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Coordination of parental performance is breeding phase-dependent in the Dovekie (Alle alle), a pelagic Arctic seabird
Changes in parental coordination during breeding
https://orcid.org/0000-0002-1475-3287
Grissot Antoine Conceptualization Data curation Formal analysis Investigation Methodology Writing – original draft Writing – review & editing 1 *
Altmeyer Lauraleen Conceptualization Data curation Formal analysis Methodology Writing – review & editing 1 2 3
Devogel Marion Data curation Writing – review & editing 1
https://orcid.org/0009-0001-8469-792X
Zalewska Emilia Data curation Writing – review & editing 1
Borrel Clara Data curation Writing – review & editing 1 2 3
https://orcid.org/0000-0001-6706-7793
Kidawa Dorota Funding acquisition Resources Writing – review & editing 1
https://orcid.org/0000-0002-1879-4342
Jakubas Dariusz Conceptualization Methodology Resources Writing – review & editing 1
https://orcid.org/0000-0001-6230-0509
Wojczulanis-Jakubas Katarzyna Conceptualization Data curation Formal analysis Funding acquisition Methodology Resources Writing – review & editing 1
1 Faculty of Biology, Department of Vertebrate Ecology and Zoology, University of Gdańsk, Gdańsk, Poland
2 Université de Rennes 1, Rennes CEDEX, France
3 L’institut Agro (AgroCampus Ouest Rennes), Rennes Cedex, France
Brundage Cord M. Editor
University of Wisconsin-La Crosse, UNITED STATES OF AMERICA
Competing Interests: The authors have declared that no competing interests exist.

* E-mail: antoine.grissot@gmail.com
4 9 2024
2024
19 9 e03067964 12 2023
24 6 2024
© 2024 Grissot et al
2024
Grissot et al
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Currently, parental care is becoming increasingly perceived as male and female cooperation, instead of being primarily shaped by sexual conflict. Most studies examining cooperating performance consider coordination of parental activities, and doing so focuses on a short time-window including only one stage of breeding (i.e., incubation or chick rearing period). Here, we considered the cooperation of breeding partners, investigating the coordination of parental care in a long-lived seabird species with long and extensive biparental care, the Dovekie (or Little Auk), Alle alle, and looked at the issue throughout the breeding season. Previous studies on this species revealed coordinated chick provisioning, but parental coordination during incubation remains unstudied. Using video recordings collected over the course of two breeding seasons, we tested whether coordination was subject to small-scale changes within each stage and whether there was a relationship between coordination levels across the two stages. We found that the level of parental coordination is overall high and increases during the incubation period but decreases through the chick rearing phases. There were some inter-annual differences in the coordination level both at the incubation and chick rearing stages. We also found some dependency between the coordination during the incubation and chick rearing periods. All these results suggest that coordination is not a fixed behavior but breeding-phase dependent. The present study thus provides insights into how parental care and parents’ cooperation is shaped by brood needs and conditions. It also highlights a relationship between coordination levels during chick rearing and incubation periods, suggesting some extent of temporal dependence in coordination of parental performance within the breeding season.

http://dx.doi.org/10.13039/501100004442 Narodowym Centrum Nauki 2017/25/B/NZ8/01417 https://orcid.org/0000-0001-6230-0509
Wojczulanis-Jakubas Katarzyna http://dx.doi.org/10.13039/501100004281 Narodowe Centrum Nauki 2017/26/D/NZ8/00005 https://orcid.org/0000-0001-6706-7793
Kidawa Dorota The study was supported by Poland through National Science Centre (no: 2017/25/B/NZ8/01417 to KWJ, and no: 2017/26/D/NZ8/00005 to DK). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Data AvailabilityThe data underlying this study and the script required for result reproduction are available online at: https://doi.org/10.57745/DH9MKM.
Data Availability

The data underlying this study and the script required for result reproduction are available online at: https://doi.org/10.57745/DH9MKM.
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pmcIntroduction

Parental care is widely spread among animals, allowing a parent to increase its inclusive fitness through successful reproduction [1, 2]. However, investing in care is costly in terms of time and energy devoted to the offspring [3] and a parent engaging into the care of the current offspring could jeopardize its survival and/or future reproduction [4, 5]. Therefore parenting individuals have to balance resource allocation between current offspring care and self-maintenance [6]. When two parents are involved in care, as is the case in 81% of avian species [7], the complexity of interactions increases and sexual conflict over the care arises (summarised by Parker et al. [8]). This sexual conflict is illustrated by one individual free-riding on the other’s effort, as both partners benefit from joint investment in care provided to the offspring but each pays a cost of providing that care on their own [4, 9–12]. This interplay of conflicted partners may lead to lower fitness of the offspring, as demonstrated both theoretically [13] and empirically [14]. However, a cooperation manifested by coordination in parental activities was proposed as a mitigation of this conflict, with a focus on bird species with biparental care [15, 16] and reviewed by Griffith [17].

An increasing number of studies suggests that the coordination of parental performance in birds with biparental care system, such as synchronization or alternation of nest visits during the incubation or chick rearing period, may increase the breeding success [18–22]. For example, Eurasian Blackcap, Sylvia atricapilla, parents synchronize their feeding visits in respect to each other. This way, they minimize the disturbance around the nest and, in turn, reduce the risk of nest predation [23]. Parents adjusting their performance in respect to each other may also mutually improve their own body condition, which is essential for future reproduction [24–26]. The latter issue is particularly relevant in avian species with a long-term pair bond [20], where both partners benefit from their higher survival owing to the familiarity effect (i.e., reduced time investment in pair bonding in successive breeding seasons and/or more efficient parental care with a known partner) and partner value (i.e., long-term advantages of staying with the same partner; see Griffith [17]). Indeed, there is evidence that partners that meet earlier and/or stay together for a longer period of time exhibit better breeding performance than newly formed pairs [27, 28].

Studies on parental coordination in birds initially focused on the feeding of offspring and most of the work has been performed on passerines [18, 19, 29]. Recently, other species and stages of breeding (incubation and chick rearing) have been investigated, revealing a very broad range of species-specific behavioral patterns and mechanisms [24]. However, many studies considering parental coordination still focus on a short time-window, within a single breeding stage, rather than considering it over a longer period of time, such as a whole breeding stage or the whole breeding season. Even when a breeding stage is considered in its entirety [24, 30], changes in parental coordination over the course of the period are often overlooked. Since each breeding stage has its own specific characteristics, for instance in parental behavior [31, 32], metabolic rate [33, 34], levels of various hormones [31, 35] and body conditions parameters [36], one could expect that these characteristics also influence the coordination of parental performance.

Parental coordination at particular stages of breeding (i.e., incubation or chick rearing) may be expected to be an outcome of environmental pressures, as the parental care system evolved in response to environmental conditions [37–39]. Harsh and/or unpredictable environmental conditions impose obligatory biparental care, whereas habitats with temporarily abundant food resources make biparental care facultative and condition-dependent [7, 40–42]. Similarly, changes in environmental conditions over the course of breeding may force parents to coordinate during particular stages of breeding at a level dependent to environmental challenges. As a consequence, one may expect coordination to be higher during the incubation than the chick rearing period in some species. For example, in those living in a harsh environment, where low ambient temperature would be a key environmental variable, parents may exhibit higher coordination during the incubation than during the chick rearing period, as a developing embryo may be more sensitive to parental neglect than a hatched chick. However, in most bird species parents will not coordinate their activities at all during the incubation period, as each of them has their sex-specific tasks, with females often incubating on their own and males guarding the nest site/territory [7]. Then, during the chick rearing, when tasks are similar for male and female parents [7], factors such as thermal dependency of the chicks, food availability and/or predation pressure may elicit parental coordination. For example, in the context of high predation pressure in the environment, parents may coordinate food delivery to the offspring in a way that minimizes disturbance around the nest, and so the risk of predation [23]. Finally, similar level of parental coordination may be expected during the incubation and chick rearing period in species where full engagement into parental care by both the female and male is crucial to raise the brood successfully [7], although drivers of the coordination may be different for each phase.

Within a breeding stage parental coordination may also change, as both needs of the brood and the environmental context change over time. During the incubation, parental coordination may be most important at a later phase of the period, as well developed embryos may be more sensitive to parent neglect than an embryo that just started to develop [43]. If this is the case, parental coordination is expected to increase over the incubation period. During chick rearing, young chicks may be thermally dependent on the parents (require brooding) as well as more sensitive to both predation and starvation than older ones. Thus, parents may better coordinate their provisioning at the early phase of the chick rearing. Indeed, some studies demonstrate that the level of parental coordination is higher at the beginning of the chick rearing than later in the season [23], but see Baldan & Griggo [44]. Then, environmental conditions related to ambient temperature and food abundance may also change during the breeding period, affecting birds’ overall performance, including parental coordination. For example, piscivorous seabirds breeding in large colonies face depleted food resources over the breeding season in close vicinity of the colony (so called “Storer-Ashmole” or “halo” effect [45, 46]), which results in increased duration of the foraging trips [47–49]. Changes in duration of the foraging trips are then likely to impose changes in parental coordination of food provisioning.

For species that exhibit coordinated parental care during both incubation and chick rearing periods, an unanswered question is whether the parents are somehow consistent in their performance over the whole breeding season (but see McCully et al. [50]). Due to different behavioral and coordinational patterns (e.g., alternation of incubation and synchronization of nest visits to reduce predation pressure during chick rearing period), as well as levels of parental investment and associated costs during the two periods, one could expect them to be unrelated to each other. On the other hand, at the beginning of the season, parents may need time to adjust to each other and synchronise their actions. Then, physiological changes over the season may further affect the parental performance [51], leading to higher parental coordination later in the season than at its onset. Understanding this interconnection between breeding stages is an important step to fully understand mechanisms behind all the observed patterns of parental coordination.

Pelagic seabirds are top marine predators, with life-history traits that make them ideal model species for investigating cooperation in parental care. Most species are long-lived, socially and genetically monogamous with a long-term pair bond, and long, extensive biparental care. Contribution of breeding partners is usually similar in all the parental tasks (i.e., incubation, brooding, and provisioning the offspring [52]), and partner value is usually high [17]. In such a system, parental cooperation is likely to be favoured by selection [17]. Besides, as seabirds forage on food resources that are unpredictable in space and time [53], raising their offspring may be particularly costly. Therefore, both parents’ contribution is essential for successful breeding [52]. Thus, coordination of parental activities in seabirds is thought to be a key adaptation for coping with the harsh and variable environment they breed in. Indeed, it has already been demonstrated that seabird parents coordinate their parental performance [22, 24–26].

In this study, we focus on a small Arctic seabird, the Dovekie (or Little Auk), Alle alle, to study changes in parental coordination across the whole breeding season, and a potential interconnection between levels of coordination during the incubation and chick rearing periods. The Dovekie exhibits a life-history strategy typical to seabirds (i.e., long-lived, socially monogamous with long-term pair bond, and long and extensive biparental care over a brood of small size, here restricted to a single chick), which makes it a good model species to study coordination (reviewed in Wojczulanis-Jakubas et al. [54]). The coordination of parental duties in this species has been demonstrated, although solely focusing on chick provisioning during the mid phase of the chick rearing period [25, 26]. Thus here, we aim to extend previous work on Dovekie parental coordination, by investigating it both during the incubation and chick rearing periods, and analyzing its level (and consistency) both within and between the two periods.

Egg protection and thermoregulation may be crucial for hatching success in the conditions of the cold Arctic summer [55]. However, the egg has apparently some tolerance to temporary neglection (no precise data available but our personal observations suggest a few minutes to up to a couple of hours) We thus hypothesized that Dovekie parents coordinated their activities during the incubation period in a way that would maximize the presence of one parent in the nest (thus possibly also the hatching success). If that is the case, we expected that when one parent was incubating the egg (offspring maintenance), the other was foraging (self-maintenance) and they would exchange; the egg would then be continuously incubated and both partners could replenish their body reserves after a long incubation bout. We further expected a positive progression of this coordination over the course of the incubation period due to, for instance, hormonal changes [56]. Since the pelagic life-style of the Dovekie imposes long lasting foraging trips, we also hypothesized that parents would coordinate these trips during the chick rearing period in a way that optimized the food delivery rate to the chick. We further hypothesized that this coordination would be particularly important at early phase of the chick’s life, when chick is not yet thermoregulatory independent (first week of life) and may be more prone to starvation [57–59]. Consistently, we expected that parental coordination in chick provisioning will be higher at early than mid chick rearing phase. Finally, expecting some sort of dependency in parental behavior between the incubation and chick rearing periods, we hypothesized that coordination established during the incubation would be related to the coordination at the later phases of breeding, with pairs highly coordinated during incubation sustaining high level of coordination also during the chick rearing period.

Methods

Study site and video recordings

We performed the fieldwork in two consecutive breeding seasons, 2019 and 2020 (June to August) in the Dovekie colony at Ariekammen slope (77°00′ N, 15°33′ E) in Hornsund, SW Spitsbergen. This very well-studied colony is located in one of the densest breeding concentrations of Dovekies in Svalbard (ca 590,000 breeding pairs [60]). All fieldwork was performed under supervision of KWJ and DJ (having the relevant qualifications and experience). While marking birds, we handled them for no more than 5 minutes and put them back in the nest unharmed just after the procedure. We recorded and handled the birds under permission of the Norwegian Animal Research Committee and the Governor of Svalbard (2007/00150-9, 2007/00150-11, 17/00663-2, 17/00663-7). We monitored 23 breeding pairs in 2019, and 20 out of theses 23 pairs were monitored again in 2020. We established phenology (egg laying, hatching, and fledging date) by recording nest content (i.e., egg/chick) every day for a week before an expected event, according to known phenology from previous seasons and usual length of incubation and chick rearing periods (28 and 21 days respectively for hatching and fledging [55]). In 2020, egg laying events could not be monitored, thus for both seasons hatching date was used as a reference point of bird phenology. We established breeding success based on whether or not the breeding attempt led to a successful fledging, and only included successful pairs in further analyses, resulting in 18 pairs in 2019, and 16 in 2020 (with 13 pairs monitored and successful in both studied seasons), accounting in total for 21 different pairs over the two investigated seasons. Although considering failed breeders could be helpful in understanding of coordination mechanisms, it would change the study question and our sample size would not be sufficient. Thus, with the main aim to analyze the parents’ performance across the whole breeding season, we focused on successful breeders only. Hence, our inference on parental coordination dynamics applies only to successful breeding pairs.

Each parent in each pair was metal-ringed and molecularly sexed in previous seasons, and additionally marked in the study seasons by a unique combination of colour rings and a colour mark on the breast’s feathers (waterproof markers, Sharpie USA). The area surrounding the monitored pair’s nest was video-recorded using a separate video camera (commercial HD model of JVC, Japan) placed in front of its entrance. Chosen settings allowed to record presence/absence and behavior of focal parents within a 3 m radius from their nest entrance. This is the principal area where the birds spent their time when in the colony (based on own direct observations of bird behavior in the study colony). All recordings were made in a time-lapse mode (1 frame per sec), which allowed to capture all the birds presence and behaviors of interest, while economizing memory space and later processing of the video material.

