DOI: 10.5061/dryad.r2280gbqg
title: Long-term insights into who benefits from brood reduction

description: The resource-tracking/facultative brood reduction hypothesis suggests
 that, under food stress, many altricial birds sacrifice the youngest brood
 members to enhance the growth and survival of their siblings. Studies
 examining staggered hatching and food shortage have generally supported
 this idea, although staggered hatching may serve additional purposes.
 However, the direct beneficiaries of this selective mortality remain
 unclear, as most research has overlooked parents and post-fledging
 outcomes. A life history perspective has rarely been applied to brood
 reduction. Using a 34-year individual-based dataset on blue-footed booby
 (Sula nebouxii) reproduction, we investigated whether siblicidal reduction
 of food-stressed two-chick broods benefits mothers, fathers, or surviving
 offspring. Results revealed that mothers of reduced broods were ~16% more
 likely to survive to the next breeding season than mothers of intact
 broods, indicating a significant maternal benefit. Moreover, cessation of
 sibling competition allowed surviving chicks to achieve fledging body
 condition, breeding probability, longevity, and lifetime reproductive
 success comparable to chicks from intact broods. Thus, sacrificing the
 subordinate chick ensures adequate—not privileged—growth of the surviving
 sibling and enhances maternal survival, while apparently providing no
 survival benefit to fathers. However, experimental confirmation is
 required to validate these findings and further explore the underlying
 mechanisms.
description: <em>Colony monitoring</em>
  Between 1989 and 2023, the contents of all booby nests in two
 study areas of Isla Isabel, off the Pacific coast of Mexico (21°50’59”N,
 105°52’54”W), were monitored every 3 days throughout the first three
 months of every five-month breeding season and every 6 days subsequently
 (details in Drummond et al., 1986, 2003). Hatchlings were labelled
 according to hatching order with coloured leg-wires, then numbered plastic
 bands, and at 70 days (a proxy of fledging, which can occur as early as 80
 days) they were weighed, measured (culmen and ulna), and fitted with
 alphanumeric steel bands. Sex of breeders was identified by voice (females
 grunt, males whistle) but sex of chicks was normally unknown until they
 recruited into the breeding population a few years after fledging. Due to
 limited natal dispersal in this population (30.5 ± 1.7 m in males and 36.6
 ± 1.4 m in females; 𝑥 ± 𝑠𝑒) and lifetime philopatry (Kim et al. 2007),
 this monitoring captured the development and fledging of every clutch and
 brood, along with the recruitment, annual survival and reproductive
 performance of offspring of all but the most recent cohorts across their
 life spans. <em>Benefits to parents
 </em> We evaluated whether parents that
 experienced brood reduction (one chick died) outperformed parents of the
 same sex that successfully fledged both chicks, in terms of survival,
 early laying, and breeding success in the subsequent year. Our sample was
 all reproductive events between 1993 and 2022 involving known-age parents
 (banded at fledging) with a brood of two hatched chicks. First, we
 compared the probability of surviving to the subsequent breeding season
 between parents that experienced brood reduction versus those that fledged
 both chicks. Death of a parent was inferred when an individual failed to
 breed in the study areas during five consecutive years, and ascribed to
 the last year it bred (only 2% of breeders take more than five gap years;
 Drummond et al., unpublished data). Second, for parents that survived, we
 compared laying dates and breeding success, measured as the number of
 fledglings produced, in the subsequent year between those that experienced
 brood reduction and those whose broods fledged intact.
 <em>Benefits to chicks</em> Using
 all two-chick broods that hatched between 1989 and 2023, we first compared
 the fledging body condition (next paragraph) of fledglings from two-chick
 broods hatched between 1995 and 2023, contrasting individuals of the same
 hatch order from reduced versus intact broods. We also compared fledglings
 from reduced versus intact two-chick broods that fledged between 1995 and
 2011 for recruitment success (whether they cared for a clutch within the
 first 12 years of life), longevity, and lifetime reproductive success
 (total fledglings produced). Recruitment after 12 years is rare (Drummond
 et al., 2011). In addition, for males and females that recruited and died
 between 1999 and 2017, we compared age at recruitment, longevity, and
 lifetime reproductive success of individuals of the same sex from intact
 versus reduced broods. Body condition at fledging was
 assessed using a scaled mass index, which adjusts body mass relative to
 body size, thereby accommodating fluctuations in the body mass-size
 relationship of each individual over its life span (equation 1; Peig and
 Green 2009). Senior fledglings from intact and reduced broods weighed 1665
 ± 238 grams and 1549 ± 243 grams, respectively, with ulna lengths of 205 ±
 11 mm and 205 ± 11 mm[HD1] , respectively. Junior
 fledglings from intact and reduced broods weighed 1614 ± 245 grams and
 1560 ± 236 grams, respectively, with ulnas measuring 204 ±11 mm and 203 ±
 11 mm, respectively. Equation 1. Scaled mass
 index  denotes the scaled mass
 index value,  is body mass (grams),
 <em>L<sub>0</sub> </em>is the population’s mean
 ulna length (mm),  is the individual ulna length, and
 <em>b</em> is the scaling exponent, estimated as the slope of
 the Standardized Major Axis (SMA) regression of the log-transformed body
 mass on ulna length. Brood reduction, whether by
 starvation or attacks by adult neighbours on chicks seeking adoption,
 respectively, was inferred when monitors found a chick older than 7 days
 dead on the parents’ territory, or absent from that territory and its
 surroundings. When both chicks died within nine days of each other (within
 3 consecutive nest checks), their deaths were attributed to nest
 abandonment. Disappearance of chicks younger than 7 days from the nest was
 attributed to predation by milk snakes (Lampropeltis polyzona), the only
 local predator of chicks (Ortega et al. 2021). Only chicks younger than 7
 days are small enough to be consumed by snakes, given the constraints of
 their mandibular gape. While sibling aggression begins around 5–6 days old
 (Drummond et al., 1991), brood reduction by expulsion is unlikely at this
 stage since younger chicks lack the locomotor ability to leave the nest.
