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Parental incubation patterns and the effect of group size in a Neotropicalcooperative breederAuthor(s): Jennifer L. Mortensen and J. Michael ReedSource: The Auk, 135(3):669-692.Published By: American Ornithological Societyhttps://doi.org/10.1642/AUK-17-236.1URL: http://www.bioone.org/doi/full/10.1642/AUK-17-236.1

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Volume 135, 2018, pp. 669–692DOI: 10.1642/AUK-17-236.1

RESEARCH ARTICLE

Parental incubation patterns and the effect of group size in a Neotropicalcooperative breeder

Jennifer L. Mortensena* and J. Michael Reed

Department of Biology, Tufts University, Medford, Massachusetts, USAa Current address: University of Arkansas, Fayetteville, Arkansas, USA* Corresponding author: [email protected]

Submitted December 11, 2017; Accepted March 11, 2018; Published May 30, 2018

ABSTRACTIn many cooperatively breeding species, young (‘‘helpers’’) from one year help other adults raise offspring thefollowing year. In contrast to helper effects during the nestling or postfledging stages of the avian breeding cycle,potential benefits from helpers during incubation are poorly studied. We analyzed 39 clutches and recorded 6,027 off-bouts to document incubation behavior in the White-breasted Thrasher (Ramphocinclus brachyurus), an endangeredNeotropical facultative cooperative breeder. Our goal was to test the prediction that cooperation confers benefitsduring incubation in terms of increased nest attendance and hatching success. We found that 65% of active hours(0500–2100) are spent on the nest, values somewhat lower than average for a tropical passerine with uniparentalincubation. Highest incubation constancy was observed at a rare 4-egg clutch, which was attended by putative joint-nesters. Excluding this clutch, differences in incubation behavior between pair and cooperative groups were subtleand context dependent. We found temporal variation in incubation behavior, whereby off-bout frequency declined asthe breeding season progressed, but more quickly for cooperative groups. Maximum ambient temperature was alsoan influential abiotic predictor. Across both social group types, incubation constancy declined as temperatureincreased to ~308C, above which constancy remained high. As expected, we found that the behavior of birds withfailed and successful clutches differed. Specifically, failed clutches experienced high early-season constancy, despitetemperature data suggesting insufficient warming during that time, and successful cooperative clutches had higherlate-season constancy than pairs. Other factors important in avian systems were not predictive of incubation behaviorhere, and in general, high individual variation for all incubation behaviors swamped most other sources of variation.Results from this work highlight the individuality in incubation behavior and suggest that breeding females incooperative groups have more flexibility in shifting between incubation demands and maintenance behaviors than dolone pairs.

Keywords: Caribbean, cooperative breeding, fitness, Neotropical, nest attendance, Ramphocinclus brachyurus,tropical, White-breasted Thrasher

Patrones de incubacion parental y efecto del tamano de grupo en un ave neotropical de crıa cooperativa(Ramphocinclus brachyurus)

RESUMENEn muchas especies de crıa cooperativa, los jovenes (‘ayudantes’) de un ano ayudan a otros adultos a criar a lospolluelos el ano siguiente. En contraste a los efectos de los ayudantes durante los estadios de volanton o post-emplumamiento del ciclo reproductivo de las aves, los beneficios potenciales de los ayudantes durante la incubacionhan sido poco estudiados. Analizamos 39 nidadas y registramos 6027 eventos de salida de servicio para documentar elcomportamiento de incubacion en Ramphocinclus brachyurus, un ave neotropical en peligro, de crıa cooperativafacultativa. Nuestro objetivo fue evaluar la prediccion que la cooperacion confiere beneficios durante la incubacion enterminos de mayor presencia en el nido y exito de eclosion. Encontramos que el 65% de las horas activas (0500-2100)transcurren en el nido, valores que son algo mas bajos que el promedio para un paserino tropical con incubacion uni-parental. La mayor constancia de incubacion fue observada en una rara nidada de 4 huevos, que estuvo atendida porindividuos que anidaron de forma putativa. Excluyendo esta nidada, las diferencias en comportamiento de incubacionentre las parejas y los grupos cooperativos fueron sutiles y dependientes del contexto. Encontramos variaciontemporal en el comportamiento de incubacion, por lo que la frecuencia fuera de servicio disminuyo a medida queavanzo la estacion reproductiva, pero mas rapidamente para los grupos cooperativos. La temperatura ambientalmaxima fue tambien un predictor abiotico influyente. A traves de ambos tipos de grupos sociales, la constancia deincubacion disminuyo a medida que la temperatura aumento hasta ~30 8C, por sobre la cual la constancia permanecioalta. Como se esperaba, encontramos que el comportamiento de las aves con nidadas fallidas y exitosas fue diferente.

Q 2018 American Ornithological Society. ISSN 0004-8038, electronic ISSN 1938-4254Direct all requests to reproduce journal content to the AOS Publications Office at [email protected]

mailto:[email protected]

Especıficamente, las nidadas fallidas experimentaron una alta constancia a inicios de la estacion, a pesar de los datosde temperatura que sugirieron calor insuficiente durante ese tiempo, y las nidadas cooperativas exitosos tuvieronmayor constancia a finales de la estacion en relacion con las parejas. Otros factores importantes en los sistemas aviaresno fueron predictivos del comportamiento de incubacion y, en general, la alta variacion individual para todos loscomportamientos de incubacion opacaron la mayorıa de las otras fuentes de variacion. Los resultados de este trabajosubrayan la individualidad en el comportamiento de incubacion y sugieren que las hembras reproductivas en gruposcooperativos tienen mas flexibilidad para cambiar entre las demandas de la incubacion y los comportamientos demantenimiento de lo que presentan las parejas solitarias.

Palabras clave: aptitud biologica, Caribe, crıa cooperativa, Neotropical, presencia en el nido, Ramphocinclusbrachyurus, tropical

INTRODUCTION

Cooperative breeding involves individuals (helpers) caring

for young that are not their own offspring. This behavior

seems to be more common in birds than in other

vertebrates (Russell 2004, Lukas and Clutton-Brock

2012), but it is still found in only 2–9% of avian species

(Brown 1987, Cockburn 2006), with the estimate depend-

ing on how cooperative breeding is defined and the degree

of confidence in the data. Despite being fairly uncommon,

many long-term avian field studies have focused on

cooperative breeders (Stacey and Koenig 1990), partially

because of the puzzling, apparently altruistic act of

individuals helping to raise the offspring of others. Much

of the focus of cooperative breeding research has been on

understanding why helpers help and how much helpers

actually benefit the breeders they help (reviewed by Brown

1987, Cockburn 1998, Heinsohn and Legge 1999).

Helping is generally explained by indirect fitness

benefits gained from raising non-descendent kin (inclusive

fitness) and by direct fitness benefits due to group living or

queuing for a later breeding vacancy (reviewed by Koenig

and Dickinson 2004, 2016, Hatchwell 2009, Hatchwell et

al. 2013). Many studies of facultative cooperative breeders

report higher direct fitness benefits associated with

helpers, e.g., larger clutch size (Woxvold and Magrath

2005, Lejeune et al. 2016), shorter inter-clutch interval

(Woxvold and Magrath 2005, Blackmore and Heinsohn

2007), higher nest success (reviewed by Kingma et al.

2010), increased offspring survival and recruitment (re-

viewed by Li et al. 2015, Preston et al. 2016, Loock et al.

2017), and higher breeder survival (reviewed by Kingma et

al. 2010, Li et al. 2015). Studies of helper effects have often

focused on the nestling stage of the breeding cycle, such as

provisioning chicks. Because provisioning altricial young

has high energetic costs (Clutton-Brock 1991), helping at

this time is expected. More recently, several studies have

looked for effects of helpers during the laying stage,

specifically asking whether females base their investment

in egg production on the probable gains they will receive

by the presence or absence of helpers. Lower egg

investment in the presence of helpers has been reported

in Superb Fairy Wrens (Malurus cyaneus; Russell et al.

2007), Carrion Crows (Corvus corone; Canestrari et al.

2011), Southern Lapwings (Vanellus chilensis; Santos and

Macedo 2011), and Sociable Weavers (Philetairus socius;

Paquet et al. 2013); a higher investment in Iberian magpie

(Cyanopica cooki; Valencia et al. 2017); and no difference

in Acorn Woodpeckers (Melanerpes formicivorus; Koenig

et al. 2009). In contrast to helper effects during the laying,

nestling, or postfledging stages of the breeding cycle,

possible helper benefits to the breeders during incubation

have not yet been addressed.