Each pair was video-recorded for several continuous 48-hour sessions, aimed to be distributed equally over the whole breeding period. Throughout the incubation, we aimed to record three sessions per pair representing the early, mid, and late phases of incubation. However, due to the aforementioned lack of egg laying data for 2020, the recordings were performed in a slightly different way for the two years: in accordance with egg laying date of each pair in 2019 (i.e., adjusted to the pair phenology) and on fixed calendar days for all pairs in 2020 (i.e., a priori unknown phenology) with the incubation phase being back-calculated using the hatching date. Dovekies are highly synchronised in breeding phenology at the population level [61], and hatching dates are usually distributed over a week (Jakubas et al. [62] and personal observations). As a consequence, in 2020 the first session (supposed to be representing the early incubation phase) started when pairs were on average in the 20th day before hatching (min-max: 16–27 d), when it was the 26th day before hatching (min-max: 24–27 d) in 2019. The second session (mid incubation phase), on average, started on the 12th day before hatching (min-max: 8–19 d) in 2020, whereas it was the 15th day before hatching (min-max: 13–17 d) in 2019. The third session (late incubation phase) in 2020 started on the 4th day before hatching (min-max: 2–11 d), against the 5th day before hatching (min-max: 4–7 d) in 2019 (see S1 Table). Given the wider range of incubation phases present in each type of recording session in 2020, it was not fully comparable with 2019. Therefore, further analyses including both years used the relative days before hatching date as a measure of the incubation phase. During the chick rearing period in both studied years, we performed two recording sessions per pair, perfectly timed to hatching phenology, representing the early (session started when chick was 4 days after hatching on average; min-max: 3–5 d) and mid chick rearing phases (11 days after hatching; min-max: 11–12 d). The phase of the period is therefore represented by a different metric for incubation (number of day before hatching: continuous) and chick rearing period (early or mid: categorical), but still conveys the same concept of when the recording session was performed in respect to the breeding period (early, mid, late).

The video material was then processed using VLC software (VideoLAN, France) or QuickTime player (Apple Inc. USA). While watching the videos, we noted the time (with 1 sec precision) when focal individuals were appearing/disappearing on the frame and when they were entering/exiting the nest. We also noted the presence/absence of food in adult bird gular pouch. Videos had to be processed manually, which is time-consuming and so, for efficiency, they were split between four observers (AG, LA, CB, MD). An extensive video processing training was performed using inter-observer comparisons. For that, data from videos already processed by the lead observer (AG) were used to be compared with the output from the same videos processed by observers in training. We kept training until we reached 100% similarity of the output for few videos. The birds presence/absence and food in the gular pouch are all very conspicuous, and thus inter-observer difference in the outcome of the video watching was negligible, being solely the question of 1–2 seconds difference in the time-stamp for an event (i.e., none of the birds presence/absence with/without food was recorded differently by independent observers). Due to camera failure and/or bad quality of the framing around the nest entrance, some sessions had to be discarded, and so sample size varied slightly among the analyses (provided in details in Table 1). We extracted from the video recordings the following behavioral categories expressed by time-intervals between important events: (1) “nest”–the time interval between when a focal individual entered and exited the nest (both incubation and chick rearing period); (2) “colony”–the time interval between when a focal individual was visible in the nest vicinity but not in the nest (i.e., seen repetitively in the frame, with < 1 h gap in between each at-frame presence, both periods). Individuals, when present in the colony, spend most of their time in the surroundings of their nest (Pers. Observations). Furthermore when they leave the frame and come back with a full gular pouch, we know a foraging trip was performed. There is a possibility that they spend a little time in the colony without being seen on screen before actually departing for the foraging trip, however this time is negligible; and (3) “foraging”–the time interval when a focal individual disappeared for ≥ 1 h (the incubation period), or the time interval between when a focal individual left the frame and came back with a full gular pouch (chick rearing period only). We choose the threshold of 1 h for the foraging trip based on previous studies on foraging durations, where average duration of the short trips was 2.03–2.41 hours [53, 63–66]. We have also never observed in the present study a bird coming back to the colony with a food load (indicating foraging) after an absence shorter than one hour.

10.1371/journal.pone.0306796.t001 Table 1 Model structures and summaries for the models of coordination changes within and between breeding stages.

Model	Type of Model	Family(link)	Model structure	Explanatory variable	Df	Estimate	SE	stat	stat_value	p_value	N	
incubation	GLMM	Gamma(inverse)	incubation coordination ~ incubation phase (continuous; number of days before hatching) * year + (1|nest)	(Intercept)	1	0.00000561	0.00000018	Chisq	1011.04	0	92 recording sessions from 19 nests	
incubation phase	1	-0.00000005	0.00000001	Chisq	19.25	0	
year	1	0.00000032	0.00000027	Chisq	1.38	0.24	
incubation phase: year	1	-0.00000005	0.00000002	Chisq	6.33	0.012	
chick rearing	LMM	Gaussian 	chick rearing coordination ~ chick rearing phase (categorical; early or mid) * year + (1|nest)	(Intercept)	1	0.48840530	0.10623574	Chisq	21.14	0	66 recording sessions from 21 nests	
chick rearing phase	1	-0.45370521	0.15024002	Chisq	9.12	0.003	
year	1	-0.56859031	0.15757306	Chisq	13.02	0	
chick rearing phase: year	1	0.66636030	0.22284196	Chisq	8.94	0.003	
early chick rearing	LM	Gaussian 	early chick rearing coordination index ~ early incubation coordination + mid incubation coordination + late incubation coordination	(Intercept)	1	5.56551650	2.74963966	F.value	4.1	0.068	15 recording sessions from 15 nests	
early incubation coordination	1	-0.00001279	0.00000814	F.value	2.47	0.144	
mid incubation coordination	1	-0.00000470	0.00000720	F.value	0.43	0.527	
late incubation coordination	1	-0.00001446	0.00001428	F.value	1.03	0.333	
mid chick rearing	LM	Gaussian 	mid chick rearing coordination index ~ early incubation coordination + mid incubation coordination + late incubation coordination	(Intercept)	1	2.45268550	2.62706064	F.value	0.87	0.371	15 recording sessions from 15 nests	
early incubation coordination	1	-0.00001996	0.00000778	F.value	6.59	0.026	
mid incubation coordination	1	0.00002316	0.00000688	F.value	11.33	0.006	
late incubation coordination	1	-0.00002005	0.00001364	F.value	2.16	0.17	
Significant explanatory variables are indicated by a bold p value. Df: degrees of freedom; Estimate: unstandardised effect size indicating the relationship between the response variable and each explanatory variable; SE: Standard Error; N: sample size of specific models.

All data manipulations and statistical analyses were performed in R environment version 4.1.2 [67], using custom made functions or existing packages, specified in the relevant context. Statistical significance was considered at alpha level of < 0.05.

Coordination of parental care during the incubation period

To investigate parental coordination during the incubation period, we focused on the three behavioral categories described above: “nest”, “colony” and “foraging”. They represent, quite accurately, main Dovekie parental activities during the incubation period. Indeed, to ensure successful development of the embryo resulting in hatching, the egg needs to be kept within viable temperatures, and therefore cannot be left unattended for too long [55]. Thus, each parent is faced with a trade-off between the need to incubate the egg (represented here by “nest” category, i.e., the time they spend in the nest) and their own need to maintain body reserves (“foraging” category, i.e., the time they spend in foraging). When considering the Dovekie pair, potential conflict could rise from both partners addressing the trade-off independently from each other (e.g., foraging at the same time and leaving the egg unattended, or simultaneously present at the colony and risking depletion of their body reserves). This conflict could be mitigated by coordination, i.e., partners doing the opposite activity in respect to each other (“nest” vs “foraging” or vice versa). To establish whether sexual conflict is apparent or is mitigated by coordination during the incubation, we calculated the amount of time when one partner was in the nest, while the other partner was foraging, and tested its significance by comparison with what could be expected by chance. We used a Monte Carlo randomization approach, following Wojczulanis-Jakubas et al. [25] and Grissot et al. [26], where this procedure was used for the investigation of coordinated chick provisioning. During the randomization procedure, performed separately for every recording session, we shuffled 10,000 times the observed continuous pattern of the three activity categories (“nest”, “colony” and “foraging”) for both male and female of each pair in each incubation session, with specific constraints (e.g., a “colony” activity always present before and after each “nest” and “foraging” activities), and then we compared the obtained randomised patterns with the originally observed pattern. In total, in the two investigated seasons we performed the procedure for 92 recording sessions of 19 different pairs. We calculated a p-value for each session, as the proportion of randomisation iterations where the observed value (i.e., the observed proportion of time spent performing opposite activities for a given pair) was smaller than the expected random value (i.e., the proportion of time spent performing opposite activities calculated for each randomisation iteration). We assumed that if parents spend more time doing opposite activities than what is expected by chance, then they are actively coordinating their parental activities.

Changes in parental coordination throughout the incubation period

For further analyses, the amount of time when the two parents performed opposite activities (i.e., one partner was in the nest, while the other was foraging) was used as a proxy for their coordination. We chose to use the duration per se instead of using the calculated p-value, or calculating an index based on our randomisation procedure (as for the coordinated provisioning, here and in Wojczulanis-Jakubas et al. [25], Grissot et al. [26]), to account for the fact that during the incubation period, the time prevalence of two main activities (i.e., incubation and foraging bouts) leaves little space for chance in the randomization procedure in the finite unit of 48 h that we considered. If coordination index during the incubation was to be calculated following the previously used procedures [25, 26], the described constraints could lead to a flattened value of the index. Instead, a crude duration of time intervals with overlapping partners activities exhibits considerable variation over the time. Importantly, the amount of time when the two parents performed opposite activities represents the coordination of parental performance well, and this is despite an increase in the duration of incubation bouts and/or foraging trips over time. This is because in the finite unit of time each parent can perform three behavioral activities (“nest”, “colony” and “foraging”), with only two of them representing the needs of offspring (“nest”) and themselves (“foraging”), the more they perform opposite activities satisfying one or the other need, in regard to each other, the more they are coordinating in the sense we consider in the present study.

To explore the changes in coordination of parental activities during the incubation period, we constructed a generalised linear mixed model with the amount of time partners performed opposite activities during a recording session as the response variable, and the phase of incubation (represented by the number of days before hatching, taken as a continuous variable) as well as the year and their interaction as explanatory variables. We included the year and its interaction with the incubation phase, as inter-annual meteorological and oceanographic variations between the two years [68] could lead to different incubation constraints. Given the fact that the response variable is an amount of time and thus follows a gamma distribution, we used this type of distribution, with an inverse link function within the glmer() function from the lme4 package [69]. To account for pseudoreplication associated with multiple representation of the same pairs in data set, we also included pair identity as a random effect. We tested significance of explanatory variables with the Anova() function, using type III Wald Chi-square tests from the package car [70]. Assumptions of homoscedasticity and normal distribution of residuals were verified in the model by visual inspection of diagnostic plots. All details of model structure and results of this model, including p-values for each variable tested, as well as unstandardised effect sizes in the form of estimates of the models and standard errors are provided in Table 1.

Parental coordination throughout the chick rearing period

To investigate parental coordination during the chick rearing period, we focused on chick provisioning as the main parental activity. To do so, and following Grissot et al. [26], we considered “foraging” and “at colony” activities, with the latter being “nest” and “colony” activities combined, as during the chick rearing period, the time spent in the nest is mainly dedicated to chick provisioning and therefore consists of quick visits. Besides, in contrast to incubation, Dovekies in the study population exhibit bimodal foraging trip strategy during the chick rearing period, where a parent alternates between long trips (primarily to maintain their own body condition, as birds gain body mass during these trips) with a consecutive series of short trips (for chick provisioning, with some body mass loss for themselves [71]. Thus, the two types of foraging trips well represent parental trade-offs over care and self-maintenance during the chick rearing period. It has been shown previously during mid chick rearing that potential conflict generated by this situation can be avoided through coordination by the two parents, effectively avoiding the performance of long trips at the same time [25, 26]. Here, we adopted a procedure previously utilized in similar context [25, 26], and split the “foraging” activity into “short trips” and “long trips”, according to the method proposed by Welcker et al. [63]. This method consisted in finding a threshold value of trip duration, that split data into two groups (short and long trips) of minimum sum of variances, given their log-transformed data distribution. The data were log-transformed to better separate the two groups (otherwise the division of the two groups is fuzzy and finding a cut-off point is not straightforward). This procedure was done separately for each chick rearing phase (i.e., early and mid) in each season, and the two optimal groups were obtained with a threshold at 6.1, 6.0 hours for the early chick rearing phase of 2019 and 2020, respectively, and at 8.95 and 8.55 for the mid chick rearing phase of 2019 and 2020, respectively (detailed information about mean duration of both trip categories for each chick rearing phase in the two investigated seasons is provided in S2 Table). Then, we calculated the observed within pair amount of time that one individual was performing a short foraging trip, and its partner a long foraging trip. We then shuffled with constraints (“at colony” always before and after a foraging trip) 10,000 times the chick provisioning patterns of the two partners. We calculated, for each iteration, the amount of time when one individual was performing a short foraging trip, while its partner was performing a long foraging trip within the obtained shuffled pattern and compared it with the originally observed one. We performed the procedure for 66 chick rearing recordings sessions from 21 different nests and we calculated a p-value for each session as the proportion of randomisation iterations where the observed value was smaller than the expected random value.

We then calculated the coordination index coined by Wojczulanis-Jakubas et al. [25] using the formula: [obs—exp] x exp−1, where obs is the observed amount of time with one partner performing a short trip and the other on a long trip and exp is the mean of all the values obtained during the randomisation procedure. For the chick rearing period, we decided to use the coordination index instead of crude values of short-long trip overlaps between the partners to reduce some “noise” in the data related to how short and long trips were calculated. To split the trips into the two types we used the method proposed by Welcker et al. [63], where a cut-off is applied for the continuous variable, resulting in trips of duration around the cut-off point being somehow uncertain in respect to their purpose.

We explored the changes of the coordination index over the course of the chick rearing period by fitting a linear mixed model using the lmer() function of the package lme4, with the coordination index as the response variable, and the phase of the chick rearing period (representing whether the recording session was performed in the early or mid phase of the chick rearing period, a categorical variable) as well as the year and their interaction as explanatory variables (for the same reasons as for the incubation period detailed above). To account for pseudoreplication (multiple representation of given pairs), we also included pair identity as a random effect. Significance of explanatory variables was established as for the models in the incubation period. Whenever we found qualitative explanatory variables or their interactions to be significant, we performed post-hoc Tukey tests to assess specific differences, using the emmeans() function from the emmeans package [72]. We performed the Tukey tests with all possible pair-wise combination, despite it being conservative, to prioritise control of 1st type error, but we reported in the results and on Fig 2 only the biologically meaningful comparisons. Assumptions of homoscedasticity and normal distribution of residuals were also verified in the model by visual inspection of diagnostic plots. We provided details of the structure and results of this model in Table 1.

