When multiple carers invest in a shared brood, there is likely to be conflict among individuals over how much each carer invests. This conflict results in suboptimal investment to the detriment of all carers. It has been proposed that conditional cooperation, i.e. ‘turn-taking’ or ‘alternation’, may resolve this conflict by preventing exploitation. This contentious idea has received some empirical support, but distinguishing active alternation from that expected via passive processes has proved challenging. The aim of this study was to use detailed observations of provisioning to examine whether carers at biparental (parents only) and cooperative (parents and helpers) nests of the long-tailed tit Aegithalos caudatus behave in a context-dependent manner that enhances the level of alternation. First, we show that carers who had been the last to feed waited near the nest (loitering) for longer before feeding when they next arrived at the nest and allowed others to feed first, thus facilitating alternation. Secondly, we found that the arrival of carers near the nest and their subsequent feeds were tightly synchronised, with overlapping loitering periods, allowing them to monitor the effort of other carers. Finally, we show that measures of coordination were influenced by carers arriving in a status-dependent order, with breeding females consistently arriving first and helpers last. Together, these results show how patterns of alternation and synchrony arise in long-tailed tits and reveal the behavioural mechanisms underpinning coordination of care.

Study system and data collection

Field work was conducted in 2020–2021 on a total of 23 breeding pairs of long-tailed tits in an intensively monitored population in the Rivelin Valley, Sheffield, UK (53°23′N, 1°34′W) as part of a long-term study running since 1994. The ~3km² field site is primarily comprised of deciduous woodland, agricultural pasture and scrub. Individuals were identified by a unique combination of two colour rings which were applied, along with a BTO metal ring (under British Trust for Ornithology licence), to nestlings for birds hatched within the field site or upon capture in mist-nets for adult immigrants (see ethical note below). Nests were found by following adults gathering nest material and once located were checked every two days, with daily checks as nests approached incubation and hatching. Nests were typically built <2m from the ground within brambles Rubus fruticosus, gorse Ulex sp., rose Rosa sp., holly Ilex sp., or >3m from the ground in the forks of tree branches, although only nests within reach of observers, where clutch and brood size could be readily measured, were used for this study. Clutch size (median 10, range 7–11, N = 23) was measured once laying had ceased and incubation started. Incubation lasts ~15 days (Hatchwell 2016), and all eggs that hatch typically do so within the same day (day 0). Brood size (median 9, range 6–11, N = 23) was recorded on day 11 and was assumed to remain constant for the full duration of provisioning observation (day 6–16) (Hatchwell et al. 2004).

Provisioning watches (hereafter ‘watches’) were performed every other day from day 6 until fledging (day ~16), because for ~5 days after hatching nestlings are brooded by their mothers for much of the time and provisioned indirectly by fathers who pass food to the mother on the nest, so no coordination of carer visits is possible until day 6. Long-tailed tits are facultative cooperative breeders, so nests may be provisioned biparentally (2 parents) or cooperatively (2 parents and ≥1 helper). Our dataset included 101 unique watches with 2–6 active carers per watch, with 49% watches being biparental and 32%, 9%, 7% and 4% watches from cooperative nests with 3, 4, 5 and 6 carers, respectively. Watches were conducted at 23 unique nests, including 21 unique breeding females (hereafter ‘females’), 23 unique breeding males (hereafter ‘males’) and 25 unique helpers. Watches were performed between 0700 and 1630 hours and started after a 10-minute habituation period to minimise observer disturbance. Watches were typically conducted for 60 minutes following the first observed feed, with the final watch duration recorded as the time between first and last feeding visits (mean duration (± SD) = 58.5 ± 5.9 minutes; range 41.2–78.3; N = 101 watches). We omitted one watch of duration <30 minutes.

