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Journal of Ornithology

, Volume 160, Issue 1, pp 137–144 | Cite as

Extra-pair paternity in socially monogamous Streaked Shearwaters: forced copulation or female solicitation?

  • Miho SakaoEmail author
  • Hirohiko Takeshima
  • Koji Inoue
  • Katsufumi Sato
Original Article

Abstract

Seabirds are long-lived birds that invest in offspring at very high levels, for which male parental care is indispensable. These characteristics are thought to explain seabirds’ generally low level of extra-pair paternity (EPP). Although the Streaked Shearwater (Calonectris leucomelas) is a socially monogamous seabird, it is known to copulate outside its social pair bond, which implies the frequent occurrence of EPP. In the closely related Cory’s Shearwater Calonectris borealis, cuckoldry is related to body size of the social male. To determine whether body-size-related EPP occurs among Streaked Shearwaters, we established 39 new microsatellite markers for parentage analysis and compared body size between cuckolded and non-cuckolded males. With the new markers, we found that extra-pair males sired 17 (15.0%) of 113 offspring during the 2014–2016 study period, which included three 1.5-month chick-rearing periods. This percentage is among the highest recorded for seabirds. We also found the bill and wing length of cuckolded males to be significantly shorter than those of non-cuckolded males, and that females can reject attempted copulations. These observations imply that EPP in this species is size related and involves female acceptance.

Keywords

Extra-pair copulation Microsatellite Pair bond Parental care Cuckoldry 

Zusammenfassung

Fremdvaterschaft bei sozial monogamen Weißgesicht-Sturmtauchern: erzwungene Kopulation oder weibliche Aufforderung?

Seevögel gehören zu den langlebigen Vogelarten, welche in hohem Maße in ihre Nachkommen investieren, was eine väterliche Fürsorge unerlässlich macht. Diese Eigenschaften sollen den generell geringen Grad an Fremdvaterschaften (engl. extra-pair paternity, EPP) bei diesen Vögeln erklären. Obwohl der Weißgesicht-Sturmtaucher (Calonectris leucomelas) zu den sozial monogamen Seevögeln gehört, sind bei dieser Art Kopulationen außerhalb des sozialen Paarbundes bekannt, was ein häufiges Auftreten von EPP nahelegt. Beim nahverwandten Gelbschnabel-Sturmtaucher Calonectris borealis hängt das Fremdgehen mit der Körpergröße des sozialen Männchens zusammen. Um festzustellen, ob eine körpergrößenbezogene EPP beim Weißgesicht-Sturmtaucher vorkommt, haben wir 39 neue Mikrosatellitenmarker für die Vaterschaftsanalyse etabliert und die Körpergröße zwischen „betrogenen“und „nicht betrogenen“Männchen verglichen. Mit den neuen Markern konnten wir zeigen, dass Männchen außerhalb des Paarbundes 17 (15,0%) von 113 Nachkommen während des Untersuchungszeitraumes 2014-2016 zeugten. Der Untersuchungszeitraum umfasste drei Jungaufzuchten von jeweils 1,5 Monaten. Dieser prozentuale Anteil gehört zu den größten, die bislang bei Seevögeln ermittelt wurden. Weiterhin haben wir festgestellt, dass Schnabel- und Flügellänge der „betrogenen“Männchen signifikant kürzer als bei den „nicht betrogenen“Männchen waren. Zudem zeigte sich, dass Weibchen Kopulationsversuche abwehren können. Unsere Beobachtungen lassen bei dieser Art eine größenbezogene EPP vermuten, bei der die Akzeptanz des Weibchens erforderlich ist.

Introduction

Although most bird species are socially monogamous, genetic studies have revealed extra-pair paternity (EPP) in an increasing number of species, and thus social monogamy is distinguished from genetic monogamy (Griffith et al. 2002). EPP reflects the conflicts of interest in reproduction between males and females. Males can increase their reproductive success substantially by siring extra-pair offspring (Trivers 1972; Griffith et al. 2002). Females in some species may increase the number and genetic quality of their offspring through extra-pair copulation (EPC) (Griffith et al. 2002; Westneat and Stewart 2003). However, females in other species obtain no benefit from EPC, and EPP can even occur by forced copulation (Jouventin et al. 2007; Hsu et al. 2015). Thus, the reasons for EPC are not as clear for females as they are for males (Forstmeier et al. 2014).