Link between the coordination in incubation and chick rearing

We investigated a potential relationship between the coordination of the two breeding stages (i.e., incubation and chick rearing). To account for differences within the incubation period, we selected only data from 2019, for which we performed three recording sessions clearly separated in terms of phenology, therefore the phase of incubation is here represented as a categorical variable with three levels (early, mid, and late). We also included in this analysis only the pairs for which we had three incubation recording sessions successfully performed, as well as two full chick rearing recording sessions, resulting in a sample size of 15 pairs. We fitted a linear model with coordination index in the chick rearing period as a response variable, and coordination during each phase of the incubation period (i.e., amount of time partners are performing opposite activities) as explanatory variables. In order to account for differences between phases of the chick rearing period (i.e., early and mid), we fitted two separate models, one for each phase of the chick rearing period, and we included in the models parental coordination in each phase of the incubation (early, mid, and late) as independent explanatory variables. We checked the non-multicollinearity of the explanatory variables in both models by calculating the variance inflation factor (1.08, 1.07 and 1.01 for early, mid and late incubation coordination, respectively) using the vif() function from the car package. Like previously, we tested their significance with type III Wald Chi-square. We also verified assumptions of homoscedasticity and normal distribution of residuals in these models by visual inspection of diagnostic plots (S1, S2, S4 and S5 Figs in S1 File). Due to relatively small sample size and potentially influential points (Fig 3), we additionally evaluated the estimates of the models with a bootstrap procedure (results presented in S1 File). We provide structure and results of the models in Table 1.

Results

Parental coordination throughout incubation

During the incubation period, the amount of time when one partner was incubating in the nest while the other was foraging at sea was overall high and, on average, represented 88% (interquartile range: 79–98%) of the time of a given recording session. This value was greater than expected by chance in 91% (84 out of 92) of the investigated recording sessions, indicating that partners often spent more time than expected by chance performing opposite activities in the studied population.

The amount of time when partners performed opposite activities (i.e., a proxy of the incubation coordination) was significantly affected by the incubation phase (GLMM, gamma family, χ2 = 19.25, P < 0.001, Table 1) and its interaction with the year (GLMM, gamma family, χ2 = 6.33, P = 0.012, Table 1). The amount of time when partners performed opposite activities increased with time, being the highest just before the hatching date (Fig 1). This increase was more accentuated in 2020, compared to 2019 (Fig 1).

10.1371/journal.pone.0306796.g001 Fig 1 Changes in the coordination of parental performance between partners during the incubation period.

The dots (with colours representing years of the study) represent a given 48 h recording session for one focal pair. The incubation coordination is the amount of time from this particular recording session that partners spent performing opposite activities (i.e., one partner incubating in the nest, while the other was foraging at sea). Incubation phase is expressed as the number of days before the hatching date of the given pair on which the recording session was performed (i.e., the lower the number, the closer to the hatching date, illustrated by an egg to the left side and a chick to the left). Lines (with particular years indicated by colours) represent the regression obtained from the candidate GLMM, with shaded areas representing 95% confidence intervals.

Parental coordination throughout chick rearing

During the chick rearing period, the amount of time one partner was performing a long trip while the other was performing a short trip was relatively high and on average represented 27% (interquartile range: 16–36%) of the time of a given recording session. Such an amount of time was greater than expected by chance in 15% (10 out of 66) of the recording sessions, indicating that coordination of long and short trips of both partners happens but is not that frequent in the studied population.

The coordination index was significantly affected by the chick rearing phase (LMM, χ2 = 9.12, P = 0.002, Table 1), as well as by the year (LMM, χ2 = 13.02, P < 0.001, Table 1), and their interaction (LMM, χ2 = 8.94, P = 0.003, Table 1). Early chick rearing was characterised by a higher coordination index compared to the mid phase in one season (2019) but rather similar in the other (2020; post-hoc Tukey test, with P < 0.05 for significant comparisons; see Fig 2).

10.1371/journal.pone.0306796.g002 Fig 2 Differences in the coordination index during early and mid phases of the chick rearing periods in two consecutive years.

Values of the coordination index above 0 indicate coordination, i.e., considerable overlap of short and long foraging trips of the partners. Violin plots represent the distribution, dots the coordination value for each pair, and triangles the mean for the phase in given year (indicated by color). Difference between every combination was tested with a pair-wise post-hoc Tukey test, and significance is indicated at the top of black horizontal lines. (N.S.: P > 0.05; *: P < 0.05; **: P < 0.01; ***: P < 0.001).

Link between the coordination in incubation and chick rearing

The coordination index of the early phase of the chick rearing period was negatively related to the way partners coordinated their activities during any of the incubation phases, and none of the estimates were significant in the standard-testing procedure (LM, F = 3.81, P = 0.07 for early incubation, F = 0.99, P > 0.05 and F = 1.02, P > 0.05 for the mid and late incubation phases respectively, Table 1). The estimates for early and late incubation became significant, however, when the bootstrap procedure was applied in the modelling (S3 Fig in S1 File). At the mid phase of the chick rearing period, the coordination index was significantly related to the coordination at the early (LM, F = 6.91, P = 0.02, Table 1) and mid phases of the incubation (LM, F = 10.95, P < 0.01, Table 1). The direction of the relationship was the opposite for these two phases (see Fig 3), with the pairs highly coordinated during chick rearing exhibiting a lower level of coordination during early incubation but a higher level of coordination in mid incubation (Fig 3). The estimates established with the bootstrap procedure remained of quite similar values and significance as in the standard approach, with the exception for mid incubation, where the value became marginally significant (P = 0.08, S6 Fig in S1 File).

10.1371/journal.pone.0306796.g003 Fig 3 Relationship between coordination during incubation and the coordination index during the mid phase of the chick rearing period.

The dots represent a focal pair. The incubation coordination is the amount of time from the early (A) or mid (B) phase of incubation that partners spent performing opposite activities (i.e., one partner incubating in the nest, while the other was foraging at sea). Lines represent the regressions obtained from the candidate LM, with shaded areas representing the 95% confidence intervals.

Discussion

We showed that Dovekie partners coordinate their performance in respect to each other throughout incubation and also tend to do it during the chick-rearing period, with specific patterns in each breeding stage corresponding to the different constraints imposed on the reproduction attempt. Our results provide an insight into the way that parents optimize their parental performance in a long-lived monogamous seabird. Furthermore, our results reveal changes in coordination within the course of each studied breeding stage and in response to the year, suggesting that biparental care performance, even in strictly biparental care system, might not be a fixed sensu (“sealed bid” as suggested by Houston & Davies [9]) but a flexible behavior, even though additional studies on the matter are needed.

Cooperation in parental care is receiving growing and well deserved attention but few studies take into consideration more than one breeding stage at a time. Here, our study species was already known for its coordination of the chick provisioning [25, 26] but by being examined in the mid chick rearing period only. Then, the incubation period remained unstudied in the same context. We bridged this gap by showing that Dovekie parents spend more time than expected by chance performing opposite activities during the incubation period (i.e., one partner incubating the egg, and the other foraging), which is likely to be an effect of their active coordination of parental activity. Concerning the coordination of chick provisioning, initially highlighted by Wojczulanis-Jakubas et al. [25] and Grissot et al. [26], we showed here that some parents during the chick rearing period actively alternate their short and long trips in respect to each other but this is apparently not so straightforward, as only some parents seem to be able to coordinate better than by chance. Additionally, the level of this coordination is also season- and phase-dependent (higher in early chick rearing in some seasons). The fact that coordinated parental care is exhibited by the Dovekie during both incubation and chick rearing indicates that both stages present their own constraints and parents are apparently able to mitigate these effects through the coordination of their parental activities. Such coordination throughout the whole breeding season is not surprising, given high energy requirements in Dovekies [58, 73, 74], harsh breeding environment [55], including quite challenging and unpredictable foraging conditions [26, 53].

We showed that within incubation and chick rearing periods, Dovekie pairs exhibit changes in coordination levels. Those changes seem to be going in opposite directions in the two examined breeding stages, as coordination during incubation is on average increasing over the course of this stage (Fig 1), and during the chick rearing period, coordination is higher in early chick rearing than the mid phase of the same period (Fig 2), even though this pattern seems to be season dependent. This is, in general, in accordance with our initial hypotheses but direct factors shaping the patterns remain unknown, and require further investigation. For the time being, we can only suggest some intrinsic drivers and mechanisms. During incubation, there could be a growing need of the developing embryo for a constantly high incubation temperature, thus increasing parental coordination could favour embryo development. For chick rearing, increasing thermal independence and decreasing sensitivity to starvation of the chick as it ages [57, 58] might decrease the need for parental coordination. Hormonal changes in adults are likely to play a role in the regulation of parental behavior, especially during the incubation period. It is, for instance, known that the level of prolactin increases over the course of the incubation period in the Dovekie parents [35, 56] but whether this increases their propensity to incubate, and therefore their level of coordination, remains unknown and will require specific studies.

Although we did not aim to examine inter-annual differences in parental behavior, conducting the study across two breeding seasons, we considered the effect of the year and its interaction with the different phases of breeding stages. Interestingly, in both breeding stages we found some interannual differences (see Table 1 and Figs 1 and 2). During the incubation period, although we found coordination to increase in the course of the period in both studied seasons, the intercept for the increase differed between the seasons, indicating that Dovekie parents were more coordinated in their incubation activities in one season (2019) compared to the other (2020). During chick rearing, we found that chick provisioning was more coordinated in early chick rearing compared to the mid phase in one season (2019) but not the other (2020). Putting all these results together, we can conclude that in the 2019 season, birds were more coordinated than in 2020. With only two seasons being examined, without properly investigated environmental context, it is hard to interpret inter-annual differences in the observed patterns. We can only speculate that environmental conditions may affect parental coordination, as was shown in other species (Charadrius spp.) relating to biparental care [75] where parental coordination increased with temperature stochasticity.

Grissot et al. [26] suggested some effects of environmental conditions on parental coordination during the chick rearing period, even though no clear inter-year differences could be highlighted in that study. Given that the two studies were conducted in the same species and colony, with similar methodologies, it is intriguing that we could highlight in the present study an inter-annual variation that was not highlighted in the previous one. Based on the suggestion made that the range of environmental conditions was not extreme enough to highlight changes in coordination strategy in the previous study, we could hypothesize that years investigated in the present study represented a wider range of environmental conditions. Another explanation for the inter-annual differences in coordination revealed in the present study could come from the greater range of temporal scale used here. Grissot et al. [26] focused solely on coordination during the mid phase of the chick rearing period, which seems to be the least subject to inter-year differences in the present study (Fig 2). Given that coordination of parental performance during chick rearing is decreasing between the early and mid phases, and that breeding constraints (e.g., chick thermoregulation and feeding) are at their highest level [55], one could assume that the coordination of chick provisioning is therefore more crucial at the early phase, just after the hatching date. Therefore, coordination at mid chick rearing seems to influence the breeding outcome less, which is also concordant with the apparent lack of significant effects of coordination at the mid chick rearing period on the chick growth rate, as reported by Wojczulanis-Jakubas et al. [25] and Grissot et al. [26]. All these findings clearly show that examining parental coordination in different breeding stages (and different environmental contexts) allows to capture fine-scale changes in parental behavior and is important for recognizing all the factors influencing parental cooperation.

Our results indicated the existence of some relationships between parental coordination during the incubation and chick rearing stages (Fig 3). However, given the instability of the results between linear modelling and the bootstrap procedure (S1 File), the opposite directions of relationships, and the fact the link between the stages has been understudied in general, the results are hard to interpret. We found no effect of incubation coordination on the coordination index of the early phase of chick rearing, although the relationships (negative) became significant in an alternative bootstrap procedure. With such differences, we do not even try to interpret these findings. The relationship between the coordination index of mid chick rearing and early and mid-incubation coordination was stably significant, however, with opposite direction for the early and mid phases. To interpret this, one possibility is that parental coordination during mid chick rearing, is dominated by parental constraints rather than being related to brood needs and might reflect pair quality. Then, early and mid-incubation periods, during which partners are in the process of re-bonding and habituating to parental activities, seem to be dominated only by parental constraints rather than the chick’s, and parental coordination could also reflect pair quality. The link found between mid chick rearing and early/mid incubation substantiate this argument, and would thus inform us about partners’ communication and/or pair quality. How to interpret this quality is a separate question. Coordination during late incubation, in that context, being the most important from the perspective of a developing embryo, would mask the pair-quality effect. Such reasoning about the functionality of coordination during late incubation could be supported by the very high level of the coordination reached by all the pairs, and low inter-pair variation (Fig 1). Clearly, the pair-quality-based interpretation is very speculative and further investigation on the link between coordination during incubation and chick rearing, with a bigger sample size and/or an experimental approach is apparently needed. We also cannot exclude the possibility that revealed relationships are random and do not have any biological meaning.

Our study is based on successful breeders only, and for those we found some evidence of parental coordination, both during incubation and chick rearing. However, further studies are needed, possibly with experimental approaches, to properly examine the consequences of parental coordination on reproductive success. It is possible that parental coordination during the incubation period is the most important component of reproductive success, as there is quite high inter-pair variability in hatching success (e.g., hatching success for different sub-colonies 66–95% [76]). Once the chick hatches, its chances for successful fledging are high (e.g., chick survival up to 14 days, for different sub-colonies: 85–100% [76]). Thus, examining parental coordination at the early incubation phase along with hatchability could provide valuable insight into the significance of parental coordination.

To conclude, our study highlights the importance of considering coordination not only during a short time-window of a specific breeding stage, but also using a broader temporal scale. Indeed, Dovekie adults adjust their parental behavior and coordination with their mate throughout the breeding, possibly to match the offspring’s needs. However the level of coordination within each breeding stage is influenced by breeding/environmental conditions. The exact drivers of parental coordination remain to be identified, but future studies should consider the importance of temporal changes in parental behavior.

Supporting information

S1 File Supplementary materials.

Containing detailed information on egg development phases and age of the chick during recording sessions, on the threshold used for short trip/ long trip classification, as well as on the bootstrap procedure used to evaluate the estimates of the models.

(DOCX)

S1 Table Egg development phases and age of the chick.

Values are expressed in number of days before (resp. after hatching date), at the beginning of the recording session.

(TIF)

S2 Table Threshold used for the classification of short and long trips during the chick rearing period.

Values are expressed in number of hours.

(TIF)

We thank Martyna Cendrowska for her help in the field, the Polish Polar Station for hosting us even in pandemic times, and Łukasz Pracki for his precious IT help in the field. We also thank Jacob Ligorria for proof-reading the manuscript and, as a native English speaker and specialist in ecology, for the substantial improvements he made.

10.1371/journal.pone.0306796.r001
Decision Letter 0
Radwan Lamiaa Mostafa Academic Editor
© 2024 Lamiaa Mostafa Radwan
2024
Lamiaa Mostafa Radwan
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Submission Version0
15 Jan 2024

PONE-D-23-40200Coordination of parental performance is breeding phase-dependent in the Dovekie (Alle alle), a pelagic Arctic seabirdPLOS ONE

Dear Dr. Grissot,

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Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

Dear Dr., Antoine Grissot

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we have decided that your manuscript needs Major Revision.

