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Behavioral Ecology Vol. 15 No. 3: 462-468
Behavioral Ecology vol. 15 no. 3 © International Society for Behavioral Ecology 2004; all rights reserved
Rapid temporal change in frequency of infanticide in a passerine bird associated with change in population density and body condition
Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to A. P. Møller. E-mail: amoller{at}snv.jussieu.fr.
Received 3 February 2003; revised 25 July 2003; accepted 4 August 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexually selected infanticide, whereby unmated males obtain a mate by killing the dependent offspring of an already mated female, is a common alternative reproductive strategy in many animals. I estimated the frequency of infanticide in a population of barn swallows, Hirundo rustica, during the period 1977–2002. Population size decreased by more than a factor 10 during this period, and this decrease was associated with an increase in mortality, selecting for adults with better body condition. Density-dependent effects acted on infanticide through the relationship between the relative number of unmated males and population size. Because males in prime condition are better able to defend their nests against infanticidal males, the frequency of infanticide decreased as mean tail length and mean body condition of males increased during the study period. Therefore, a rapid decrease in population size, a decrease in the abundance of unmated males, and a concomitant increase in body condition have changed the importance of infanticide from being a major cause of mortality accounting for more than 25% of all nestling mortality to being almost completely absent during a period of 25 years.
Key words: alternative reproductive strategy, condition dependence, density dependence, Hirundo rustica, unmated males.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Sexual selection results from competition among individuals for reproductive success. Commonly studied mechanisms of sexual selection include variance in social mating success (Andersson, 1994
) and variance in genetic mating success (Birkhead and Møller, 1998). However, many other components of sexual selection can considerably increase the variance in success among individuals. These include courtship feeding; differential parental investment, including skew in sex ratios; parental investment; abortion; and infanticide (for review, see Hardy, 2002; Hausfater and Hrdy, 1984; Møller, 1994).
Infanticide is a component of sexual selection that has received little attention. Although infanticide occurs commonly across most taxa, the frequency is often thought to be low (Hausfater and Hrdy, 1984). Thus, there are logistic problems with studies of infanticide owing to its apparent rarity. However, the rarity may arise from difficulties of quantifying its frequency rather than from uncommon occurrence of the phenomenon. For example, studies of infanticide in primates have left the impression that infanticide is relatively rare, and it has even been claimed to be an artefact arising from human presence. Recently, van Schaik (2000) has been able to predict interspecific differences in the frequency of infanticide across primates based upon the probability of reproduction after an infanticide event. Infant mortality owing to infanticide is now considered to be a major component of mortality in primates. Whether that is also the case in other taxa remains to be determined.
Sexually selected infanticide is a means for individuals excluded from reproduction to increase their reproductive success by causing reproductive failure of conspecifics (Bertram, 1975). In addition, human behavior such as sex-specific hunting policies can increase the frequency of infanticide because replacement males habitually kill any dependent offspring in their home range as described for brown bears, Ursus arctos (Swenson et al., 1997). In many birds such as the barn swallow, Hirundo rustica, infanticide is mainly owing to unmated males killing dependent offspring, thereby causing females to remate and relay (Crook and Shields, 1985; Emlen et al., 1989; Møller, 1988; Wolff and Cicirello, 1989). In other species, females can also be important contributors to infanticide when they increase their probability of reproductive success by causing a reproductive failure of conspecifics (see Emlen et al., 1989; Hrdy, 1979; Robertson, 1990; Veiga, 1990).
Studies of infanticide are generally of short-term duration. They do not take temporal change in the frequency of infanticide into account. Therefore, there are, to the best of my knowledge, no studies investigating the effects of temporal changes in population density or abundance of potential infanticide perpetrators on the frequency of infanticide.