Application of molecular genetics tools to the study of avian breeding systems has revealed striking variation in the level of EPP within socially monogamous bird species (Petrie and Kempenaers 1998; Wink and Dyrcz 1999), ranging from no EPP, e.g., in the Western Gull (Gilbert et al. 1998) to over 55% of chicks being sired through EPC, e.g., in the Reed Bunting (Andrew et al. 1994; Griffith et al. 2002). Although EPP occurs in the vast majority of bird species, fewer than 10% of the approximately 450 seabird species have been studied for EPP, and the average degree of EPP documented in seabirds thus far (6.2%) is much lower than the average documented across all bird species [21.5% (Quillfeldt et al. 2011)]. Theory predicts that females of species in which parental care is important for successful breeding will not engage in EPC (Trivers 1972; Griffith et al. 2002; Bried et al. 2010). Seabirds show very high levels of parental investment, and male parental care is indispensable for this, which might be one of the reasons why the level of EPP is generally low among seabirds (Griffith et al. 2002; Quillfeldt et al. 2011). In addition, the existing variation in EPP rates between conspecific populations and between years within the same population (Petrie and Kempenaers 1998; Wink and Dyrcz 1999) suggests that some extrinsic factors promote EPCs (Hoi-Leitner et al. 1999; Bried et al. 2010). For example, in Cory’s Shearwater, the variation in the EPP rate between three populations ranged from 0 to 11.6% (Bried et al. 2010; Rabouam et al. 2000; Swatschek et al. 1994).

In Procellariiformes, an order of seabirds comprising albatrosses, petrels, and shearwaters, body size-related traits may influence reproductive performance and may also indicate individual quality. A relatively large bill, for example, is advantageous to both sexes in defending their nests (Navarro et al. 2009; Nava et al. 2014). In Cory’s Shearwater, a species closely related to the Streaked Shearwater, smaller vs. larger males tend to be cuckolded, which implies that larger males may have advantages for male–male competition (Bried et al. 2010). In some seabird species, assortative mating by body size has been documented (Einoder et al. 2008; Wojczulanis-Jakubas et al. 2018). In other, terrestrial, bird species, female preference towards larger males exists and EPP is female driven (Kempenaers et al. 1997). However, among Wandering Albatross (Diomedea exulans), the main cause for EPP might be forced copulation (Jouventin et al. 2007). Sexual size dimorphism is considerable in this species, therefore rejection of EPC risks injury to the female (Jouventin et al. 2007).

Streaked Shearwaters (Calonectris leucomelas) are long lived, socially monogamous seabirds that produce a single offspring per season. They are burrow-nesting shearwaters that breed in colonies on isolated islands in East and Southeast Asia between April and early November. Regardless of their high parental investment, they frequently copulate outside their social pair bonds, but within colonies, in June; we have recorded video data (M. Sakao personal observation; Supplemental video 1) of this. However, the criteria for choosing a mate remains poorly understood in Streaked Shearwaters (Yoshida 1981), and parentage analysis has been hampered by a lack of highly sensitive molecular markers such as microsatellite DNA. We developed 39 novel microsatellite DNA markers using next-generation sequencing (NGS) techniques to determine the rate of EPP in Streaked Shearwaters and compared morphological traits between cuckolded and non-cuckolded males to identify the occurrence of size-related EPP in this species.

Methods

Field study

Data was gathered from a Streaked Shearwater breeding ground at Funakoshi-Ohshima Island, northern Japan (141.99°E, 39.40°N) between 2014 and 2016. The study included three incubation and chick-rearing periods, each of which lasted from early September to early October. During these periods, we caught adult birds (n = 338) and offspring (n = 199) in their nests by hand and collected from five to ten feathers from the breast of each individual. DNA was extracted from each feather and stored in 100% ethanol. The nests were marked with numbered flags. Before releasing the adults back to their nest, we recorded bill length and depth, total head length, and tarsus length (to the nearest 0.1 mm with a Vernier caliper) as described by Arima and Sugawa (2004) and wing length (to the nearest 1 mm with a ruler) of both males and females to compare morphological traits of cuckolded and non-cuckolded males, and those of females with and without an extra-pair chick. We collected the feathers from adult birds during the incubation period and the chick-rearing period. To avoid any disturbance that would change the birds’ behavior during the incubation period, we did not measure their bodies at this time. During the chick-rearing period, however, we measured adult body size. Therefore, there is a difference in sample size between males and females. Between-group differences in morphological traits were analyzed by means of the Mann–Whitney U-test. Data covering both males and females of 25 breeding pairs including pairs with extra-pair young and 20 pairs in which cuckoldry had not occurred were used for analysis of assortative mating. The within-pair correlation was examined by means of Pearson correlation testing executed by R version 3.3.3. Significance for all statistical tests was accepted at P < 0.05.

