DOI: 10.5061/dryad.9p8cz8wqj
title: Data from: Coordination of care reduces conflict and predation risk in a cooperatively breeding bird

description: When two or more individuals cooperate to provision a shared brood, each
 carer may be able to maximize their payoffs by coordinating provisioning
 in relation to what others are doing. This investment ‘game’ is not simply
 a matter of how much to invest, but also of the relative timing of
 investment. Recent studies propose that temporal coordination of care in
 the forms of alternation (i.e. turn-taking) and synchrony (i.e.
 provisioning together) function to mitigate conflict between carers and
 reduce brood predation risk, respectively. Such coordination is widespread
 in biparental and cooperatively breeding birds, yet the fitness
 consequences have rarely been empirically tested. Here, we use a long-term
 study of long-tailed tits Aegithalos caudatus, a facultative cooperatively
 breeding bird with active coordination of care, to assess the support for
 these hypothesized functions for coordination of provisioning visits.
 First, we found evidence that turn-taking mitigates conflict between
 carers because, in cooperative groups, provisioning rates and offspring
 recruitment increased with the level of active alternation exhibited by
 carers, and with the associated increase in provisioning rate parity
 between carers. In contrast, offspring recruitment did not increase with
 alternation in biparental nests, although it was positively correlated
 with parity of provisioning between carers, which is predicted to result
 from conflict mitigation. Secondly, synchronous nest visits were
 associated with a reduced probability of nest predation and thus increased
 brood survival, especially when provisioning rates were high. We attribute
 this effect to synchrony reducing carer activity near the nest. We
 conclude that temporal coordination of provisioning visits in the forms of
 alternation and synchrony both confer fitness benefits on carers, and
 despite being intrinsically linked, these different kinds of coordination
 appear to serve different functions.
description: <strong>Methods</strong>
 <strong>Study system and general field
 protocol</strong> Data were collected during the
 breeding seasons (March–June) of 1994–2022 from an intensively studied
 wild population of long-tailed tits (Rivelin Valley, UK;
 c.3km<sup>2</sup>; <em>53°23′N</em>,<em>
 1°34′W</em>). Nests were located by following adults building nests,
 typically in low-lying (≤3m) shrubs (c.73% of nests; Higgot 2019) such as
 <em>Rubus fruticosus</em>, but sometimes in inaccessible tree
 forks. Nests were monitored at 1–3 day intervals but daily approaching
 incubation, hatching, and fledging. Incubation starts once the clutch is
 complete, lasts c.15 days, and all eggs that hatch do so within 24h of the
 first. After hatching (d0), both parents deliver prey items, such as
 flies, spiders, and caterpillars. Helpers may join a group at any point
 between hatching and fledging (d16–18), although helping is more common
 later in development. Long-tailed tits suffer only minimal chick
 starvation (0.2% daily per chick; Hatchwell et al. 2004) but lose 71.9% of
 clutches and broods to predation (Hatchwell <em>et al.</em>
 2013), typically by corvids (e.g. Eurasian jay <em>Garrulus
 glandarius</em>) and mammals (e.g. stoat <em>Mustela
 erminea</em>). Therefore, most brood mortality can be attributed to
 complete depredation events, although broods may occasionally be partially
 depredated (3.9% of successful nests; 9/233). Clutch
 size (median = 10; range 4–12;<em> N </em>= 293) in accessible
 nests was recorded during incubation. Brood size (median = 9; range
 1–11;<em> N </em>= 275), and the mass (to 0.1g; mean = 7.4g ±
 0.0142 SE;<em> N </em>= 1970) and tarsus length (to 0.1mm;
 mean = 18.3mm ± 0.0188 SE;<em> N </em>= 1970) of nestlings was
 recorded on d11. Each chick was ringed under British Trust for Ornithology
 (BTO) license with a unique combination of color rings. We took 5–20µl of
 blood by brachial venipuncture (under UK Home Office license) for genetic
 sex determination of nestlings using
 the <em>P2</em>–<em>P8</em> sex-typing primers
 (Griffiths <em>et al. </em>1998). Because clutch and/or brood
 size were important covariates, we limited our analysis to low nests where
 these metrics were sampled. The biometrics and sex of every chick was
 known in 77.7% (185/238) of broods. All applicable international,
 national, and institutional guidelines for the use of animals were
 followed and all regulated procedures were approved by the Animal Welfare
 and Ethical Review Body at the University of Sheffield.
