Shifts in maternal foraging strategies during pregnancy promote offspring health and survival in a marine top predator

Abstract

The success of maternal foraging strategies during the rearing period can greatly impact the physiology and survival of dependent offspring. Surprisingly though, little is known on the fitness consequences of foraging strategies during the foetal period. In this study, we characterized variation in maternal foraging strategy throughout pregnancy in a marine top predator (South American fur seal, Arctocephalus australis), and asked if these shifts predicted neonatal health and postnatal survival. We found that during early pregnancy all pregnant females belonged to a single, homogenized foraging niche without evident clusters. Intriguingly though, during late pregnancy, individual fur seal mothers diverged into two distinct foraging niches characterized by a benthic-nearshore and a pelagic-offshore strategy. Females that shifted towards the benthic-nearshore strategy gave birth to pups with greater body mass, higher plasmatic levels of glucose and lower levels of blood urea nitrogen. The pups born to these benthic females were eight times more likely to survive compared to females using the pelagic-offshore foraging strategy during late pregnancy. These survival effects were mediated primarily by the impact of foraging strategies on neonatal glucose independent of protein metabolic profile and body mass. Benthic-nearshore foraging strategies during late pregnancy potentially allow for the greater maternal transfer of glucose to the foetus, leading to higher chances of neonatal survival. These results call for a deeper understanding of the balance between resource acquisition and allocation provided by distinct foraging polymorphisms during critical life-history periods, and how this trade-off may be adaptive under certain environmental conditions.

Full text

Vol.:(0123456789)
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Oecologia
https://doi.org/10.1007/s00442-022-05200-0
PHYSIOLOGICAL ECOLOGY – ORIGINAL RESEARCH
Shifts inmaternal foraging strategies duringpregnancy promote
offspring health andsurvival inamarine top predator
MauricioSeguel1 · BlancaE.Molina‑Burgos2,10· DiegoJ.Perez‑Venegas3 · GustavoChiang4 ·
ChrisHarrod5,6,7 · EugeneDeRango8· HectorPaves9
Received: 21 September 2021 / Accepted: 21 May 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022
Abstract
The success of maternal foraging strategies during the rearing period can greatly impact the physiology and survival of
dependent offspring. Surprisingly though, little is known on the fitness consequences of foraging strategies during the foetal
period. In this study, we characterized variation in maternal foraging strategy throughout pregnancy in a marine top preda-
tor (South American fur seal, Arctocephalus australis), and asked if these shifts predicted neonatal health and postnatal
survival. We found that during early pregnancy all pregnant females belonged to a single, homogenized foraging niche
without evident clusters. Intriguingly though, during late pregnancy, individual fur seal mothers diverged into two distinct
foraging niches characterized by a benthic-nearshore and a pelagic-offshore strategy. Females that shifted towards the benthic-
nearshore strategy gave birth to pups with greater body mass, higher plasmatic levels of glucose and lower levels of blood
urea nitrogen. The pups born to these benthic females were eight times more likely to survive compared to females using the
pelagic-offshore foraging strategy during late pregnancy. These survival effects were mediated primarily by the impact of
foraging strategies on neonatal glucose independent of protein metabolic profile and body mass. Benthic-nearshore foraging
strategies during late pregnancy potentially allow for the greater maternal transfer of glucose to the foetus, leading to higher
chances of neonatal survival. These results call for a deeper understanding of the balance between resource acquisition and
allocation provided by distinct foraging polymorphisms during critical life-history periods, and how this trade-off may be
adaptive under certain environmental conditions.
Keywords Foraging strategy· Individual variation· Pregnancy· Marine top predators· Neonatal survival
Communicated by Helene Marsh.
* Mauricio Seguel
mseguel@uoguelph.ca
1 Department ofPathobiology, Ontario Veterinary
College, University ofGuelph, 419 Gordon St, Guelph,
ONN1G2W1, Canada
2 Facultad de Medicina Veterinaria y Agronomía, Universidad
de las Americas, Manuel Montt 948, 7500000Santiago,
Chile
3 Centro de Investigación y Gestión de Recursos Naturales
(CIGREN), Instituto de Biología, Facultad de Ciencias,
Universidad de Valparaíso, Valparaíso, Chile
4 Departamento de Ecología y Biodiversidad andCentro
de Investigación Para La Sustentabilidad (CIS), Facultad
de Ciencias de La Vida, Universidad Andrés Bello,
8370251Santiago, Chile
5 University ofAntofagasta Stable Isotope Facility, University
ofAntofagasta, Antofagasta, Chile
6 Instituto de Ciencias Naturales Alexander Von Humboldt,
Universidad de Antofagasta, Antofagasta, Chile
7 Nucleo Milenio INVASAL, Concepción, Chile
8 Department ofAnimal Behaviour, Bielefeld University,
Bielefeld, Germany
9 Departamento de Ciencias Básicas, Facultad de Ciencias,
Universidad Santo Tomas, Osorno, Chile
10 Centro de Investigación Para La Sustentabilidad, Facultad
de Ciencias de La Vida, Universidad Andres Bello,
8370251Santiago, Chile

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Introduction
Foraging strategies, or the behavioural traits related to the
search and capture of food resources, are a fundamental
driver of individual success in highly diverse environments
(Wilson 1998; Franco-Trecu etal. 2012). The ability to
acquire resources directly determines how individuals
will expend energy and invest into self-preservation or
reproduction (Schoener 1971). This is especially true for
animals which invest heavily into dependent offspring, as
the parental foraging strategy could have a direct and sig-
nificant impact on offspring health and survival during
the rearing period. Additionally, in the case of placental
mammals, intrauterine development comprises a substan-
tial portion of total parental investment (Padmanabhan
etal. 2016; Reynolds etal. 2019). Therefore, the foraging
strategies used by mothers during gestation should have
a substantial impact on foetal growth and neonatal health
traits at birth (Reynolds etal. 2019; Li etal. 2020). These
relationships, however, are rarely reported in free-ranging
mammals. Consequently, it is also currently unknown how
downstream effects of maternal foraging strategies on the
foetus can escalate to fitness outcomes.