Numbered metal rings were used to identify social parents during subsequent encounters with families in the field. We checked nests every 3–5 days during the chick-rearing periods to identify the breeding adults in each nest. If a certain individual was seen in the same numbered nest more than twice, that individual was designated as the social mother or father of the chick. Individual adult birds occasionally used a nesting burrow of other birds. Therefore, when two or more adults of the same sex were seen in a particular nest, we checked the nest every 2–3 days until a specific individual of each sex was caught there more than four times, and those individuals were designated as the breeding adults.

Development of microsatellite markers

We constructed a mixed sequencing library with two types of NGS libraries, i.e., a shotgun library and a microsatellite-enrichment library, as described previously (Takeshima et al. 2017), and we sequenced the mixed library using a 454 GS Junior System (Roche Diagnostics, Basel, Switzerland). We obtained 38,301 sequences from the NGS run with an average sequence length of 400 base pairs. The output standard flowgram format file is available in the DNA Data Bank of Japan Sequence Read Archive under accession number DRA005324. We detected 7245 microsatellite-containing sequences and sufficient numbers of primer sets to develop microsatellite markers (2420 sequences).

We screened the 111 designed primer pairs for Streaked Shearwater. Single-locus polymerase chain reactions (PCR) were performed with respect to four individuals in a reaction mixture with a total volume of 7 μL and containing 1× GoTaq Green Mastermix (Promega, Madison, WI), 0.2 μM of each primer, and approximately 50–300 ng of template DNA. The thermal cycling protocol consisted of denaturation at 95 °C for 5 min, followed by 40 cycles of 94 °C for 15 s, 59 °C for 15 s, and 72 °C for 30 s; and a final extension at 60 °C for 7 min. PCR products were separated by electrophoresis on 2% agarose gels. Of the 111 primers, 56 were successfully amplified and subsequently tested for polymorphisms in a total of 129 adult individuals. To facilitate multiplex PCR, the forward primer for each locus was synthesized with one of four tail sequences (Table S1; see also Blacket et al. 2012) with fluorescence-labeled forward primers.

Primer sets were amplified in seven multiplex PCR reactions (Table S1). Multiplex PCRs were performed with a Type-it Microsatellite PCR Kit (QIAGEN, CA) in a 7-μL reaction mixture containing the forward, reverse, and universal tail primers in a 1:2:1 ratio (Blacket et al. 2012); each universal tail primer was fluorescently labeled with 6-FAM, VIC, NED, or PET (Applied Biosystems, CA). The final concentration of each primer was optimized for each marker (Table S1). The thermal cycling protocol consisted of denaturation at 95 °C for 5 min, followed by 40 cycles of 94 °C for 15 s, 59 °C for 15 s, and 72 °C for 30 s, and a final extension at 60 °C for 30 min. A 2-μL volume of PCR product was mixed with 0.3 μL GeneScan 500 LIZ dye Size Standard (Applied Biosystems) and 9.7 μL Hi-Di formamide. Alleles were separated by means of capillary electrophoresis on an ABI 3130xl Genetic Analyzer, and sizes were assigned with the use of GeneMapper 3.7 software (Applied Biosystems).

The number of alleles (Na), observed heterozygosity (Ho), and expected heterozygosity (He) were assessed with the use of Cervus 3.0.7 (Marshall et al. 1998). Departures from Hardy–Weinberg equilibrium (HWE) and linkage disequilibrium among loci were tested, and a Markov chain method was applied with the following chain parameters: 10,000 dememorization steps, 100 batches, and 5000 iterations per batch with the use of GENEPOP 4.2.0 (Raymond and Rousset 1995; Rousset 2008). To avoid a type I error, a sequential Bonferroni correction (Rice 1989) was applied to P-values from multiple tests. The presence of null alleles at each locus was checked with Micro-Checker 2.2.3 (van Oosterhout et al. 2004), which was also used to calculate null allele frequencies at each locus. The probability of observing identical multilocus genotypes between two individuals sampled from the same population (probability of identity, PID) and the polymorphic information content (PIC) were calculated with Cervus 3.0.7.