 Successful local recruitment was recorded when a fledgling
 attempted to breed in the field site in a subsequent year. Long-tailed
 tits exhibit female-biased dispersal, so 20–25% of male, but &lt;10%
 of female fledglings recruit locally (Sharp <em>et al.</em>
 2008, 2011). Therefore, we estimated recruitment success from resightings
 of male fledglings breeding in subsequent years. We used the number of
 fledged males that were (median = 1; range = 0–5;<em> N </em>=
 170 broods), or were not resighted per brood (median = 3; range =
 0–7;<em> N </em>= 170) to model the proportion that recruited
 locally (mean = 0.241 ± 0.0212 SE;<em> N </em>= 170). In our
 open population, c.40% of breeders were immigrants to our field site
 <em>per annum</em>; these were captured in mist-nets and
 ringed. Since the project started, 1531 individuals have been recorded
 breeding in the site, but many of these never raised a brood and only 576
 (37.6%) birds were recorded provisioning broods in watches matching our
 criteria, which included 239 unique breeding females, 227 breeding males,
 and 171 helpers (61 of which were also breeders).
 <strong>Calculating coordination</strong>
 Provisioning watches (hereafter ‘watches’) were typically
 performed from d2 every other day until nest failure or fledging.
 Coordination is not possible when females are brooding young chicks (≤d5),
 so analysis was restricted to watches when both parents provisioned
 full-time (median = 3 watches per nest; median brood age = d10; range
 d6–18;<em> N </em>= 894). Each season c.95% of carers were
 identifiable by their unique combination of color rings. If an unringed
 carer provisioned during a watch (4.36% of watches; 39/894) we assumed all
 feeds were by the same unringed individual and omitted watches including
 &gt;1 unringed birds. The watch protocol was
 consistent throughout the study. Following a c.10 min habituation period,
 watches usually lasted for one hour between 04:00–19:30, unless curtailed
 by inclement weather (minimum duration: 30 mins). When a carer provisioned
 the brood its identity and time was recorded to the nearest minute, either
 by direct observation through binoculars (15–25m away) or video camera
 (1–5m away). Watch duration was the time between the first and last feed
 (mean = 54 mins 1 ± 25 seconds SE; range = 30–117 mins;<em> N
 </em>= 894). We excluded any watch where identities of feeds or
 hatch date were unknown, and from nests subjected to experimental
 manipulation. Long-tailed tits provision their nestlings frequently, with
 a mean rate of 23.8 feeds/h ± 0.320 SE<em> </em>(range
 4.53–69.2; <em>N </em>= 894) per group, in the sample used in
 this study. The total number of alternated and synchronized feeds was
 calculated per watch. An alternated feed was any that occurred following a
 feed by another carer (median = 15 per watch; range 1–68;<em> N
 </em>= 894), meaning that alternation did not require a consistent
 pattern of feeds (e.g. A-B-C-A-B-C), just non-consecutive feeds (e.g.
 A-B-A-C-B-A). A synchronized feed was any non-consecutive feed that
 occurred within 2 minutes of the previous feed (median = 8 per watch;
 range 0–55;<em> N </em>= 894). This 2-minute window was chosen
 to facilitate comparison with prior studies of coordination in this
 species, which found that rates of synchrony using different window
 lengths were highly correlated (r<sub>p</sub> ≥ 0.94;
 Halliwell <em>et al.</em> 2022) and key results were
 qualitatively the same (Bebbington & Hatchwell 2016; Halliwell
 <em>et al.</em> 2022). In watches where one carer performed
 &gt;50% of feeds some cannot be alternated or synchronized, so we
 calculated the ‘Maximum possible coordination’ (mean = 87.4% ± 0.414
 SE;<em> N </em>= 894) for each watch, which functions as a
 proxy for provisioning rate parity between carers.