Kind regards,

Prof. Lamiaa Mostafa Radwan, Ph.D.

Academic Editor

PLOS ONE

Editor Comments:

1- The manuscript needs Editing language

2- Material and methods need more clarity

3- Discussing results requires citing references that explain those results

Reviewer1

It is possible to follow a logic between methods, results and discussion, The authors are careful in the design, even when the Dovekie is broadly studied this work offers different approach.

This work follows the statistical analysis and design according to the characteristics of behavior, reproductive performance, and breeding sites characteristics.

All data is available in the manuscript or supporting materials.

On the line 309 the authors mentioned about inter-annual meteorological and oceanographic variables between years to construct the generalized liner mixed model, but little is mentioned about these variables in the results section, however on the discussion the author mentioned the importance of environmental variables.

Author must review references. Line 50 Parker et al 2002; Line 496 Wojczulanis-Jakuba et al (2018) are not listed. Otherwise on line 704 Jakubas, D., Wojczulanis-Jakubas, K., & Kreft, R. (2008). Sex differences in body condition and hematological parameters in Little Auk Alle alle during the incubation period. Ornis Fennica, 85, 90–97 is on references but not on manuscript.

Reviewer2

This manuscript explores coordination of parental effort for Dovekies breeding in Svalbard. The study adopts a novel whole-season perspective, whereby the authors consider coordination throughout the entire breeding period and investigate correlations between incubation and chick-rearing, two distinct periods of care underlain by different parental behaviours. While the study poses an intriguing question, and acknowledging the authors' comprehensive approach, I have concerns. The writing is a little raw and difficult to follow, especially in the methods section, where complex approaches lack full explanation. Many conclusions in the discussion seem weakly supported, with unclear logical chains, and insufficient appraisal of the wider literature. However, my major concern is that the authors may not be measuring coordination during incubation accurately.

The defined metric, 'time parents spend on opposite activities,' seems flawed, as continuous egg incubation means parents must nearly always be engaged in opposite activities. As a result, this metric instead seems to just measure respective foraging time/nest attendance, not coordination. Furthermore, I question the randomization procedure, as the null hypothesis represents a pattern of behaviour that fundamentally cannot happen – i.e., two parents behave with no regard to one another, which would leave long periods of egg neglect or overlap at the nest. This is particularly problematic considering that the authors only use successful nests, which presumably are much less likely to have neglected the egg – the only behaviour that would give rise to ‘low’ coordination in this metric. This is a valuable dataset, but I recommend a revised analytical approach – for example, by comparing the nest shifts/trip durations of each parent, as has been done in many other species. Alongside this, I would like to see clearer methods, and a more cautious interpretation of the results.

As a general point, I note quite a few issues with the language usage. In parts, this made it difficult to follow the text and it took me significant effort to parse the meaning. I recognize the complexity of writing in a second language and appreciate the authors' efforts. However, improving this will significantly benefit the overall flow and comprehension and ensure the paper is understood and read by a wide audience. I would strongly suggest that a proficient English speaker is involved in the revision process to ensure that the intended meaning is effectively conveyed, particularly as PLOS ONE does not offer copy editing. I hope that the Editor can facilitate this.

Below I have outlined my thoughts in more detail. I hope this helps the authors improve their manuscript, and I look forward to seeing an updated version.

Introduction

The introduction contains the required theory to understand the background of the study, which is well justified. However, I’m afraid I feel it needs work. The presentation of theory is quite disorganised, with several vague explanations and examples. Additional citations, concrete examples, and supporting details are needed in various parts. Similarly, the study's description at the end is unclear, especially regarding the definition of coordination in this context.

One issue is that the context and focus of the introduction is not well established – it is unclear whether it focuses on all caregiving animals, species with biparental care, or just long-term monogamous parents. The entire introduction seems bird-centric, yet this isn't explicitly acknowledged. Clarifying the focus and explicitly setting the scene is necessary to improve clarity. For example, it might be easiest to explain that the introduction is focusing on birds that are long-term monogamous, and then introduce the relevant literature in a clear way.

My line-by-line comments are follows:

L42-45: This sentence sets up a false contrast. The time and energy devoted to offspring is costly precisely because it impacts survival and/or future reproduction. If there was no future survival or reproduction (i.e., the species is semelparous), the cost of parental investment wouldn’t matter. Furthermore, I don’t think ‘evolutionarily’ is the right word here – this is describing an individual trade-off. Finally, ‘somehow jeapordizes’ makes it sound like you don’t know how – I suggest removing ‘somehow’.

L50-56: The theory is oversimplified here. Cooperation itself isn’t a solution to sexual conflict because it is evolutionarily unstable. A cooperating pair is always vulnerable to one partner free-loading on the other – there needs to be enforcement for it to be maintained. For long-term monogamous species, this enforcement may come about through the intrinsic benefit of retaining the partner – for example, because there is a high cost to divorce. Cooperation emerges only when (1) parents cannot provide uniparental care and (2) there is a high cost to losing that partner. This concept of ‘partner value’ is reviewed in Griffith 2019.

L59-60: For balance, it is probably worth noting that some studies suggest/show that sexual conflict between the parents can mean that offspring end up receiving less investment in biparental care than would be expected given the sum of the parents’ possible individual contribution, e.g.:

McNamara JM, Houston AI, Barta Z, Osorno JL. 2003. Should young ever be better off with one parent than with two? Behavioral Ecology. 14(3):301–310. doi:10.1093/beheco/14.3.301.

Royle NJ, Hartley IR, Parker GA. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature. 416(6882):733–736. doi:10.1038/416733a.

L63: I’m not sure the Tyson paper shows a positive relationship between parental body condition and coordination.

L66: It’s unclear what is meant by ‘short time of pair-bonding’

L84: I suggest ‘likely to be /a/ prime driver’ (rather than /the/) – ‘the’ suggests that this is the only driver of parental behaviour, which I suspect is unlikely.

L84-87: I’m not sure what these sentences mean. Is this saying that environmental variables might affect coordination, and might additionally affect coordination differently during different breeding periods? And if this is the case, then we might have different expectations of coordination depending on environmental context?

L88-91: This needs some citations and examples.

L91-92: Why would coordination be more pronounced during chick rearing? There is an example given for incubation but not here.

L93-97: This section really needs some references and examples to support it – it’s quite vague and unspecific. I would also like to see some percentages supporting the statement that most parents don’t coordinate during incubation (I don’t disagree, but you need to substantiate this). Similarly you need to substantiate the claim that tasks are generally more similar between the parents during chick-rearing

L102: Contribution of both parents to care does not necessarily equal coordination. For example, if the female takes on the whole of incubation, and the male takes on the whole (or part) of chick-rearing, they are both contributing to/engaging in care, but no coordination is required.

L108: Is this a general phenomenon? Or are there specific species where this has been tested?

L117: Some authors have indirectly investigated this – e.g. McCully et al 2022 find similar levels of coordination in incubation and brooding:

McCully FR, Weimerskirch H, Cornell SJ, Hatchwell BJ, Cairo M, Patrick SC. 2022. Partner intrinsic characteristics influence foraging trip duration, but not coordination of care in wandering albatrosses Diomedea exulans. Ecology and Evolution. 12(12). doi:10.1002/ece3.9621.

L117-119: This is very vague – please explain fully why they would differ.

L120: What is meant by a runway?

L121: Is there actually evidence for such a short-scale familiarity effect? My understanding is that the familiarity effect moreso relates to the idea that you don’t have to learn a new individual’s behavioural each year (i.e., is more of an annual phenomenon)

L127: I would argue that most species are not genetically monogamous. Extra-pair copulation is extremely common, including in seabirds.

L129-130: It needs to be made clear that cooperation is favoured due to partner value, not similarity in contribution – this is a circular argument.

L152-153: My understanding is that in little auks, the egg is never left unattended. So does this not mean that coordination in this context is a given, i.e. birds are constrained to wait for their partner at the nest? As a general related point, it’s quite unclear what is actually being measured in the study and what the response variables are.

L159: What does ‘habituation to the parental mode’ mean?

L161-162: What is optimized food delivery rate?

L168: Missing the word ‘period’ after incubation (or else remove ‘the’)

Methods

The methods are, in many parts, very difficult to follow. I have done my best to draw a reasonable conclusion about the approaches but there are several sentences that need to be rephrased. Additionally, as discussed above, I am not sure that the methods outlined here actually measure coordination during incubation.

L180: How was an ‘expected event’ determined?

L186-187: I appreciate the intention between only focusing on successful breeders, but there is an interesting question about whether failed breeders coordinate less (which is even mentioned in the discussion), and so I wonder why there is no analysis of this –some sort of simplistic approach that ends up in the Supplementary Materials might be interesting from the perspective of future study, even if it comes with caveats that mean it has to be cautiously interpreted.

L205-208: If I’ve interpreted this correctly, does this mean: in 2019, recordings were taken at fixed intervals following egg laying, and due to the lack of lay dates in 2020, the recordings were taken at fixed calendar dates across the colony (i.e. all birds have the same recording dates)?

L210-212: It would be useful to know how long incubation and chick rearing last for in this species.

If lay date was unknown, how were the recording days determined? It says here ‘days before hatching’ was used, but surely hatching date was unknown if lay date was unknown (at the time of planning the recordings)?

L221: ‘well-adjusted to respective phenology’ – what does this mean? Perhaps ‘timed to hatching phenology’?

L226: I think ‘precision’ rather than ‘accuracy’

L228: Were all videos watched by all observers? Or were they split between observers? If they were split, did you conduct any analysis to look for observer bias?

L229-232: Are there stats to substantiate this, e.g. in the supplementary?

L242-242: Is it possible that the individual could be present at colony for a proportion of this time? Does this matter?

L256: I’m not sure what is meant by constraints. It’s probably enough to say that they represent the main parental activities during incubation.

L258-259: See my earlier comments: if the egg needs to be incubated continuously, how can coordination as established in the introduction exist?

L268-270: If the egg is never left attended, then surely there are very rarely situations when this isn't the case? This seems to be set up as the null hypothesis, but I don't think this is realistic as we know biologically this is always the case, so how can there ever be a situation where coordination is not observed? This approach makes sense for chick-rearing where the requirement for overlap is not so strict, but I'm not sure this approach makes sense for incubation, unless egg neglect is very common.

L279-280: What is the 'observed value'? I’m not sure what is actually being measured here?

L281: Can parents ever do the same activity? If they have to incubate the egg continuously, I'm not sure how one could observe coordination in this context (except maybe in chick rearing). This approach seems to be comparing parental behaviour to something that never happens.

L288: I think this means a correlation between foraging and nest time - this makes more sense and matches previous literature.

L288-293: I’m not sure I follow this.

L295-303: I also don’t follow this.

L305-306: I don't think this is measuring coordination - it sounds like this is just measuring trip duration/nest attendance, because parents always have to be conducting opposite activities

L306-307: Minor point: phase of incubation seems a bit misleading as this is a continuous numeric variable. Perhaps just day of incubation or days until hatching?

L311: What is the distribution? I’m still not clear on what the response variable actually is.

L317: Please explain that verification was ‘by visual inspection of diagnostic plots’ (my interpretation based on the supplementary).

L343: What is a ‘chick-rearing phase’?

L347-351: On one hand, I think the short and long trips for each parent are shuffled in time and compared to the original pattern - this makes sense. But I'm not sure what the 'observed within-pair amount of time...' is.

L357: Mean of what values?

L358-359: I don’t think I understand this, because there doesn’t seem to be a coordination index for incubation.

L366-367: The phase of chick rearing should be explained much earlier on. Why is it split in this way rather than for example using days since hatching (a numeric value), as is done for incubation?

L385: Why not include the phases in the model? Given separate models are fitted, what corrections are applied to account for multiple hypothesis testing?

L386-387: Earlier, phase seems to be days until hatching (numeric), but here it's categorical. In the figures it seems to be numeric. How are these categories chosen and why is this approach used?

Results

L417-419: Perhaps I’ve misunderstood this, but I think it would be more interesting to report how frequently they take trips that are opposite, as opposed to representing this as a percentage time of the recording.

L420: Is 15% a high enough value to claim that coordination is occurring? This seems very low.

L435-436: This seems to be a post-hoc test and not justified in the methods, though I may have missed something. I am a bit concerned about this alternative approach and why the authors have used it – it feels a little like searching for a significant result.

Discussion

I feel the conclusions in the discussion are not always supported by the results, and the inferential chains aren’t always logical. I can see this difficulties in interpreting quite a mixed picture of results, and I wonder if this is partially because coordination is measured during incubation in such a different way to chick-rearing. Generally speaking, the discussion needs to be much better rooted in the published literature. There is very little reference to the wider literature, and the literature cited is a bit too dependent on the authors' previous work (while of course acknowledging that much of this lays the foundation for this study).

L486-487: I don't disagree that the behaviour is flexible, but I don't think this is something that was actually analysed here.

L493-495: I don’t agree with this interpretation – but see my previous comments.

L499-500: Different level is vague and not really what is meant - coordinate better than by chance, I think.

L501-504: This is quite a strong statement when two sentences prior, the authors make the point that there is limited evidence for coordination in chick rearing.

L507: If coordination were integral to this, surely we would expect (and find) quite strong evidence for it?

L511: I don’t think ‘as’ makes sense; the second part of the sentence doesn’t follow from the first part.

L513: ‘As we expected’ – where was this prediction made?

L514-515: I don't see anywhere where it was hypothesised that coordination would depend on the season?

L523-525: This is getting the causation backwards. Hormonal changes are a mechanistic explanation for the behaviour, not an ultimate one. In other words, hormone changes have likely evolved to facilitate the coordination pattern itself, the coordination doesn't emerge because of the hormone changes.

L526: Indeed, I don’t believe you can examine inter-annual differences with just two years, especially with different methodologies.

L535-536: I'm not sure how this conclusion is reached. How is efficiency measured?

L539: Can this be related back to the literature e.g. examples where this is the case?

L543-545: I don't think there is much evidence for this argument, and I don't think it adds anything.

L546: This is still only two years, and chick rearing is short - I doubt the temporal scale makes much difference.

L550-551: But according to the authors coordination is stronger during incubation? So why is coordination not established then (rather than after hatching)?

L560-561: This seems to be the first reference to ‘instability’ – what does this mean? (Same problem on L565).

L570: Not clear what ‘the same’ refers to.

L571-572: This needs to be better substantiated. How would a link between mid-chick rearing and mid incubation tell us anything about quality? What evidence is there for this?.

Reviewer 3

This study is well designed, and the manuscript provides valuable insights into how parental performance in a long-lived, monogamous seabird, emphasizing the flexibility of bi-parental care behavior rather than a fixed approach. It successfully navigates through the complexities of seasonal, stage-dependent, and inter-annual variations in parental coordination, contributing to the broader understanding of bi-parental care in seabirds.

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Additional Editor Comments:

Dear Dr., Antoine Grissot

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we have decided that your manuscript needs Major Revision.

Kind regards,

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Editor Comments:

1- The manuscript needs Editing language

2- Material and methods need more clarity

3- Discussing results requires citing references that explain those results

Reviewer1

It is possible to follow a logic between methods, results and discussion, The authors are careful in the design, even when the Dovekie is broadly studied this work offers different approach.