In birds, incubation is typically costly because it requires

maintaining high egg temperatures (Monaghan and Nager

1997, Turner 2002, Nord and Williams 2015). Parental

costs of incubation include heat transferred to eggs, which

accounts for 10–30% of basal metabolic rate in passerines,

as well as lost foraging opportunities (Clutton-Brock 1991,

Reid et al. 2002). Incubation constancy, defined as the

proportion of time spent in contact with the egg,

influences embryo viability and development (Webb

1987, McClintock et al. 2014) and can affect nestling

survival and phenotype (DuRant et al. 2013, Berntsen and

Bech 2016). Consequently, helpers might increase breeder

fitness and their own inclusive fitness by participating in

activities during incubation. Participation might include

sharing incubation duties (Parry 1973, Heinsohn and

Cockburn 1994, Komdeur 1994), allofeeding the incubator

(Reyer 1980, Poiani 1992, Valencia et al. 2003, Radford

2004, Lloyd et al. 2009), antipredator behavior, or territory

defense (Woolfenden and Fitzpatrick 1984, Komdeur

1994). In some systems, there is evidence that the presence

of helpers leads to increased hatching success (Woolfenden

and Fitzpatrick 1984, Komdeur 1994, Innes and Johnston

1996, Legge 2000, Klauke et al. 2013; but see Mumme

1992, Valencia et al. 2003, Woxvold and Magrath 2005,

Canestrari et al. 2008) and that larger cooperative groups

can have higher incubation constancy (Yuan et al. 2005).

However, none of this work has evaluated the potential for

differential incubation constancy in cooperative breeders

to affect reproductive success or survival.

We hypothesized that incubation constancy is a benefit

of cooperative breeding via increasing hatching success.

We tested this hypothesis in a Neotropical, monogamous,

facultative cooperative breeder, the White-breasted

The Auk: Ornithological Advances 135:669–692, Q 2018 American Ornithological Society

670 Incubation patterns of White-breasted Thrasher J. L. Mortensen and J. M. Reed

Thrasher (Ramphocinclus brachyurus). In this species,

cooperative groups have higher nesting success (�1 chick

fledged nest�1) than unaided pairs, although group size

does not appear to be correlated with timing of laying,

clutch size, nestling condition, or number fledged per

successful nest (Temple 2005). It is not known whether, or

how, helpers contribute to the pattern of increased

productivity. The only mechanism that has been investi-

gated in this regard is provisioning rates of chicks, which

did not differ between group types (Temple 2005). Recent

data for this species suggest that hatching success is higher

in cooperative groups than at pair territories, but nestling

loss does not differ between group types (J. L. Mortensen

personal observation). In White-breasted Thrashers, only

the dominant female has been reported to incubate and

helpers do not allofeed (J. L. Mortensen personal

observation). Allofeeding of the incubator is uncommon

and performed only by the dominant male. However,

White-breasted Thrasher helpers are known to participate

in nest defense (Freeman 2015) and are frequently

observed in the vicinity of the nest during the incubation

period (J. L. Mortensen personal observation). Helpers,

therefore, have an opportunity to increase the breeder’s

nest attentiveness by participating in other maintenance

activities like antipredator behavior and territory defense.

Consequently, our research had 2 goals. The first was to

document incubation behavior for the first time in this

species. The second was to test hypotheses about the

potential benefits of cooperative breeding: we expected (1)

cooperatively breeding groups to have greater incubationconstancy and (2) increased incubation constancy to lead

to greater hatching success.

METHODS

Study Species and Field MethodsThe White-breasted Thrasher is an endangered songbird

endemic to the Caribbean islands of Saint Lucia and

Martinique (BirdLife International 2018). Within its 2-

island range, the species is restricted to 3 areas of seasonal

deciduous forest—1 in Martinique and 2 in Saint Lucia—in

a total area of ,1,076 ha (Mortensen et al. 2017, Sass et al.

2017). The Saint Lucian Mandele population is the largest

for the species (,1,500 individuals; Mortensen et al. 2017)

and is the focus of our field study (13.898N, 60.898W).

Our work took place during the White-breasted

Thrasher’s breeding season. Breeding generally spans

April–September (Temple 2005), and we collected field

data during June–August in 2012 and 2013. Breeding

groups consist of 2 breeders and 0–4 helpers (Mortensen

2009, Temple et al. 2009), and the incidence of plural

breeding is thought to be low. Most cooperative groups

have only 1 helper (Mortensen 2009, Temple et al. 2009),

which is typically a second-year offspring of the breeding

pair in a nearly 1:1 sex ratio (Temple et al. 2009), and the

proportion of territories containing �1 helpers varies

temporally (e.g., 30–73%; Temple 2005, Mortensen 2016).

We studied a previously color-banded population and

captured unmarked individuals using mist nets, banding

each individual with an aluminum band and a unique

combination of colored leg bands. We assessed the size of

social groups by repeated observations of active nests

during the building, laying, incubation, and nestling stages.

Besides passive behavioral observations, we used a

standardized tape playback of White-breasted Thrasher

chick alarm calls and a call from an adult White-breasted

Thrasher mobbing a Gray Trembler (Cinclocerthia guttur-

alis) to attract territory birds to the nest area.

Incubation MonitoringWhite-breasted Thrasher nests are open cup, 1.0–1.5 m

high, conspicuous, and often in the same location from

year to year. White-breasted Thrashers lay a 2-egg clutch

97% of the time (Temple 2005). Upon finding a nest with

eggs, we determined egg age by candling, laying date, orback calculating from hatching date or chick age. Egg age

when we found the nests varied from 0 (lay date) to 21

days.

We used Thermochron iButtons (DS1921G, MaximIntegrated Products, San Jose, California, USA; accuracy 6

18C)—small, self-contained data loggers—to monitor nest-

cup temperature. Temperature data recorded by iButtons

can indicate on- and off-bout periods used to infer

incubation dynamics (Cooper and Mills 2005); nest

temperature drops when the incubating bird leaves the

nest and rises again when incubation resumes. We placed

an iButton in the inner cup of each nest adjacent to the

eggs (,10 mm) and fastened it to the nest with a small

wire to prevent birds from ejecting the device. Visual

inspection confirmed that iButtons were not covered with

nesting material. Because iButtons were not in direct

contact with the clutch, we did not measure actual

temperatures experienced by the eggs, but rather an index

of heat that should be consistent across nests and that gave

us a strong signal of on- and off-bouts. Hatching rate in the

present study (64%, n¼ 47 clutches; described below) was

similar to rates in previous work on the same species (60%,

n ¼ 96 clutches [Temple 2005]; 60%, n ¼ 105 clutches

[Mortensen 2009]), which suggests that the presence of

data loggers in the nest did not interfere with incubation

behavior or hatching success.

From preliminary surveys, we found that 2 min intervals

for recording temperatures allowed for the best combina-

tion of detecting incubation bouts and maximizing

recording length. We could determine from the temper-

ature traces when a bird left the nest, and this sampling

rate allowed for ~3 days of continuous temperature

monitoring. We replaced each iButton every 3 days for as


J. L. Mortensen and J. M. Reed Incubation patterns of White-breasted Thrasher 671

long as the nest contained eggs. We used the following

criteria to delineate off-bouts: 2 min minimum off-bout

duration, 18C minimum off-bout depth (i.e. decrease in

temperature during an off-bout), and 0.18C min�1

minimum cooling. We inspected the Rhythm output in

Raven (Bioacoustics Research Program 2014) for each

temperature record to verify on- and off-bouts and

manually selected off-bouts not identified by the program.

We censored data on days when we disturbed the nest at

length, including activities such as mist netting and nest

watches. Our sample included viable and inviable clutches.

We excluded data from inviable clutches after the time of

nest abandonment, defined as the time at which iButton

nest temperature data commenced tracking ambient air

temperature, as well as data from inviable clutches still

being incubated after 15 days, which is one standard

deviation beyond the mean incubation period (14 days;

Temple 2005). Finally, we excluded data collected before

clutch completion and from clutches that remained active

at the end of the field season. We performed nestobservations at a subset of nests and verified that recorded

iButton data paralleled actual incubation patterns.

We were interested in 3 measures of incubation

behavior: incubation constancy (the proportion of timethe clutch was incubated), off-bout frequency (number of

off-bouts taken per hour), and off-bout duration (the

length in minutes of each off-bout). We note that although

these measures are related, there is no particular reason to

expect that they are strongly correlated across most values

(for all pairwise comparisons, maximum rs , 0.6). We

assessed off-bout duration in 3 ways: off-bout duration,

mean off-bout duration per clutch-day, and variation

(standard deviation, SD) in off-bout duration per clutch-

day.