The objective of the present long-term study on the barn swallow was to investigate temporal change in frequency of infanticide and its importance for nestling mortality. Second, I attempted to identify factors that could account for such a change. These potential factors included changes in population size and changes in the abundance of unmated males, which are the main perpetrators of infanticide. As the size of this population decreased, I expected that infanticide would become less important as a cause of mortality. Likewise, I expected that the frequency of infanticide would increase with the abundance of potential perpetrators. Barn swallows have shown a dramatic change in body condition associated with recent climatic change (Møller AP, unpublished data). This increase in body condition of breeders should improve their ability to fend off potential infanticidal males from nests. In addition, when environmental conditions are favorable during migration, many barn swallows of poor phenotypic quality survive (Møller AP, unpublished data), and this should result in the presence of many potential infanticide perpetrators, but also in many potential victims that are unable to defend their nests.
The barn swallow is a approximately 18-g, migratory, semicolonial passerine that breeds commonly throughout most parts of the Palearctic and Nearctic temperate regions. Previous studies of infanticide in this species have shown that this is a common cause of nestling mortality (Crook and Shields, 1985; Møller, 1988). Previous studies have shown that infanticide occurs in two different contexts. First, the male nest owner dies and the live nestlings are ejected by the replacement male. This category comprise most of the reported cases of infanticide (Crook and Shields, 1985; Møller, 1988). Because female barn swallows are fully able to successfully rear nestlings on their own (Møller, 2000), females are likely to have greater reproductive success in the absence of infanticide, because infanticide causes a delay in reproduction. Second, the male nest owner is replaced by another male, which subsequently throws out live nestlings from the nest. This category is rarer than the first one but, nevertheless, contributes significantly to the total number of cases of infanticide (Crook and Shields, 1985; Møller, 1988). Adult barn swallows avoid infanticide by guarding their nests against potential infanticide perpetrators, and removal of adults from their nests for even short periods of time increases the frequency of infanticide (Møller, 1988). Infanticide is more common in large colonies than in small colonies or among solitary barn swallows because unmated males aggregate in large colonies owing to the larger probability of finding a potential infanticide victim in colonies (Møller, 1988). Therefore, the intensity of anti-infanticide nest guarding increased with colony size as the risk of infanticide increased (Møller, 1988). Perpetrators are usually short-tailed, unmated, yearling males, and successful perpetrators tend to have longer tails than unsuccessful males (Møller, 1994).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study area
I studied barn swallows at Kraghede (57°12' N, 10 °00' E), Denmark (since 1970), as part of a long-term project. Detailed information on infanticide has been collected from 1977–2002. The total study area covered approximately 30 km2 from 1977–1986, 45 km2 from 1987–1997, and 55 km2 from 1998–2002. These increases occurred to compensate for the reduction in population size over the years. The study site at Kraghede consists of open farmland with pastures, cereals, potatoes, and rape with mixed plantations, hedges, and ponds. Barn swallows breed within barns and other buildings (for further details, see Møller, 1994
).
Assessing the frequency of infanticide
Infanticide was recorded in either of two ways. First, direct observations of removal of nestlings during regular nest observations provided unambiguous evidence of infanticide. This occurred in a total of 17 cases during the years. Among these 17 cases, 11 were owing to a new male pecking and/or removing nestlings from a nest, where the male nest owner had disappeared, whereas the remaining six cases were owing to a male ousting a male nest owner and subsequently pecking and/or removing live nestlings from the nest. Cases of nest failure in which nestlings die, the male nest owner subsequently disappears, and a replacement male throws out the dead nestlings have never been recorded. In fact, nests with dead nestlings are generally deserted by both nest owners, and the dead nestlings can remain in such nests for several years. Second, sudden disappearance of nestlings during their first week of life is associated with the appearance of a new male as the nest owner, when infanticide takes place (Crook and Shields, 1985; Møller, 1988). Mate replacement occurs because the original male either died or disappeared owing to divorce. Therefore, these characteristic events can be used to indirectly infer the occurrence of infanticide. Other causes of sudden disappearance of nestlings are rare and include rare cases of nest predation by house sparrows, Passer domesticus, or nest destruction. Neither of these events is associated with male replacement. I checked nests at least weekly and usually daily around the supposed time of laying and hatching. Thus, nests were checked at regular intervals throughout the study. The number of first clutches per year ranged from 27–186, with a mean value of 98 clutches per year.