Genotyping for parentage analysis

The microsatellite markers were used to obtain genetic profiles for each sampled bird and to assign parentage. We combined fluorescence-labeled primer pairs into multiplexes and typed 39 variable microsatellite markers (Table S1). Multiplex PCRs were carried out as described above.

Parentage analysis

We checked the parentage of chicks whose social parents were identified. The number of chicks studied per year varied from 23 to 49 (Table 1). For each candidate mother, we accepted three mother–offspring mismatches with a 5% error rate. This was the basis upon which we designated the social mothers as genetic mothers of offspring. For each candidate male, we used Cervus 3.0.7 to calculate the natural logarithm of the likelihood ratio (LOD score), which is an estimate of the probability that the candidate male is the genetic sire of the offspring relative to the likelihood that a randomly chosen individual from the study population is the genetic sire. We used simulations from allele frequency data in the population to calculate the critical differences in LOD scores (ΔLOD) between the two most likely candidate males that were necessary for assignment with 95% confidence. Simulations were run for 10,000 cycles. If the LOD score was significantly higher than that for the second-highest-ranked candidate male, paternity was assigned to the highest-ranked male. If the LOD score for the highest-ranked male was similar and not significantly different from scores for other males, all candidate males with a positive LOD score were considered potential sires. If the LOD score of the social male was a negative number, we called its social chick an extra-pair chick.
Table 1

Information related to the total offspring studied during the three annual chick-rearing periods

Year

Chicks with social father of known genotype

Within-pair chicks

Chicks with unknown genetic father

Extra-pair chicksa

% Extra-pair chicksa

2014

49

37

7

5

10.2

2015

23

8

11

4

17.4

2016

41

26

7

8

19.5

Total

113

71

25

17

15.0

Number of offspring is shown

aIndividuals whose genetic father and social father are different

Results

Genetic markers

For the 39 variable loci, the genetic variability parameters Na, He, and Ho ranged from 2 to 14, 0.005–0.728, and 0.005–0.741, respectively. According to the Micro-Checker-based analysis, five loci (Cale-012, Cale-025, Cale-027, Cale-030, Cale-072) exhibited an apparent excess of homozygotes across all allele classes (Table S1). No markers showed significant deviation from HWE after sequential Bonferroni correction, and, after such correction, significant linkage disequilibrium was not found for any of the pairs. The PID values per locus are shown in Table S1, and the combined PID was estimated to be 2.08 × 10−11 (Table S1). Among the 39 polymorphic markers, PIC values ranged from 0.01 to 0.688, two markers were highly informative (PIC > 0.5; Cale-002, Cale-023) and 17 markers were reasonably informative (0.5 > PIC > 0.25) according to the classification system of Botstein et al. (1980) (Table S1).

EPP ratio and morphological traits of social males

We obtained the genotype at the 39 loci for 49 complete families (i.e., the two parents and their single chick) in 2014, for 23 in 2015, and for 41 in 2016, so we checked the paternity of 113 chicks in 3 years. Of the total 83 social male–female pairs, 12 pairs were captured and then recaptured during two subsequent chick-rearing periods, and nine pairs were captured during three subsequent chick-rearing periods. The social partners were designated the most probable genetic fathers of 71 chicks (within-pair chicks, 62.8%; Table 1). However, in 25 cases, LOD scores of the social fathers were similar to those of other candidate fathers, as assigned by Cervus. According to our predefined criteria, we categorized each of these nestlings as “a chick with an unknown genetic father.” Of the total 113 chicks, we found 17 extra-pair chicks. The EPP rate varied from 10.2 to 19.5% between 2014 and 2016 (Table 1). Extra-pair sires were identified for four of the 17 extra-pair offspring. In two nests, EPP occurred twice from 2014 to 2016 (for details, see Table S2). Only one male sired an extra-pair offspring and lost paternity in his own nest. None of the extra-pair chicks were neglected by paired males, and they all fledged at the end of October in all 3 years.