Statistical AnalysesWe used R 3.2.2 (R Core Team 2014) for all statistical tests.

Values reported are means 6 SD, unless noted otherwise.

Incubation behavior modeling. To assess whether

social group type (cooperative vs. pair breeder) influenced

incubation behavior, we analyzed the incubation parame-

ters in 2 ways: (1) one-tailed t-tests paired by date, to

control for the possible effect of environmental conditions

on incubation behavior; and (2) linear mixed-effects

models, to include environmental conditions and variables

known to affect incubation behavior in other bird species.

For mixed models, we log transformed each of the

incubation variables except incubation constancy to meet

model assumptions (Sokal and Rohlf 1995). We included

several factors known to influence incubation behavior in

other species (Clutton-Brock 1991, Deeming 2002b,

Cooper and Voss 2013, Coe et al. 2015): clutch size, stage

of egg development, temporal elements (year and day of

year), and weather (rainfall and ambient temperature).

Since clutch-age was not known for all clutches in our

sample, we used a 2-step process to analyze the incubation

data in mixed models (Skagen and Adams 2012). We first

constructed a base model set for each incubation behavior

that included the clutch-related variables, clutch size and

clutch age (where day 0 is the lay date of the first egg in the

clutch), and territory ID as a random factor. Including

territory ID considers that we monitored some groups in

both years and that some groups had multiple clutches

within years, as well as the repeated measures of

incubation behavior within each clutch. In step 2, we

added our variables of interest to each top base model. In

addition to social group type, we included year (2012 or

2013) as a fixed factor; total daily rainfall (i.e. over 24 hr),

minimum and maximum daily temperature, the interac-

tion between mean daily temperature and rainfall, and day

of year as covariates; and territory ID as a random factor.

We also investigated 2-way interactions between social

group type and each of the temporal- and weather-related

predictors. High correlations among predictor variablescan lead to unreliable estimates of regression coefficients,

affecting inference. The highest correlation coefficient (r)

between our predictors was only 0.43, between minimum

and maximum daily temperature, so variable reduction or

aggregation was not needed. Our goal with this set of

models was to determine whether social group type

affected incubation behavior over the clutch-day (i.e.

incubation parameters were analyzed per day for each

clutch). Many studies measure incubation for only a few

hours per day, but we saw no reason to censor our data,

given that there was no clear diurnal pattern in timing of

off-bouts (see below).

For a finer-scale model, we assessed the effect of social

group type, and of conditions at the exact time of the off-

bout, on off-bout duration. This model included 2-way

interactions of group type with time and ambient

temperature. As in the previous set of models, territory

ID was included as a random factor. The correlation

coefficient between the 2 continuous predictors was 0.29.

In this final model, we censored off-bouts where ambient

temperature data were not available for the exact time that

the off-bout began.

We built mixed model sets using the lmer function in

the lme4 package (Bates et al. 2015). We compared models

within each set using an information-theoretic approach,

assessing models based on their second-order Akaike’s

Information Criterion (AIC) corrected for small sample

sizes (AICc), AICc differences (DAICc), and Akaike weights

(x; Burnham and Anderson 2002). The simpler model was

chosen when nested models within 2 DAICc of each other

differed by only one parameter (Burnham and Anderson

2002, Arnold 2010). As another test of model fit and to

calculate the proportion of explained variation, we

calculated marginal r2 and conditional r2 (MuMIn;



Nakagawa and Schielzeth 2013, Barton 2015). These

pseudo-r2 values describe, respectively, the proportion of

variance explained by the fixed factors alone and the

proportion explained by both the fixed and random

factors. We calculated these pseudo-r2 values for one

cumulative model per incubation behavior (i.e. we

identified the fixed factors within the top model set for

each behavior and created a model containing only those

factors plus the random structure). We assessed the

random factor (territory ID) in the mixed models by

calculating intraclass correlation 1 and 2 (ICC1 and ICC2).

This is done by running a null model containing only the

random structure. These measures indicate, respectively,

how much variance in the outcome can be explained by

the random factor and how reliably levels within the

random factor can be differentiated by the response

variable (Zuur et al. 2009), and they are bound by 0 and

1; ICC2 values .0.7 are considered highly reliable (Kensler

et al. 2009).

Clutch viability modeling. We used cumulative link

mixed models (CLMM; Christensen 2015) and an

information-theoretic approach to assess whether incuba-

tion behavior affected clutch fate (0, 1, or 2 eggs hatched).

In this set of models, we investigated each incubation

behavior, as well as (1) the 2-way interaction between the

behavior and each fixed factor found to be important in

the incubation mixed models described above; and (2) the

3-way interaction between the behavior, each important

fixed factor, and social group type. Territory ID was

included as a random factor. Finally, we used ordered

logistic regression (Venables and Ripley 2013) to deter-

mine whether clutch fate varied seasonally by social group

type.

Weather MonitoringWe used several data sources for weather conditions. We

collected ambient temperature data by placing iButtons at

the edge of abandoned White-breasted Thrasher nests;

temperature was recorded every 2 min. For the days that

we did not have ambient temperature data (6 of 80), we

used hourly temperature data collected at Hewanorra

International Airport, located ~17 km southeast of our

study site (data from Weather Underground, http://www.

wunderground.com). As with the experimental data

(described below), we used only ambient temperatures

from 0500 to 2100 hours. We used all dates (n¼ 80) from

our sample period to test the correlation between ambient

temperature at the 2 sites. Values collected at the airport

were consistently higher than those collected by the

iButtons, but the relationship was nonlinear. Using

curve-fitting software (CurveExpert Basic 2.1.0; Hyams

Development, https://www.curveexpert.net/), we found

that a sinusoidal function best fit the data and applied

the regression equation to the airport data to adjust for the

temperature difference. Rainfall data were collected at the

Patience weather station, ~3 km southeast of our study

site and at a similar elevation and distance to the coast.

RESULTS

Our incubation behavior data came from 47 White-

breasted Thrasher clutches. Of the 47 clutches, 25 fully

hatched, 10 experienced partial clutch loss due to egg

inviability, and 12 failed. Fifty-eight percent of clutch

failures were due to depredation (n¼ 7) and 42% were due

to egg inviability (n ¼ 5). Overall hatching rate was 64 6

43%. Hatching rates were similar between social group

types (pair: 71 6 39%, n ¼ 24 clutches; cooperative: 68 6

41%, n ¼ 19 clutches), as was the cause of clutch failure

(pair: depredation¼ 25%, inviability¼ 75%, n¼ 4 clutches;

cooperative: depredation ¼ 50%, inviability ¼ 50%, n ¼ 4

clutches). The 4 clutches of unknown social group type

failed as a result of depredation, and all 7 depredatedclutches were excluded from subsequent analysis. Also

excluded was a suspected joint-nesting group with a rare

4-egg clutch, leaving a sample of 39 White-breasted

Thrasher clutches meeting our criteria (n ¼ 23 pair, n ¼16 cooperative) that were monitored over 74 days (n¼ 12

clutches over 26 days in 2012; n¼ 27 clutches over 48 days

in 2013).

We found that White-breasted Thrashers typically

incubate eggs constantly throughout the night, so here

we analyzed daytime (‘‘active’’) data only (i.e. 0500–2100

hours). To prevent possible biases by lack of coverage for

some nests in our sample (mean monitoring time per nest-

day ¼ 14.5 6 3.5 hr, range: 2.5–16 hr), we assessed

differences in coverage by social group type. The group

types were monitored for the same amount of time per day

(t259¼�0.4, P¼0.7). They both had low temporal variation

in off-bout duration (Appendix Figure 6), with a flattened

to bimodal pattern in timing of off-bouts that may have

been related to ambient temperature peaking mid-day

(Appendix Figure 7). Because the group types were similar,

we retained all data regardless of coverage. Within the 39-

clutch sample, iButtons were installed for a total of 4,055

active clutch-hours (104 6 43 hr clutch�1, range: 32–176)

over 279 clutch-days (7 6 3 days per clutch, range: 2–12)

and recorded 6,027 off-bouts (154.5 6 68 off-bouts

clutch�1, range: 39–285).