Marine ecosystems can place great pressure on ani-
mals to adapt and secure the most efficient foraging strat-
egy, as marine food patches can be highly dynamic and
unpredictable (Doniol-Valcroze etal. 2011; Ferraro etal.
2017). Therefore, species which thrive in these environ-
ments can be intriguing candidate systems to study inter-
actions between foraging behaviour and fitness dynam-
ics. In marine birds, for instance, foraging zones centred
around colonies often vary in quality, thus facilitating dif-
ferences in the survival of the dependent brood (Patrick
and Weimerskirch 2014a). Similarly, in marine mammals,
mothers alter their foraging strategies to adjust to seasonal
fluctuations in the abundance of marine resources and to
the increasing demands of a growing offspring or foetus.
For instance, otariids (fur seals and sea lions) are known
to modify the length of their foraging trips and/or foraging
areas between early pregnancy and early lactation (Drago
etal. 2010; Hoskins and Arnould 2013; Kernaléguen etal.
2015). These changes likely reflect a balance between
energy expenditure (distance travelled) and acquisition
(amount and quality of prey), improving the allocation
of resources to the foetus or pup (Baylis etal. 2016;
Jeanniard-Du-dot etal. 2017). The development of forag-
ing strategies in these marine predators is quite complex
and varies according to several ecological factors, such as
intra- and interspecific competition and landscape produc-
tivity, favoring a scenario where multiple foraging strat-
egies can coexist within a population with a significant
degree of individual plasticity to switch between foraging
strategies (Costa etal. 2004; Trillmich etal. 2014; de Lima
etal. 2019). Although there has been increased awareness
of this individual plasticity among marine top predators
(Kernaléguen etal. 2015; Kuhn etal. 2014; Páez-Rosas
etal. 2017; Riverón etal. 2021), the fitness consequences
of individual variability are still unclear, especially during
critical life-history periods such as pregnancy.
The maternal fetal relationship portends an interest-
ing trade-off between self-maintenance and immedi-
ate reproductive investment. These trade-offs could be
especially pronounced in environments with unpredict-
able resources and in species with long pregnancies and
significant investment on individual offspring such as
otariids. All otariids follow a demanding capital breeding
strategy, wherein females dually optimize their foraging
strategies and commitment to maternal care (Costa 2007).
Adult females alternate intermittent periods of foraging
at sea, with nursing and maternal attendance taking place
on land (Trillmich etal. 1991). In some species, such as
the South American fur seal (Arctocephalus australis),
these foraging-nursing cycles extend for up to 12months
despite a prolonged gestation of 9months and comple-
tion of one breeding cycle each year (Pavés etal. 2016).
Therefore, when females become pregnant, they take on
the dual role of providing energy both to their nursing pup
and to the developing foetus (Costa 2007). The intraspe-
cific strategies which females use to acquire food can
present several potential trade-offs that affect energetic
investment and allocation (Costa 2007; DeRango etal.
2021). For instance, higher trophic level prey is usually
larger and more energy dense but are sometimes located
farther from the reproductive colonies than immediately
available yet calorie deficient prey (Villegas-Amtmann
etal. 2008; Kernaléguen etal. 2015; Páez-Rosas etal.
2017; Foo etal. 2019b). Additionally, individuals can
expend greater energy to dive deeper, thus accessing prey
rarely exploited by competing species or conspecifics,
expanding available niches (McHuron etal. 2016, 2018).
Because these different foraging niches have vastly differ-
ent behavioral repertoires with associated energetic costs,
it is likely that the optimality of these strategies can affect
foetal development during a critical window. Accordingly,
in fur seal species, limited food supply can increase the
number of stillbirths and/or decrease the weight of new-
borns (Soto etal. 2004; Forcada and Hoffman 2014; Elor-
riaga-Verplancken etal. 2016), suggesting impaired foetal
development when energy supply is insufficient (Forcada
and Hoffman 2014). Suboptimal foetal energy balance is a
well-established predictor of adverse health and survival
outcomes in domestic and laboratory animals (Stanley
etal. 2012; Reynolds etal. 2019); however, this effect
has rarely been explored in wild animal populations. In
this context, the prolonged gestational period and high

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intraspecific diversity of foraging behaviour of otariids
make them excellent models to understand the impacts
of shifts in foraging strategies on foetal development and
neonatal survival of free-ranging animals.