 Because some alternation and synchrony are expected by chance
 (Schlicht <em>et al.</em> 2016, Ihle <em>et
 al.</em> 2019a, Santema <em>et al.</em> 2019) we used a
 null model to estimate levels of expected coordination (e.g. Halliwell
 <em>et al.</em> 2022; Ihle <em>et al.</em> 2019a,
 b; Johnstone <em>et al.</em> 2014). We randomized the order of
 each carer’s intervisit intervals within a watch 1000 times, which were
 then recombined to produce 1000 randomized sequences, and the median
 number of alternated and synchronized feeds were the expected levels for
 that watch. Observed and expected alternation and synchrony were used to
 generate measures of how much each watch deviated from expected, termed
 ‘Active alternation score’ (mean = 0.0663 ± 0.00499 SE;<em> N
 </em>= 894) and ‘Active synchrony score’ (mean = 0.206 ± 0.00884
 SE;<em> N </em>= 894), respectively. Alternation scores were
 calculated from log(observed alternated feeds + 0.5) – log(expected
 alternated feeds + 0.5), and synchrony scores likewise. Therefore, a
 positive score means that carers coordinated more than expected by random
 chance (i.e. if they provisioned independently), while a negative score
 denotes less coordination than expected, which may occur if carers
 provision in a manner that actively avoids alternation (i.e. in bouts of
 successive uninterrupted feeds by the same carer). We added 0.5 to each
 value to avoid taking the log of zero.
 <strong>Statistical analysis</strong>
 Statistical analysis was performed on R version 4.2.3 (R Core
 Team 2023). Models were built using lme4 (Bates <em>et
 al.</em> 2015), coxme (Therneau 2022), and analyzed with lmerTest
 (Kuznetsova <em>et al.</em> 2017). Figures were produced using
 ggplot2 (Wickham 2016), survminer (Kassambara <em>et al.</em>
 2021) and cowplot (Wilke 2020). When investigating the influence of
 alternation and synchrony on reproductive success we used ‘Active
 alternation score’ and ‘Active synchrony score’, respectively. These were
 analyzed in separate models because they are intrinsically correlated as
 synchronized feeds are, by definition, alternated. Additionally, because
 previous studies found that active alternation decreased with helper
 presence, and active synchrony with provisioning rate (Halliwell
 <em>et al.</em> 2022), we included these terms and their
 interactions with each coordination score as explanatory terms in our
 alternation and synchrony analyses, respectively. A significant
 interaction term indicates that the importance of coordination varied with
 the presence of helpers (‘Helped during watch?’ – binary factor denoting
 whether a pair was assisted by helpers in each watch, and ‘Nest helped’ –
 a binary factor denoting whether a pair was helped within the range of
 watches analyzed) or ‘(aggregate) provisioning rate’ – a continuous
 numerical variable denoting the number of feeds performed per hour by all
 carers per watch (or across several watches).
 <em>Provisioning rate (Prediction 1a):</em>
 We used a normally distributed linear mixed effects model (LMM)
 to investigate the relationship between alternation and provisioning rate
 in the<strong> Full sample </strong>of watches (N = 871 at 275
 nests; Figure S1). The response variable was the log-transformed
 provisioning rate per watch and the explanatory terms of interest were
 ‘Active alternation score’ and its interaction with ‘Helped during
 watch?’. Covariates and random effects used here and throughout are
 described below. <em>Chick mass (Predictions
 1b):</em> We fitted normally distributed LMMs to
 investigate the relationship between alternation and chick mass using a
 subset of watches taken prior to biometric assessment from nests where all
 chicks’ biometrics and sexes were known (<strong>Chick mass sample
 sex known</strong>;<em> N </em>= 360 at 185 nests
 containing 1533 chicks). The response variable was each chick’s mass on
 d11. Terms of interest were ‘Active alternation score’ (aggregated across
 each appropriate watch) and its interactions with ‘Nest helped?’ and
 ‘Aggregate provisioning rate’. <em>Recruitment
 rate (Predictions 1c):</em> We fitted a
 binomially distributed generalized LMM to investigate the relationship
 between alternation and recruitment rate, using a subset of watches from
 successful nests where each chick’s sex was known (<strong>Recruit
 sample</strong>;<em> N </em>= 574 watches at 170 nests
 containing 719 male chicks). The response variable was a two-column
 variable (number of males recruited, number of males not recruited), which
 functions as a measure of proportion recruited. Terms of interest were
 ‘Aggregate active alternation score’ and its interaction with ‘Nest
 helped?’. Because this interaction term was significant, we also repeated
 this analysis on sub-samples of biparental (2 carers) watches (N = 331 at
 101 nests containing 420 male chicks) and cooperative (&gt;2 carers)
 watches (N = 243 at 69 nests containing 299 male chicks).