Incubation Behavior ModelingIncubation constancy (the proportion of time between

0500 and 2100 hours spent in contact with the egg) ranged

from 41% to 80% clutch�1. Relatively short (,17 min),

infrequent (,1.5 hr�1) off-bouts resulted in the highest

constancy values, with similar variation across clutches in

off-bout duration (CV¼ 22%) and off-bout frequency (CV

¼ 27%; Appendix Figure 8). High-constancy-pair clutches



http://www.wunderground.com

http://www.wunderground.com

https://www.curveexpert.net/

tended to exhibit infrequent off-bouts of longer duration,

whereas the cooperative clutches with high constancy

values tended to show the opposite strategy of more

frequent off-bouts of shorter duration. However, there was

little difference in mean values between pair and

cooperative groups for any of the incubation parameters

examined (Appendix Table 2). When controlling for day (n

¼ 43 days of paired data), there were more days on which

pairs had longer and more variable off-bouts, and

consequently lower incubation constancy, than coopera-

tive groups (Figure 1), though only the difference in mean

off-bout duration was significant (incubation constancy:

t42¼ 1.5, P¼ 0.08, d¼ 1.99; off-bout frequency: t42¼�0.3,P¼ 0.3, d¼�0.02; mean off-bout duration: t42¼�1.8, P¼0.04, d¼�0.9; variation in off-bout duration: t42¼�0.9, P¼0.2, d ¼�0.3).

Our preliminary set of mixed models assessed the effects

of clutch-related variables (i.e. clutch age and size) on

incubation behavior. For all behaviors, the clutch-related

predictors failed to increase explanatory power over the

null model (Appendix Table 3) and therefore were not

included in the next step of analysis.

The second mixed model set, which considered social

group type and temporal and weather-related variables,

showed small effects of group type on some of the

incubation behaviors (Table 1 and Appendix Table 4). The

top incubation constancy model included the interaction

between social group type and maximum temperature.

Incubation constancy declined as maximum daily temper-

ature increased in cooperative groups, whereas the reverse

was seen for breeding pairs (Figure 2A). On average, pairs

had 3.1% lower incubation constancy on cool days (268C)

and 11% higher incubation constancy on days when

temperature spiked (368C), with the trend lines crossing

at 28.58C. Social group type was also an informative

parameter for off-bout frequency. The top model in this set

included the interaction between social group type and day

of year, where off-bout frequency decreased in both group

types as the season progressed, but at a faster rate in

cooperative groups (Figure 2B). However, this model was

only marginally better supported than the null model.

Social group type was not included in any of the

competitive models for the off-bout duration parameters

(Appendix Table 4). The interaction between the 2

FIGURE 1. Differences in White-breasted Thrasher incubation behavior during the 2012 and 2013 breeding seasons in our studypopulation in Saint Lucia between social group types by date (n¼ 43 days of paired data). The zero line represents no differencebetween the group types. Points above the zero line indicate higher values for cooperative breeders, whereas points below the lineindicate higher values for pairs. In each plot, the x-axis has been reordered in descending order, based on y-axis values. Data wereback transformed for ease of viewing.



environmental variables was among the top set for off-

bout frequency but was less supported than the null

model. Here, off-bout frequency was predicted to be high

under moderately rainy, cold conditions, and low when

conditions were either dry or very wet and cold.

Unlike social group type, year was informative across all

incubation behaviors (Table 1). Year was the sole top model

for 2 of the 4 behaviors (mean and variation in off-bout

duration) and the second to top model for the other 2

(incubation constancy and off-bout frequency), though

interannual differences were small. Incubation constancy

was higher in 2012 than in 2013 (d¼2.5%), which was driven

by both shorter (d ¼ 0.8 min) and less frequent (d ¼ 0.07

hr�1) off-bouts. Off-bout duration was also less variable in

2012 than in 2013 (d ¼ 1.8 min). No other variables were

important across all the behaviors. Because the 2 study years

differed in several possibly important ways—days in the 2012

sample were warmer (i.e. higher maximum temperatures;

2012: 30.2 6 3.78C; 2013: 28.0 6 1.68C), drier (2012: 3.4 6

6.4 mm rain; 2013: 6.5 6 10.7 mm rain), and sampled later in

TABLE 1. Summary of competing models of effects of temporal, environmental, and social group type (group) on White-breastedThrasher incubation behavior during the 2012 and 2013 breeding seasons in our study population in Saint Lucia. Criterion forcomparing models within each set include K (number of estimated parameters), DAICc, and x (AICc weight). Only the top model andthose within 2 DAICc for each behavior are shown.

Year Response variable Models K DAICc x

2012–2013 Incubation constancy a Max. temperature 3 group 6 0 0.25Year 4 0.84 0.17Day of year 4 1.20 0.14Null 3 1.76 0.10

Off-bout frequency a Day of year 3 group 6 0 0.19Year 4 0.41 0.16Null 3 0.44 0.15Mean temperature 3 rain 6 1.41 0.09

Mean off-bout duration a Year 4 0 0.67Variation in off-bout duration a Year 4 0 0.8

2012 Incubation constancy Rainfall 4 0 0.41Rainfall 3 group 6 1.59 0.19

Off-bout frequency Rainfall 4 0 0.40Null 3 1.83 0.16

Mean off-bout duration Null 3 0 0.28Rainfall 4 1.34 0.14Min. temperature 4 1.19 0.15Max. temperature 4 1.81 0.11Day of year 4 1.99 0.10

Variation in off-bout duration Null 3 0 0.19Rainfall 3 group 6 0.54 0.15Max. temperature 4 0.94 0.12Max. temperature 3 group 6 1.06 0.11Min. temperature 4 1.31 0.10Rainfall 4 1.67 0.08

2013 Incubation constancy Null 3 0 0.24Day of year 4 0.57 0.18Max. temperature 4 1.28 0.13Min. temperature 4 1.30 0.13

Off-bout frequency Day of year 4 0 0.41Mean off-bout duration Day of year 4 0 0.29

Null 3 1.13 0.16Mean temperature 3 rain 6 1.71 0.12

Variation in off-bout duration Day of year 4 0 0.38Min. temperature 4 1.46 0.18

2012–2013 Off-bout duration b Temperature 4 0 0.52Temperature 3 group 6 0.19 0.48

2012 Off-bout duration Temperature 4 0 0.812013 Off-bout duration Temperature 4 0 0.81

a Variable calculated from daily averages of each monitored clutch (n¼ 67 clutch-days at 12 clutches in 2012; n¼ 212 clutch-days at27 clutches in 2013).

b Variable calculated from every off-bout taken throughout incubation (n¼1,255 off-bouts at 12 clutches in 2012; n¼4,061 off-boutsat 27 clutches in 2013).



the breeding season (2012: June 27–August 4; 2013: June 4–

July 29)—we also ran model sets for each year separately.

Rainfall was important in 2012 (Table 1 and Appendix

Table 4). It was the top model for incubation constancy

(Figure 3A) and off-bout frequency (Figure 3B), and in the

top model set for the other 2 behaviors. Despite the strong

support, its effect was small; rainless days in 2012 saw 0.07

fewer off-bouts per hour and 1.8% lower constancy, on

average, compared to rainy (22 mm) days. There was also

some support for the interaction of rainfall and social

group type on incubation constancy and variation in off-

bout duration; rainfall had no effect on behavior of pairs,

whereas increasing rainfall was associated with increased

incubation constancy (Figure 3A) and decreased variation

in off-bout duration for cooperative groups. On rainy days,

this resulted in 8% higher incubation constancy and 3.6

min lower variation in off-bout duration for cooperative

groups on average. Rainfall was not as important in 2013

(Table 1 and Appendix Table 4). Its only occurrence was in

an interaction with temperature, where cold and low-

FIGURE 2. Relationship between social group type and extrinsic factors—(A) maximum daily temperature and (B) day of year—onWhite-breasted Thrasher incubation behavior during the 2012 and 2013 breeding seasons in our study population in Saint Lucia.Each point represents a clutch-day (n ¼ 156 cooperative, n ¼ 123 pair). Regression lines are shown with their corresponding 95%confidence bands. Data were back transformed for ease of viewing.

FIGURE 3. Effects of (A, B) rainfall and (C–E) day of year on White-breasted Thrasher incubation behavior by year in our studypopulation in Saint Lucia. Each point represents a clutch-day (n¼ 67 in 2012, n¼ 212 in 2013). Regression lines are shown with theircorresponding 95% confidence bands. Data were back transformed for ease of viewing.



precipitation to moderately rainy conditions resulted in

longer off-bouts, but it was less supported than the null

model.

The most influential parameter in 2013 was day of year,

which was the top model for all behaviors except

incubation constancy, where the null model was the best

supported for the latter behavior. Off-bouts were less

frequent (d ¼ 0.6 hr�1; Figure 3D) but longer (d ¼ 5 min;

Figure 3E) at the end of the 2013 breeding season than at

the beginning, resulting in little change to incubation

constancy as the season progressed (Figure 3C). In

contrast to rainfall and day of year, the temperature-

related variables received little support in either of the

annual model sets (Table 1 and Appendix Table 4).