In this study, we characterized maternal foraging strate-
gies during pregnancy and tested how they impact neona-
tal health and survival in a marine top predator, the South
American fur seal. We hypothesized that (i) given the
rising energy demands from a growing late-term foetus,
foraging strategies would become more variable towards
the end of pregnancy based on offspring condition. We
also hypothesized that (ii) more energy-efficient strate-
gies towards the end of pregnancy would translate to the
birth of larger pups with higher chances of survival. We
found support for our first hypothesis and a large effect of
late pregnancy foraging strategies on neonatal survival.
However, these survival effects were not influenced by
the pup’s birth mass and depended only on birth glucose
levels, highlighting that the pup’s metabolic state is an
important mediator of the survival effects of maternal for-
aging strategy during pregnancy. These findings suggests
that maternal effects during pregnancy play a critical role
in the fitness of mammalian top predators.
Materials andmethods
Animal sampling
Between December 2016 and March 2017, we captured
60 South American fur seal (SAFS) pups at Guafo Island,
Northern Chilean Patagonia (43.593029° S 74.713481°
W). Pups were first captured when they were between 1
and 2days-old, and subsequentially recaptured at least
once a month (total 2–3 captures per pup). In the pup’s
first capture, we cut the largest vibrissa at its base and
collected blood (caudal gluteal vein) to obtain serum and
perform a biochemical panel and obtain several indica-
tors of metabolic health (glucose, albumin, creatinine,
blood urea nitrogen [BUN] and triglycerides) following
previously described methods for this species (Seguel
etal. 2016). During each capture, we recorded the pup’s
mass and total length to calculate their body mass index
(BMI) (weight/total length). SAFS foraging and maternal
attendance cycles at Guafo Island begin 48–72h after birth
(Montalva etal. 2019), therefore, we considered the pup’s
BMI and metabolic health traits a consequence of maternal
energy investment during pregnancy rather than a result
of maternal investment during the rearing period. Pups
were followed for up to 68days through daily rookery
observation (6h per day) performed from an elevated point
located 50–100 mts from the rookery.
Stable isotopes
The foraging strategies developed by marine top predators
such as otariids can be quantified using the known circula-
tion of major elements within marine ecosystems (de Lima
etal. 2019; Kernaléguen etal. 2015; Kuhn etal. 2014; Páez-
Rosas etal. 2017; Riverón etal. 2021). Carbon, for instance,
is higher in nearshore habitats and prey in these areas tend
to have higher levels of the stable isotope carbon-13 (δ13C)
(Fry 2013). Therefore, animals consuming prey primarily in
nearshore habitats accumulate a higher proportion of δ13C
in their tissues while offshore predators accumulate a lower
proportion of this stable isotope (Baylis etal. 2016; Drago
etal. 2016; Amador-Capitanachi etal. 2020; Páez-Rosas
etal. 2020). In the case of nitrogen, the stable isotope nitro-
gen-15 (δ15N) is enriched through the trophic chain, there-
fore predators occupying a higher trophic level tend to con-
sume a higher proportion of this stable isotope (Hückstädt
etal. 2012; McHuron etal. 2018; Villegas-Amtmann etal.
2008). Sulfur is another useful marker of trophic interactions
in aquatic ecosystems. The stable isotope sulfur-34 (δ34S) is
incorporated from terrestrial sources into the coastal envi-
ronment, and though bacteria and plankton transformation
are depleted down the water column (Fry 2013). Therefore,
deeper waters (benthic environments) tend to have a lower
proportion of this stable isotope compared to more superfi-
cial waters (epipelagic environment) (Hoekstra etal. 2002;
Niño-Torres etal. 2006; Hussey etal. 2012; Fry 2013; Szpak
and Buckley 2020). The δ13C, δ15N and δ34S stable isotopes
in the prey are used as building blocks in the different tissues
of the consumer and depending on the tissue’s metabolism,
these building blocks can be reutilized as required by the
overall C, N and S balance in the body (Fry 2013; Baeta
2019). However, in metabolically inactive tissues such as
hair and vibrissae, δ13C, δ15N and δ34S isotopes remain inert
(Fry 2013; Baeta 2019). Therefore, δ13C, δ15N and δ34S
values in these tissues represent a snapshot of the foraging
environment and trophic level of the consumer at the time
that tissue was formed (DeRango and Schwarz, 2021; Páez-
Rosas etal. 2017; Riverón etal. 2021).
To explore the foraging niche of fur seal females, we
determined stable isotope ratios (δ13C, δ15N and δ34S) of
their pup’s vibrissae as a proxy of maternal foraging behav-
iour during pregnancy (Elorriaga-Verplancken etal. 2016;
Jones etal. 2020). Vibrissae were kept refrigerated and
transported to a mainland laboratory to perform the stable
isotope analyses (Universidad de Antofagasta Stable Isotope
Facility, Antofagasta, Chile). Our analyses focused on two
sections of vibrissae, the oldest (distal end) and the new-
est (proximal end). We cut 1cm of each vibrissae section,
obtaining two subsamples from each pup; a base section
(proximal end) and a tip section (distal end). Because we
collected vibrissae when pups were no more than 2days-old,

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and because we cut vibrissae at their base instead of pulling
from their root, we considered these samples representative
of early/mid (tip section, hereafter “early” [3–7months]) and
late (base section [8–9months]) pregnancy stages (Urquía
and Páez-Rosas 2019; Jones etal. 2020). Vibrissae were
cleaned using a Chloroform–Methanol (2:1) mixture (3
times until a clear solution is obtained) rinsed with distilled
water and then dried in a drying oven for 18h at 50°C (Hus-
sey etal. 2012). Each vibrissae subsample was sectioned to
obtain a mass of ~ 0.5mg and samples were packed in tin
capsules. We estimated elemental percentages for carbon,
nitrogen, sulphur and stable isotope ratios (δ13C, δ15N and
δ34S) using a Pyrocube (Elementar, Langenselbold, Ger-
many) elemental analyser linked to a visION (Elementar,
Langenselbold, Germany) continuous-flow isotope ratio
mass spectrometer. Stable isotope ratios were expressed in
δ units for Vienna Pee Dee Belemnite for carbon, air for
nitrogen and Vienna Canyon Diablo Troilite for sulphur as
isotopic standards. Different international standards were
used in each batch run to calibrate and assess analytical
error using the ionOS software package (Elementar, Lan-
genselbold, Germany). Certified reference material USGS40
and USGS41 were used for carbon and nitrogen and IAEA-
SO-5, IAEA-SO-6 and IAEA-S-2 were used for sulphur.