 If, however, siblicide by the older sibling occurred, the chick’s body
 would have been found in the nest during monitoring and categorized as
 brood reduction. Lifetime reproductive success was the number of
 fledglings produced by each male or female breeder over its complete
 breeding history. Note that sample sizes in Results
 differ between parent and chick analyses wherever (1) chicks were excluded
 because missing morphological or body mass data prevented calculation of
 their scaled mass index, or (2) parental identities were
 unknown. Statistical
 analyses <em>Benefit to
 parents.</em> Models evaluating the benefits of
 brood reduction to parental mortality (i.e., the probability of surviving
 to the next breeding season) and reproductive performance (i.e., number of
 fledglings produced) included a two-way interaction between brood
 reduction (yes, no) and sex (male, female). Both the linear and quadratic
 expressions of the parent’s age were included as covariables to
 accommodate quadratic age-related changes in the boobies’ performance
 (Torres and Velando 2007; Beamonte-Barrientos et al. 2010). Parental
 identity, nest number, and current year were included as random effects;
 the first two of these factors accounted for statistical non-independence,
 while the year accounted for unmeasured environmental variables during the
 breeding season (e.g., food availability, parental provisioning,
 population density; Ancona and Drummond 2013). To measure the influence of
 brood reduction on the probability of surviving to the subsequent year, we
 constructed Bernoulli generalized linear mixed models (GLMMs) with logit
 link function. To analyse laying date and breeding success (number of
 fledglings produced), we used a LMM with an identity link function and a
 Poisson GLMM with a log link function.
 <em>Benefit to chicks.</em> Our
 models assessed differences in life history and reproductive outputs
 between individuals from intact broods and those from reduced broods. All
 models incorporated brood reduction and hatching order (senior, junior) as
 fixed effects, and birth cohort and nest number as random effects. Birth
 cohort accommodated unmeasured environmental factors during the
 recruits' natal years which could affect sibling competition (Ancona
 and Drummond 2013), while nest number controlled for statistical
 non-independence when two siblings were included in the same
 model. To compare the influence of brood reduction on
 body condition at fledging and recruitment probability we built two
 GLMMs.  For body condition we employed a Gaussian model with an identity
 link function, and for recruitment probability we fitted Bernoulli models
 with a logit link function. In these models we examined a three-way
 interaction involving brood reduction, hatching order and hatching date
 (standardized with November 3rd as day 1), the latter to account for
 intraseasonal weather variations. Inclusion of hatching date was crucial
 because as the breeding season progresses on Isla Isabel, rainfall
 decreases, sea surface temperature rises, and primary productivity of the
 ocean declines, all of which collectively contribute to increased
 mortality of chicks hatched late in the season (Ortega et al. 2022). The
 three-way interaction explored whether the possible benefit of brood
 reduction to the surviving sibling increases with lateness of hatching, as
 adverse environmental conditions later in the season potentially intensify
 the antagonistic interactions between competing siblings.
 We compared effects of brood reduction on age at first
 reproduction, longevity and lifetime reproductive success (total number of
 fledglings produced) of recruits (all of which were sexed) using Poisson
 models with a log link function. These models examined a three-way
 interaction involving reduction of the natal brood, sex, and body
 condition at fledging to test for possible sex-related and long-term
 effects of nestling growth following brood reduction. The longevity and
 lifetime reproductive success models included age at first reproduction as
 a fixed effect. Additionally, lifetime reproductive success was included
 as a fixed effect on the longevity analysis, while longevity was added as
 an independent variable to the lifetime reproductive success models. Age
 at first reproduction was included because late recruitment could reduce
 the number of breeding years available to a booby; longevity controlled
 for selective disappearance (van De Pol and Verhulst 2006); and total
 number of fledglings produced controlled for possible effects of the
 trade-off between reproduction and somatic maintenance.