Temperature was important, however, when considered

on a much finer scale (i.e. at the exact time of the off-bout;

Table 1). Longer off-bouts became more frequent as

temperature increased, though short off-bouts still oc-

curred across all recorded ambient temperatures. This

relationship held to ~308C, above which off-bout duration

was relatively short regardless of ambient temperature

(Figure 4).

The proportion of variance explained by the informative

fixed factors was fairly low for each of the incubation

behaviors (1.8–7.7%), though modeling the years separate-

ly generally improved explanatory power (marginal r2

values; Appendix Table 5). These low marginal r2 values

are partially a consequence of high inter-clutch variation

across the incubation behaviors. For example, incubation

constancy ranged from 41% to 80% per clutch-day and

from 53% to 75% overall per clutch (Appendix Figure 9).

Accordingly, in contrast to the fixed factors, the high ICC1

(23–51%) and ICC2 values (72–90%) showed the impor-

tance of territory (i.e. the random effect) in explaining

variance in the outcome of the incubation models.

Clutch Viability ModelingWhite-breasted Thrasher clutch fate (0, 1, or 2 eggs

hatched) was influenced by incubation behavior. The top

clutch-fate model included the interaction between

incubation constancy, day of year, and social group type

and contained 68% of the weight in the data. This model

was 2.33more likely than the second, similar, top model,

which was the interaction between off-bout frequency,

day of year, and social group type (DAICc¼ 1.7, x¼ 0.3).

No other models came within 2 AICc (Appendix Table 6),

which suggests that differences in incubation constancy

were driven by changes in off-bout frequency rather than

off-bout duration. Incubation constancy began high and

then declined as the season progressed for the failed

clutches, whereas the opposite pattern occurred in the

successful ones (i.e. 1 or 2 eggs hatched; Figure 5).

Despite high early-season constancy values for the

ultimately failed attempts, temperature data suggested

FIGURE 4. Effect of ambient temperature on White-breasted Thrasher off-bout duration in our study population in Saint Luciaduring the 2012 and 2013 breeding seasons. Inset figure shows enlargement of values in the off-bout duration range of 5–20 min.Each point represents an off-bout (n¼5,316). Regression lines are shown with their corresponding 95% confidence bands. Data wereback transformed for ease of viewing.



that these clutches were warmed to lower temperatures

than successful clutches (Appendix Figure 10). Incuba-

tion constancy patterns in successful clutches differed

slightly by social group type; cooperative clutches

experienced lower constancy values earlier in the season

and higher values later in the season compared to pairs

(Figure 5).

Given that (1) fewer off-bouts late in the season was

associated with clutch success and (2) off-bout frequency

was lower for cooperative breeders at the end of the

season, we would expect cooperative breeders to have

higher hatching success in late-season clutches than pairs,

and the reverse for early-season clutches. This pattern was

observed if we regressed social group type and estimated

date of clutch initiation against hatching success (Appen-

dix Figure 11), though the interaction between date and

social group type was only marginally significant (ordinal

regression, t ¼�1.9, P ¼ 0.06, n ¼ 35 clutches).

DISCUSSION

Avian systems have been at the core of research on

cooperative breeding (Koenig and Dickinson 2016).

However, much of the work in the field has come from

the study of temperate species and helper effects on the

nestling and postfledging stages of the nesting cycle.

Consequently, our goals with this work were to document

incubation behavior in a cooperative Neotropical songbird

and test hypotheses about the potential benefits of

cooperative breeding during incubation in that system.

We found that like many songbirds that sleep on the nest

after clutch completion (Ricklefs et al. 2017), White-

breasted Thrashers incubate constantly through the night.

Across both pair and cooperative groups, the species

spends, on average, 65% of active hours (0500–2100) on

the nest; the afternoon period, the warmest part of the day,

is the lowest point of nest attendance in the daily cycle.

Nest attendance in this system is somewhat lower than the

average for some other single-incubating cooperative

breeders (74.4 6 12.9%, n ¼ 13 species; Skutch 1962,

Long and Heath 1994, Conway and Martin 2000b,

Eisermann et al. 2011), but not very different from those

cooperative species restricted to the Neotropics (69.2 6

9.2%, n ¼ 6 species; Skutch 1962, Long and Heath 1994,

Conway and Martin 2000b, Eisermann et al. 2011). Taken

together, our modeling results suggest a weak relationship

between incubation behavior, group size, and hatching

success that is mediated by timing of nesting within the

breeding season.

Differences in incubation behavior between social group

types were subtle and context dependent. Controlling for

day, we saw our predicted pattern of cooperative clutches

experiencing more days with shorter and less variable off-

bouts, and consequently higher incubation constancy, than

pair clutches. Small differences in incubation time and

patterns, ultimately driven by clutch temperature, can

FIGURE 5. Relationship between White-breasted Thrasher incubation constancy, day of year, social group type, and clutch fateduring the 2012 and 2013 breeding seasons in our study population in Saint Lucia. Each point represents a clutch-day (100% pair, n¼ 92; 50% pair, n¼ 43; 0% pair, n¼ 21; 100% cooperative, n¼ 71; 50% cooperative, n¼ 32; 0% cooperative, n¼ 20). Regression linesare shown with their corresponding 95% confidence bands.



affect a suite of traits, including embryo development rate

and viability and offspring phenotype (Deeming and

Ferguson 1991, Martin et al. 2007, DuRant et al. 2013,

Ben-Ezra and Burness 2017). Consequently, although

small, our observed differences between group types could

become meaningful when considered over the duration of

embryonic development. For instance, the 2% increase in

incubation constancy for cooperative groups translates to

an additional ~20 min of incubation per day, and 4 hr over

the course of the egg stage.

Similarly, our mixed models that explicitly considered

the weather-related and temporal variables in addition to

social structure showed small effects of cooperation on

some of the incubation behaviors. For instance, maximum

ambient temperature and social group type affected

incubation constancy, whereby constancy increased for

pairs on hotter days but decreased for cooperative groups.

The behavior of cooperative groups in our study was

consistent with previous work showing a negative rela-

tionship between nest attendance and ambient tempera-

ture (Conway and Martin 2000a, Londono et al. 2008,

Boulton et al. 2010, MacDonald et al. 2014, Walters et al.

2016). This is thought to indicate adults taking advantage

of warmer temperatures to expend more energy on self-

maintenance activities rather than incubation (Ardia et al.

2009). Our unexpected finding that pair breeders exhibited

the reverse pattern is probably due to a nonlinear

relationship between incubation constancy and tempera-

ture that was obscured by the granularity of the data

(Conway and Martin 2000a). When we used finer-scale

temperature data (i.e. ambient temperature at the exact

time the incubator left the nest), the social group types had

the same response—longer off-bouts became more com-

mon as ambient temperature increased through the 22–

298C range, becoming less common again at highertemperatures. This pattern is in accordance with the idea

that in the tropics, incubation patterns are often consistent

with minimizing exposure to high rather than low ambient

temperatures, because high temperatures can cause

embryo death (Webb 1987). The altered behavior observed

in our study and in other avian systems at high

temperatures can be a response to the thermoregulation

needs of either the embryo or the incubator (Downs and

Ward 1997, Amat and Masero 2007). For example, King

Rails (Rallus elegans) take shorter incubation recesses in

hot conditions, with the additional time on the nest spent

shading rather than incubating. This transition from

heating to cooling behavior occurs at ~308C (Clauser

and McRae 2017), the value at which we also observed a

behavioral change. Our nest temperature data suggest that

short off-bouts at high ambient temperatures are also due

to birds remaining on the nest to cool the clutch or

themselves; nest temperatures at the start of an off-bout

were higher than ambient, except at the hottest ambient

temperatures, which showed the reverse pattern (Appen-

dix Figure 12). Minimizing exposure of developing

embryos to high temperatures, as opposed to incubators,

may be of little concern in the White-breasted Thrasher

system, as evidenced by our observations of (1) off-bout

duration being longest at midday, often the warmest part

of the day, and (2) ambient temperatures below those

lethal to developing embryos (38–398C for multiday and

40.58C for short-duration exposure; Webb 1987). Further-

more, because incubating White-breasted Thrashers

exhibited thermoregulatory behavior indicative of thermal

stress (e.g., panting) under high temperatures, we predict

that the primary function of high nest attendance by

White-breasted Thrashers in hot conditions is to regulate

their temperature rather than that of the clutch (Clauser

and McRae 2017).