Repeated analysis of standards showed that analytical errors
(± 1 SD) were ± 0.06 % for δ13C, ± 0.05 % for δ15N and ± 0.3
5 for δ34S. We used two calibration standards, (a) sulfona-
mide (Elementar, Germany) and (b) an in-house standard
(rainbow trout) to correct for machine drift.
Data analyses
Isotopic variation
To describe the level of within and between-individual vari-
ation in stable isotopes in each individual, we calculated the
between and within-individual variances on these isotopes
using a univariate Markov chain Monte Carlo generalized
linear mixed model (MCMC GLMM) implemented within
the R package “MCMCglmm” (Hadfield 2010). In these
models, stable isotope values were fitted as the response of
“pregnancy stage” and animal ID was included as a random
effect to obtain within- and between-individual variances
in relation to the female’s pregnancy stage. We calculated
the repeatability for these isotopes using the posterior dis-
tribution of their within- and between-individual variances
(Houslay and Wilson 2017). Later, to test if variation in the
isotopic values of the mothers between early and late gesta-
tion resulted in differentiation into different foraging niche
groups, we used a Gaussian Finite Mixture Model imple-
mented within the R package ‘Mclust’ (Scrucca etal. 2016).
This model uses a Bayesian framework to calculate two-
dimensional ellipsoids with standard deviation analogues,
selecting the best fitting model using Bayesian Information
Criteria (BIC). We applied these models separately to iso-
topic values from early pregnancy and late pregnancy to
detect if isotopic niche clusters differed for the same indi-
viduals between these two stages.
To test if changes in the classification of a foraging group
at the population level were associated with within-individ-
ual variation between early and late pregnancy in isotope
values or to increase between individual distances in iso-
tope values, we fitted bivariate MCMC GLMMs using δ13C
or δ15N and foraging niche group (benthic-nearshore vs
pelagic-offshore) as responses of pregnancy stage. In these
models, animal ID was added as a random effect. These
bivariate MCMC GLMMs provided the residual covariance
structure, which represents the within-individual changes
over time (with pregnancy stage) in the response vari-
able (stable isotope values and differentiation into benthic-
nearshore or pelagic-offshore foraging groups). The random
effect (animal ID) covariance represents the between-indi-
vidual changes over time in relation to change in foraging
group classification. For the random effect and the residuals,
we calculated the posterior distribution for the variance and
covariance between isotopes and foraging niche along with
the effect of the deviance of an isotope on the foraging niche
at each hierarchal level (random effect and residuals) as fol-
low (σ2 = variance, σx,y = covariance):
This quotient estimates the slope of a given isotope on a
foraging niche for a particular hierarchal level. Slopes were
calculated along with the posterior distribution of each vari-
ance structure, allowing the calculation of mean and 95%
credible intervals. Slopes were deemed significant if 95%
credible intervals did not overlap with zero. A significant
residual slope would indicate that changes in an individ-
ual isotope value in relation to its own previous values are
correlated with its classification into the benthic foraging
group while a significant animal ID slope would indicate
that changes in an animal isotope values in relation to other
animals in the population were necessary to be classified in
the benthic foraging group.
Bivariate models were run for 5 × 105 iterations, with
4.5 × 104 burn-in and a thinning interval of 300. For all
MCMC GLMMs we used parameter expanded uninforma-
tive priors (no assumption of previous data distributions) to
decrease computation time and aid in model convergence
(Hadfield 2010; Houslay and Wilson 2017). All models
estimated unstructured variance–covariance matrices for the
specified random effect. We checked models for robustness
to different prior structures by introducing slight changes in
Σ
Isotope, foraging niche (benthic=1)
/
𝜎2
Isotope

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the variance components of the random effects and residuals.
We tested models for autocorrelation by examining diag-
nostic plots and model convergence was assessed using the
“geweke.diag” and “gelman.diag” diagnostic functions in
the MCMCglmm package (Hadfield 2010).