Capturing adults and recording their phenotype
Barn swallows were captured at least weekly from arrival in spring until the end of the breeding season by using mist nets at all entrances to the barns with breeding birds. Mark–recapture analyses of the data have revealed that the capture probability of birds exceeds 98% (Møller and Szép, 2002). The number of adults captured were therefore slightly more than twice the number of first clutches (see above) because unmated males were also captured.
Upon capture, all adults were measured for a large number of phenotypic characters, recorded in a similar standardized way upon first capture. In the present study, I only used body mass, recorded with a Pesola spring balance to the nearest 0.1 g, and the length of the outermost tail feathers recorded with a ruler to the nearest millimeter. Repeated measurements of the same individuals in the same season or over different seasons revealed a repeatability of more than 90% (Møller, 1994; Møller AP, Cadee N, unpublished data).
All individuals were only included in their first year of capture, which can be considered to equal their first year of life. The latter statement is justified by the fact that among 160 local recruits ringed as nestlings in the study area, all with the exception of a single individual were recaptured as 1-year-old breeding birds. The single exception was recaptured as 2 years old. Likewise, breeding site fidelity is extremely high, with only four of 3057 adults ever moving to another breeding farm, and then in all cases to the nearest neighboring farm (maximum distance moved = 400 m). The use of each individual only once prevents any pseudo-replication. All individuals that were included in experiments were excluded, unless they belonged to untreated control groups. This should not cause any bias because treatments were assigned randomly to individuals.
Estimating reproductive success
Breeding barn swallows have been censused in the study area since 1970. Intensive searches for nest sites have been made weekly and all nestlings were ringed when 12–14 days old. The number of breeding pairs was estimated as the number of pairs building nests.
Reproduction of barn swallows was recorded during regular visits to nests throughout the breeding season, often daily around the time of laying, hatching, and fledging, but at least twice per week. I recorded all cases of nestling mortality, and these were attributed to infanticide as described above or to other causes.
All reproductive events were recorded in all years.
Estimating the frequency of unmated males
Male barn swallows defend a territory upon arrival and attempt to attract a female to this territory (Møller, 1994). Unmated males remain in their breeding territory during the breeding season, until the end of the first brood in late July, when they start deserting the breeding colonies while moving away and sleeping at communal roosts (Møller, 1994). Unmated males are very conspicuous in their behavior by singing considerably more than mated males. They also chase mated females repeatedly and commonly attempt extrapair copulations. In addition, they visit neighboring nests, where they attempt to remove nestlings to induce divorce between the female and the male nest owner. I estimated the frequency of unmated males as the number of males without a female. Almost all unmated males were ringed during the regular catching events.
Normalized Difference Vegetation Index
I estimated environmental conditions during migration and winter from the Normalized Difference Vegetation Index (NDVI), based on satellite images indicating the condition of rainfall-dependent vegetation in space and time (Prince and Justice, 1991). NDVI provides a measure of the amount and vigor of vegetation at the land surface that is directly related to the level of photosynthetic activity (Prince and Justice, 1991). Because many migratory birds rely directly on insects for food, which in turn depend on plant productivity, the NDVI is likely to reflect the abundance of insect food. This is particularly likely to be the case for species such as the barn swallow that rely on swarming insects such as termites that become active in direct response to precipitation. NDVI is derived from data collected by National Oceanic and Atmospheric Administration (NOAA) satellites and processed by the Global Inventory Monitoring and Modeling Studies at the National Aeronautics and Space Administration (NASA; Prince and Justice, 1991). Vegetation indices derived from the NOAA Advanced Very High Resolution Radiometer sensor have been used for both qualitative and quantitative studies of numerous phenomena related to the condition of the vegetation (Tucker et al., 1991). NDVI can be used as an indicator of relative biomass and greenness of the vegetation (Boone et al., 2000; Chen, 1998; Paruelo et al., 1997), precipitation (Schmidt and Karnieli, 2000), and quantity and quality of bird habitats (Wallin et al., 1992). Maurer (1994) indicated a correlation between abundance of birds and NDVI, and NDVI has the potential to be used for mapping bird distributions at large spatial scales (Osborne et al., 2001). The NDVI data are available at NASA for the entire African continent at http://edcintl.cr.usgs.gov/adds/adds.html. These images are calibrated for intersensor and intrasensor degradation for the period 1982–2001.