 <em>Predation and survival</em> <em>(Prediction
 2):</em> To investigate survival time, we used a
 Cox proportional hazard mixed model (Therneau 2022) with the two-column
 response variable (days until event, fledged or failed) applied to
 the <strong>Predation sample, </strong>which included watches
 from nests depredated prior to ringing, for which brood size was assumed
 equal to clutch size (N = 894 watches at 293 nests). Data were right
 censored with all fledged broods defined as age 18. Terms of interest were
 ‘Aggregate active synchrony score’ and its interaction with ‘Aggregate
 provisioning rate’. <em>Covariates and random
 effects:</em> We controlled for biologically
 important covariates that could influence provisioning behavior.
 ‘Provisioning rate variation’ – a continuous numerical variable denoting
 variation in the provisioning rate during each watch (mean = 0.582 ±
 0.00733 SE;<em> N </em>= 894); included because as carers’
 intervisit intervals become more consistent, the null model’s ability to
 disrupt patterns of coordination fundamentally diminishes (supplementary
 material Tables S1 and S2; Figure S2). ‘Brood size’ (linear and quadratic)
 – an integer numerical variable denoting the number of live chicks on d11;
 included because it affects demand on carers. ‘Watch duration’ – a
 continuous numerical variable denoting the time (minutes) between the
 first and last recorded feeds per watch; included because the total number
 of feeds increases with watch duration. ‘Watch start time’ – a continuous
 numerical variable denoting the time each watch started (mean = 9:54am ± 5
 mins SE;<em> N </em>= 894); included because long-tailed tits
 have higher provisioning activity soon after sunrise (Hatchwell
 <em>et al.</em> 2004; MacColl & Hatchwell 2002).
 ‘Maximum possible coordination’ – a continuous numerical variable denoting
 the highest theoretical percentage of feeds that could be alternated (or
 synchronized) during a given watch. ‘Hatch date’ (linear and quadratic) –
 an integer numerical variable denoting the number of days between March 1
 and hatching (Median = May 3; range April 15–June 6;<em> N
 </em>= 293); included to account for within-season environmental
 variation. ‘Brood age’ – an integer numerical variable denoting the number
 of days between hatching and a watch; included because provisioning rate
 increases with age. ‘Chick sex’ – a binary factor denoting whether a chick
 was male or female; included because male chicks are typically heavier
 (Nam <em>et al.</em> 2011). ‘Brood sex ratio’ – a continuous
 numerical variable denoting the ratio of female:male chicks within a given
 brood (mean = 0.511 ± 0.0124 SE;<em> N </em>= 185); included
 to account for differences in chick mass between broods with different sex
 ratios. ‘Tarsus length’ (linear and quadratic) – a continuous numerical
 variable denoting chick tarsal length (mm). ‘Mean carer number’ – a
 continuous numerical variable denoting the mean number of carers observed
 provisioning during all watches of a given nest (mean = 3.21 ± 0.0798
 SE;<em> N </em>= 69, cooperative nests only). Random effects
 were as follows. ‘Year’ – factor denoting the year a watch was performed.