Eect ofisotopic variation onthehealth
ofpups atbirth
To explore the relationships between isotopic values (early
and late pregnancy) and neonatal health traits as well as the
relationships between health traits, we conducted Spearman-
rho correlations between health traits and isotopes. We used
GLMs with gaussian distribution to test if late pregnancy
foraging strategies impacted the birth levels of metabolic
biomarkers of neonatal health and energy balance. In these
models, we used the previously identified foraging groups as
predictors of BUN, creatinine, glucose, albumin, triglycer-
ides or body mass index. We preferred to use this categorical
predictor instead of the absolute change in isotope values
per individual since this predictor encompasses a single cat-
egory the trophic niche rather than only variation in forag-
ing site (δ13C and δ34S) or trophic level (δ15N). All these
models also included sex (male or female) as a categorical
predictor to control for the potential effect of sex on health
traits. In all models, the inclusion of sex did not impact the
statistical significance of the foraging group and sex did
not have a statistically significant effect on any health traits
(TableS10). We checked models for homoscedasticity by
visually inspecting residuals plots and for overdispersion by
dividing the residuals deviance by the degrees of freedom.
A ratio < 2.0 was considered adequate.
To explore the potential impact of maternal foraging dur-
ing pregnancy and/or neonatal metabolic health traits on sur-
vival we fitted univariate and multivariate Cox proportional
hazard models using the “survival” R package (Therneau
2021). First, we fitted a series of univariate models using
the metabolic and energy budget traits that were influenced
by the foraging group (BMI, BUN and glucose) as the sole
predictors of time to death. We also fitted one univariate
model using foraging group during late pregnancy as a cat-
egorical predictor. This model revealed an important sur-
vival effect of the foraging group. Therefore, we tested if
these survival effects were independent of the impact of
maternal foraging groups on health and metabolic traits by
fitting several multivariate Cox proportional hazard models
that used foraging group as predictor while controlling for
BUN, glucose and BMI. In these models, we avoided the
simultaneous inclusion of two highly correlated predictors
(e.g. glucose and BMI) to avoid collinearity and model con-
vergence issues. Finally, to identify the best fitting models,
we ranked univariate and multivariate candidate models by
their corrected Akaike Information Criteria (AICc) value
using the R package “MuMIn” (Barton 2018). We consid-
ered models with a difference of > 6.0 AICc to be significa-
tively different (Hodgson etal. 2018). For all Cox propor-
tional hazard models, the proportional hazard assumption of
predictors was checked by plotting the Schoenfeld residuals
versus time for continuous predictors and by plotting the
log–log-transformed Kaplan–Meier survival curves for cat-
egorical predictors.
Results
a) Fur seal females change their foraging strategy
betweenearly andlate pregnancy
The mean isotopic ratios of δ13C and δ15N did not differ at
the population level between early and late pregnancy while
levels of δ34S were slightly higher during late pregnancy
compared to early pregnancy (Tables S1–S3). However, vis-
ualization of the individual slopes of the raw isotopic ratios
of δ13C and δ15N suggested a significant degree of within-
individual variation in these isotopes and more consistent
between individual differences in δ34S ratios (Fig.1a–c).
In support of this inference, we observed a higher propor-
tion of the δ13C and δ15N variance at the within-individual
level (δ13C = 60%, δ15N = 65%) and a higher proportion
of the variance of δ34S at the between-individual level
(δ34S = 78%), suggesting that individual pregnant females
changed their foraging trophic level (δ15N) and foraging site
(δ13C) between early and late pregnancy while maintaining
consistent differences between them in the level of the water
column where their forage (δ34S) (Tables S1–S3). In support
of these observations, cluster analyses revealed no clear clus-
ters or foraging niche differentiation of SAFS females during
early pregnancy while during late pregnancy there were two
distinct foraging clusters. The first group foraged at variable
trophic levels (variable δ15N) but used more offshore habi-
tats (lower δ13C) and more superficial waters (higher δ34S)
(hereafter “pelagic group”). The second group foraged at
an intermediate trophic level and used more inshore habi-
tats (higher δ13C) and deeper waters (lower δ34S) (hereafter
“benthic group”) (Fig.1). Multivariate analyses revealed that
within-individual changes in δ13C and δ34S but not in δ15N
were more important than differences between individuals
to categorize females as benthic or pelagic (Tables S4-S6).
More precisely, individuals that increased their δ13C val-
ues and decreased their δ34S values during late pregnancy
respective to their own early pregnancy values were usually
classified as benthic foragers (MCMC GLMM; δ13C and
benthic within-individual correlation = 0.27, 95% credible
interval [95% CI] = 0.06–0.48; δ34S and benthic within-
individual correlation = −0.31, 95% CI = −0.52 to −0.99).

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These findings indicate that fur seal mothers exhibit different
degrees of within-individual variation in foraging strategies
during pregnancy, leading some of them to exploit a benthic
foraging strategy during late pregnancy.