The protocol during watches was to record the identity of a carer and time, to the nearest second, they arrived near the nest (within 15m) and then provisioned the brood. Prior to beginning a watch, a video camera was placed ~2m from the nest, recording the nest entrance so that the identity of carers and time of feed, to the nearest second, could be determined by video review. Meanwhile, an observer sat ≥20m from the nest, where they identified carers arriving near the nest, recording the identity and time of arrival to the nearest second. The time a carer spent near the nest prior to feeding is hereafter referred to as the ‘loitering’ period. The order of arrivals near the nest was important for our analysis, so when carers arrived simultaneously observers recorded the arrival times as equal but noted which carer was identified first. After 7.1% (N = 2470) of arrivals, the carers left the area without provisioning, so these instances were excluded. Watches were conducted only at nests with good visibility of surroundings; but 5.3% ± 6.1% (SD) of arrivals that resulted in a feed (recorded by video) were missed (range 0–21%, N = 101 watches); one watch where more than 25% of arrivals were missed was omitted. Gaps were filled by substituting time first seen on camera for arrival time, reasoning that the longer a carer loitered the lower the chance that it would be missed, so missed arrivals would likely have preceded very short loitering periods. Observations were conducted by three observers: 73/101 watches were conducted by CH and the remainder by SJB (13) and MG (15), with distance estimation standardised in joint watches before data collection started.

Calculating coordination

Alternation and synchrony were analysed as the absolute number of alternated and synchronised visits performed within each provisioning watch. An alternated feed was defined as any feed that avoided consecutive feeds by the same individual, ensuring turn-taking between two or more carers. For example, the sequence A-B-A-C-B-C avoids consecutive feeds by the same carer, so all these would be considered alternated (except the first); note that in cooperative nests alternation did not require repeated patterns of feeds by all carers e.g. A-B-C-A-B-C, simply non-consecutive feeds. A synchronised feed was defined as any alternated feed that occurred within a brief time window of the previous feed, for example, if three feeds occur within quick succession after a gap in provisioning, e.g. A-B-C then feeds B and C are considered synchronised, but feed A is not because it did not occur within the synchrony window of the previous feed. We investigated the synchrony of arrivals near the nest and feeds using two different synchrony window lengths: long (2-minutes) and short (30-seconds), a synchronised arrival being any that occurred within the specified window of the previous arrival by another carer. The long (2-min) window was chosen to match prior studies of coordination (Bebbington and Hatchwell 2016, Ihle et al. 2019a, Halliwell et al. 2022) which measured feed times to the nearest minute and produced qualitatively the same results with 1-min, 2-min and 3-min synchrony windows. In this study, since we recorded feed and arrival times to the nearest second, we utilised this increased resolution to compare the level of active synchrony using a long (2-min) and a short (30-sec) window; a difference between them could indicate whether arrivals or feeds were more or less tightly synchronised than previously shown.

A certain level of passive coordination (alternation and synchrony) is expected by chance (Schlicht et al. 2016, Ihle et al. 2019a, Santema et al. 2019), and factors such as predator threat, local resource abundance and changing weather can increase apparent coordination through their common effect on all carers at a watch. Refractory periods (the foraging time needed to obtain food for chicks) may also contribute to apparent coordination as they create a period during which a consecutive visit is not possible, but an alternated visit is. Therefore, to determine the extent to which observed coordination was due to active coordination behaviours we compared observed coordination metrics to an expected passive level of coordination generated through null model randomisation. We used a modified version of the within-watch, within-individual intervisit interval randomisation procedure (Figure 1a,c) that randomised the times between an individual carer’s feeds within a given watch, i.e. the intervisit intervals (e.g. Johnstone et al. 2014, Savage et al. 2017, Ihle et al. 2019b, Halliwell et al. 2022; Figure 1c). Here, we split the intervisit interval into ‘time away’ (mean duration (± SE): 357.6s ± 7.3, N = 2010) from and ‘time near’ (loitering) (50.3s ± 1.5, N = 2307) the nest (Figure 1a). We found no correlation between ‘time away’ and ‘time near’ (Pearson correlation: r₁₀₀ = 0.137, P = 0.171), so we randomised these time periods independently of one another (Figure 1b). This approach more precisely defines the length of the refractory period, which is now contained within ‘time away’, thus creating a more biologically realistic approximation of the level of apparent coordination expected by chance. We applied our null model to the observed dataset, generating 1000 randomised sequences which we used as a framework for generating expected values for a given metric of coordination. For example, to test whether carers alternated more than expected by chance, we calculated the median ‘expected’ number of alternated feeds per watch from these 1000 randomised sequences and compared that to the ‘observed’ number of alternated feeds seen in that watch. The difference between these observed and expected values is hereafter referred to as ‘active’ coordination.

