Cooperative Breeding System Of Ground Tits In The Northeast Tibetan Plateau

The ground tit (Parus humilis) is a facultative cooperative breeding passerine, which is endemic to Qinghai-Tibet Plateau. The data were collected during four consecutive years (2009-2012) near the Tianjun County (37°17’N,99°06’E,3400m asl.), northeastern of Qinghai-Tibet Plateau. This study mainly focused on the population biology of ground tits and the main results were summarized as follows:1. Breeding ecology of ground titsThe ground tit was involved in breeding activities in early-April (e.g. courtship copulation and burrow-excavating). The mating system seemed to be socially monogamous. This species is territorial and defends all-purpose territories. The ground tit is a cooperative breeding species, with48.6%of the nests containing1-3helpers (n=171). Breeders and helpers actively participate in burrow-excavating and nest-building, which last3-7days and4-6days, respectively. The distribution of burrow entrances was far from random, with mostly facing east and southwest. Egg-laying took place between early-April and mid-May (mean=116day, n=153). Clutch size averaged6.95(n=40) and no difference was detected in clutch size between bi-parental and cooperative groups. The birds only made a single nesting attempt per year. Mean brood size was5.9(n=153). Incubation undertaken by female lasted14.1days, and young in the nest were fed by parents with helpers for26.2days. Nest breeding success was90.6%. Fledglings were still fed by adults for at least10days till they get independence.Compared to other populations studied in Tibetan Plateau, the high-altitude ground tits start breeding later, excavate shorter burrow, produce fewer but bigger eggs, and have a longer nestling period. The observed patterns are consistent with an adaptive life history strategy that high-elevation species tend to have reduced fecundity but allocate more energy into each offspring to cope with the harsh conditions. Besides, clutch size variation is consistent with "latitudinal variation hypothesis" that clutch size increases with latitude.2. Social organization and mating systemThe Ground tit is a facultative cooperative breeding species, with47.1%of the nests have helpers (n=153). A cooperative nest typically comprised a pair with one helper. Helpers were exclusive males (n=95). Cooperative broods have an average of1.32helpers (range:1-3). Helpers were the relative of breeders, wherein81%of them assisted one or both of their parents. Most of the helpers (81%) were yearlings while others (19%) were2-3years old. The probability of obtaining a mate for a helper increased with its contribution (years of helping).Parentage analysis of a two-year data (81nests) based on eight microsatellite markers revealed that extra-pair paternity occurred in6.2%(5/81) of the nests and1.3%(6/468) of the nestlings. No case of extra-pair maternity (egg-dumping) was detected. Helpers never share any paternity within in their own family groups and all the extra-pair offspring was sired by the individuals outside the groups. Parentage analysis indicated this species is socially monogamous as helpers never obtain any paternity within group. By contrast, its genetic mating system was much more complicated:genetic monogamy (90.1%of nests), genetic polyandry (6.2%of nests) and genetic polyandry (3.7%of nests).3. Sex-ratio manipulationSex ratio allocation theory predicts that bird could flexibly adjust their offspring’s sex ratio. However, a total of884nestlings from153broods (2009-2012) yielded a balanced sex ratio (0.49, χ12=0.113, P=0.74). Similar result was found in one-sample t-test (t152=0.459, P=0.65). No significant difference was found in offspring sex ratio between independent (0.490, χ12=0.176, P=0.67) or cooperative nests (0.499, χ12=0.002, P=0.96). GLMMs analysis also showed that offspring sex ratio was not statistically affected by breeders’ body quality, territory quality, whether cooperative, brood size, incubation date or years. In contrast, however, the adults’sex ratio was strongly male-biased during the breeding season (0.62,χ12=23.7, P<0.001).4. Helper effects on breeding success and breeders’survivalThe benefits of helpers were considered to increase breeding success or individual survival. Taking both the aspects into account is essential to understanding the value of helping behavior. A four-year study was conducted on Ground tits in Tibetan Plateau to explore helper effects on fecundity (breeding success) and the survival of breeders and their offspring. Of the153broods collected during4breeding seasons, no helping effect was detected on the brood size at fledging in GLMMs. However, helping behaviors played a significant role in winter survival of male juveniles, while the downstream effect (in the next spring) for male juveniles was weak. Other variables were not significant in the GLMMs. Similar results were detected in independent t-tests on helper effects (no. of male fledglings:2.77vs.2.94; juvenile males’ survival:1.11vs.1.88in winter and0.60vs.0.85in the next spring). Of the overall male juveniles, winter apparent survival was55.2%while their survival in next spring25.4%, which differed significantly (xi2=33.65, P<0.001).Helpers had significant positive effect on male breeders’ survival through the winter to the next spring. However, the survival of breeding females was not affected by helper effects. Independent t-tests show similar results to that of the GLMMs above (male breeders’ survival in bi-parental and cooperative nests:0.80vs.0.91in winter and0.45vs.0.77*in the next spring; female breeders’survival:0.78vs.0.81in winter and0.47vs.0.60in the next spring). Winter survival of breeders was high, both for males (86.1%) and females (80.6%). By contrast, Annual survival for both male and female breeders declined to60.2%and53.1%, respectively. All of them did not differ between the sexes (χ12<1.15, P>0.28).5. Winter group structureEven in winter, Ground tits show strong territoriality. Two categories of groups arose in winter:family groups and mixed groups. Family group consist of breeder(s) with their offspring. Most of the winter groups were family groups (86.4%,70/81) while others were mixed groups which consist of two or more family groups. Group size averaged5.4±2.1(3-13), wherein90%of the groups have3-7members. Groups size in winter were significantly larger than that of breeding season (5.4vs.2.6, t80=11.8, P<0.001).Each winter group had an average of1.04±0.12immigrants (n=81groups). A proportion of42/70in family groups had at least one immigrant while the proportion in mixed groups was9/11, and no statistical difference of the proportions was found between the two category of groups (χ12=1.941, P=0.164). Remaining juveniles were mainly males (75.0%of retained juveniles) while immigrants were often juvenile females (75.4%of the immigrants).Shortly after the breeding season, the population sex-ratio was balanced (0.48, χ12=1.19, P=0.28). However, in winter (December), the sex ratios of both the adults and juveniles strongly skewed to male. Female-biased mortality in juveniles caused the population sex-ratio strongly male-biased. In a socially monogamous mating system and female-based dispersal species like ground tits, male-biased sex ratio implies that surplus males could not obtain a mate in the current year. Under this condition, remaining and helping in the natal territory may be a better choice for them in future production. Thus, mate shortage may facilitate the cooperative breeding of the ground tits.