b) Late pregnancy benthic foraging strategy
promotes neonatal health andsurvival
Stable isotope ratios during early pregnancy were not cor-
related with health traits (TableS7), however δ15N and
δ34S ratios during late pregnancy were correlated with the
new-born glucose levels (δ15N r = 0.38, P < 0.003; δ34S
r = − 0.37, P = 0.004), suggesting some impact of late
pregnancy foraging strategies on neonatal health. Confirm-
ing these observations, we found that late pregnancy for-
aging groups, but not early pregnancy isotope values, pre-
dicted the new-born levels of metabolic and health traits
(TableS8–S10). Pups born to mothers that shifted towards
a benthic foraging strategy were born with higher BMI and
glucose and lower levels of BUN compared to pups born
to females that shifted towards the pelagic foraging strat-
egy (Fig.2). Late pregnancy foraging groups did not impact
the neonatal values of albumin, triglycerides and creati-
nine (Fig.2). More importantly, we found that late preg-
nancy maternal foraging groups significatively impacted
early-life survival with pups born to mother that used the
Fig. 1 South American fur seal (Arctocephalus australis) foraging
strategies change between early and late pregnancy. The slopes on
the individual raw δ13C (A) and δ15N (B) isotopic ratios reveal a sig-
nificant and random level of variation in females foraging strategies
between early pregnancy and late pregnancy. While some females
increase their δ13C and/or δ15N values, others decrease δ13C and/
or δ15N values (each slope colour represents a specific animal ID,
N = 58). For δ34S (C) there is less within individual variation but
more consistent differences between individuals. These within-indi-
vidual differences from early to late pregnancy led to differentiation
into two distinct foraging niches in late pregnancy. D In early preg-
nancy, there is homogeneous variation in foraging niche between
individuals without evident clusters (best model cluster analysis,
number clusters = 1, log-likelihood = − 80.7, n = 58, df = 5, BIC = −
181.7). D During late pregnancy, fur seal mothers diverge from the
main foraging cluster, forming 2 distinct foraging niche clusters; a
benthic group (n = 20, green squares) and a pelagic group (n = 38,
purple circles) (best model cluster analysis, number clusters = 2, -log-
likelihood = − 94.3, n = 58, df = 11, BIC = − 233.2) (The ellipsoids
over clusters represent standard deviation analogues)

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pelagic strategy approximately 8 times more likely to die
during their first 68days of life compared to pups born to
females that used the benthic strategy during late pregnancy
(Cox proportional hazard model [CPHM], Hazard ratio
[HR] = 8.5 ± 1.0, 95% confidence interval [CI] = 1.1–66,
Z = 2.1, P = 0.03) (TableS11). This survival effect was
mediated by the impact of late pregnancy foraging strat-
egy on the neonate metabolic state since after controlling
for the impact of glucose, the effect of foraging groups on
survival became not significant (CPHM, HR = 6.85 ± 1.15,
95% CI = 0.88–54.5, Z = 1.56, P = 0.10). Additionally, mul-
tivariate Cox models that also incorporated BMI and BUN,
and posterior model selection (TableS12), revealed that
after controlling for these covariates and for the foraging
group, glucose was the only important predictor of sur-
vival with pups born in the lowest glucose quartile having
approximately 8.9 times higher chances of mortality com-
pared to pups born in the highest glucose quartile (CPHM,
HR = 8.92 ± 0.67, 95% CI = 2.3–33.3, Z = 3.258 P = 0.001)
(TableS13) (Fig.3).
Discussion
Maternal foraging strategies during the rearing period
are known drivers of dependent offspring survival in a
wide range of animal taxa (Jeanniard-Du-dot etal. 2017;
Patrick and Weimerskirch 2014b; Pettex etal. 2012; Soto
etal. 2004). In placental mammals, however, the intimate
and prolonged maternal foetal relationship suggests that
foraging strategies during pregnancy could have similar
or even larger implications for offspring survival. Surpris-
ingly though, there has been little testing of this hypoth-
esis and even less is known regarding foetal traits being
impacted by variation in maternal foraging strategies. In
this study, we showed that maternal variation towards a
benthic-inshore foraging strategy during late pregnancy
in fur seals increased energy balance and the metabolic
state of offspring at birth. More importantly, we found
that this positive relationship, specifically regarding the
impact of this strategy shift on glucose levels, escalated
to a significatively better survival outcome for neonates.
Fig. 2 Late pregnancy benthic
foraging strategy contributes
to neonatal health. South
American fur seal pups born
to mothers that shifted to the
benthic foraging strategy during
late pregnancy (n = 20) were
born with higher body mass
(A), higher levels of glucose (B)
and lower levels of blood urea
nitrogen (BUN) (C) compared
to pups born to females using
the pelagic foraging strategy
during late pregnancy (n = 38).
Pups born to females using
the benthic or pelagic foraging
strategy during late pregnancy
did not differ in their levels of
albumin (D), creatinine (E)
and triglycerides (E) (GLM
outputs tableS8). Asterisk
indicates significant differences
between groups (BMI, GLM
benthic = 0.06 ± 0.02, Z = 2.2,
P = 0.03; Glucose, GLM
benthic = 0.8 ± 0.3, Z = 2.2,
P = 0.03; BUN, GLM ben-
thic = −1.17 ± 0.5, Z = −2.1,
P = 0.04)

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These findings suggest that maternal foraging shifts dur-
ing pregnancy are important drivers of survival through a
direct impact on foetal metabolic state.
In several otariid species, reproductive females experi-
ence significant changes in foraging strategy during gestation
or from gestation to nursing (Drago etal. 2010; Hoskins and
Arnould 2013; Kernaléguen etal. 2015). Here, we similarly
found variable differentiation in foraging strategies between
early and late pregnancy in South American fur seals. These
shifts could reflect a response to periodic, intra-annual fluc-
tuations in prey abundance or a need to balance the rising
energetic demands from the growing foetus, as it has been
proposed for other otariids (Drago etal. 2010; Hoskins and
Arnould 2013). In addition, we observed between-individual
differences in trophic niche shifts with an additional sig-
nificant degree of within-individual variation. This pattern
has been noted in other populations of this species in the
Atlantic Ocean, wherein generalist individuals are known
to rapidly switch between foraging strategies (Riverón etal.
