polyandry) of A. grossa females by estimating the number of male parents. We observed the presence of secondary females in 35.9% of monitored families. The behaviors characterized suggest the occurrence of brood parasitism in the interaction between both females. Nevertheless, all offspring within a family were descendants only of the primary female and a single male, thus showing that A. grossa females are monandrous. The results, taken together with data on the reproductive biology reported for other treehoppers, are consistent with the occurrence of brood parasitism in A. grossa.

Extra-pair paternity and intraspecific brood parasitism in the Gentoo Penguin (Pygoscelis papua) on Elephant Island, Antarctica

Recent studies have shown that many species of apparently monogamous birds engage in extra-pair copulation (EPC). Penguins have intense shared parental care for their young, and thus have been considered monogamous. The present study aimed to assess the reproductive system of the gentoo penguin (Pygoscelis papua) on Elephant Island, Antarctica, by evaluating extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). Our data revealed high rates of EPC, with approximately 48.75% of chicks originating from EPP, corresponding to 72.5% of nests. IBP was found for ~ 17% of the gentoo penguin nests, a behavior previously recorded only for Magellanic penguins (~ 6%). The reasons for these behaviors are not clear, as increased genetic diversity or sex bias of offspring was not found. Thus, social and ecological aspects could be more important for determining the costs and benefits of EPP. Other genetic and ecological aspects must be investigated in future studies, such as genetic compatibility of the immune system or fluctuations of the EPP rate due to environmental conditions.

Individuality in Egg Colouration of Black-Headed Gulls Chroicocephalus ridibundus across the Years Confirmed through DNA Analyses

The eggshell colouration among and within certain bird species is highly variable. Although many studies have addressed this variation, the reasons for it remain largely unclear. Consistent individual differences in egg colouration may improve the ability of colonially breeding birds to recognise their clutch among other neighbouring nests. Moreover, in species with a high incidence of intraspecific brood parasitism, such as the Black-head Gull Chroicocephalus ridibundus, egg colouration patterns may allow parents to expel foreign eggs from their own clutch. Here, we used standardised photography and image processing, including UV spectral information, to investigate egg colour patterns in female Black-headed Gulls (476 eggs in 170 clutches) during four breeding seasons, from 2015 to 2018 in NE Germany. We confirmed maternity by comparing DNA extracted from eggshells with feathers from the breeding female. Our results showed a greater similarity of eggs within a clutch than among clutches (ANOSIM: R = 0.43, P = 0.001). Black-headed Gulls showed consistent individual-specific eggshell colour pattern across consecutive breeding seasons. Genetic analyses further revealed one foreign egg was present in three out of 25 clutches (12%), but these eggs were not expelled by the gulls, possibly because these eggs did not differ significantly in colouration from their own. Additionally, we conducted a clutch exchange experiment to assess the reaction of the breeding pair to a foreign clutch. After 21 neighbouring clutches had been exchanged, adults came back immediately and incubated the interchanged clutch without any negative reaction. It seems that they do not use the specific colour pattern for recognition of their clutches, but possibly use other cues that remain to be investigated. While the function of individual egg colour patterns remains unclear, our results strongly suggest colour variation is driven by internal rather than external factors in this colonially breeding species.

Molecular evidence of extra-pair paternity and intraspecific brood parasitism by the Magellanic Penguin (Spheniscus magellanicus)

Molecular studies have shown that, although most avian species are socially monogamous, they can exhibit different reproductive strategies, such as extra-pair paternity (EPP) and intraspecific brood parasitism (IBP). We investigated the genetic mating system of the Magellanic Penguin, Spheniscus magellanicus, a species that is reported to be monogamous, with little or no evidence of extra-pair paternity, high partner faithfulness over the years and intense biparental care. Thus, we proposed that if EPP does occur, the rate will be low and could be related to increased genetic diversity among offspring or the body condition of parents. As a consequence, we hypothesize that offspring from EPP will exhibit faster growth than non-EPP offspring, thus increasing their survival probability. In contrast to expectations, EPP was detected in 31% of the offspring and 48% of the nests had at least one extra-pair young. In addition, 6% of chicks were not the offspring of the putative mother or either member of the social pair, indicating evidence of IBP. However, we did not find a difference in genetic diversity between nests with or without EPP, nor did we find differences in parent body condition. Offspring from EPP showed slightly faster growth than non-EPP offspring, although this difference was not statistically significant. These results reveal a high rate of EPP and a low rate of IBP, both of which were previously unknown for this species. Our findings demonstrate that the Magellanic penguin has a more complex social mating system than previously thought.