Hypothesis 1: Loitering facilitates alternation

To test predictions of the delayed feeding hypotheses we calculated several metrics of coordination directly from provisioning watches (observed) and the median number from 1000 randomised sequences (expected) as follows. First, we calculated the number of feeds where a carer waited to ensure alternation, defined as the number of visits where, upon arrival near the nest, a carer that had been the last to feed and waited for another carer to feed before them in the current bout. Secondly, we calculated the mean loitering time for carers when, upon arrival, they were the last carer to feed previously, and mean loitering time when they were not. Similarly, we calculated the number of instances where another carer fed during the loitering period of the focal carer when, upon arrival, they were the last to feed, and the number of instances another carer fed when they were not last to feed.

Hypothesis 2: Collective arrivals facilitate synchrony

To test the predictions of the collective arrival hypothesis we first calculated the observed and expected numbers of instances of synchronous arrivals and synchronous feeds during a given watch (using both long and short synchrony windows). Secondly, we calculated the number of observed and expected cases when the focal carer arrived near the nest with another carer already present, and when another carer fed during the loitering period of the focal carer. For this analyses, all measures were calculated as the total number of cases by all carers present during a given watch.

Hypothesis 3: Status dependent order of visits

To test the predictions of the status-dependent arrival hypothesis, first we calculated the observed and expected number of instances where the focal carer arrived near the nest with another carer already nearby. These metrics were calculated for each individual carer, allowing comparison of the number of these cases between carers of different statuses.

Secondly, we quantified the orders in which carers arrived and fed during synchronised bouts. We restricted this investigation to biparental (two carers: M male and F female) watches and cooperative watches with one helper (three carers: M, F and H helper) which together made up 80% of our watches, because as the number of carers increases, the number of possible orders carers may arrive or feed in increases exponentially, from two possible orders with two carers (F_M and M_F), six with three carers, 24 for four carers, and so on. For these analyses, we considered only ‘isolated’ synchronised bouts (2-minute window). For a synchrony bout to be isolated it must be separated from the previous bout by at least 2 minutes to avoid one bout influencing another. For example, if a biparental nest has a female-first synchronised feed bout (F_M) followed shortly after by another synchronised bout then the female is more likely to arrive first in the subsequent bout because feeding first in the previous bout afforded her a head start. For these analyses, our null expectation was that carers of different statuses would occupy randomly each position within a sequence, i.e. 50% per position for biparental watches and 33.3% per position for cooperative watches.

For biparental watches, we determined the number of female-first and male-first arrival and feed sequences per watch, our model structure accounting for multiple bouts from the same watch with random effect terms. In total we identified 294 synchronised bouts from 46 biparental watches (median = 6 per watch); three watches contained no suitable bouts. For cooperative watches, we determined the position within arrival and feed sequences by females, males and helpers. We identified 82 synchronised bouts from 27 cooperative watches (median = 3 per watch); five watches contained no suitable bouts. Of the 82 bouts, in three instances the same carer arrived twice within the synchronised bout, so these bouts were omitted from the arrival order analysis. For analysis of cooperative bouts, we determined the number of times carers of each status occupied a position (first, middle and last) for both arrivals and feeds. Finally, to investigate whether carers at cooperative nests were more closely associated with other specific carers, we determined the number of times a carer synchronised with one other carer only during isolated synchronised bouts (i.e. F&M, F&H and M&H) regardless of the order of arrivals or feeds. In total, we found 102, 96 and 58 instances of a female, male and helper synchronising with another carer, respectively.

Raw provisioning data are available as it was directly recorded from field observation. This file can be viewed using Microsoft Excel.

Data were processed using code supplied (Script 1 - Script 7) using the programming software R using RStudio.