 ‘Nest ID’ – factor denoting the identity of a nest. ‘Pair ID’ – factor
 denoting the unique combination of parents. ‘Female ID’ and ‘Male ID’ –
 factors denoting the unique identity of each mother and father,
 respectively. ‘Rowref’ – observation level random effect used to account
 for overdispersion in Poisson-distributed models. Full model details are
 available in the supplementary material (Table S3).
description: This README.md file was generated on XX-XX-2024 by Chay Halliwell GENERAL
 INFORMATION 1. Title of Dataset: 'Data for: Coordination of care
 improves reproductive success by increasing investment and reducing
 predation risk in a cooperative bird.' 2. Author Information
 Corresponding Investigator Name: Dr. Chay Halliwell Institution:
 University of Sheffield, Sheffield, UK Email:
 [challiwell1@sheffield.ac.uk](mailto:challiwell1@sheffield.ac.uk)
 Co-investigator 1 Name: Prof. Andrew P. Beckerman Institution: University
 of Sheffield, Sheffield, UK Email:
 [a.beckerman@sheffield.ac.uk](mailto:a.beckerman@sheffield.ac.uk)
 Co-investigator 2 Name: Dr. Samatha Patrick Institution: University of
 Liverpool, Liverpool, UK Email:
 [samantha.patrick@liverpool.ac.uk](mailto:samantha.patrick@liverpool.ac.uk) Co-investigator 3 Name: Prof. Ben J. Hatchwell Insitution: University of Sheffield, Sheffield, UK Email: [b.hatchwell@sheffield.ac.uk](mailto:b.hatchwell@sheffield.ac.uk) 3. Date of data collection: 1994-2022 4. Geographic location of data collection: Rivelin Valley, Sheffield, UK 5. Keywords: Aegithalos caudatus, coordination of care, facultative cooperative breeding, synchrony, alternation, conflict resolution, parental care, depredation, antipredator defence 6. Language information: English DATA AND FILE OVERVIEW 1. Description of dataset This is a dataset of provisioning watches taken at long-tailed tit (Aegithalos caudatus) nests during the period where both parents (and sometimes helpers) provisioning their brood together (Day 6-16). These data were collected either by direct observation via binoculars or via video camera and subsequent review. During each provisioning watch the time (to the nearest minute) and identity of each carer was recorded upon observing them provision the brood. This dataset contains information specific to each watch, such as watch duration, the maximum theoretical number of coordinated feeds, the brood age when watched, the provisioning rate, the watch time and whether the nest was helped by a non-breeder. This dataset contains information specific to each nest, such as hatch date, brood size, brood sex ratio and whether a nest was helped by non-breeders. This dataset contains information specific to each chick, such as sex, weight and tarsus length. These raw data were processed using the coding language R (on Rstudio) to calculate 'active coordination scores' per watch and per nest, these values were then regressed against important predictors of reproductive success, such as chick mass, fledging success, nest survival and offspring recruitment. 1. File list File 1 name: df_chick_mass_1994-2022.csv File 1 description: Full list of each bird that was weighed as a chick on day 11 post-hatching, their natal nest, their mass (in grams), their tarsus lengths (in mm) and their sex. File 2 name: df_prov_watches_1994-2022.csv File 2 description: Full list of the time and identity of each carer that provisioned their brood during each watch, as well as the nest identity, the age during each provisioning watch and the year the watch was performed. File 3 name: df_watch_data_1994-2022.csv File 3 description: Full list of all watch and nest specific details including: year, brood age, whether a nest was predated, clutch size, brood size, hatch date, watch start time, carer IDs, number fledged, number recruited, watch duration, number of feeds, provisioning rate, brood sex ratio etc. METHODOLOGICAL INFORMATION These data were collected as part of a long-term intensive monitoring project of long-tailed tits in the Rivelin Valley field site located near Sheffield, UK. Nest and chick specific data were collected throughout the nest's development, with several key details collected during biometric assessment at day 11 post-hatching. During biometric assessment, half of all chicks were removed from the nest, weighed (in g), tarsus lengths measured (in mm) and blood samples (5–20µl) taken before being returned to the nest and the process immediately repeated for the other half of the brood. Provisioning watches were typically conducted (either by direct observation or by video camera) every other day from when both parents provision the brood directly (day 6) until either failure of fledging (typically day 16-17). The time and identity of each provisioning visit was collected during a watch, as well as