This work follows the statistical analysis and design according to the characteristics of behavior, reproductive performance, and breeding sites characteristics.

All data is available in the manuscript or supporting materials.

On the line 309 the authors mentioned about inter-annual meteorological and oceanographic variables between years to construct the generalized liner mixed model, but little is mentioned about these variables in the results section, however on the discussion the author mentioned the importance of environmental variables.

Author must review references. Line 50 Parker et al 2002; Line 496 Wojczulanis-Jakuba et al (2018) are not listed. Otherwise on line 704 Jakubas, D., Wojczulanis-Jakubas, K., & Kreft, R. (2008). Sex differences in body condition and hematological parameters in Little Auk Alle alle during the incubation period. Ornis Fennica, 85, 90–97 is on references but not on manuscript.

Reviewer2

This manuscript explores coordination of parental effort for Dovekies breeding in Svalbard. The study adopts a novel whole-season perspective, whereby the authors consider coordination throughout the entire breeding period and investigate correlations between incubation and chick-rearing, two distinct periods of care underlain by different parental behaviours. While the study poses an intriguing question, and acknowledging the authors' comprehensive approach, I have concerns. The writing is a little raw and difficult to follow, especially in the methods section, where complex approaches lack full explanation. Many conclusions in the discussion seem weakly supported, with unclear logical chains, and insufficient appraisal of the wider literature. However, my major concern is that the authors may not be measuring coordination during incubation accurately.

The defined metric, 'time parents spend on opposite activities,' seems flawed, as continuous egg incubation means parents must nearly always be engaged in opposite activities. As a result, this metric instead seems to just measure respective foraging time/nest attendance, not coordination. Furthermore, I question the randomization procedure, as the null hypothesis represents a pattern of behaviour that fundamentally cannot happen – i.e., two parents behave with no regard to one another, which would leave long periods of egg neglect or overlap at the nest. This is particularly problematic considering that the authors only use successful nests, which presumably are much less likely to have neglected the egg – the only behaviour that would give rise to ‘low’ coordination in this metric. This is a valuable dataset, but I recommend a revised analytical approach – for example, by comparing the nest shifts/trip durations of each parent, as has been done in many other species. Alongside this, I would like to see clearer methods, and a more cautious interpretation of the results.

As a general point, I note quite a few issues with the language usage. In parts, this made it difficult to follow the text and it took me significant effort to parse the meaning. I recognize the complexity of writing in a second language and appreciate the authors' efforts. However, improving this will significantly benefit the overall flow and comprehension and ensure the paper is understood and read by a wide audience. I would strongly suggest that a proficient English speaker is involved in the revision process to ensure that the intended meaning is effectively conveyed, particularly as PLOS ONE does not offer copy editing. I hope that the Editor can facilitate this.

Below I have outlined my thoughts in more detail. I hope this helps the authors improve their manuscript, and I look forward to seeing an updated version.

Introduction

The introduction contains the required theory to understand the background of the study, which is well justified. However, I’m afraid I feel it needs work. The presentation of theory is quite disorganised, with several vague explanations and examples. Additional citations, concrete examples, and supporting details are needed in various parts. Similarly, the study's description at the end is unclear, especially regarding the definition of coordination in this context.

One issue is that the context and focus of the introduction is not well established – it is unclear whether it focuses on all caregiving animals, species with biparental care, or just long-term monogamous parents. The entire introduction seems bird-centric, yet this isn't explicitly acknowledged. Clarifying the focus and explicitly setting the scene is necessary to improve clarity. For example, it might be easiest to explain that the introduction is focusing on birds that are long-term monogamous, and then introduce the relevant literature in a clear way.

My line-by-line comments are follows:

L42-45: This sentence sets up a false contrast. The time and energy devoted to offspring is costly precisely because it impacts survival and/or future reproduction. If there was no future survival or reproduction (i.e., the species is semelparous), the cost of parental investment wouldn’t matter. Furthermore, I don’t think ‘evolutionarily’ is the right word here – this is describing an individual trade-off. Finally, ‘somehow jeapordizes’ makes it sound like you don’t know how – I suggest removing ‘somehow’.

L50-56: The theory is oversimplified here. Cooperation itself isn’t a solution to sexual conflict because it is evolutionarily unstable. A cooperating pair is always vulnerable to one partner free-loading on the other – there needs to be enforcement for it to be maintained. For long-term monogamous species, this enforcement may come about through the intrinsic benefit of retaining the partner – for example, because there is a high cost to divorce. Cooperation emerges only when (1) parents cannot provide uniparental care and (2) there is a high cost to losing that partner. This concept of ‘partner value’ is reviewed in Griffith 2019.

L59-60: For balance, it is probably worth noting that some studies suggest/show that sexual conflict between the parents can mean that offspring end up receiving less investment in biparental care than would be expected given the sum of the parents’ possible individual contribution, e.g.:

McNamara JM, Houston AI, Barta Z, Osorno JL. 2003. Should young ever be better off with one parent than with two? Behavioral Ecology. 14(3):301–310. doi:10.1093/beheco/14.3.301.

Royle NJ, Hartley IR, Parker GA. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature. 416(6882):733–736. doi:10.1038/416733a.

L63: I’m not sure the Tyson paper shows a positive relationship between parental body condition and coordination.

L66: It’s unclear what is meant by ‘short time of pair-bonding’

L84: I suggest ‘likely to be /a/ prime driver’ (rather than /the/) – ‘the’ suggests that this is the only driver of parental behaviour, which I suspect is unlikely.

L84-87: I’m not sure what these sentences mean. Is this saying that environmental variables might affect coordination, and might additionally affect coordination differently during different breeding periods? And if this is the case, then we might have different expectations of coordination depending on environmental context?

L88-91: This needs some citations and examples.

L91-92: Why would coordination be more pronounced during chick rearing? There is an example given for incubation but not here.

L93-97: This section really needs some references and examples to support it – it’s quite vague and unspecific. I would also like to see some percentages supporting the statement that most parents don’t coordinate during incubation (I don’t disagree, but you need to substantiate this). Similarly you need to substantiate the claim that tasks are generally more similar between the parents during chick-rearing

L102: Contribution of both parents to care does not necessarily equal coordination. For example, if the female takes on the whole of incubation, and the male takes on the whole (or part) of chick-rearing, they are both contributing to/engaging in care, but no coordination is required.

L108: Is this a general phenomenon? Or are there specific species where this has been tested?

L117: Some authors have indirectly investigated this – e.g. McCully et al 2022 find similar levels of coordination in incubation and brooding:

McCully FR, Weimerskirch H, Cornell SJ, Hatchwell BJ, Cairo M, Patrick SC. 2022. Partner intrinsic characteristics influence foraging trip duration, but not coordination of care in wandering albatrosses Diomedea exulans. Ecology and Evolution. 12(12). doi:10.1002/ece3.9621.

L117-119: This is very vague – please explain fully why they would differ.

L120: What is meant by a runway?

L121: Is there actually evidence for such a short-scale familiarity effect? My understanding is that the familiarity effect moreso relates to the idea that you don’t have to learn a new individual’s behavioural each year (i.e., is more of an annual phenomenon)

L127: I would argue that most species are not genetically monogamous. Extra-pair copulation is extremely common, including in seabirds.

L129-130: It needs to be made clear that cooperation is favoured due to partner value, not similarity in contribution – this is a circular argument.

L152-153: My understanding is that in little auks, the egg is never left unattended. So does this not mean that coordination in this context is a given, i.e. birds are constrained to wait for their partner at the nest? As a general related point, it’s quite unclear what is actually being measured in the study and what the response variables are.

L159: What does ‘habituation to the parental mode’ mean?

L161-162: What is optimized food delivery rate?

L168: Missing the word ‘period’ after incubation (or else remove ‘the’)

Methods

The methods are, in many parts, very difficult to follow. I have done my best to draw a reasonable conclusion about the approaches but there are several sentences that need to be rephrased. Additionally, as discussed above, I am not sure that the methods outlined here actually measure coordination during incubation.

L180: How was an ‘expected event’ determined?

L186-187: I appreciate the intention between only focusing on successful breeders, but there is an interesting question about whether failed breeders coordinate less (which is even mentioned in the discussion), and so I wonder why there is no analysis of this –some sort of simplistic approach that ends up in the Supplementary Materials might be interesting from the perspective of future study, even if it comes with caveats that mean it has to be cautiously interpreted.

L205-208: If I’ve interpreted this correctly, does this mean: in 2019, recordings were taken at fixed intervals following egg laying, and due to the lack of lay dates in 2020, the recordings were taken at fixed calendar dates across the colony (i.e. all birds have the same recording dates)?

L210-212: It would be useful to know how long incubation and chick rearing last for in this species.

If lay date was unknown, how were the recording days determined? It says here ‘days before hatching’ was used, but surely hatching date was unknown if lay date was unknown (at the time of planning the recordings)?

L221: ‘well-adjusted to respective phenology’ – what does this mean? Perhaps ‘timed to hatching phenology’?

L226: I think ‘precision’ rather than ‘accuracy’

L228: Were all videos watched by all observers? Or were they split between observers? If they were split, did you conduct any analysis to look for observer bias?

L229-232: Are there stats to substantiate this, e.g. in the supplementary?

L242-242: Is it possible that the individual could be present at colony for a proportion of this time? Does this matter?

L256: I’m not sure what is meant by constraints. It’s probably enough to say that they represent the main parental activities during incubation.

L258-259: See my earlier comments: if the egg needs to be incubated continuously, how can coordination as established in the introduction exist?

L268-270: If the egg is never left attended, then surely there are very rarely situations when this isn't the case? This seems to be set up as the null hypothesis, but I don't think this is realistic as we know biologically this is always the case, so how can there ever be a situation where coordination is not observed? This approach makes sense for chick-rearing where the requirement for overlap is not so strict, but I'm not sure this approach makes sense for incubation, unless egg neglect is very common.

L279-280: What is the 'observed value'? I’m not sure what is actually being measured here?

L281: Can parents ever do the same activity? If they have to incubate the egg continuously, I'm not sure how one could observe coordination in this context (except maybe in chick rearing). This approach seems to be comparing parental behaviour to something that never happens.

L288: I think this means a correlation between foraging and nest time - this makes more sense and matches previous literature.

L288-293: I’m not sure I follow this.

L295-303: I also don’t follow this.

L305-306: I don't think this is measuring coordination - it sounds like this is just measuring trip duration/nest attendance, because parents always have to be conducting opposite activities

L306-307: Minor point: phase of incubation seems a bit misleading as this is a continuous numeric variable. Perhaps just day of incubation or days until hatching?

L311: What is the distribution? I’m still not clear on what the response variable actually is.

L317: Please explain that verification was ‘by visual inspection of diagnostic plots’ (my interpretation based on the supplementary).

L343: What is a ‘chick-rearing phase’?

L347-351: On one hand, I think the short and long trips for each parent are shuffled in time and compared to the original pattern - this makes sense. But I'm not sure what the 'observed within-pair amount of time...' is.

L357: Mean of what values?

L358-359: I don’t think I understand this, because there doesn’t seem to be a coordination index for incubation.

L366-367: The phase of chick rearing should be explained much earlier on. Why is it split in this way rather than for example using days since hatching (a numeric value), as is done for incubation?

L385: Why not include the phases in the model? Given separate models are fitted, what corrections are applied to account for multiple hypothesis testing?

L386-387: Earlier, phase seems to be days until hatching (numeric), but here it's categorical. In the figures it seems to be numeric. How are these categories chosen and why is this approach used?

Results

L417-419: Perhaps I’ve misunderstood this, but I think it would be more interesting to report how frequently they take trips that are opposite, as opposed to representing this as a percentage time of the recording.

L420: Is 15% a high enough value to claim that coordination is occurring? This seems very low.

L435-436: This seems to be a post-hoc test and not justified in the methods, though I may have missed something. I am a bit concerned about this alternative approach and why the authors have used it – it feels a little like searching for a significant result.

Discussion

I feel the conclusions in the discussion are not always supported by the results, and the inferential chains aren’t always logical. I can see this difficulties in interpreting quite a mixed picture of results, and I wonder if this is partially because coordination is measured during incubation in such a different way to chick-rearing. Generally speaking, the discussion needs to be much better rooted in the published literature. There is very little reference to the wider literature, and the literature cited is a bit too dependent on the authors' previous work (while of course acknowledging that much of this lays the foundation for this study).

L486-487: I don't disagree that the behaviour is flexible, but I don't think this is something that was actually analysed here.

L493-495: I don’t agree with this interpretation – but see my previous comments.

L499-500: Different level is vague and not really what is meant - coordinate better than by chance, I think.

L501-504: This is quite a strong statement when two sentences prior, the authors make the point that there is limited evidence for coordination in chick rearing.

L507: If coordination were integral to this, surely we would expect (and find) quite strong evidence for it?

L511: I don’t think ‘as’ makes sense; the second part of the sentence doesn’t follow from the first part.

L513: ‘As we expected’ – where was this prediction made?

L514-515: I don't see anywhere where it was hypothesised that coordination would depend on the season?

L523-525: This is getting the causation backwards. Hormonal changes are a mechanistic explanation for the behaviour, not an ultimate one. In other words, hormone changes have likely evolved to facilitate the coordination pattern itself, the coordination doesn't emerge because of the hormone changes.

L526: Indeed, I don’t believe you can examine inter-annual differences with just two years, especially with different methodologies.

L535-536: I'm not sure how this conclusion is reached. How is efficiency measured?

L539: Can this be related back to the literature e.g. examples where this is the case?

L543-545: I don't think there is much evidence for this argument, and I don't think it adds anything.

L546: This is still only two years, and chick rearing is short - I doubt the temporal scale makes much difference.

L550-551: But according to the authors coordination is stronger during incubation? So why is coordination not established then (rather than after hatching)?

L560-561: This seems to be the first reference to ‘instability’ – what does this mean? (Same problem on L565).

L570: Not clear what ‘the same’ refers to.

L571-572: This needs to be better substantiated. How would a link between mid-chick rearing and mid incubation tell us anything about quality? What evidence is there for this?.

Reviewer 3

This study is well designed, and the manuscript provides valuable insights into how parental performance in a long-lived, monogamous seabird, emphasizing the flexibility of bi-parental care behavior rather than a fixed approach. It successfully navigates through the complexities of seasonal, stage-dependent, and inter-annual variations in parental coordination, contributing to the broader understanding of bi-parental care in seabirds.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Partly

Reviewer #3: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: N/A

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: No

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: It is possible to follow a logic between methods, results and discussion, The authors are careful in the design, even when the Dovekie is broadly studied this work offers different approach.

This work follows the statistical analysis and design according to the characteristics of behavior, reproductive performance, and breeding sites characteristics.

All data is available in the manuscript or supporting materials.

On the line 309 the authors mentioned about inter-annual meteorological and oceanographic variables between years to construct the generalized liner mixed model, but little is mentioned about these variables in the results section, however on the discussion the author mentioned the importance of environmental variables.

