Our study revealed that in Chinese penduline tits, total parental provisioning and brooding for nestlings were similar for nests with different care types – biparental care versus uniparental care. Feeding frequency significantly contributed to the body mass of offspring, but brooding duration did not; neither influenced fledging success. Parental removal experiments executed in biparental care nests indicated that the remaining parent fully compensated for the feeding frequency in the absence of its partner but did not for the brooding duration. Parents may be confronted with a trade-off in allocating parental efforts while dealing with the partner’s absence, and they allocated more effort to the more influential one for offspring fitness. Sex-biased feeding and brooding effort was not found in naturally biparental nests or in compensation for the partner’s absence. These results suggest that the evolution of biparental care in Chinese penduline tits may not be driven by the low feeding capability of the partner but related to the ability of the partner to efficiently arrange different parental tasks.
Although the sample size of this research is not considerable, the statistical power analysis indicated that we can draw concrete conclusions (80% power) when the sample size is 10 and the coefficient of determination (R2) is bigger than 0.50; or when the sample size is 11 and R2 is bigger than 0.47. These are the sample sizes for respectively the natural-nest comparisons and parental removal experiments. The values of R2 of our statistic models indicate that we can reasonably draw the above conclusions.
Different responses to parental removal in species with and without natural uniparental care
Uniparental care does not commonly evolve in birds, especially in passerine species, where nestlings demand close attendance from both parents (Cockburn, 2006). In most species where both care strategies occur, uniparental care is more likely an optional parenting strategy. Its occurrence has been found to be influenced by resource abundance, skewed adult sex ratio or energy reservation for moulting and migration in the late season (Eberhart-Phillips et al., 2018; Eldegard & Sonerud, 2009; Wojczulanis-Jakubas & Jakubas, 2012). However, studies have scarcely explored whether parents invest differently under uni- and biparental care conditions (Porkert & Špinka, 2004; Wiebe, 2005). Our results revealed that the single parent in uniparental care nests invests as efficiently as both parents in biparental care nests regardless of feeding or brooding. This indicates that the overall parental effort did not differ in the two types of nests. This result was consistent with the findings in common redstart (Phoenicurus phoenicurus; Porkert & Špinka, 2004), magnificent frigatebird (Fregata magnificens; Osorno & Székely, 2004) and Tengmalm’s owl (Aegolius funereus; Eldegard & Sonerud, 2009). Those parents who were naturally deserted by the partner were able to fully compensate for the feeding loss to the same standards as biparental nests.
Our parental removal experiment found that in biparental care nests of Chinese penduline tits, one parent could completely compensate for the absence of food provisioning. This indicates that in biparental care nests, the two parents resolved sexual conflict by withholding their provisioning effort under the condition of guaranteeing sufficient care to the offspring (Hardling & Kaitala, 2005; Parker, 2006). Moreover, consistent with some theoretical predictions (Fromhage & Jennions, 2016; Houston et al., 2005), male and female penduline tits resolved the conflict by reaching conditional cooperation through evenly sharing the feeding and brooding task.
Conversely, in zebra finch (Taeniopygia guttata), a species that provides biparental care only, a study showed that after experimental removal of one parent during provisioning from some nests, broods reared by one parent were fed significantly less frequently than those raised by two parents (Royle et al., 2006). A meta-analysis on parental response to experimental reductions in partner provisioning efforts found that the mean response for most biparental care species was not full compensation (Harrison et al., 2009). The conclusions drawn above are based on species where biparental care is the norm and in which a parent was experimentally removed to force a uniparental approach. This finding, together with our results, implies that uniparental care probably evolved as a stable pattern only when the efficiency of raising offspring by a single parent was relatively high.
Parents from biparental care nests confront a trade-off during singly feeding
Our study investigated the parenting capability of parents from natural uni- and biparental nests in Chinese penduline tits by removing one parent from biparental care nests. The full compensation of nestling feeding during partner removal indicated that the parents in biparental nests may not necessarily have a lower ability in food provisioning than parents from uniparental nests. However, the remaining parent did not compensate for the reduced brooding duration. This agrees with the claim that comparable provisioning rates could result in less time spent on brooding nestlings (in common redstart; Porkert & Špinka, 2004). In contrast, the brooding duration in natural-uniparental care nests is comparable to that in biparental care nests over nestling ages based on our observations.