2021). In otariids, this individual-level foraging variability is
considered the result of avoidance of intra-specific competi-
tion during periods of high energetic demand (Kernaléguen
etal. 2015; de Lima etal. 2019). Alternatively, it has been
proposed that variable environments favour the selection of
individuals with more plastic foraging strategies since these
could be advantageous when food supply is unpredictable
(Jeglinski etal. 2012; Kernaléguen etal. 2015; Páez-Rosas
etal. 2017). Both hypotheses assume a fitness advantage
of foraging variability but surprisingly, few studies have
assessed health and survival impacts (Jeanniard-Du-dot etal.
2017; Phillips etal. 2017). This study fills this important gap
by illustrating the impact of foraging changes during foetal
development on the health and survival of the neonate as a
direct proxy for maternal fitness.
In humans and domestic animals, the foetal environment
is a well-known modulator of neonatal and adult health
(Padmanabhan etal. 2016; Reynolds etal. 2019). In domes-
tic animals, gestational caloric and nutritional deficiencies
can significatively impact birth weight, metabolic markers
and immune function (Reynolds etal. 2019; Li etal. 2020).
Less is known in wild animals regarding the role of the foe-
tal environment on neonatal health, but preliminary studies
suggest that maternal body condition and overall health dur-
ing pregnancy affect foetal growth (Christiansen etal. 2014;
Aleuy etal. 2020). Our study confirms that maternal forag-
ing strategy during pregnancy is another key factor affecting
neonatal health. We found that mothers that shifted during
late pregnancy towards the benthic strategy had pups with
higher BMI and plasmatic glucose and lower BUN levels,
all important proxies of neonatal health in wild mammals
(Greig etal. 2010).
BMI at birth is a general proxy for foetal growth and
in utero energy balance while plasmatic glucose is a more
specific and direct measurement of a neonate’s immediate
energy source (Reynolds etal. 2019). In mammals, neonatal
birth glucose levels are directly linked to maternal plasma
glucose since this metabolite readily crosses the placental
barrier (Mendiola etal. 1982; Hay 2006). Therefore, in our
study, a higher BMI and birth glucose suggest that moth-
ers using the benthic strategy during late pregnancy had
greater energy balance or an increased capacity to transfer
their energy reserves to the foetus. This energetic advan-
tage could be related to the fact that our benthic group also
used nearshore foraging areas, which could have facilitated
Fig. 3 The boost of neonatal glucose levels by the maternal inshore
foraging strategy promoted the survival of fur seal pups. A Individu-
als born to mothers that used the benthic foraging strategy during late
pregnancy (n = 20) were 8 times more likely to survive compared to
pups born to females that shifted to the pelagic foraging strategy dur-
ing late pregnancy (n = 38) (Cox proportional hazard model [CPHM],
Hazard ratio [HR] = 8.5 ± 1.0, 95% confidence interval [CI] = 1.1–66,
Z = 2.1, P = 0.03). B However, after controlling for the effect of glu-
cose on survival, the effect of the inshore foraging strategy became
not significant, suggesting that the impact of maternal foraging
strategy on survival is associated with its impact on glucose levels
(CPHM, HR = 6.85 ± 1.15, 95% CI = 0.88–54.5, Z = 1.56, P = 0.10).
C Glucose levels at birth had a significant impact on survival,
even after controlling for the effect of the maternal foraging group,
with pups born in the highest glucose quartile with almost 9 times
higher chances of survival compared to pups born in the lowest glu-
cose quartile (CPHM, HR = 8.92 ± 0.67, 95% CI = 2.3–33.3, Z = 3.3,
P = 0.001)

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more frequent and/or longer resting periods in land during
pregnancy (Baylis etal. 2016, 2018; Jeanniard-Du-dot etal.
2017; Foo etal. 2019a), potentially favoring energy trans-
fer to the foetus. This hypothesis is also supported by the
impact of foraging strategies on foetal BUN levels. BUN
provides a general assessment of the protein and N balance
in the foetus with lower BUN levels indicating less use of
protein and amino acids as energy sources. Therefore, lower
levels of BUN in the pups of benthic females suggest that
fat and/or carbohydrates were used in higher proportion as
energy sources in this group compared to the pelagic moth-
ers. Similar to glucose, this could have been related to more
frequent access to food and/or shorter foraging trips in the
benthic-nearshore foraging areas, decreasing the chances
of maternal muscle catabolism to maintain foetal growth.
Additionally, if these strategies are maintained as part of
the maternal foraging-attendance cycles during the rearing
period, the pups could have more frequent access to milk,
which could be particularly important to maintain a positive
energy balance when pups are less than two weeks old and
their stomachs cannot hold a large amount of milk. However,
if late pregnancy foraging strategies are maintained during
the rearing period is unknown for the SAFS population at
Guafo Island.
Maternal foraging strategies during late pregnancy also
impacted survival, although this effect disappeared after
controlling for birth glucose levels. This suggests that the
survival effect of the benthic foraging strategies is likely
mediated through its boost of birth glucose levels. Glucose
is the fastest source of energy for pups and higher levels of
this metabolite could imply more fuel for skeletal muscle
and other essential tissues which contribute to movement
and other essential behaviour (Seguel etal. 2013; Spraker
and Lander 2010). Interestingly, glucose levels are directly
linked to survival of intestinal hookworm infection (Unci-
naria sp.), a main cause of mortality in this study popula-
tion (Seguel etal. 2018b), providing a potential link for the
survival effects of this metabolite and foraging strategies.