Our study also demonstrated temporal variation in

incubation patterns. The strongest seasonal effect we

observed was on off-bout frequency, which declined

through the breeding season but, interestingly, more

quickly for cooperatively breeding groups. This result

suggests that breeding females in cooperative groups have

more flexibility than lone pairs in shifting between

incubation demands and maintenance behaviors. Our

annual models indicate that seasonal variation was an

important predictor in primarily 1 yr of the study only,

with off-bout frequency and duration responding in

opposite directions resulting in relatively invariant con-

stancy across time. Several factors, not evaluated here,

could be driving the general importance of day of year on

incubation behavior, as well as the differential response

between social group types seen in the combined years

model. Incubation behavior in other bird species is

influenced by prey availability (Pearse et al. 2004,

Zimmerling and Ankney 2005, Duncan Rastogi et al.2006, Londono et al. 2008, Amininasab et al. 2016) and

predation risk (Martin and Ghalambor 1999, Sasvari and

Hegyi 2000, Fontaine and Martin 2006, Martin et al. 2015),

both of which can vary seasonally. We predict that prey

availability is less important than predation risk in driving

the observed seasonal incubation patterns for the White-

breasted Thrasher because (1) lack of allofeeding suggests

that prey is not limited and (2) the social group types have

territories of similar quality, including prey abundance

(Temple 2005). Conversely, our data are consistent with an

analysis of North American songbirds (Conway and

Martin 2000b), where higher nest predation selects more

strongly for reduced activity at the nest rather than overall

nest attentiveness. While temporal variation in White-

breasted Thrasher predator abundance is not known,

predation is an important cause of reproductive failure for

the species; almost 40% of eggs fail to hatch, and the

majority of these failures are due to depredation (Temple

2005, Mortensen 2009, present study). Furthermore, social



group types could be differentially affected by predator

abundance. WhileWhite-breasted Thrasher helpers do not

visit the nest during incubation, they are not actively

excluded from the nest area (Temple 2005, J. L. Mortensen

personal observation). Consequently, a role for helpers in

buffering incubation may be via territory defense when

clutch predation risk is high. Helper presence late in the

breeding season may also allow breeding females to

increase investment in incubation rather than other

behaviors that affect fitness components, such as feeding

already fledged young. As in other cooperative systems

(Langen 2000), renesting in White-breasted Thrashers

occurs before fledgling independence, with helpers partic-

ipating in feeding these offspring (Temple 2005). However,

whether prey availability, predator abundance, helper

contributions, or a combination thereof drives temporal

dynamics of White-breasted Thrasher incubation behavior

remains to be assessed.

Our suite of predictors explained only a small amount of

variation in White-breasted Thrasher incubation behavior,

including only a subtle benefit of being in a cooperative

group, as shown by the low marginal r2 values for each

cumulative model (3–8%). The low explanatory power of

our models is likely due to a combination of factors. First,

we may have excluded variables important in isolation or

in interactions with our extant set of predictors. Possible

candidates influential in other systems (which lack of data

prevents us from addressing) include parental traits like

breeder age, experience or condition (e.g., Komdeur 1996,

Lv et al. 2016), and perceived predation risk (e.g., Martin et

al. 2015). Second, that climate conditions such as rainfall

were not as important as we anticipated could be due to

the coarseness of the available data (i.e. conditions

preceding an off-bout should be more predictive of

incubation patterns than daily rainfall totals or tempera-ture averages). Finally, incubation behavior has been

generally challenging to explain and predict within bird

species (Skutch 1962, Conway and Martin 2000a, Ardia et

al. 2009, Coe et al. 2015). This difficulty in many systems,

including ours, is due in part to high variation in

incubation patterns between individual birds. In our study,

clutch identification explained �22% of the variation in

each of the incubation parameters (i.e. ICC1), and

conditional r2 values were upward of 28%. Skutch

(1962:136) wrote of incubation constancy that ‘‘there

remain inexplicable vagaries which we can attribute only

to that mysterious factor in bird behavior which for want

of a better term we call ‘temperament.’ Some birds are

stolid and restful, others mercurial and restless.’’ Our data

add to accumulating evidence that, in conjunction with

temporal, parental, and weather-, clutch-, and habitat-

related variables, inherent differences between individuals

are important in understanding intraspecific variation in

avian incubation.

Other studies of incubation of pair-breeding cooperative

species also report a lack of a straightforward relationship

between incubation and cooperation. Presence or number

of helpers at Laughing Kookaburra (Dacelo novaeguineae)

nests had no effect on incubation constancy (Legge 2000).

Additionally, in the cooperatively breeding species Green

Woodhoopoe (Phoeniculus purpureus; Radford 2004) and

Karoo Scrub-Robin (Erythropygia coryphaeus; Lloyd et al.

2009), higher allofeeding rates of the incubating female

were correlated with higher incubation constancy over the

short term, but provisioning was not related to group size.

By contrast, several studies of incubation in cooperative

breeding systems with joint nesting (i.e. when .1 female

lays in the same nest) reported relationships between

incubation behavior and cooperation. For example, Taiwan

Yuhina (Yuhina brunneiceps) groups with 3 sets of

breeders had significantly higher incubation constancy

than groups with a single set of breeders (Yuan et al. 2005).

Similarly, Seychelles Warbler (Acrocephalus sechellensis)

nests with more incubating females had higher incubation

constancy but also had higher egg loss, thought to be due

to females jockeying for position on top of the clutch

(Komdeur 1994). Interestingly, the highest incubation-

constancy values for the White-breasted Thrasher in our

study (84–90%) were recorded at a nest that we suspect

was a case of joint nesting, which is not common in our

system (Temple 2005, Mortensen 2009). This nest

contained a rare 4-egg clutch and was one of the few

nests at which 2 individuals were observed incubating

simultaneously. All together, these results suggest thatincubation behavior may be affected by group size in

cooperatively breeding birds, but predominantly in joint-

laying systems, where it is increased via incubation by

multiple individuals.

Consistent with previous work showing that incubationbehavior has strong effects on fitness (Deeming 2002a,

Zangmeister et al. 2009, Ben-Ezra and Burness 2017), we

found that the behavior of birds with failed clutches

differed from those with successful ones. Specifically, our

data show that early-season successful clutches experi-

enced lower nest attendance than late-season ones,

whereas the reverse pattern was observed for failed

clutches. Surprisingly, the early-season failed clutches

had higher incubation constancy than the successful ones,

despite the temperature data suggesting that failed

clutches were not being warmed to the same high

temperatures as were the successes. We do not know

why these failed breeders had high-quantity and low-

quality incubation, but failure to warm the eggs could be

due to behavioral or physiological factors (Turner 2002).

Social structure also influenced hatching success; for

successful clutches, cooperative groups had higher con-

stancy later in the season than pairs. While our data

suggest that higher nest attendance by cooperative groups



late in the season is associated with higher hatching

success, additional data are needed to test the prediction

that social structure and temporal incubation patterns

interact to influence fitness.

To our knowledge, this is the first attempt to evaluate

the potential for differential incubation constancy in

cooperative breeders to affect reproductive success. Our

results suggest that cooperative breeding in this and other

avian species may relax trade-offs between incubation, self-

maintenance, and other duties, with downstream effects on

fitness. The differences between White-breasted Thrasher

social group types were more subtle than expected;

incubation behavior was influenced by a complex set of

factors and underlain by tremendous individual variation.

Ultimately, it is not clear what benefits, if any, helpers have

in the White-breasted Thrasher system, but a strong effect

on incubation constancy does not appear to be one of

them.

ACKNOWLEDGMENTS

We are grateful to the Saint Lucia Department of Forest and

Land Resources Development (Ministry of Agriculture,

Natural Resources, and Co-operatives) for research permis-

sions and logistical support, and to the Saint Lucia WaterResource Management Agency (Ministry of Agriculture,

Natural Resources, and Co-operatives) for access to rainfall

data. Our thanks to naturalist S. Lesmond; field technicians G.

Kramer, T. Mink, and M. Philgence; and lab technicians B.

Barnes and T. Mink. Thanks also to the Romero Lab Group at

Tufts University for lending equipment, to K. Quinn for

MATLAB scripts, and to H. Mills and C. Cooper for providing

Rhythm software.

Funding statement: This research was supported by the

American Ornithologists’ Union, Tufts Institute of the

Environment, and a P.E.O. Scholar Award to J.L.M. The

funders had no input into the content of the manuscript, nordid they require approval of the manuscript before submission

or publication.