Author must review references. Line 50 Parker et al 2002; Line 496 Wojczulanis-Jakuba et al (2018) are not listed. Otherwise on line 704 Jakubas, D., Wojczulanis-Jakubas, K., & Kreft, R. (2008). Sex differences in body condition and hematological parameters in Little Auk Alle alle during the incubation period. Ornis Fennica, 85, 90–97 is on references but not on manuscript.

Reviewer #2: This manuscript explores coordination of parental effort for Dovekies breeding in Svalbard. The study adopts a novel whole-season perspective, whereby the authors consider coordination throughout the entire breeding period and investigate correlations between incubation and chick-rearing, two distinct periods of care underlain by different parental behaviours. While the study poses an intriguing question, and acknowledging the authors' comprehensive approach, I have concerns. The writing is a little raw and difficult to follow, especially in the methods section, where complex approaches lack full explanation. Many conclusions in the discussion seem weakly supported, with unclear logical chains, and insufficient appraisal of the wider literature. However, my major concern is that the authors may not be measuring coordination during incubation accurately.

The defined metric, 'time parents spend on opposite activities,' seems flawed, as continuous egg incubation means parents must nearly always be engaged in opposite activities. As a result, this metric instead seems to just measure respective foraging time/nest attendance, not coordination. Furthermore, I question the randomization procedure, as the null hypothesis represents a pattern of behaviour that fundamentally cannot happen – i.e., two parents behave with no regard to one another, which would leave long periods of egg neglect or overlap at the nest. This is particularly problematic considering that the authors only use successful nests, which presumably are much less likely to have neglected the egg – the only behaviour that would give rise to ‘low’ coordination in this metric. This is a valuable dataset, but I recommend a revised analytical approach – for example, by comparing the nest shifts/trip durations of each parent, as has been done in many other species. Alongside this, I would like to see clearer methods, and a more cautious interpretation of the results.

As a general point, I note quite a few issues with the language usage. In parts, this made it difficult to follow the text and it took me significant effort to parse the meaning. I recognize the complexity of writing in a second language and appreciate the authors' efforts. However, improving this will significantly benefit the overall flow and comprehension and ensure the paper is understood and read by a wide audience. I would strongly suggest that a proficient English speaker is involved in the revision process to ensure that the intended meaning is effectively conveyed, particularly as PLOS ONE does not offer copy editing. I hope that the Editor can facilitate this.

Below I have outlined my thoughts in more detail. I hope this helps the authors improve their manuscript, and I look forward to seeing an updated version.

Introduction

The introduction contains the required theory to understand the background of the study, which is well justified. However, I’m afraid I feel it needs work. The presentation of theory is quite disorganised, with several vague explanations and examples. Additional citations, concrete examples, and supporting details are needed in various parts. Similarly, the study's description at the end is unclear, especially regarding the definition of coordination in this context.

One issue is that the context and focus of the introduction is not well established – it is unclear whether it focuses on all caregiving animals, species with biparental care, or just long-term monogamous parents. The entire introduction seems bird-centric, yet this isn't explicitly acknowledged. Clarifying the focus and explicitly setting the scene is necessary to improve clarity. For example, it might be easiest to explain that the introduction is focusing on birds that are long-term monogamous, and then introduce the relevant literature in a clear way.

My line-by-line comments are follows:

L42-45: This sentence sets up a false contrast. The time and energy devoted to offspring is costly precisely because it impacts survival and/or future reproduction. If there was no future survival or reproduction (i.e., the species is semelparous), the cost of parental investment wouldn’t matter. Furthermore, I don’t think ‘evolutionarily’ is the right word here – this is describing an individual trade-off. Finally, ‘somehow jeapordizes’ makes it sound like you don’t know how – I suggest removing ‘somehow’.

L50-56: The theory is oversimplified here. Cooperation itself isn’t a solution to sexual conflict because it is evolutionarily unstable. A cooperating pair is always vulnerable to one partner free-loading on the other – there needs to be enforcement for it to be maintained. For long-term monogamous species, this enforcement may come about through the intrinsic benefit of retaining the partner – for example, because there is a high cost to divorce. Cooperation emerges only when (1) parents cannot provide uniparental care and (2) there is a high cost to losing that partner. This concept of ‘partner value’ is reviewed in Griffith 2019.

L59-60: For balance, it is probably worth noting that some studies suggest/show that sexual conflict between the parents can mean that offspring end up receiving less investment in biparental care than would be expected given the sum of the parents’ possible individual contribution, e.g.:

McNamara JM, Houston AI, Barta Z, Osorno JL. 2003. Should young ever be better off with one parent than with two? Behavioral Ecology. 14(3):301–310. doi:10.1093/beheco/14.3.301.

Royle NJ, Hartley IR, Parker GA. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature. 416(6882):733–736. doi:10.1038/416733a.

L63: I’m not sure the Tyson paper shows a positive relationship between parental body condition and coordination.

L66: It’s unclear what is meant by ‘short time of pair-bonding’

L84: I suggest ‘likely to be /a/ prime driver’ (rather than /the/) – ‘the’ suggests that this is the only driver of parental behaviour, which I suspect is unlikely.

L84-87: I’m not sure what these sentences mean. Is this saying that environmental variables might affect coordination, and might additionally affect coordination differently during different breeding periods? And if this is the case, then we might have different expectations of coordination depending on environmental context?

L88-91: This needs some citations and examples.

L91-92: Why would coordination be more pronounced during chick rearing? There is an example given for incubation but not here.

L93-97: This section really needs some references and examples to support it – it’s quite vague and unspecific. I would also like to see some percentages supporting the statement that most parents don’t coordinate during incubation (I don’t disagree, but you need to substantiate this). Similarly you need to substantiate the claim that tasks are generally more similar between the parents during chick-rearing

L102: Contribution of both parents to care does not necessarily equal coordination. For example, if the female takes on the whole of incubation, and the male takes on the whole (or part) of chick-rearing, they are both contributing to/engaging in care, but no coordination is required.

L108: Is this a general phenomenon? Or are there specific species where this has been tested?

L117: Some authors have indirectly investigated this – e.g. McCully et al 2022 find similar levels of coordination in incubation and brooding:

McCully FR, Weimerskirch H, Cornell SJ, Hatchwell BJ, Cairo M, Patrick SC. 2022. Partner intrinsic characteristics influence foraging trip duration, but not coordination of care in wandering albatrosses Diomedea exulans. Ecology and Evolution. 12(12). doi:10.1002/ece3.9621.

L117-119: This is very vague – please explain fully why they would differ.

L120: What is meant by a runway?

L121: Is there actually evidence for such a short-scale familiarity effect? My understanding is that the familiarity effect moreso relates to the idea that you don’t have to learn a new individual’s behavioural each year (i.e., is more of an annual phenomenon)

L127: I would argue that most species are not genetically monogamous. Extra-pair copulation is extremely common, including in seabirds.

L129-130: It needs to be made clear that cooperation is favoured due to partner value, not similarity in contribution – this is a circular argument.

L152-153: My understanding is that in little auks, the egg is never left unattended. So does this not mean that coordination in this context is a given, i.e. birds are constrained to wait for their partner at the nest? As a general related point, it’s quite unclear what is actually being measured in the study and what the response variables are.

L159: What does ‘habituation to the parental mode’ mean?

L161-162: What is optimized food delivery rate?

L168: Missing the word ‘period’ after incubation (or else remove ‘the’)

Methods

The methods are, in many parts, very difficult to follow. I have done my best to draw a reasonable conclusion about the approaches but there are several sentences that need to be rephrased. Additionally, as discussed above, I am not sure that the methods outlined here actually measure coordination during incubation.

L180: How was an ‘expected event’ determined?

L186-187: I appreciate the intention between only focusing on successful breeders, but there is an interesting question about whether failed breeders coordinate less (which is even mentioned in the discussion), and so I wonder why there is no analysis of this –some sort of simplistic approach that ends up in the Supplementary Materials might be interesting from the perspective of future study, even if it comes with caveats that mean it has to be cautiously interpreted.

L205-208: If I’ve interpreted this correctly, does this mean: in 2019, recordings were taken at fixed intervals following egg laying, and due to the lack of lay dates in 2020, the recordings were taken at fixed calendar dates across the colony (i.e. all birds have the same recording dates)?

L210-212: It would be useful to know how long incubation and chick rearing last for in this species.

If lay date was unknown, how were the recording days determined? It says here ‘days before hatching’ was used, but surely hatching date was unknown if lay date was unknown (at the time of planning the recordings)?

L221: ‘well-adjusted to respective phenology’ – what does this mean? Perhaps ‘timed to hatching phenology’?

L226: I think ‘precision’ rather than ‘accuracy’

L228: Were all videos watched by all observers? Or were they split between observers? If they were split, did you conduct any analysis to look for observer bias?

L229-232: Are there stats to substantiate this, e.g. in the supplementary?

L242-242: Is it possible that the individual could be present at colony for a proportion of this time? Does this matter?

L256: I’m not sure what is meant by constraints. It’s probably enough to say that they represent the main parental activities during incubation.

L258-259: See my earlier comments: if the egg needs to be incubated continuously, how can coordination as established in the introduction exist?

L268-270: If the egg is never left attended, then surely there are very rarely situations when this isn't the case? This seems to be set up as the null hypothesis, but I don't think this is realistic as we know biologically this is always the case, so how can there ever be a situation where coordination is not observed? This approach makes sense for chick-rearing where the requirement for overlap is not so strict, but I'm not sure this approach makes sense for incubation, unless egg neglect is very common.

L279-280: What is the 'observed value'? I’m not sure what is actually being measured here?

L281: Can parents ever do the same activity? If they have to incubate the egg continuously, I'm not sure how one could observe coordination in this context (except maybe in chick rearing). This approach seems to be comparing parental behaviour to something that never happens.

L288: I think this means a correlation between foraging and nest time - this makes more sense and matches previous literature.

L288-293: I’m not sure I follow this.

L295-303: I also don’t follow this.

L305-306: I don't think this is measuring coordination - it sounds like this is just measuring trip duration/nest attendance, because parents always have to be conducting opposite activities

L306-307: Minor point: phase of incubation seems a bit misleading as this is a continuous numeric variable. Perhaps just day of incubation or days until hatching?

L311: What is the distribution? I’m still not clear on what the response variable actually is.

L317: Please explain that verification was ‘by visual inspection of diagnostic plots’ (my interpretation based on the supplementary).

L343: What is a ‘chick-rearing phase’?

L347-351: On one hand, I think the short and long trips for each parent are shuffled in time and compared to the original pattern - this makes sense. But I'm not sure what the 'observed within-pair amount of time...' is.

L357: Mean of what values?

L358-359: I don’t think I understand this, because there doesn’t seem to be a coordination index for incubation.

L366-367: The phase of chick rearing should be explained much earlier on. Why is it split in this way rather than for example using days since hatching (a numeric value), as is done for incubation?

L385: Why not include the phases in the model? Given separate models are fitted, what corrections are applied to account for multiple hypothesis testing?

L386-387: Earlier, phase seems to be days until hatching (numeric), but here it's categorical. In the figures it seems to be numeric. How are these categories chosen and why is this approach used?

Results

L417-419: Perhaps I’ve misunderstood this, but I think it would be more interesting to report how frequently they take trips that are opposite, as opposed to representing this as a percentage time of the recording.

L420: Is 15% a high enough value to claim that coordination is occurring? This seems very low.

L435-436: This seems to be a post-hoc test and not justified in the methods, though I may have missed something. I am a bit concerned about this alternative approach and why the authors have used it – it feels a little like searching for a significant result.

Discussion

I feel the conclusions in the discussion are not always supported by the results, and the inferential chains aren’t always logical. I can see this difficulties in interpreting quite a mixed picture of results, and I wonder if this is partially because coordination is measured during incubation in such a different way to chick-rearing. Generally speaking, the discussion needs to be much better rooted in the published literature. There is very little reference to the wider literature, and the literature cited is a bit too dependent on the authors' previous work (while of course acknowledging that much of this lays the foundation for this study).

L486-487: I don't disagree that the behaviour is flexible, but I don't think this is something that was actually analysed here.

L493-495: I don’t agree with this interpretation – but see my previous comments.

L499-500: Different level is vague and not really what is meant - coordinate better than by chance, I think.

L501-504: This is quite a strong statement when two sentences prior, the authors make the point that there is limited evidence for coordination in chick rearing.

L507: If coordination were integral to this, surely we would expect (and find) quite strong evidence for it?

L511: I don’t think ‘as’ makes sense; the second part of the sentence doesn’t follow from the first part.

L513: ‘As we expected’ – where was this prediction made?

L514-515: I don't see anywhere where it was hypothesised that coordination would depend on the season?

L523-525: This is getting the causation backwards. Hormonal changes are a mechanistic explanation for the behaviour, not an ultimate one. In other words, hormone changes have likely evolved to facilitate the coordination pattern itself, the coordination doesn't emerge because of the hormone changes.

L526: Indeed, I don’t believe you can examine inter-annual differences with just two years, especially with different methodologies.

L535-536: I'm not sure how this conclusion is reached. How is efficiency measured?

L539: Can this be related back to the literature e.g. examples where this is the case?

L543-545: I don't think there is much evidence for this argument, and I don't think it adds anything.

L546: This is still only two years, and chick rearing is short - I doubt the temporal scale makes much difference.

L550-551: But according to the authors coordination is stronger during incubation? So why is coordination not established then (rather than after hatching)?

L560-561: This seems to be the first reference to ‘instability’ – what does this mean? (Same problem on L565).

L570: Not clear what ‘the same’ refers to.

L571-572: This needs to be better substantiated. How would a link between mid-chick rearing and mid incubation tell us anything about quality? What evidence is there for this?

Reviewer #3: This study is well designed, and the manuscript provides valuable insights into how parental performance in a long-lived, monogamous seabird, emphasizing the flexibility of bi-parental care behavior rather than a fixed approach. It successfully navigates through the complexities of seasonal, stage-dependent, and inter-annual variations in parental coordination, contributing to the broader understanding of bi-parental care in seabirds.

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Attachment Submitted filename: PONE-D-23-40200 Done.pdf

10.1371/journal.pone.0306796.r002
Author response to Decision Letter 0
Submission Version1
13 Mar 2024

Please find below a copy of the Decision letter, with specific replies to comments. This can also be found in the provided document OTHER/Response to Review, for easier identification of questions and replies using a color code.

Dear Dr. Grissot,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

==============================

Dear Dr., Antoine Grissot

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we have decided that your manuscript needs Major Revision.

Kind regards,

Prof. Lamiaa Mostafa Radwan, Ph.D.

Academic Editor

PLOS ONE

Editor Comments:

1- The manuscript needs Editing language

2- Material and methods need more clarity

3- Discussing results requires citing references that explain those results

Dear PlosOne editor,

Thank you very much for your consideration of our work and your positive and constructive comments. Please find in the revision our updated version of the manuscript, that we hope will satisfy the comments raised by you and the three reviewers. Concerning your three specific comments:

1- We carefully edited the manuscript with special care for language.

2- Following this and mainly reviewer 2 comments, we did our best to explain better and clarify everything in the Method section

3- We improved the discussion and added needed references.

