DOI: 10.5061/dryad.37pvmcvpq
title: Data for: Coordination of care is facilitated by delayed feeding and collective arrivals in the long-tailed tit

description: 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.
description: 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 ~3km<sup>2</sup> 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 &lt;2m from the ground within
 brambles <em>Rubus</em> <em>fruticosus</em>, gorse
 <em>Ulex</em> sp., rose <em>Rosa</em> sp., holly
 <em>Ilex</em> sp., or &gt;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 &lt;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:
 r<sub>100</sub> = 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.
description: 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.