watch specific data such as watch duration and brood age. Data were processed such that scores for how much each group alternated and synchronised their provisioning visits during each watch and aggregated over the course of several watches per nest. Active alternation and synchrony scores were calculated by deducting the log of the number of expected alternated (or synchronised) visits from the log of the number of observed alternated (or synchronised feeds). An alternated visit was any which followed the feed of another carer, rather than the feed by oneself. A synchronised visit was any which followed the feed of another carer and occurred within 2 minutes of the previous feed. Active alternation and synchrony scores were regressed (in separate models) against important metrics of reproductive success e.g. chick mass, fledging success, nest survival and recruitment. DATA-SPECIFIC INFORMATION FOR: df_chick_mass_1994-2022.csv 1. Number of variables: 5 2. Number of rows: 2311 3. Variable list: Nest: unique identifier for each nest which was watched BirdID: unique identifier for each bird sampled as a chick within the nest Weight.round: the mass, in grams, of each chick to the nearest 0.1g Tarsus.round: the length, in millimetres, of each chick to the nearest 0.1mm Chick.sex: the sex of each chick 4. Missing data codes: NA - Not applicable 5. Abbreviations used: ID - Identification 6. Other relevant information: NA DATA-SPECIFIC INFORMATION FOR: df_prov_watches_1994-2022.csv 1. Number of variables: 12 2. Number of rows: 23305 3. Variable list: ID: unique identifier for each provisioning watch performed Year: unique identifier for the year upon which a watch was performed Nest: unique identifier for each nest which was watched Day: the number of days since hatching that a watch was performed on, i.e. the brood age real.time: the time that each feeding visit occurred Female.ID/Male.ID/Helper1/Helper2/Helper3/Helper4/Helper5: unique identifier for which carer performed this row's corresponding feed 4. Missing data codes: NA - Not applicable 5. Abbreviations used: ID - Identification 6. Other relevant information: NA DATA-SPECIFIC INFORMATION FOR: df_watch_data_1994-2022.csv 1. Number of variables: 32 2. Number of rows: 1070 3. Variable list: ID: unique identifier for each provisioning watch performed Nest: unique identifier for each nest which was watched Day: the number of days since hatching that a watch was performed on, i.e. the brood age Fate: factor designating whether a nest was fully predated, partially predated, fledged or failed for other reasons Age.known: binary factor designating whether the age at which a nest was predated was known Fate.grouped: factor designating whether a nest was predated or fledged (all other outcomes = NA) Year: unique identifier for the year on which a nest was watched clutch.size: the number of eggs found within a nest following the start of incubation brood.size: the number of live chicks found within a nest on day 11 post-hatching fledged.number: the number of chicks per nest that successfully fledged not.fledged.number: the number of chicks per nest that hatched, but did not successfully fledge JulianHatchDate: the number of days after March 1 of each year that each nest hatched watch.start.time: the time of day upon which a watch first commenced FemaleID/MaleID/Helper1ID/Helper2ID/Helper3ID/Helper4ID/Helper5ID: unique identifer for each bird that was the breeding female/breeding male/helper at a given nest Number.males: the number of live male chicks recorded in each nest on day 11 post-hatching All.sexes.known: binary factor designating whether the sexes of each chick within a brood were known Biometrics.known: binary factor designating whether the masses and tarsus lengths of each chick within a brood were known Number.male.recruits: the number of male chicks per nest which successfully recruited into the local breeding population Number.males.not.recruited: the number of male chicks per nest which did not successfully recruit into the local breeding population Proportion.males.recruited: the proportion of male chicks per brood which were successfully recruited into the local breeding population Carer.number: the number of carers recorded as provisioning a brood during a given watch Watch.duration.mins: the time (in minutes) between the first and last recorded feeding visits of a given watch Total.feeds: the total number of feeding visits recorded by all carers during a given watch Feeds.per.hour: the hourly provisioning rate by all carers during a given watch Brood.sex.ratio: the ratio of live male chicks to live female chicks recorded in a given nest on day 11 post-hatching 4. Missing data codes: NA - Not applicable 5. Abbreviations used: ID - Identification 6. Other relevant information: NA