 All analyses used the R statistical environment (R Development
 Core Team. 2024). Prior to model fitting, continuous fixed variables were
 z-score normalized to enhance the interpretability of parameter estimates
 (Grueber et al. 2011; Cade 2015). To ensure computational stability,
 prevent overfitting, and mitigate the risk of erroneous estimations of
 large effect sizes, weakly informative priors were incorporated into all
 models (Gelman et al. 2008; Lemoine et al. 2016). For all fixed effects in
 the models, a normal prior of N(0,1) was assigned, implying an expectation
 that the majority of responses would fall within one standard deviation of
 the average response values, making large effects an unusual occurrence
 (Lemoine et al. 2016). Variable standardization was performed using the
 built-in scale function (R Development Core Team 2023), and the brms
 function within the brms package was used to fit all models (Bürkner 2023;
 Stan Modeling Language Users Guide and Reference Manual, 2.35 2024). For
 each dependent variable, we calculated the contrast of interest between
 the estimated mean effects using the emmeans package (Lenth et al.
 2022). The posterior distributions of the parameters,
 accompanied by their 89% highest posterior density intervals (HPD),
 representing high-probability interval of parameter values (McElreath,
 2020), were drawn by executing five randomly initiated Markov chains. Each
 chain underwent 10,000 iterations, with a burn-in period of 1000
 iterations. Posterior predictive checks were performed for each
 generalized linear mixed models (GLMMs) using the launch-shinystan
 function of the shinystan package (Gabry Jonah et al. 2022). Complete
 model summaries are provided in Supplementary Material. Models that
 exhibited divergent transitions were excluded to avoid unreliable
 inferences. 
  [HD1]Yes,
 these two values are the same.
description: ## Long-term insights into who benefits from brood reduction We have
 submitted our raw data in five datasets. These datasets include
 information on known-age adults that either fledged both offspring or
 experienced brood reduction, and their subsequent survival and
 reproductive performance. **PARENTAL_SURVIVAL** *Variable name and
 description* YEAR = Calendar year in which the focal adult either fledged
 both offspring or experienced brood reduction. NEST_ID = Unique identifier
 of the focal adult's nest. REDUCTION = Brood outcome: 1 = both
 offspring fledged; 0 = brood reduction occurred. RING = Identity of the
 focal adult. AGE = Age of the focal adult (in years) at the time of
 fledging both offspring or experiencing brood reduction. SEX = Sex of the
 focal adult: 0 = male; 1 = female. SURVIVAL = Whether the adult survived
 to the subsequent breeding season: 1 = yes; 0 = no.
 **PARENTAL_OUTPUT_SUBSEQUENT_YEAR** *Variable name and description* YEAR =
 Calendar year in which the focal adult either fledged both offspring or
 experienced brood reduction. NEST_ID = Unique identifier of the focal
 adult's nest. REDUCTION = Brood outcome: 1 = both offspring fledged;
 0 = brood reduction occurred. RING = Identity of the focal adult. AGE =
 Age of the focal adult (in years) at the time of fledging both offspring
 or experiencing brood reduction. SEX = Sex of the focal adult: 0 = male; 1
 = female. FLEDS_SUBSEQUENT_YEAR = Number of fledglings produced by the
 focal adult in the year following the observed brood status.
 ST_DATE_SUBSEQUENT_YEAR = Standardized laying date (relative to annual
 mean) when the focal adult established its nest in the following year.
 **SMI** *Variable name and description* YEAR = Hatching year of the focal
 offspring. NEST_ID = Unique identifier of the natal nest of the focal
 offspring. ST_HATCHING_DATE = Standardized hatching date (relative to Nov
 3rd). RANK = Hatching order: 1 = senior chick (first-hatched); 2 = junior
 chick (second-hatched). REDUCTION = Whether the natal nest experienced
 brood reduction: 1 = yes; 0 = no. SMI  = Scaled Mass Index — a body
 condition index adjusted for body size (in grams). **RECRUITMENT**
 *Variable name and description* YEAR = Hatching year of the focal
 offspring. NEST_ID = Unique identifier of the natal nest of the focal
 offspring. ST_HATCHING_DATE = Standardized hatching date (relative to Nov
 3rd). RANK = Hatching order: 1 = senior chick (first-hatched); 2 = junior
 chick (second-hatched). REDUCTION = Whether the natal nest experienced
 brood reduction: 1 = yes; 0 = no. SMI = Scaled Mass Index — a body
 condition index adjusted for body size. RECRUITED = Whether the offspring
 recruited into the breeding population: 1 = yes; 0 = no. **TOTAL_OUTPUTS**
 *Variable name and description* RING = Identity of the focal adult. SEX =
 Sex of the focal offspring: 0 = male; 1 = female. REDUCTION = Whether the
 natal nest experienced brood reduction: 1 = yes; 0 = no. BIRTH_COHORT =
 year of birth AGE_AT_FIRST_REPRODUCTION = Age (in years) at which the
 focal offspring was first recorded as a breeder. LONGEVITY = Number of
 years of life of the focal individual. TOTAL_FLEDS = Total number of
 fledglings produced by the focal offspring across its reproductive
 lifetime. NATAL_NEST_ID = Unique identifier of the natal nest of the focal
 offspring. SMI = Scaled Mass Index — a body condition index adjusted for
 body size. ***Code/software*** All analyses used the R statistical
 environment (R Development Core Team. 2024)