Parasitic cuckoo catfish exploit parental responses to stray offspring.

Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus, the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue 'The coevolutionary biology of brood parasitism: from mechanism to pattern'.

Cold weather events provoke egg ejection behaviour in open‐nesting passerines

We analysed 25 conspecific egg ejection events from a large sample of nests (n = 762) of three passerine species. In two species, most of the events could not be explained by intraspecific brood parasitism or nest sanitation behaviour. At least some of these cases were behavioural responses to unfavourable weather conditions in the spring of 2017. We conclude that clutch size adjustment through egg ejection may be more widespread among passerines than previously thought.

The role of the mating system and intraspecific brood parasitism in the costs of reproduction in a passerine bird.

Limited resources trigger trade-offs in resource allocation. Reproduction is one of the most demanding activities in terms of energy, and costs related to reproduction can be apparent either as reduced future reproduction or as survival. However, costs are not always detected, because individual heterogeneity in quality and resource acquisition may explain variation in costs among individuals. We conducted a comprehensive study in spotless starlings (Sturnus unicolor) nesting in Central Spain to determine whether costs of reproduction could be detectable in the short and/or long term and whether prenatal or postnatal investment were driving these costs. We took into account the lifehistory of the species, where egg volume is highly repeatable, males are facultatively polygynous, and intraspecific brood parasitism occurs. Females with a high reproductive effort in a breeding event also had a high reproductive effort in the second event of the season. The mating system and maternal age were reliable predictors of breeding success within a breeding event: monogamous and primary females, as well as older mothers, raised more nestlings than secondary females and 1-year-old females, respectively. However, when high-investing females suffered intra-brood parasitism in 1 year, we found a negative correlation between current and futurereproduction. These results suggest that, under some circumstances, females are able to skip the short-term costs of reproduction, but when extra effort is added, trade-offs arise. While most studies have focused on different aspects of individual quality on costs, the ecological context seems to represent an important component that should be taken into account.

Extrapair paternity and nest parasitism in two sympatric quail

ABSTRACT We conducted a comparative study of 2 closely related and sympatric species, Northern Bobwhite (Colinus virginianus) and Scaled Quail (Callipepla squamata), to explore the drivers of interspecific variation in alternative reproductive strategies. Specifically, we used parentage analyses to determine rates of extrapair paternity and intraspecific brood parasitism for each species, and evaluated possible mechanisms for explaining variation in these rates between the 2 species. During 2013–2014, we genotyped hatched (n = 388 for Northern Bobwhite and n = 214 for Scaled Quail) and unhatched (n = 32 for Northern Bobwhite and n = 9 for Scaled Quail) eggshells from 34 Northern Bobwhite and 22 Scaled Quail nests in western Oklahoma, USA. Extrapair paternity occurred in 85% of Northern Bobwhite nests and 9% of Scaled Quail nests. The number of sires for each nest was greater in Northern Bobwhite nests (x = 2.29 ± 0.14 SE sires per nest) than in Scaled Quail nests (x = 1.09 ± 0.06 sires per nest). Intras...

Extra-pair paternity in the black-headed gull: is it exceptional among colonial waterbirds?

Although nesting at high densities promotes frequent interactions with individuals other than social mates, the rate of extra-pair paternity (EPP) in colonial waterbirds is generally low. So far, the highest EPP rate within this group has been reported in the black-headed gull Chroicocephalus ridibundus breeding in a colony in Czech Republic (33% broods with extra-pair offspring). In this study, we used a set of microsatellite loci to analyse parentage in 34 gull families (102 nestlings) from northern Poland. We recorded intra-specific brood parasitism in 10.8% of broods, but no evidence for EPP was found. The striking discrepancy between our results and previous estimates of EPP rate in the black-headed gull strongly indicate that promiscuity is a context-dependent strategy in this species and that its prevalence may greatly vary between populations. We recommend that a special care should be taken while using single-population data on EPP in the inter-specific comparative analyses.

