Avian sibling cannibalism: Hoopoe mothers regularly use their last hatched nestlings to feed older siblings
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摘要: 同胞相食在自然界中相对常见，但同胞相食这一行为如何在鸟类及其他具有双亲照顾的脊椎动物中进化已少有提及。然而，该研究显示，在欧亚大陆的两个欧洲戴胜种群(Upupa epops)中，同胞相食是一种普遍发生的行为，这需要进一步探讨其可能的适应性或非适应性。我们的研究表明，西班牙种群(51.7%)的同胞相食现象比奥地利种群(5.9%)更频繁。在这两个种群中，戴胜的窝卵数大小和离巢雏鸟数量相似，但奥地利种群的孵化失败率更高。因此，西班牙种群中，会有更多的雏鸟死亡，这可能解释了同胞相食发生率较高的原因。根据这种解释，雏鸟先后孵出的时间间隔、孵化率，而不是繁殖日期，解释了西班牙戴胜种群同胞相食高的可能性，但是这三个变量都预测了离巢雏鸟数量减少的强度。此外，实验性增加食物供应降低了同胞相食的可能性，但并没有减少离巢雏鸟数量减少的强度。 最后，当面临饥饿时，雌鸟将更少的资源分配给最小的雏鸟，但最小的雏鸟是否被用作其他同胞的食物却不一定。这些结果表明，戴胜繁殖时会产下额外的卵，在减少孵化失败和食物短缺的情况下，将最小的雏鸟用于喂养年长的雏鸟。这些发现提供了鸟类同胞相食是一种普遍行为的第一个实验性证据，从而有助于我们深入理解动物界中窝卵数、异步孵化、亲子冲突、杀婴和同胞相食等是如何进化的。Abstract: Sibling cannibalism is relatively common in nature, but its evolution in birds and certain other vertebrates with extended parental care had been discarded. Here, however, we demonstrate its regular occurrence in two European populations of the Eurasian hoopoe (Upupa epops) and explore possible adaptive and non-adaptive explanations. Results showed that sibling cannibalism was more frequently detected in Spain (51.7%) than in Austria (5.9%). In these two populations, the hoopoes laid similar clutch sizes, resulting in similar fledging production, but hatching failures were more frequent in the northern population. Consequently, having more nestlings condemned to die in the southern population may explain the higher incidence of sibling cannibalism. In accordance with this interpretation, hatching span and failure, but not breeding date, explained the probability of sibling cannibalism in the Spanish hoopoes, while all three variables predicted brood reduction intensity. Furthermore, experimental food supply reduced the probability of sibling cannibalism, but not the intensity of brood reduction. Finally, females allocated fewer resources to the smallest nestlings when they were going to starve, but not necessarily when they were going to be used as food for their siblings. These results suggest that hoopoes produce extra eggs that, in the case of reduced hatching failure and food scarcity, produce nestlings that are used to feed older siblings. These findings provide the first evidence that sibling cannibalism occurs regularly in a bird species, thus expanding our evolutionary understanding of clutch size, hatching asynchrony, parent-offspring conflict, infanticide, and sibling cannibalism in the animal kingdom.
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Key words:
- Brood reduction /
- Clutch size /
- Hatching asynchrony /
- Ice-box hypothesis /
- Infanticide /
- Siblicide /
- Sibling hierarchy /
- Upupa epops
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Figure 1. Sibling cannibalism and experimental food supply
Probability of sibling cannibalism (±95% CI) and number of nestling deaths in first 10 days after hatching (brood reduction) (±95% CI) in hoopoe nests with experimental food supply (Exp.) or in control nests.
Figure 2. Cannibalism and life history traits
Associations between intensity of cannibalism and brood reduction, clutch size, and hatching failure. Lines are regression lines and 95% CI, and point size is proportional to log-transformed number of nests with such values.