When providing Line numbers, we refer to the document with TRACK CHANGE activated.

Reviewer1

It is possible to follow a logic between methods, results and discussion, The authors are careful in the design, even when the Dovekie is broadly studied this work offers different approach.

This work follows the statistical analysis and design according to the characteristics of behavior, reproductive performance, and breeding sites characteristics.

All data is available in the manuscript or supporting materials.

Dear Reviewer1, thank you very much for your work on our manuscript and your comments.

On the line 309 the authors mentioned about inter-annual meteorological and oceanographic variables between years to construct the generalized liner mixed model, but little is mentioned about these variables in the results section, however on the discussion the author mentioned the importance of environmental variables.

REPLY : Sorry if that wasn’t clear in the method section, but only year was included as a variable in the model, not the meteorological and oceanographic variables. We believe including the year can be useful to take into consideration variation in environmental conditions, without including them directly, as this would complicate the model a lot and is not the main purpose of the study. We also included importance of environmental variables in the discussion, as it is known from the literature cited, but once again was not the main purpose here.

Author must review references. Line 50 Parker et al 2002; Line 496 Wojczulanis-Jakuba et al (2018) are not listed. Otherwise on line 704 Jakubas, D., Wojczulanis-Jakubas, K., & Kreft, R. (2008). Sex differences in body condition and hematological parameters in Little Auk Alle alle during the incubation period. Ornis Fennica, 85, 90–97 is on references but not on manuscript.

REPLY : References were carefully checked in the revised version. Regarding Wojczulanis-Jakubas et al. (2018), this was just an omission of the “2018a”. The two other mentioned occurrences were respectively added for Parker et al 2002 and removed for Jakubas et al 2008.

Reviewer2

This manuscript explores coordination of parental effort for Dovekies breeding in Svalbard. The study adopts a novel whole-season perspective, whereby the authors consider coordination throughout the entire breeding period and investigate correlations between incubation and chick-rearing, two distinct periods of care underlain by different parental behaviours. While the study poses an intriguing question, and acknowledging the authors' comprehensive approach, I have concerns. The writing is a little raw and difficult to follow, especially in the methods section, where complex approaches lack full explanation. Many conclusions in the discussion seem weakly supported, with unclear logical chains, and insufficient appraisal of the wider literature. However, my major concern is that the authors may not be measuring coordination during incubation accurately.

REPLY : We thank the reviewer for the comments on our manuscript, and hope we addressed present and detailed concerns in a satisfying manner

The defined metric, 'time parents spend on opposite activities,' seems flawed, as continuous egg incubation means parents must nearly always be engaged in opposite activities. As a result, this metric instead seems to just measure respective foraging time/nest attendance, not coordination. Furthermore, I question the randomization procedure, as the null hypothesis represents a pattern of behaviour that fundamentally cannot happen – i.e., two parents behave with no regard to one another, which would leave long periods of egg neglect or overlap at the nest. This is particularly problematic considering that the authors only use successful nests, which presumably are much less likely to have neglected the egg – the only behaviour that would give rise to ‘low’ coordination in this metric. This is a valuable dataset, but I recommend a revised analytical approach – for example, by comparing the nest shifts/trip durations of each parent, as has been done in many other species. Alongside this, I would like to see clearer methods, and a more cautious interpretation of the results.

REPLY : We understand the reviewer’s concerns about methodology, and did our best to explain in a clearer way all the methods used. However, we disagree concerning the alleged flaws in the coordination metrics and the randomisation method.

First, we added in the text (lines 273-275) some nuance about the constant need for incubation. Indeed, from previous work and the present study, we know there is some amount of tolerance for the egg not to be constantly incubated. Thermoregulation of the egg depends on incubating behavior of parents, but if left unattended, temperature of the egg does not drop below a critical threshold straight away and therefore can be left alone for some time. While processing the videos we could notice that sometimes an incubating parent would leave the nest before the other parent would return, and this, if happening rarely, didn’t seem to affect hatching success.

Additionally, the time performing opposite activities does not “just measure respective foraging time/nest attendance” because of the presence of the third category (“colony”), that can reduce the performance of opposite activities. Some individuals spent a considerate amount of time in the colony, either alone or with the partner, and even if the function of this behaviour is not very well known, it could serve as an alternative resting for a non-incubating individual (staying in colony instead of performing a foraging trip while partner incubates the egg), or as a bonding time between parents. Additionally, the two other categories, “nest” and “foraging”, perfectly represent the needs of respectively the egg and the parents, but only when performed simultaneously do they represent an optimisation of the time allocation of both parents in accord with each other. Thus, with the extent of tolerance for egg being left alone, and other activities being possibly performed, the performance of opposite activities really represents coordination between the two parents. This is also supported by the fact that there is actual variability in the dataset of this study in the time that parent spent performing opposite activities, so parents are not nearly always engaged in opposite activities as suggested by the reviewer. Indeed, even though all the pairs included in the study were successful, amount of time performing opposite activities is not same for all the pairs (mean = 88%, [min – max] : [48 – 99] %).

Regarding the randomisation process, the idea is to test whether the actual patterns from both parents are different from what is expected by chance. So one of the chance possibilities is what the reviewer suggest (where two parents behave completely with no regard to one another) and we agree that this pattern is not compatible with successful hatching, however our null hypothesis also encompasses a whole range of different situations in between. Therefore, we believe that testing the significance of this observed pattern compared to what could arise by chance is still valuable in itself.

As a general point, I note quite a few issues with the language usage. In parts, this made it difficult to follow the text and it took me significant effort to parse the meaning. I recognize the complexity of writing in a second language and appreciate the authors' efforts. However, improving this will significantly benefit the overall flow and comprehension and ensure the paper is understood and read by a wide audience. I would strongly suggest that a proficient English speaker is involved in the revision process to ensure that the intended meaning is effectively conveyed, particularly as PLOS ONE does not offer copy editing. I hope that the Editor can facilitate this.

REPLY : Thank you for acknowledging the efforts and complexity of writing in a second language. We did our best to correct the present manuscript with language in mind, and once every scientific issues are resolved and manuscript is deemed satisfying by the editor, we will submit the last version of the text to a native English speaker who is also a specialist in ecology, for proof reading and improve the language.

Below I have outlined my thoughts in more detail. I hope this helps the authors improve their manuscript, and I look forward to seeing an updated version.

Introduction

The introduction contains the required theory to understand the background of the study, which is well justified. However, I’m afraid I feel it needs work. The presentation of theory is quite disorganised, with several vague explanations and examples. Additional citations, concrete examples, and supporting details are needed in various parts. Similarly, the study's description at the end is unclear, especially regarding the definition of coordination in this context.

One issue is that the context and focus of the introduction is not well established – it is unclear whether it focuses on all caregiving animals, species with biparental care, or just long-term monogamous parents. The entire introduction seems bird-centric, yet this isn't explicitly acknowledged. Clarifying the focus and explicitly setting the scene is necessary to improve clarity. For example, it might be easiest to explain that the introduction is focusing on birds that are long-term monogamous, and then introduce the relevant literature in a clear way.

REPLY : We tried to make it clearer in the introduction that we are mainly focusing on bird species with bi-parental care. Given that PlosOne is a Journal with a wide range of scientific interests, we started the introduction quite widely on parental care and narrowed it down to the specific case of seabirds with long-term pair bond and biparental care.

My line-by-line comments are follows:

L42-45: This sentence sets up a false contrast. The time and energy devoted to offspring is costly precisely because it impacts survival and/or future reproduction. If there was no future survival or reproduction (i.e., the species is semelparous), the cost of parental investment wouldn’t matter. Furthermore, I don’t think ‘evolutionarily’ is the right word here – this is describing an individual trade-off. Finally, ‘somehow jeapordizes’ makes it sound like you don’t know how – I suggest removing ‘somehow’.

REPLY : We rephrased the sentence, see lines 42-45.

L50-56: The theory is oversimplified here. Cooperation itself isn’t a solution to sexual conflict because it is evolutionarily unstable. A cooperating pair is always vulnerable to one partner free-loading on the other – there needs to be enforcement for it to be maintained. For long-term monogamous species, this enforcement may come about through the intrinsic benefit of retaining the partner – for example, because there is a high cost to divorce. Cooperation emerges only when (1) parents cannot provide uniparental care and (2) there is a high cost to losing that partner. This concept of ‘partner value’ is reviewed in Griffith 2019.

REPLY : We removed mention of “solution” (see line 55) but nonetheless believe that coordination allows some mitigation of the conflict, through the two mechanisms mentioned by the reviewer, that provide stability.

L59-60: For balance, it is probably worth noting that some studies suggest/show that sexual conflict between the parents can mean that offspring end up receiving less investment in biparental care than would be expected given the sum of the parents’ possible individual contribution, e.g.:

McNamara JM, Houston AI, Barta Z, Osorno JL. 2003. Should young ever be better off with one parent than with two? Behavioral Ecology. 14(3):301–310. doi:10.1093/beheco/14.3.301.

Royle NJ, Hartley IR, Parker GA. 2002. Sexual conflict reduces offspring fitness in zebra finches. Nature. 416(6882):733–736. doi:10.1038/416733a.

REPLY : Text was modified and suggested references added, see line 61.

L63: I’m not sure the Tyson paper shows a positive relationship between parental body condition and coordination.

REPLY : The discussion of the Tyson paper briefly mentions parents could have direct “benefit by coordinating, for instance by determining which partner is in greater need of a long, self-maintenance foraging trip”.

L66: It’s unclear what is meant by ‘short time of pair-bonding’

REPLY : It means that the familiarity effect can reduce the time dedicated to re-establishing the pair bond after winter separation.

L84: I suggest ‘likely to be /a/ prime driver’ (rather than /the/) – ‘the’ suggests that this is the only driver of parental behaviour, which I suspect is unlikely.

REPLY : Corrected

L84-87: I’m not sure what these sentences mean. Is this saying that environmental variables might affect coordination, and might additionally affect coordination differently during different breeding periods? And if this is the case, then we might have different expectations of coordination depending on environmental context?

REPLY : As explained by the following sentences (lines 90-96), it is indeed meaning that environmental conditions could influence coordination, and could do so differently for different breeding periods.

L88-91: This needs some citations and examples.

REPLY : This paragraph is used to introduce a very important part of the study that is actually missing from literature. There is no study, in our knowledge, that investigated coordination at both incubation and chick rearing period. Therefore, we present here hypotheses of what is likely to happen depending on differences in species’ ecology.

L91-92: Why would coordination be more pronounced during chick rearing? There is an example given for incubation but not here.

REPLY : As mentioned above, no other study investigated the coordination in both breeding periods, and therefore this sentence highlights that we do not have full understanding of what happens, but we can expect differences between species.

L93-97: This section really needs some references and examples to support it – it’s quite vague and unspecific. I would also like to see some percentages supporting the statement that most parents don’t coordinate during incubation (I don’t disagree, but you need to substantiate this). Similarly you need to substantiate the claim that tasks are generally more similar between the parents during chick-rearing

REPLY : We couldn’t find accurate percentages, but Cockburn (2006) describes quite well all the claims of this section.

L102: Contribution of both parent

10.1371/journal.pone.0306796.r003
Decision Letter 1
Radwan Lamiaa Mostafa Academic Editor
© 2024 Lamiaa Mostafa Radwan
2024
Lamiaa Mostafa Radwan
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Submission Version1
3 Apr 2024

PONE-D-23-40200R1Coordination of parental performance is breeding phase-dependent in the Dovekie (Alle alle), a pelagic Arctic seabirdPLOS ONE

Dear Dr. Grissot,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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Kind regards,

Lamiaa Mostafa Radwan, Ph.D.

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments:

Dear Dr., Antoine Grissot

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we have decided that your manuscript needs Minor Revision.

Comment Editor:

It is necessary to make all amendments and corrections requested by Reviewer 2

Kind regards,

Prof. Lamiaa Mostafa Radwan, Ph.D.

Academic Editor

PLOS ONE

Reviewer1

Accept

Reviewer2

Many thanks to the authors for their efforts in revising their manuscript. I appreciate that they have implemented some of my feedback, as well as their additional clarification regarding the coordination metrics. However, while the authors have addressed my comments in their rebuttal letter, and for the most part done so very well and clearly, I found that these changes have not consistently translated into edits to the manuscript itself. Consequently, many of my comments below are identical to those provided in the previous review, with explicit requests that the well-explained responses provided by the authors are integrated directly into the manuscript text. Rectifying this should involve little effort beyond incorporating the content from the rebuttal directly into the manuscript, as is standard practice during revisions.

My concerns about the analyses have been somewhat alleviated but there is one part I still do not understand – the authors make the argument that their coordination analyses work on the basis that birds can engage in three different behaviours: nest, colony, and foraging. Yet, in the rebuttal, they state:

‘Individuals when present in the colony usually spend most of their time in the surroundings of their nest. Furthermore when they leave the frame and come back with a full gular pouch, we know a foraging trip was performed. There is a possibility they spend a little time in the colony before actually departing for the foraging trip, but assume that it is negligible.’

If colony time is assumed to be negligible, I don’t understand how the rest of the analyses follow? This is very likely a misunderstanding on my part, but it has come from unclear explanations. If the authors address this, please ensure this is reflected in the manuscript rather than just the response.

Finally - this is more of a point to the editor - as the authors acknowledge, the manuscript still requires proof reading, but I note that they have made arrangements to do this for their next revision. I have therefore not addressed any typographical or grammatical errors.

My relevant line-by-line comments are below, and refer to the ‘tracked changes’ version of the manuscript.

Introduction

L54: Possibly debatable whether 10 years ago is ‘recently’, I’d suggest removing this word.

L61: These papers show *lower* offspring fitness due to biparental care, and so are improperly cited. The point of my original comment is that while biparental care may improve offspring fitness, this is not guaranteed. McNamara demonstrates this theoretically; Royle shows this experimentally in zebra finches. All this requires is something like ‘(*but see* Royle et al 2003, McNamara et al 2003)’ but I also suggest reading the papers as they are important pieces of theory.

L68: Suggest ‘reduced time investment in pair bonding’ rather than ‘short time of pair-bonding’ for clarity.

L87-88: It is still necessary to explain why environment is likely to be important i.e. give some examples of why/when environment impacts coordination and why it differs between stages. E.g. food availability might differ seasonally, which could be more important in chick rearing when energetic constraints are higher. I appreciate that the authors are investigating novel questions, but they are not plucked from thin air, it’s important to evidence the hypotheses.

L90: Similarly, there are examples in the literature that could be provided here. Even if other authors haven’t specifically compared breeding phases, there are plenty of other studies that could be used to support this e.g. those showing differences between breeding phases in trip duration, in parental behaviour, in specific constraints. ‘May thus be specific…’ is too vague.