The NDVI data for each pixel, which covers 8 x 8 km (64 km2), were extracted from the Web site. They were then averaged to obtain a mean value for each square of 0.25 x 0.25 degrees and for each period (fall [September–November], winter [December–February], and spring [March–May]) using the WinDisp v4.0 software (http://www.fao.org/WAICENT/faoinfo/economic/giews/english/windisp/windisp.htm). NDVI data were calculated for squares in which at least 30% of the pixels had valid data. I only included squares in the analyses if there was NDVI data available for each year for which we had survival estimates. This excluded 15% of the approximately 40,000 squares in Africa.
Analyses of NDVI across Africa revealed six areas that explained significant amounts of variance in annual adult survival rate estimated from capture–mark–recapture analyses (Møller AP and Szép T, unpublished data). Two of these areas identified through correlation analysis with annual adult survival rates showed a high consistency with the distribution of recoveries of ringed birds (South Africa in spring and Algeria in spring). Subsequent analyses of these data only revealed significant relationships between infanticide and NDVI in Algeria in spring, even when using sequential Bonferroni correction.
Statistical analyses
The measurements were used to calculate annual means and standard errors for each character. Because these values were based on yearlings only, each single estimate can be considered to represent the estimate for a generation.
I used multiple linear regression to tease apart the independent effects of two factors influencing a dependent variable. Collinearity between variables can cause problems, but when r <.70 as in the present study, this is generally not considered problematic (Green, 1979).
We adjusted the degrees of freedom for tests of significance of correlation coefficients for temporal autocorrelation (Bartlett, 1952), ensuring that the adjusted degrees of freedom was equal to the actual sample size.
Values reported are means (SE).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Infanticide was a relatively rare event, affecting on average 1.807% of all nests (SE = 0.395, N = 25 years). During the period 1977–2002, my assistants and I witnessed a total of 17 cases, and an additional 21 cases were inferred according to the criteria listed in the Methods.
The frequency of infanticide decreased significantly during the period 1977–2002 (Figure 1). Although most early years had frequencies of infanticide ranging from 2–5% of all first clutch nests, this frequency decreased significantly to none in most recent years (Figure 1).
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Unmated males are the perpetrators of infanticide, and the frequency of infanticide should therefore increase with the abundance of unmated males. Indeed, infanticide increased significantly with the frequency of unmated males (Figure 2A). Infanticide should increase with increasing population density because shorter distances to the nearest neighbor will allow closer monitoring of neighbors, and it will result in more intense male-male competition. The frequency of infanticide increased significantly with population size (Figure 2B). Unmated males were significantly more abundant when the barn swallow population was large (Figure 3). The independent effects of the frequency of unmated males and population density on frequency of infanticide were investigated in a multiple linear regression. A multiple linear regression model with infanticide as the dependent variable and the frequency of unmated males and population size as independent variables revealed significant partial regression coefficients for both variables (Table 1). The frequency of infanticide increased with the abundance of unmated males and, to a smaller extent, population size.