Ethics statement: All capture and handling procedures wereapproved by the Tufts University Institutional Animal Care

and Guidelines to the Use of Wild Birds in Research (http://

naturalhistory.si.edu/BIRDNET/guide/), and conducted with

the requisite Government of Saint Lucia permits.

Author contributions: J.L.M. and J.M.R. conceived the idea,

design, and experiment and wrote the paper. J.L.M. performed

the experiments and analyzed the data.

Data deposits: Data are deposited with Dryad and can be

accessed at https://datadryad.org.

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APPENDIX

APPENDIX FIGURE 6. No strong pattern was seen between off-bout duration and time of day in either White-breasted Thrashersocial group type (pair: circles, solid line, n¼3,361 off-bouts; cooperative: triangles, dashed line, n¼ 2,666 off-bouts) during the 2012and 2013 breeding seasons in our study population in Saint Lucia. Loess trend lines for the social group types are shown with theircorresponding 95% confidence bands.

APPENDIX FIGURE 7. White-breasted Thrasher off-bouts (gray line ¼ cooperative, black line ¼ pair; n ¼ 6,027 off-bouts over 279clutch-days) occurred throughout the day during the 2012 and 2013 breeding seasons in our study population in Saint Lucia. Off-bouts peaked in the morning and early evening, coinciding with lower ambient temperatures (n¼ 79,604 temperature recordingscollected during June–August 2012 and June–July 2013).



APPENDIX FIGURE 8. Relationship between social group typeand White-breasted Thrasher incubation behavior during the2012 and 2013 breeding seasons in our study population inSaint Lucia. Each circle represents a clutch (n ¼ 39 clutches,including 23 pair and 16 cooperative clutches), and fill shadecorresponds to incubation constancy value.

APPENDIX FIGURE 9. High intra- and inter-clutch variation in incubation constancy (proportion of 0500–2100 hours spentincubating) across White-breasted Thrasher social group types during the 2012 and 2013 breeding seasons in our study populationin Saint Lucia. Each point represents a clutch (n¼ 23 pair, n¼ 17 cooperative). Pairs are represented by white bars and cooperativegroups by gray bars. Values above the x-axis correspond to the number of days each clutch was montiored. The clutch shown herewith the highest incubation constancy values was excluded from all analyses. In each box plot, the horizontal bar is the median,boxes correspond to the first and third quartiles, and whiskers extend to the highest value within 1.5*interquartile range; databeyond the whiskers are plotted as points.



APPENDIX FIGURE 10. Effect of nest temperature and day of year on White-breasted Thrasher hatching success during the 2012and 2013 breeding seasons in our study population in Saint Lucia. Nest temperature at the start of an off-bout corresponds to theincubator departing the nest. Each point represents a clutch-day (0 eggs hatched, n¼ 41; 1 egg hatched, n¼ 75; 2 eggs hatched, n¼163).



APPENDIX FIGURE 11. Predicted probability curves for the effect of clutch initiation date on hatching success by White-breastedThrasher social group type (n ¼ 20 pair clutches, n ¼ 15 cooperative clutches) during the 2012 and 2013 breeding seasons in ourstudy population in Saint Lucia.



APPENDIX FIGURE 12. Relationship between maximum ambi-ent temperature and White-breasted Thrasher nest temperatureduring the 2012 and 2013 breeding seasons in our studypopulation in Saint Lucia. Nest temperature at the start of an off-bout corresponds to the incubator departing the nest. Eachpoint represents a clutch-day (n ¼ 279). Points above the 1:1horizontal indicate higher values for mean nest temperaturethat day, whereas points below the line indicate higher valuesfor ambient temperature that day.

APPENDIX TABLE 2. Components of White-breasted Thrasher incubation behavior by social group type during the 2012 and 2013breeding seasons in our study population in Saint Lucia (n¼ 156 clutch-days at 23 pair clutches, 123 clutch-days at 16 cooperativeclutches). Values are means 6 SD, followed parenthetically by range. Cohen’s d comparison is between means for pair andcooperative groups.

Incubation parameter Overall mean Pair Cooperative Effect size

Incubation constancy (%) 64.4 6 7.4 (40.7–80.2) 64.4 6 7.5 (48.2–80.2) 64.6 6 7.4 (40.7–77.9) 0.01Off-bout frequency (n hr�1) 1.5 6 0.4 (0.8–3.4) 1.5 6 0.4 (0.8–3.4) 1.5 6 0.3 (0.8–2.6) 0Mean off-bout duration (min) 14.7 6 3.3 (7.9–27.6) 14.8 6 3.5 (7.9–27.6) 14.6 6 3.1 (8.6–23.9) �0.06Variation in off-bout duration (min) 8.4 6 3.7 (1.5–22.1) 8.2 6 3.4 (1.5–22.1) 8.7 6 4.1 (2.4–20.2) 0.13



APPENDIX TABLE 3. Base model sets for effects of clutch characteristics on White-breasted Thrasher incubation behavior during the2012 and 2013 breeding seasons in our study population in Saint Lucia (n¼ 58 clutch-days at 11 clutches in 2012; n¼ 192 clutch-days at 24 clutches in 2013). Criteria for comparing models within each set include K (number of estimated parameters), DAICc, andx (AICc weight). Values for the top model and those within 2 DAICc are in bold. All clutches in 2012 contained 2 eggs.

Year Model

Incubation constancy Off-bout frequency Mean off-bout duration Variation in off-bout duration

K DAICc x K DAICc x K DAICc x K DAICc x

2012–2013

Null 3 0 0.5 3 0 0.6 3 0 0.49 3 0 0.66

Clutch age 4 0.28 0.43 4 1.77 0.25 4 0.97 0.30 4 1.91 0.25Clutch size 6 5.28 0.04 6 3.49 0.11 6 2.71 0.13 6 4.60 0.07Clutch sizeþ age

7 5.61 0.03 7 5.40 0.04 7 3.47 0.09 7 6.54 0.02

2012 Null 3 0.07 0.49 3 0 0.73 3 0 0.63 3 0 0.70Clutch age 4 0 0.51 4 2.00 0.27 4 1.07 0.37 4 1.74 0.30

2013 Null 3 0.74 0.39 3 0 0.57 3 0 0.52 3 0 0.69Clutch age 4 0 0.56 4 1.31 0.3 4 1.01 0.32 4 2.08 0.24Clutch size 6 6.52 0.02 6 3.77 0.09 6 3.39 0.10 6 5.34 0.05Clutch sizeþ age

7 5.73 0.03 7 5.27 0.04 7 4.14 0.07 7 7.49 0.02

APPENDIX TABLE 4. Competing models for effects of temporal, environmental, and social group type (group) on White-breastedThrasher incubation behavior during the 2012 and 2013 breeding seasons in our study population in Saint Lucia. Criteria forcomparing models within each set include K (number of estimated parameters), DAICc, and x (AICc weight). Values for the top modeland those within 2 DAICc are in bold.

Year Model

Incubationconstancy a

Off-boutfrequency a

Mean off-boutduration a,b

Variation inoff-bout duration a


2012–2013 Max. temperature 3Group

6 0 0.25 6 5 0.02 6 7.71 0.01 6 8.29 0.01

Year 4 0.84 0.17 4 0.41 0.16 4 0 0.67 4 0 0.80Day of year 4 1.20 0.14 4 2.46 0.06 4 7.44 0.02 4 12.77 0Null 3 1.76 0.10 3 0.44 0.15 3 6.13 0.03 3 12.82 0Group 4 2.63 0.07 4 2.38 0.06 4 5.92 0.03 4 12.88 0Min. temperature 4 2.84 0.06 4 2.05 0.07 4 8.13 0.01 4 6.91 0.03Max. temperature 4 3.61 0.04 4 2.41 0.06 4 8.08 0.01 4 8.63 0.01Day of year 3 group 6 3.66 0.04 6 0 0.19 7.97 0.01 6 14.62 0Rainfall 4 3.81 0.04 4 2.10 0.07 4 7.60 0.02 4 14.82 0Mean temperature 3

rain6 4.17 0.03 6 1.41 0.09 6 7.10 0.02 6 11.13 0

Year 3 group 6 4.39 0.03 6 3.67 0.03 6 3.31 0.13 6 3.50 0.14Min. temperature 3

Group6 6.08 0.01 6 5.92 0.01 6 9.99 0 6 9.21 0.01

Rainfall 3 group 6.79 0.01 6 5.35 0.01 6 8.65 0.01 6 17.00 0Mean temperature 3

rain þ meantemperature 3 group

8 7.12 0.01 8 5.39 0.01 8 8.66 0.01 8 13.92 0

Mean temperature 3rain þ rain 3 group

8 7.54 0.01 8 4.82 0.02 8 8.63 0.01 8 13.94 0

2012 Rainfall 4 0 0.41 4 0 0.40 4 1.34 0.14 4 1.67 0.08Rainfall 3 group 6 1.59 0.19 6 3.71 0.06 6 4.51 0.03 6 0.54 0.15Null 3 2.84 0.10 3 1.83 0.16 3 0 0.28 3 0 0.19Max. temperature 3

group6 4.05 0.05 6 3.77 0.06 6 5.86 0.01 6 1.06 0.11

Day of year 4 4.25 0.05 4 3.63 0.06 4 1.99 0.10 4 2.25 0.06Min. temperature 4 4.42 0.05 4 4.04 0.05 4 1.19 0.15 4 1.31 0.10Mean temperature 3

rain6 4.57 0.04 6 3.84 0.06 6 5.06 0.02 6 3.22 0.04

Group 4 5.07 0.03 4 4.09 0.05 4 2.26 0.09 4 2.22 0.06



APPENDIX TABLE 4. Continued.