We found the bills, head, and wings of cuckolded males (n = 9) to be significantly shorter than those of non-cuckolded males (n = 30) P < 0.05 (U = 67), P < 0.01 (U = 41.5), and P < 0.05 (U = 74.5), respectively, by Mann–Whitney U-test (Fig. 1). There were no significant differences in morphological characteristics between females with (n = 8) and females without (n = 28) an extra-pair chick (Fig. S1). We did not find any evidence for assortative mating by body size in Streaked Shearwater (Table 2).
Fig. 1

Presence (n = 9) and absence (n = 30) of extra-pair chicks in relation to the social male’s bill length (a), head length (b), tarsus length (c), wing length (d), and bill depth (e). Box plots show the median value, range, 25th and 75th percentiles, and outliers. P- and U-values were obtained by Mann–Whitney U-test

Table 2

Results of correlation analysis of within-pair morphological traits of Streaked Shearwater

Measurement

Males

Females

n (pairs)

r

P value

Bill length (mm)

51.87 ± 1.59 (52.13 ± 1.56)

48.20 ± 1.26 (48.20 ± 1.38)

25 (20)

0.17 (0.29)

0.43 (0.22)

Bill depth (mm)

12.62 ± 0.57 (12.62 ± 0.55)

11.31 ± 0.70 (11.30 ± 0.73)

25 (20)

− 0.11 (0.04)

0.6 (0.87)

Head length (mm)

104.41 ± 1.66 (104.70 ± 1.64)

98.37 ± 2.10 (98.29 ± 2.14)

25 (20)

0.03 (0.12)

0.91 (0.62)

Tarsus length (mm)

53.48 ± 1.15 (53.56 ± 1.13)

51.75 ± 1.59 (51.83 ± 1.70)

25 (20)

0.36 (0.39)

0.08 (0.092)

Wing length (mm)

322.41 ± 7.42 (323.92 ± 7.33)

318.01 ± 8.86 (317.96 ± 9.66)

25 (20)

0.28 (0.28)

0.18 (0.24)

Mean ± SD values are shown. r-values are Pearson correlation coefficients. Results from pairs without extra-pair chicks are shown in parentheses

Discussion

In our study of Streaked Shearwater, we found 10.2–19.5% EPP. Although this rate is low relative to that of a highly promiscuous species, it is high in comparison to the average level of EPP in seabirds studied thus far [6.5% (Quillfeldt et al. 2011); see also Fig. 2]. Given the importance of male parental care, female seabirds can avoid or refuse EPCs to avoid the risk of losing the investment by their partners (Quillfeldt et al. 2001, 2011). However, during the 3-year study period, none of the extra-pair chicks we observed were neglected by paired males, and all 17 fledged by the end of October. Therefore, males may not be aware of the EPCs of their social partners. Indeed, observed EPCs occurred away from the nests (Yoshida 1981; M. Sakao, personal observation). Social pairs stayed in their nests together at night during the mating period, but often the mates returned to their nests separately from their foraging trips and would occasionally forage in different areas (Yamamoto et al. 2011; M. Sakao, personal observation). Therefore, if females participate in or accept EPC outside of the nest, paired males may be unaware of it. In this study, we identified extra-pair sires for only four of 17 extra-pair chicks. We marked 121 nests in our study colony. However, the number of adult birds at the study site was estimated to be close to 1000 (Oka 2004). Therefore, we genotyped only ca. 10% of the Funakoshi-Ohshima Island Streaked Shearwater population, so many potential extra-pair sires may not have been sampled.
Fig. 2

Prevalence of extra-pair paternity in seabirds relative to that of other bird species (Other birds)

[Data for other birds were extracted from Table S15 in Cornwallis et al. (2010). Data for seabirds were extracted from Table 1 in Quillfeldt et al. (2011) and Table S15 in Cornwallis et al. (2010)]

Jouventin et al. (2007) suggested that EPC in Wandering Albatross (10.8% EPP) is beneficial to males, but that it occurs randomly in females, which is consistent with the hypothesis that EPP results from forced EPCs. Although Streaked Shearwater exhibits significant sexual size dimorphism (Arima et al. 2014), female shearwaters seem capable of warding off forced copulation (Supplemental video 2). We found no significant differences in morphological traits between females with extra-pair chicks and those with within-pair chicks (Fig. S1). From this perspective, it appears that EPP in Streaked Shearwater may not be the result of forced copulation. A prior study by Petrie and Kempenaers (1998) indicated that if females control the success of copulation attempts, the costs and benefits of EPP to females will largely dictate the level at which it occurs. Interestingly, smaller males were more likely to lose paternity than larger males (Fig. 1). This phenomenon also occurs in some short-lived terrestrial bird species (Kempenaers et al. 1997; Verboven and Mateman 1997; Hutchinson and Griffith 2008) and in one long-lived seabird species, Cory’s Shearwater (Bried et al. 2010). In this latter species, the males’ large bills may be the sexually selected trait (Navarro et al. 2009). In Streaked Shearwaters, the bill is a sexually dimorphic structure, as it is in many bird species (Arima et al. 2014). Male and female Streaked Shearwater do not differ in their choice of feeding area during the incubation period, suggesting that males and females invest the same effort when searching for food (Yamamoto et al. 2011). This implies that sexual dimorphism in bill size in Streaked Shearwater is most likely driven by sexual selection. This phenomenon is consistent with female preference toward large males (Kempenaers et al. 1997). Larger bills could be an advantage in terms of territory or nest defense and mate acquisition, and male–male competition (Székely et al. 2000; Shirai et al. 2013; Bried et al. 2010). One possible explanation for body-size-related EPP is that smaller males are not able to guard their mates and thus lose paternity. However, we did not observe mate-guarding behavior outside of the nest in our Streaked Shearwater colony. During the mating period, paired males and females stayed inside the nest at night; they left the nest separately and walked around it during predawn hours. Therefore, larger bills appear to be important for nest defense during the mating period, but it is unclear whether larger bills are advantageous for mate guarding outside of the nest.