Glucose levels are the most important predictor for T cell
reactivity and production of hookworm specific IgG, both
important immune components for clearance of hookworms
from the intestine and survival from infection (Seguel etal.
2018a, 2019). Therefore, by boosting glucose levels or avail-
ability, the maternal benthic foraging strategy during preg-
nancy could give pups better tools to overcome the most
common causes of mortality during the neonatal period.
A survival advantage attributed to specific shifts in for-
aging strategy portends an important question as natural
selection does not coalesce into this strategy during late
pregnancy in all individuals. The development of foraging
strategies in otariids is complex and related to social, physi-
ological and environmental factors (Costa and Gales 2003;
Jeglinski etal. 2012; Kuhn etal. 2014; Leung etal. 2014;
Vales etal. 2015; Amador-Capitanachi etal. 2020). For
instance, in New Zealand sea lions, adult females develop
unique foraging strategies that are consistent across seasons
and environmental conditions (Chilvers 2008; Chilvers and
Wilkinson 2009). In our study, since we assessed a single
reproductive season, we do not know if the observed dif-
ferences between females are consistent and independent
of environmental conditions, therefore, a combination of
individual and environmental stimuli could have resulted
in the lower proportion of individuals exploiting the yet
more advantageous benthic strategy. For instance, it is pos-
sible that only a smaller proportion of foraging females had
the physiological and cognitive capacity to exploit benthic
resources around Guafo Island. The main food resource of
fur seals at Guafo Island is the southern hake (Merluccius
australis), an overexploited, energy-dense benthic fish spe-
cies (Seguel etal. 2013; Neira and Arancibia 2021). The
abundance of this hake species in areas nearby Guafo Island
can be quite variable depending on changes in marine pro-
ductivity and migratory behaviour of stocks (Flores etal.
2019; Toledo etal. 2019). Similarly, in the greater Pacific
Ocean, during periods of higher sea surface temperature,
marine productivity declines along with pelagic prey, forc-
ing more individuals to exploit benthic resources (Elorriaga-
Verplancken etal. 2016; Amador-Capitanachi etal. 2020;
Páez-Rosas etal. 2020). Therefore, a reduction in hake or
other primary food resource could have increased intraspe-
cific competition allowing only certain female groups to
exploit hake stocks during the study period. However, given
the significant proportion of females that followed a pelagic
strategy during late pregnancy, it can be inferred that under
different conditions, for instance with a higher abundance
of pelagic resources, this strategy could provide a survival
advantage, allowing the maintenance of this foraging pheno-
type within the population. More importantly, our data indi-
cate that females classified as benthic during late pregnancy
where those that foraged at late pregnancy in deeper waters
and more nearshore habitats respective to their own early
pregnancy foraging habitats. These findings suggest that
beyond the considerations for the advantages that a benthic
or pelagic strategy can confer to pregnant females in certain
environments, is the capacity to switch and occupy differ-
ent foraging areas that confers fitness advantages. There-
fore, understanding the factors that influence this individual
level of plasticity becomes highly relevant, especially under
the current scenario of unpredictable and declining marine
ecosystems.
In most long-living mammal species, the foetal stage
comprises a large proportion of the total parental depend-
ence period. Surprisingly though, little is still known about
the parental traits that affect offspring in utero and whether
these traits could have fitness consequences. In this study,
we showed in a long-living mammal that changes towards

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a benthic maternal foraging strategy during late pregnancy
provided important energetic and metabolic advantages to
neonates that translated into better survival outcomes. These
results indicate that variation in maternal foraging strategy
during pregnancy have indirect and almost immediate fit-
ness consequences for the mother, suggesting that pregnancy
effects could facilitate selection for foraging plasticity in
marine top predators.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s00442- 022- 05200-0.
Acknowledgements We appreciate the logistical support of the Chil-
ean Navy, Artisanal fishermen of Quellon (Vessel crews Marimar
II, Nautylus V and Matias Jesus), and the crews of the Guafo Island
Chilean Navy lighthouse. We thank the tireless field assistance of Dr.
Josefina Gutierrez, Felipe Montalva, Emma Milner, Piero Becker, Sian
Tarrant, Suzette Miller, and Emily Morris.
Author contribution statement MS, BM and HP conceived the study
and drafted the manuscript; MS, BM carried out the statistical analyses;
MS, BM, DP-V, GC, CH, EDR collected data and critically revised the
manuscript. All authors gave final approval for publication and agree
to be held accountable for the work performed therein.
Funding Research partially funded by Morris Animal Foundation
(D16ZO-413), Universidad Santo Tomas research funds and Rufford
Small Grants (11815-1).CH is supported by Chilean Association
Research and Development,Millennium Science Initiative NCN2021-
056: Millennium Nucleus of Austral Invasive Salmonids.
Data availability All data used in this study will be publicly available
in a data repository before publication (datadyrad.org). Data is also
provided as electronic supplementary materials.
Declarations
Conflict of interest We declare no competing interests.
Ethical approval Study conducted under authorization of the Chilean
subsecretary of fisheries (Res. Ex. 976 2016) and under approval from
the Institutional Animal Care and Use Committee of the University of
Georgia, USA (IACUC #A2013 11-004-Y3-A0).
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