Table 1. Life history traits of Spanish and Austrian hoopoes in two different study years
Between-year comparisons Comparisons Mean (CI 95%) Mean (CI 95%) Stat. df P Spanish population 2017 (N=61) 2018 (N=44) Clutch size 7.23 (6.93–7.53) 7.57 (7.16–7.97) F=1.92 1,103 0.169 Hatching failures 0.70 (0.45–0.96) 1.14 (0.83–1.44) F=4.81 1,103 0.031 Hatching failure prevalence 44.26% 70.45% χ2=7.09 1 0.008 Brood size 6.56 (6.27–6.84) 6.43 (6.02–6.84) F=0.27 1,103 0.602 Fledgling production 3.78 (3.39–4.17) 4.45 (3.98–4.92) F=5.62 1,103 0.020 Brood reduction 2.82 (2.37–3.26) 1.98 (1.50–2.45) F=6.53 1,103 0.012 Brood reduction (Day 8) 1.23 (0.89–1.57) 1.61 (1.18–2.04) F=1.94 1,104 0.166 Brood reduction prevalence 86.9%, 75.0% χ2=2.44 1 0.119 Austrian population 2009 (N=29) 2010 (N=38) Clutch size 7.59 (7.04–8.13) 6.58 (6.08–7.08) F=7.62 1,65 0.007 Hatching failures 2.17 (1.51–2.83) 1.32 (0.88–1.75) F=5.29 1,65 0.025 Hatching failure prevalence 82.76% 68.42% χ2=1.79 1 0.181 Brood size 5.41 (5.03–5.80) 5.26 (4.84–5.69) F=0.27 1,65 0.606 Fledgling production 4.66 (4.09–5.22) 3.68 (3.16–4.21) F=6.43 1,65 0.014 Brood reduction 0.76 (0.40–1.12) 1.58 (1.22–1.93) F=10.5 1,65 0.002 Brood reduction prevalence 51.7% 86.84% χ2=9.98 1 0.002 Between-population comparisons Spain (2017–18)
(N=105)Austria (2009–10)
(N=67)Mean (CI 95%) Mean (CI 95%) Clutch size 7.37 (7.13–7.61) 7.01 (6.64–7.39) F=2.77 1,170 0.098 Hatching failures 0.89 (0.69–1.08) 1.69 (1.31–2.07) F=16.7 1,170 <0.001 Hatching failure prevalence 55.24% 74.63% χ2=6.58 1 0.010 Brood size 6.50 (6.27–6.74) 5.33 (5.04–5.61) F=39.6 1,170 <0.001 Fledgling production 4.04 (3.74–4.34) 4.10 (3.71–4.50) F=0.07 1,170 0.789 Brood reduction 2.47 (2.14–2.80) 1.22 (0.96–1.49) F=28.0 1,170 <0.001 Brood reduction prevalence 81.90% 71.64% χ2=2.50 1 0.114 Averages, confidence intervals (CI 95%), and sample sizes of life history characteristics, including clutch size, hatching failure, brood size, fledgling production, and intensity and prevalence of brood reduction in breeding hoopoes of Spanish and Austrian populations. Sample sizes and results from between-year and between-population comparisons are also shown. Statistically significant (P<0.05) differences are shown in bold. Stat.: Statistics. 
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Table 2. Factors affecting sibling cannibalism and brood reduction
Sibling cannibalism Brood reduction Prevalence Intensity Prevalence Intensity Estimate (SE) χ21 P Beta (SE) F1,44 P Estimate (SE) χ21 P Beta (SE) F1,44 P Hatching date 0.017 (0.014) 1.46 0.226 0.212 (0.133) 2.53 0.119 -0.009 (0.025) 0.12 0.726 0.386 (0.109) 12.43 0.001 Hatching span 0.695 (0.299) 7.03 0.008 0.393 (0.134) 8.54 0.005 2.628 (0.820) 37.51 <0.001 0.530 (0.111) 22.98 <0.001 Exp. treatment 0.889 (0.369) 6.65 0.010 0.220 (0.133) 2.73 0.105 0.683 (0.676) 1.31 0.287 0.132 (0.109) 1.45 0.234 Results from generalized linear model (binomial distribution and logic link function) and general lineal model exploring effects of experimental food supply, hatching date (1: 1 April), and hatching span (independent factors) on prevalence and intensity of sibling cannibalism and brood reduction, respectively. Statistically significant (P<0.05) differences are shown in bold.
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