Jouventin and Bried (2001) suggested that nest availability affects social mate choice in Snow Petrel (Pagodroma nivea), and that this species seldom divorces, likely due to the high cost of divorce in terms of missed breeding years before re-mating. Therefore, social mate choice can be constrained by habitat availability and quality, and females might seek EPC to adjust their choice of a social mate while continuing to breed with the social mate (Petrie and Kempenaers 1998; Bried et al. 2010). In Cory’s Shearwater, which has strong nest-site fidelity (Swatschek et al. 1994), insufficient nest supply results in strong competition for nests, constrains social mate choice, and leads to increased EPCs in a Islet of Vila population (Bried et al. 2010). If Streaked Shearwater adults breeding at Funakoshi Ohshima Island compete for nests, female mate choice should not depend solely on a potential partner’s body size. Although we do not have sufficient data to examine whether strong competition for nests occurs on Funakoshi-Ohshima Island, new nests are found each year, intimating an increase in our study population. Our results regarding the influence of male body size on cuckoldry imply that EPP of Streaked Shearwater derives from female acceptance of EPCs. As both sexes in a number of species can actively seek EPC (reviewed by Westneat and Stewart 2003), the roles of Streaked Shearwater males and females in EPC require further investigation.

Notes

Acknowledgments

We thank Yoshinari Yonehara, Yusuke Goto, Tatsuya Shiozaki, and Takanori Sugahara for assisting with fieldwork on Funakoshi-Ohshima Island. We are grateful to Aran Garrod, Bart Kempenaers, and an anonymous referee for insightful comments that improved the manuscript. This study was supported by grants from research fellowships of the Japan Society for the Promotion of Science for Young Scientists to Miho Sakao, Tohoku Ecosystem-Associated Marine Sciences, the Bio-logging Science Program of the University of Tokyo, National Geographic (Asia 45-16), Japan Science Technology Agency Core Research for Evolutional Science and Technology (JPMJCR1685), the Cooperative Program of the Atmosphere and Ocean Research Institute, the University of Tokyo, and the Japan Society for the Promotion of Science and OP under the Japan-UK Research Cooperative Program. The authors declare no conflict of interest.

Compliance with ethical standards

All procedures performed in this study involving animals were approved by the Animal Experimental Committee of the University of Tokyo and conducted in accordance with the Guidelines for the Care of Experimental Animals. This work was conducted with permission from the Ministry of the Environment and Agency for Cultural Affairs, Japan.

Supplementary material

10336_2018_1587_MOESM1_ESM.pdf (147 kb)
Supplementary material 1 (PDF 146 kb)
10336_2018_1587_MOESM2_ESM.pdf (47 kb)
Supplementary material 2 (PDF 47 kb)
10336_2018_1587_MOESM3_ESM.eps (600 kb)
Fig. S1 Presence (n = 8) and absence (n=28) of extra-pair chicks in relation to the social female’s bill length (a), head length (b), tarsus length (c), wing length (d), and bill depth (e). Box plots show the median value, range, 25th and 75th percentiles, and outliers. P- and U-values were obtained by Mann–Whitney U-test. Supplementary material 3 (EPS 600 kb)

Supplementary material 4 (MP4 29424 kb)

Supplementary material 5 (MP4 20865 kb)

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Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2018

Authors and Affiliations

  1. 1.Atmosphere and Ocean Research InstituteThe University of TokyoKashiwaJapan
  2. 2.Research Institute for Humanity and NatureKyotoJapan

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