Intraspecific avian brood parasites avoid host nests infested by ectoparasites

Intraspecific brood parasitism is widespread among birds and provides clues for elucidating the evolutionary origin of interspecific brood parasitism. Studies suggest that brood parasitism does not occur at random, but that parasitic females select nests with advantages such as higher physical stability, reduced predation risk, or lower ectoparasite infestations. However, this evidence is sparse and mainly correlative. By experimentally increasing the abundance of Carnus hemapterus (a common, generalist and widespread ectoparasitic nest fly of a multitude of bird species) in half of the nests, we show that parasitic Spotless Starlings (Sturnus unicolor) avoid conspecific nests infested by ectoparasites. Since Carnus ectoparasites impinge costs on their avian nestling hosts, this avoidance response would be adaptive for parasitic Starlings. Further, we suggest a mechanism by which parasitic females may assess the level of ectoparasite infestation to select host nests accordingly: by using parasite cues such as faeces and blood remains. Additionally, these cues may be used by parasitic females for synchronization with the reproductive cycle of host females because ectoparasite cues also indicate that incubation has already commenced. Whatever the functionality, the mechanism suggested here may be employed by intra- and interspecific brood parasites, so it might represent a widespread strategy in nature.

Female Zebra Finches Smell Their Eggs.

Parental investment in unrelated offspring seems maladaptive from an evolutionary perspective, due to the costs of energy and resources that cannot be invested in related offspring at the same time. Therefore selection should favour mechanisms to discriminate between own and foreign offspring. In birds, much emphasis has been placed on understanding the visual mechanisms underlying egg recognition. However, olfactory egg recognition has almost been completely ignored. Here, we investigated whether female zebra finches (Taeniopygia guttata) are able to discriminate between their own and a conspecific egg based on olfactory cues alone. Zebra finches are colonial—breeding songbirds. Eggs are monomorphic, i.e. without any spotting pattern, and intraspecific brood parasitism frequently occurs. In a binary choice experiment, female zebra finches were given the choice between the scent of their own and a conspecific egg. After the onset of incubation, females chose randomly and showed no sign of discrimination. However, shortly before hatching, females preferred significantly the odour of their own egg. The finding that females are capable to smell their own egg may inspire more research on the potential of olfaction involved in egg recognition, especially in cases where visual cues might be limited.

Nest usurpation by a common eider toward a long-tailed duck

Intraspecific and non-obligate brood parasitism and nest takeover is well documented in common eiders ( Somateria mollissima borealis ) nesting in the Arctic. However, we report the takeover of a long-tailed duck ( Clangula hyemalis ) nest by a female common eider on Nasaruvaalik Island, Nunavut, Canada. The high nesting density due to limited habitat in the region may have contributed to this seemingly risky behaviour, which provides no clear benefits to the eider. Keywords: Nest takeover; sea ducks; Somateria mollissima ; Clangula hyemalis ; High Arctic; limited habitat. (Published: 26 October 2016) Citation: Polar Research 2016, 35 , 32414, http://dx.doi.org/10.3402/polar.v35.32414

A siblicidal origin for avian brood parasitism?

We present a model for the evolution of host selection by avian brood parasites from the ecological context of siblicidal brood reduction tactics. Our analysis concentrates on the fitness costs and benefits that permit the evolution of brood parasitism as an adaptive strategy from a state of obligate parental care already featuring siblicide. Limited resources delivered by provisioning parents may incite siblicidal behaviour in offspring, directed towards nestmates regardless of kinship. The extent of siblicidal behaviour (in frequency of occurrence and number of nestmates killed) can extend to the eradication of all nestmates, as has been observed in some raptors and in seabirds. For parents of siblicidal offspring, laying each egg parasitically may maximize offspring survival by eliminating competition between related but siblicidal nest mates. To permit the evolution of conspecific (intraspecific) brood parasitism, costs of siblicide by the offspring of parasitic parents must exceed costs paid by the parasitic parents when losing related conspecifics (host offspring) in a host nest. To permit the evolution of obligate interspecific brood parasitism, costs to fitness from siblicidal offspring or nest reduction of related hosts must exceed costs of heterospecific parental care. Understanding the kin structure between parasites and hosts in conspecific parasitism, and measuring the costs paid by parasitic young due to mismatched incubation, provisioning, and social behaviours by heterospecific foster parents, should provide novel insights into the opportunities and constraints of the evolution of avian brood parasitism.