L96: This is the sunk cost fallacy – animals never make decisions based on prior investment alone. If a breeding attempt is doomed to fail parents will end the attempt regardless of how much prior investment they have made. Rather, to make this argument one could discuss that it is more costly to start afresh than to continue. But this is a subtle difference. Please see Dawkins & Carlisle’s original explanation: DAWKINS, R., CARLISLE, T. Parental investment, mate desertion and a fallacy. Nature 262, 131–133 (1976). https://doi.org/10.1038/262131a0

This sentence should therefore be removed. I actually think your next few sentences (discussing the idea that many birds don’t coordinate incubation but do coordinate chick rearing) illustrates the idea that coordination might be more pronounced during chick rearing just fine. You could also discuss the increased energetic costs of chick rearing vs incubation and the increased constraints associated with dividing self-care and chick care, for which the literature is full of examples.

L122-123: It’s not enough to just discuss ‘patterns’ – please explain what you mean and give examples (e.g. lots of seabirds where foraging trips are longer during incubation than chick-rearing). As pointed out in the rebuttal, PLOS is a broad journal, so it is important to explain what this means behaviourally.

L125: ‘Runway’ is not a term I have encountered in the literature, and I doubt I’m alone – I suggest explaining as it was in the rebuttal letter i.e. parents may need time to synchronise to each other’s behaviour prior to breeding.

L126: Given there is no evidence (based on the rebuttal letter) I suggest removing; ‘familiarity’ is poorly defined in the literature anyway.

L157: It is essential to state that eggs can withstand neglect, and how long for. If eggs could only survive 10 minutes of neglect, then my original point that successful breeders are constrained to apparently coordinate would still stand. This is crucial to the rest of the analyses so needs to be stated explicitly and clearly.

L166: I still don’t understand what is meant by ‘habituation to the parental mode’ even with the rebuttal letter. This needs explanation – perhaps ‘increased within-pair synchronicity’?

L244: Please include explanation from rebuttal letter for why observer effects are not a concern. In the rebuttal it states ‘we made sure new observer would not differ’ – how, if there were no stats? Worth outlining in supplementary.

L254: Please include explanation from the rebuttal letter.

L271: See my main comments above about whether colony behaviour is negligible or not.

L272: I don’t think ‘and their constraints’ adds anything here, and it’s confusing. I suggest removing it.

L296: Please include explanation from the rebuttal letter.

L323-324: ‘Phase’ is used to mean something different for incubation and chick rearing. This is really confusing as they are

different metrics (continuous numerical vs categorical) and is misleading. Please rephrase.

L328: What is the distribution of the response variable, please state.

L360: State that the two chick rearing phases are ‘early’ and ‘mid’ (perhaps in brackets). There is a lot of reliance on readers remembering quite specific pieces of information, please restate these sorts of things when relevant to make it easier.

L364-368: This is still a very difficult sentence to follow and very long. Please rephrase.

L376-377: My confusion here arose because the phrasing suggests that there was a coordination index for both incubation

and chick rearing (‘In contrast to the incubation period, we decided to use for the chick rearing period the coordination index’), which I understand from the rebuttal letter is not correct. Please rephrase.

L384: Please include explanation from the rebuttal letter.

L506: I suggest some caveat e.g. behaviour is flexible between breeding stages, because you don’t show intra-individual flexibility and therefore can’t technically refute the ‘sealed bid’ model (e.g. parents could submit a fixed sealed bid for incubation and chick rearing separately, which doesn’t change – this is unlikely but we can’t say with certainty).

L544-545: In my original review, I did not mean that hormones don't play a role. My point is that in the discussion, you seem to be asking evolutionary/ultimate questions – i.e. what has driven the evolution of coordinated incubation? For example, you point out that coordination may evolve because it favours embryo development or because it helps to protect chicks prior to thermal independence.

Yes, hormones are likely to be a mechanism by which coordination is achieved – but *why* has this mechanism evolved? It is suggested that hormones explain why birds become more devoted to incubation over time – mechanistically this might be true, but it doesn't answer the 'why' question. Many birds fly south for winter - this could be driven by some hormonally mediated instinct, but that doesn't tell us why they do it in the first place.

It's fine to say that hormonal changes regulate behaviour, but I would put this somewhere else in the discussion and make clear that this is a mechanistic question. In fact, a better option might be to put this in the introduction to help show that levels of coordination change over time. E.g. something along the lines of: prolactin increases over the course of incubation, suggesting changes in parental care behaviour over time - but whether this increases parents’ propensity to incubate, and therefore their level of coordination, is unknown.

L565-567: Please include explanation from the rebuttal letter.

L572-573: It seems surprising to expect coordination to ‘reset’ after chick-rearing as outlined in the rebuttal; this needs further explanation (in the manuscript).

L582: I think perhaps ‘differences’ would make more sense– instability is still not clear.

L594: I suggest ‘reflect’ as ‘express’ suggests an active choice.

L595-596: Please include explanation from the rebuttal letter.

Reviewer3

Accept

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: (No Response)

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: (No Response)

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: (No Response)

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: (No Response)

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors address all comments one by one, and on those who disagree with the reviewers their argument was strong enough. The manuscript links the methods with the results and discussions. The data is fully available.

Reviewer #2: Many thanks to the authors for their efforts in revising their manuscript. I appreciate that they have implemented some of my feedback, as well as their additional clarification regarding the coordination metrics. However, while the authors have addressed my comments in their rebuttal letter, and for the most part done so very well and clearly, I found that these changes have not consistently translated into edits to the manuscript itself. Consequently, many of my comments below are identical to those provided in the previous review, with explicit requests that the well-explained responses provided by the authors are integrated directly into the manuscript text. Rectifying this should involve little effort beyond incorporating the content from the rebuttal directly into the manuscript, as is standard practice during revisions.

My concerns about the analyses have been somewhat alleviated but there is one part I still do not understand – the authors make the argument that their coordination analyses work on the basis that birds can engage in three different behaviours: nest, colony, and foraging. Yet, in the rebuttal, they state:

‘Individuals when present in the colony usually spend most of their time in the surroundings of their nest. Furthermore when they leave the frame and come back with a full gular pouch, we know a foraging trip was performed. There is a possibility they spend a little time in the colony before actually departing for the foraging trip, but assume that it is negligible.’

If colony time is assumed to be negligible, I don’t understand how the rest of the analyses follow? This is very likely a misunderstanding on my part, but it has come from unclear explanations. If the authors address this, please ensure this is reflected in the manuscript rather than just the response.

Finally - this is more of a point to the editor - as the authors acknowledge, the manuscript still requires proof reading, but I note that they have made arrangements to do this for their next revision. I have therefore not addressed any typographical or grammatical errors.

My relevant line-by-line comments are below, and refer to the ‘tracked changes’ version of the manuscript.

Introduction

L54: Possibly debatable whether 10 years ago is ‘recently’, I’d suggest removing this word.

L61: These papers show *lower* offspring fitness due to biparental care, and so are improperly cited. The point of my original comment is that while biparental care may improve offspring fitness, this is not guaranteed. McNamara demonstrates this theoretically; Royle shows this experimentally in zebra finches. All this requires is something like ‘(*but see* Royle et al 2003, McNamara et al 2003)’ but I also suggest reading the papers as they are important pieces of theory.

L68: Suggest ‘reduced time investment in pair bonding’ rather than ‘short time of pair-bonding’ for clarity.

L87-88: It is still necessary to explain why environment is likely to be important i.e. give some examples of why/when environment impacts coordination and why it differs between stages. E.g. food availability might differ seasonally, which could be more important in chick rearing when energetic constraints are higher. I appreciate that the authors are investigating novel questions, but they are not plucked from thin air, it’s important to evidence the hypotheses.

L90: Similarly, there are examples in the literature that could be provided here. Even if other authors haven’t specifically compared breeding phases, there are plenty of other studies that could be used to support this e.g. those showing differences between breeding phases in trip duration, in parental behaviour, in specific constraints. ‘May thus be specific…’ is too vague.

L96: This is the sunk cost fallacy – animals never make decisions based on prior investment alone. If a breeding attempt is doomed to fail parents will end the attempt regardless of how much prior investment they have made. Rather, to make this argument one could discuss that it is more costly to start afresh than to continue. But this is a subtle difference. Please see Dawkins & Carlisle’s original explanation: DAWKINS, R., CARLISLE, T. Parental investment, mate desertion and a fallacy. Nature 262, 131–133 (1976). https://doi.org/10.1038/262131a0

This sentence should therefore be removed. I actually think your next few sentences (discussing the idea that many birds don’t coordinate incubation but do coordinate chick rearing) illustrates the idea that coordination might be more pronounced during chick rearing just fine. You could also discuss the increased energetic costs of chick rearing vs incubation and the increased constraints associated with dividing self-care and chick care, for which the literature is full of examples.

L122-123: It’s not enough to just discuss ‘patterns’ – please explain what you mean and give examples (e.g. lots of seabirds where foraging trips are longer during incubation than chick-rearing). As pointed out in the rebuttal, PLOS is a broad journal, so it is important to explain what this means behaviourally.

L125: ‘Runway’ is not a term I have encountered in the literature, and I doubt I’m alone – I suggest explaining as it was in the rebuttal letter i.e. parents may need time to synchronise to each other’s behaviour prior to breeding.

L126: Given there is no evidence (based on the rebuttal letter) I suggest removing; ‘familiarity’ is poorly defined in the literature anyway.

L157: It is essential to state that eggs can withstand neglect, and how long for. If eggs could only survive 10 minutes of neglect, then my original point that successful breeders are constrained to apparently coordinate would still stand. This is crucial to the rest of the analyses so needs to be stated explicitly and clearly.

L166: I still don’t understand what is meant by ‘habituation to the parental mode’ even with the rebuttal letter. This needs explanation – perhaps ‘increased within-pair synchronicity’?

L244: Please include explanation from rebuttal letter for why observer effects are not a concern. In the rebuttal it states ‘we made sure new observer would not differ’ – how, if there were no stats? Worth outlining in supplementary.

L254: Please include explanation from the rebuttal letter.

L271: See my main comments above about whether colony behaviour is negligible or not.

L272: I don’t think ‘and their constraints’ adds anything here, and it’s confusing. I suggest removing it.

L296: Please include explanation from the rebuttal letter.

L323-324: ‘Phase’ is used to mean something different for incubation and chick rearing. This is really confusing as they are

different metrics (continuous numerical vs categorical) and is misleading. Please rephrase.

L328: What is the distribution of the response variable, please state.

L360: State that the two chick rearing phases are ‘early’ and ‘mid’ (perhaps in brackets). There is a lot of reliance on readers remembering quite specific pieces of information, please restate these sorts of things when relevant to make it easier.

L364-368: This is still a very difficult sentence to follow and very long. Please rephrase.

L376-377: My confusion here arose because the phrasing suggests that there was a coordination index for both incubation

and chick rearing (‘In contrast to the incubation period, we decided to use for the chick rearing period the coordination index’), which I understand from the rebuttal letter is not correct. Please rephrase.

L384: Please include explanation from the rebuttal letter.

L506: I suggest some caveat e.g. behaviour is flexible between breeding stages, because you don’t show intra-individual flexibility and therefore can’t technically refute the ‘sealed bid’ model (e.g. parents could submit a fixed sealed bid for incubation and chick rearing separately, which doesn’t change – this is unlikely but we can’t say with certainty).

L544-545: In my original review, I did not mean that hormones don't play a role. My point is that in the discussion, you seem to be asking evolutionary/ultimate questions – i.e. what has driven the evolution of coordinated incubation? For example, you point out that coordination may evolve because it favours embryo development or because it helps to protect chicks prior to thermal independence.

Yes, hormones are likely to be a mechanism by which coordination is achieved – but *why* has this mechanism evolved? It is suggested that hormones explain why birds become more devoted to incubation over time – mechanistically this might be true, but it doesn't answer the 'why' question. Many birds fly south for winter - this could be driven by some hormonally mediated instinct, but that doesn't tell us why they do it in the first place.

It's fine to say that hormonal changes regulate behaviour, but I would put this somewhere else in the discussion and make clear that this is a mechanistic question. In fact, a better option might be to put this in the introduction to help show that levels of coordination change over time. E.g. something along the lines of: prolactin increases over the course of incubation, suggesting changes in parental care behaviour over time - but whether this increases parents’ propensity to incubate, and therefore their level of coordination, is unknown.

L565-567: Please include explanation from the rebuttal letter.

L572-573: It seems surprising to expect coordination to ‘reset’ after chick-rearing as outlined in the rebuttal; this needs further explanation (in the manuscript).

L582: I think perhaps ‘differences’ would make more sense– instability is still not clear.

L594: I suggest ‘reflect’ as ‘express’ suggests an active choice.

L595-596: Please include explanation from the rebuttal letter.

Reviewer #3: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: María Félix-Lizárraga

Reviewer #2: No

Reviewer #3: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

10.1371/journal.pone.0306796.r004
Author response to Decision Letter 1
Submission Version2
7 Jun 2024

See attached file "Response to Reviewers"

Attachment Submitted filename: Response to Reviewers.docx

10.1371/journal.pone.0306796.r005
Decision Letter 2
Brundage Cord M. Academic Editor
© 2024 Cord M. Brundage
2024
Cord M. Brundage
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Submission Version2
24 Jun 2024

Coordination of parental performance is breeding phase-dependent in the Dovekie (Alle alle), a pelagic Arctic seabird

PONE-D-23-40200R2

Dear Dr. Grissot,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Cord M. Brundage, D.V.M., Ph.D.

Academic Editor

PLOS ONE

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: No

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Comments were addressed appropriately by the authors. The manuscripts its completed and ready . Thank you to the authors of the effort.

Reviewer #2: Thank you to the authors for their efforts in revising this manuscript; it is much improved as a result. I have just two very short comments. Firstly, in the abstract, L32 - the sentence claims that coordination was found to be 'condition-dependent'. This was not explored in the study, so please remove this. Secondly, throughout the manuscript, there are a few instances where the word 'the' appears before 'incubation' or 'chick-rearing' e.g. L116-117: 'During the incubation, parental coordination...' should be 'During incubation, parental coordination...'. Most of these are addressed but quite a few still remain that should be removed.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: María Félix-Lizárraga

Reviewer #2: No

**********

10.1371/journal.pone.0306796.r006
Acceptance letter
Brundage Cord M. Academic Editor
© 2024 Cord M. Brundage
2024
Cord M. Brundage
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
18 Jul 2024

PONE-D-23-40200R2

PLOS ONE

Dear Dr. Grissot,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Cord M. Brundage

Academic Editor

PLOS ONE
==== Refs
References

1 Kokko H , Jennions MD . Parental investment, sexual selection and sex ratios. Journal of Evolutionary Biology. 2008;21 : 919–948. doi: 10.1111/j.1420-9101.2008.01540.x 18462318
2 Fromhage L. Parental Care and Investment. In eLS, John Wiley & Sons, Ltd (Ed.); 2017. doi: 10.1002/9780470015902.a0021907.pub2
3 Alonso-Alvarez C , Velando A . “Benefits and costs of parental care,” in The Evolution of Parental Care, Kölliker M , Smiseth P. T , and Royle N. J . Oxford academic; 2012. doi: 10.1093/acprof:oso/9780199692576.003.0003
4 Trivers RL . Parental investment and sexual selection. In Sexual Selection and the Descent of Man, 1871–1971. Aldine Publishing Company; 1972.
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