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I predicted that infanticide was negatively related to male condition because males in better condition should be better able to guard their nests efficiently against the approach of unmated males. Indeed, I found a significant negative relationship between the two variables (Figure 4A). Because male tail length is a condition-dependent character, I also predicted a negative relationship between male tail length and the frequency of infanticide. This prediction was upheld because the frequency of infanticide was significantly negatively correlated with mean tail length of all yearling males (Figure 4B). Because the frequency of unmated males and body condition were positively correlated with each other (r =.622, N = 18, p <.01), I investigated the independent importance of frequency of unmated males and body condition as predictors of infanticide in a multiple regression. This analysis revealed a significant positive effect of the frequency of unmated males on the frequency of infanticide (Table 2). Body condition as reflected by body mass upon arrival of all yearling males had an independent significant negative effect on the frequency of infanticide (Table 2). Thus, the frequency of infanticide was predicted by both the abundance of potential perpetrators and the ability of breeding birds to defend themselves against infanticide attempts.
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Nestling mortality in first broods was on average 9.44% (SE = 1.29, N = 25 years). Nestling mortality owing to infanticide was 1.81% (SE = 0.40, N = 25 years), which equals 16.40% of all nestling mortality (SE = 4.74, N = 25 years). Nestling mortality owing to infanticide increased significantly with population size, accounting for more than 25% of all nestling mortality in years with high population density, but considerably less in other years (Fig. 5). Thus, mortality owing to infanticide acted in a density-dependent manner.
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Infanticide was significantly more common in years when environmental conditions were benign during spring migration in the North African staging areas (Figure 6). Survival rate was high in years with high NDVI (Møller AP and Szép T, unpublished data), and high survival rate may particularly have resulted in more breeders and nonbreeders of poor quality surviving. If more poor-quality individuals survived in years with high NDVI, then unmated males may have a larger probability of being successful in committing infanticide. This explanation was supported because tail length of male barn swallows was significantly negatively related to NDVI in Algeria during spring migration (F = 13.334, df = 1,16, r2 =.455, p =.0022, slope [SE] = –73.241 [20.060]). Likewise, if more males survive years with favorable environmental conditions, the frequency of potential infanticide perpetrators could increase. However, the frequency of unmated males was not significantly predicted by NDVI in Algeria during spring migration (F = 2.102, df = 1,16, r2 =.116, p =.166). This suggests that the effect of unmated males on the frequency of infanticide was not owing to a direct effect of NDVI on the abundance of unmated male barn swallows.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Frequency of infanticide in the barn swallow decreased dramatically during a period of 25 years, affecting 2–5% of all nests at the beginning of this period, but hardly any in recent years (Figure 1). The causes of this change in frequency appear to be a dramatic reduction in population size during recent years (Engen et al., 2001
) and a reduction in the frequency of unmated males (Figure 2). Unmated males were more common when the population was large (Figure 3). However, the effects of population size on infanticide did not act only through the abundance of unmated males. A multiple regression analysis revealed that both of these factors had independent effects on the frequency of infanticide (Table 1). Although the abundance of unmated males accounted for 28.7% of the variance, population size accounted for 20.5% of the variance. Thus, a large population increased the risk of infanticide independent of the number of unmated males present. A likely explanation is that large populations appear in years when selection during winter and migration is weak, leaving many individuals of poor phenotypic quality in the breeding population. Such individuals are likely to be less able to defend their nests against potential infanticide perpetrators than are high-quality individuals.