Our removal experiment may force the remaining parents into a trade-off such that compensation for feeding comes at the cost of brooding. This unequal compensation could be explained by the significant contribution of feeding frequency, but not brooding duration, to nestling body mass that we found in natural nests. Adjusting parental effort while facing a parenting trade-off has been shown, for example, in common terns (Sterna hirundo), where parents increasing incubation effort for better brood hatching success had reduced parental performance in the later brood-rearing phase (Heaney & Monaghan, 1996). In burying beetles (Nicrophorus orbicollis), parents allocate more time to care behaviours that offspring receive individually (such as feeding) but not simultaneously (such as brooding, Rauter & Moore 2004). These findings, which are in line with ours, manifest that different parental care tasks may contribute different weights to offspring development, and parents tend to make the (temporal) sacrifice that deprives the least necessary of offspring fitness.
However, we found this parenting trade-off no longer holds in natural uniparental care nests, where single parents could easily feed and brood at the same intensity as the pair in biparental care nests. The inconsistency of parental care by single parents between natural- and manipulated-uniparental care nests indicates that some fundamental differences in uniparental and biparental nests exist. For instance, (1) parents in uniparental care nests may occupy better territories, with more abundant food than in biparental care nests, so that single parents spend less time foraging and are therefore able to spend a sufficient amount of time keeping nestlings warm; (2) parents in biparental care nests are less efficient in foraging than parents in uniparental care nests. In penduline tits, uniparental care nests often appear early in the breeding season, whereas biparental care nests emerge later (Zheng, 2022). Possibilities can be that as food resources decline over the season (which could be indicated by a seasonally decreased clutch size; Zheng et al., 2021), the late parents have to cooperate to successfully raise nestlings; additionally, an intense breeding peak of penduline tits in the early season might allow individuals to socially share resource information and thereby forage more efficiently (Brandl et al., 2019; Evans et al., 2009). This may also make parents from the early nests (largely uniparental care nests) more capable of feeding on the brood alone.
The consequences of the shorter brooding duration in experimentally created uniparental nests require more investigation, such as by monitoring the physiological conditions of offspring during experiments. In addition, long-term removal should be considered, preferably over the entire nestling period, to investigate whether the remaining parents are fully competent for parental care alone or if the response changes from full to partial compensation. Based on the current results, we propose that studies should note that feeding ability, although probably the easiest measure to estimate, may not be the only parenting behaviour that matters if investigating the compensation for the partner’s care. The restrictions for parents to allocate time and energy to different parenting tasks need more investigation in further studies. Biparental care may be necessary for providing a good environment for nestling development even if one of the parents is in principle able to provision the brood sufficiently in biparental care nests (Matysioková & Remeš, 2014; Rossmanith et al., 2009).
No sex difference in response to partner removal
Our study showed that the change in food provisioning of the remaining parent before and after removing the partner was similar for male and female parents. However, sexually different responses to the absence of partners were reported in other species. Male rock sparrows allocate more care to offspring and feed at a higher frequency after being widowed, whereas females do not adjust their feeding frequency when confronted with the absence of the male partner (Cantarero et al., 2019). Male and female northern flickers (Colaptes auratus) increase the amount of food provisioning but compensate at different rates. Better compensation of males contributed to a higher nestling survival success than that of females (Wiebe, 2005). The different limitations of parental feeding capacity in both sexes or the reliance on care from one sex were proposed to be the main causes. However, we found that both male and female Chinese penduline tits showed similar facultative adjustments in compensation for partner removal. Zheng et al. (2021) also reported comparable offspring survival success in male-only and female-only cared nests. Therefore, males and females might equally evolve a high ability to solely and successfully provision offspring. The reason why female-only care nests are more prevalent than male-only care nests in the population may be caused by other traits that differ between sexes during the entire life history, such as sex bias in mortality rate or adult sex ratio (Fromhage & Jennions, 2016).
Insights from individual variations in compensation after partner removal
Although our results found, in general, that the remaining parent fully compensated for feeding and barely for brooding after removing one of the parents, the responses between individuals were variable. Individual variations in compensation indicate that the solution towards the abovementioned trade-off between feeding and brooding largely relies on individual preferences. A study of chestnut thrushes (Turdus rubrocanus) showed that the similarity of personality contributes to individual variations in compensation after removing the partner (Lou et al., 2021). Pairs with similar personalities could be better parents, which may result in higher reproductive success (Schuett et al., 2011). In addition, compatible and well-coordinated pairs may modulate the intensity of sexual conflict within pairs, as the more assortative mates would experience less conflict due to the equal labour divisions during breeding (Baldan & Griggio, 2019; Lou et al., 2021). Parents may also respond differently to mate removal due to their body condition and capability of dealing with stress (Lendvai & Chastel, 2008; Whittingham et al., 1994). However, except for evaluating the average response at the population level, further experiments are needed to explore the pattern of parental compensation by correlating mate similarity, coordination of partnership and physiological conditions.