Year Model

Incubationconstancy

Off-boutfrequency

Mean off-boutduration

Variation inoff-bout duration


Max. temperature 4 5.07 0.03 4 3.67 0.06 4 1.81 0.11 4 0.94 0.12Mean temperature 3

rain þ rain 3 group8 5.87 0.02 8 7.78 0.01 8 8.06 0 8 2.54 0.05

Day of year 3 group 6 7.11 0.01 6 8.35 0.01 6 4.53 0.03 6 5.25 0.01Min. temperature 3

Group6 8.52 0.01 6 7.47 0.01 6 5.87 0.01 6 5.52 0.01

Mean temperature 3rain þ meantemperature 3 group

8 9.59 0 8 8.88 0 8 10.01 0 8 8.12 0

2013 Null 3 0 0.24 3 2.71 0.11 3 1.13 0.16 3 2.19 0.13Day of year 4 0.57 0.18 4 0 0.41 4 0 0.29 4 0 0.38Min. temperature 4 1.28 0.13 4 3.48 0.07 4 3.12 0.06 4 1.46 0.18Max. temperature 4 1.30 0.13 4 4.78 0.04 4 2.66 0.08 4 4.06 0.05Rainfall 4 2.07 0.09 4 4.61 0.04 4 2.95 0.07 4 4.25 0.05Group 4 2.08 0.09 4 4.41 0.05 4 2.86 0.07 4 4.13 0.05Day of year 3 group 6 3.28 0.05 6 3.15 0.09 6 2.88 0.07 6 3.19 0.08Mean temperature 3

rain6 3.51 0.04 6 2.36 0.13 6 1.71 0.12 6 5.38 0.03

Max. temperature 3group

6 4.69 0.02 6 8.61 0.01 6 5.79 0.02 6 8.03 0.01

Min. temperature 3group

6 5.36 0.02 6 6.47 0.02 6 6.65 0.01 6 4.67 0.04

Rainfall 3 group 6 5.92 0.01 6 8.28 0.01 6 5.36 0.02 6 8.08 0.01Mean temperature 3

rain þ meantemperature 3 group

8 7.25 0.01 8 6.08 0.02 8 5.46 0.02 8 9.56 0

Mean temperature 3rain þ rain 3 group

8 7.54 0.01 8 6.23 0.02 8 4.75 0.03 8 9.48 0

2012–2013 Temperature – – – – – – 4 0 0.52 – – –Temperature 3 group – – – – – – 6 0.19 0.48 – – –Time – – – – – – 4 61.52 0 – – –Time 3 group – – – – – – 6 61.87 0 – – –Null – – – – – – 3 66.59 0 – – –Group – – – – – – 4 66.59 0 – – –

2012 Temperature – – – – – – 4 0 0.81 – – –Temperature 3 group – – – – – – 6 3.03 0.18 – – –Time – – – – – – 4 11.89 0 – – –Time 3 group – – – – – – 6 15.52 0 – – –Null – – – – – – 3 10.30 0 – – –Group – – – – – – 4 12.20 0 – – –

2013 Temperature – – – – – – 4 0 0.81 – – –Temperature 3 group – – – – – – 6 2.90 0.19 – – –Time – – – – – – 4 49.58 0 – – –Time 3 group – – – – – – 6 49.06 0 – – –Null – – – – – – 3 58.47 0 – – –Group – – – – – – 4 59.34 0 – – –

a Variable calculated from daily averages of each monitored clutch (n¼ 67 clutch-days at 12 clutches in 2012; n¼ 212 clutch-days at27 clutches in 2013).

b Variable calculated from every off-bout taken throughout incubation (n¼ 1,255 off-bout at 12 clutches in 2012; n¼ 4,061 off-boutsat 27 clutches in 2013).



APPENDIX TABLE 5. Percentage of variation in each incubation behavior of White-breasted Thrasher during the 2012 and 2013breeding seasons, explained by informative fixed factors (DAICc , 2) and random structure, by breeding season in our studypopulation in Saint Lucia. Pseudo-r2 values refer to a model created to contain all fixed factors with DAICc , 2 in each respectiveincubation-behavior model. The marginal value (r2M) describes the proportion of variance explained by the fixed factors alone, andthe conditional value (r2C ) is the proportion explained by both the fixed and random factors. See Table 1 for the fixed factors in eachmodel. The random factor in each model was territory ID. ICC1 (intraclass correlation 1) and ICC2 (intraclass correlation 2) assess theimportance of the random effect (territory ID); they describe, respectively, how much variance in the outcome can be explained bythe random effect and how reliably levels within the random effect can be differentiated by the response variables.

YearMeasure of

variationIncubationconstancy

Off-boutfrequency

Mean off-boutduration

Variation inoff-bout duration

Off-boutduration

2012–2013 r2M 3.4 4.4 4.2 7.7 1.8

r2C 32.1 56.2 45.4 29.4 9.3

ICC1 30.2 50.8 38.4 22.8 5.9ICC2 79.0 90.0 84.5 72.0 91.2

2012 r2M 6.3 2.9 2.2 11.6 0.1

r2C 58.7 62.1 60.5 47.7 7.6

ICC1 51.5 52.2 61.9 40.1 7.7ICC2 85.6 85.9 90.0 78.9 89.7

2013 r2M 2.1 3.4 4.9 4.6 1.4

r2C 27.0 55.4 32.9 16.1 8.3

ICC1 26.9 55.1 36.0 19.4 5.9ICC2 75.7 91.2 82.6 67.1 91.1

APPENDIX TABLE 6. Competing models of effects of incubation behavior and its predictors on White-breasted Thrasher clutch fate(0, 1, or 2 eggs hatched) during the 2012 and 2013 breeding seasons in our study population in Saint Lucia (n¼279 clutch-days at 39clutches). Criteria for comparing models within each set include K (number of estimated parameters), DAICc, and x (AICc weight).Values for the top model and those within 2 DAICc are in bold. Abbreviations: IC¼ incubation constancy, OBF¼ off-bout frequency,MOBD ¼mean off-bout duration, VOBD ¼ variation in off-bout duration, group ¼ social group type.

Model K DAICc x

IC 3 day of year 3 group 10 0 0.68OBF 3 day of year 3 group 10 1.67 0.30MOBD 3 day of year 3 group 10 7.15 0.02VOBD 3 day of year 3 group 10 15.05 0IC 3 day of year 6 30.59 0OBF 3 day of year 6 30.98 0VOBD 3 day of year 6 34.71 0MOBD 3 day of year 6 38.34 0OBF 3 rainfall 3 mean temperature 3 group 18 93.85 0IC 3 year 6 95.80 0OBF 3 rainfall 3 group 10 97.13 0Null 3 97.83 0IC 4 98.40 0OBF 4 99.06 0MOBD 4 99.85 0VOBD 4 99.89 0MOBD 3 year 6 101.09 0IC 3 rainfall 6 102.44 0OBF 3 rainfall 6 102.77 0IC 3 rainfall 3 group 10 103.29 0MOBD 3 rainfall 10 103.62 0VOBD 3 rainfall 6 103.64 0VOBD 3 year 6 103.69 0OBF 3 year 6 103.78 0VOBD 3 rainfall 3 group 6 104.96 0MOBD 3 rainfall 3 group 10 109.17 0



cooperative breeder Parental incubation patterns …...Volume 135, 2018, pp. 669–692 DOI:...

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Transcript of cooperative breeder Parental incubation patterns …...Volume 135, 2018, pp. 669–692 DOI:...