Recent microevolutionary change in tail length of male barn swallows is associated with climatic change during spring migration from the winter quarters in South Africa via North Africa to Denmark (Møller AP and Szép T, unpublished data). More intense selection in recent years with adverse environmental conditions has resulted in a dramatic increase in average tail length of male barn swallows by more than 1 SD, a secondary sexual character associated with several mating advantages through female choice (Møller, 1994). Because the breeding value for tail length has increased during the study period, this implies a genetic change in the population over the study period (Møller AP and Szép T, unpublished data). Tail length is a condition-dependent character, with individuals in prime condition having much longer tails than do individuals in poor condition (Møller, 1994), and therefore, body mass of males has also increased in recent years (Møller AP, unpublished data). Males with long tails and in prime condition are likely to be better able to defend their nests against infanticide perpetrators because such males should be of high phenotypic quality. In accordance with this prediction, the frequency of infanticide decreased as mean tail length became longer and achieved higher mean body condition as reflected by their larger body mass (Figure 4). The relative importance of the abundance of unmated males and body mass of mated males as determinants of infanticide was evaluated in a multiple regression analysis. Both factors were important predictors of infanticide. Infanticide was more common when unmated males were abundant, but less common when males were in better condition (Table 2). Thus, the two factors were of similar magnitude, with the first being associated with an increase in infanticide, and the second was associated with a decrease in the frequency of infanticide.
Infanticide accounted for more than 16% of all nestling mortality in the first broods of barn swallows. However, this effect changed considerably in relation to population size, with nestling mortality caused by infanticide accounting for more than 50% of all nestling mortality in three of the 25 years (Figure 5). Nestling mortality in general was low in barn swallows compared with many other species, in which nest predation and other causes of mortality are common. Thus, it seems likely that other species with a relatively large importance of infanticide will include species with hole nests such as the house sparrow, P. domesticus, and the tree swallow, Tachycineta bicolor (Robertson, 1990; Veiga, 1990). Likewise, species severely limited by access to breeding territories such as many tropical species are likely to suffer from relatively high rates offspring mortality owing to infanticide (Emlen et al., 1989; Freed, 1987).
The frequency of infanticide appeared to be related to climatic conditions during spring migration and thus to climatic change. Barn swallows from the Danish population pass through North Africa after crossing the Sahara desert. In years with benign environmental conditions in North Africa, adult survival rate is high (Møller AP, unpublished data). However, environmental conditions did not explain variation in the frequency of unmated males among years. Tails of male barn swallows are short in benign years, suggesting that many individuals of poor phenotypic quality are breeding but unable to defend their nests against infanticidal males. Thus, the frequency of infanticide is high in years with benign environmental conditions during spring migration in Northern Africa, apparently because levels of nest defense against infanticide are low. The alternative explanation that unmated males were more common in such years was not supported by the data.
Infanticide has the potential to cause an increase in stochastic variation in population size. The reason for this is that unmated males (or other infanticide perpetrators in other species) can increase the demographic variance owing to individual variance in births and deaths (Møller, 2003). Both natural cases of infanticide (the present study) and infanticide caused by man (Swenson et al., 1997) can increase the variance in recruitment among individuals, because reproductive success by certain individuals is eliminated through infanticide. In addition, subsequent reproductive events by infanticidal individuals are likely to be delayed as compared to the situation if infanticide had not taken place. Because reproductive success generally decreases with date of reproduction (Lack, 1954), reproduction involving individuals that have committed infanticide will generally be less successful than average reproductive success in the population. Such increases in variance can have important implications for demographic stochasticity and, hence, for the survival of populations (Lande et al., 2003). Previous studies of population viability have generally only considered variance in recruitment among females, neglecting any male effects on variance components (Møller, 2003). Infanticide is one such component owing to males that at least in some species can affect reproductive success.
In conclusion, infanticide in the barn swallow was closely associated with the abundance of males that commit infanticide, but also with the ability of breeders to guard and defend their nests against potential perpetrators. The latter ability was mainly determined by the intensity of natural selection during spring migration in Northern Africa, because many individuals of poor phenotypic quality survived under benign environmental conditions. Thus, infanticide could be predicted by climatic change during spring migration in this migratory bird. These findings show that environmental conditions far from the breeding grounds can have profound effects on reproductive strategies several months later.
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ACKNOWLEDGEMENTS |
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N. Cadée, E. Flensted-Jensen, and C. Spottiswoode kindly helped with fieldwork. My research was supported by a grant from the European Community (METABIRD, contract no. EVK2-CT-1999–0017 METABIRD).
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