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Sex- and age-specific migratory strategies of blue whales in the northeast Pacific Ocean

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  • CONACYT - Ensenada Center for Scientific Research and Higher Education

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Migration is a complex behavior that has evolved in multiple taxonomic groups as a means of accessing productive foraging grounds and environmentally stable areas suitable for reproduction. For migratory whales that forage throughout the year because of their high energetic demands, changes in the abundance of prey in different areas along their migratory route(s) can have serious implications for individual fitness and population viability. Thus, identifying the regions these species use to forage and breed while evaluating their migratory plasticity at the individual level can provide key information for their management and conservation. Serial stable isotope analysis of whale baleen, a continuously growing but metabolically inert tissue, has proven useful in generating individual migratory and foraging records over several years prior to death. We measured carbon ( δ ¹³ C) and nitrogen ( δ ¹⁵ N) isotope values along the length of baleen plates collected from thirteen blue whales of different sex and age classes, representing the largest collection analyzed to date in the northeast Pacific Ocean. Adult females exhibited relatively stable seasonal movements between temperate latitude foraging grounds and subtropical breeding grounds, although two skipped migration one year and subsequently moved to the same subtropical breeding ground near the Costa Rica Dome, potentially to give birth. Adult males exhibited two movement strategies with most remaining at temperate latitudes for 3-4 years before death, while two migrated to subtropical breeding grounds. In contrast, movement patterns in juveniles were erratic. These results are potentially driven by the energetic requirements during pregnancy and nursing in adult females, intra-specific competition among adult males, and inexperience in locating prey in juveniles. We also describe baleen δ ¹⁵ N patterns in recently weaned whales (<16.5m) that reflect switching from the consumption of milk to solid food (krill). In addition, baleen δ ¹³ C data suggest that weaned whales continue to use stored nutrients (blubber) acquired during the nursing period long after they are weaned. These results broaden our understanding of habitat selection in this species, highlight the importance of nursing for the critical period after weaning, and indicate that the Costa Rica Dome is an important calving region for this endangered population.
Content may be subject to copyright.
Sex- and age-specic migratory
strategies of blue whales in the
northeast Pacic Ocean
Christina Blevins
1
, Geraldine Busquets-Vass
1,2
*,
Mario A. Pardo
3
, Diane Gendron
4
, Jeff K. Jacobsen
5
,
Francisco Go
´mez-Dı
´az
6
,He
´ctor Pe
´rez-Puig
7
,
Christian Daniel Ortega-Ortiz
8
, Gisela Heckel
9
,
Jorge Urba
´nR.
10
, Lorena Viloria-Go
´mora
10
and Seth D. Newsome
1
1
Biology Department, University of New Mexico, Albuquerque, NM, United States,
2
Laboratorio de
Macroecologı
´a Marina, Centro de Investigacio
´n Cientı
´ca y Educacio
´n Superior de Ensenada,
Unidad La Paz, La Paz, Mexico,
3
Laboratorio de Macroecologı
´a Marina, Consejo Nacional de
Ciencia y Tecnologı
´a - Centro de Investigacio
´n Cientı
´ca y Educacio
´n Superior de Ensenada,
Unidad La Paz, La Paz, Mexico,
4
Instituto Polite
´cnico Nacional, Centro Interdisciplinario de Ciencias
Marinas, La Paz, Mexico,
5
VE Enterprises, Arcata, CA, United States,
6
Museo de la Ballena y Ciencias
Marinas, La Paz, Mexico,
7
Marine Mammal Program, Prescott College Kino Bay Center for Cultural
and Ecological Studies, Bahı
´a de Kino, Mexico,
8
Facultad de Ciencias Marinas, Universidad de
Colima, Manzanillo, Mexico,
9
Departamento de Biologı
´a de la Conservacio
´n, Centro de
Investigacio
´n Cientı
´ca y de Educacio
´n Superior de Ensenada, Ensenada, Mexico,
10
Departamento
Acade
´mico de Ciencias Marinas y Costeras, Universidad Auto
´noma de Baja California Sur,
La Paz, Mexico
Migration is a complex behavior that has evolved in multiple taxonomic groups
as a means of accessing productive foraging grounds and environmentally
stable areas suitable for reproduction. For migratory whales that forage
throughout the year because of their high energetic demands, changes in the
abundance of prey in different areas along their migratory route(s) can have
serious implications for individual tness and population viability. Thus,
identifying the regions these species use to forage and breed while evaluating
their migratory plasticity at the individual level can provide key information for
their management and conservation. Serial stable isotope analysis of whale
baleen, a continuously growing but metabolically inert tissue, has proven useful
in generating individual migratory and foraging records over several years prior
to death. We measured carbon (d
13
C) and nitrogen (d
15
N) isotope values along
the length of baleen plates collected from thirteen blue whales of different sex
and age classes, representing the largest collection analyzed to date in the
northeast Pacic Ocean. Adult females exhibited relatively stable seasonal
movements between temperate latitude foraging grounds and subtropical
breeding grounds, although two skipped migration one year and
subsequently moved to the same subtropical breeding ground near the Costa
Rica Dome, potentially to give birth. Adult males exhibited two movement
strategies with most remaining at temperate latitudes for 3-4 years before
death, while two migrated to subtropical breeding grounds. In contrast,
movement patterns in juveniles were erratic. These results are potentially
driven by the energetic requirements during pregnancy and nursing in adult
Frontiers in Marine Science frontiersin.org01
OPEN ACCESS
EDITED BY
Mo
´nica A. Silva,
University of the Azores, Portugal
REVIEWED BY
Alex Aguilar,
University of Barcelona, Spain
Kerri J. Smith,
Dalhousie University, Canada
*CORRESPONDENCE
Geraldine Busquets-Vass
geraldine.busquets@gmail.com
SPECIALTY SECTION
This article was submitted to
Marine Megafauna,
a section of the journal
Frontiers in Marine Science
RECEIVED 16 May 2022
ACCEPTED 08 August 2022
PUBLISHED 02 September 2022
CITATION
Blevins C, Busquets-Vass G, Pardo MA,
Gendron D, Jacobsen JK,
Go
´mez-Dı
´az F, Pe
´rez-Puig H,
Ortega-Ortiz CD, Heckel G, Urba
´n
R. J, Viloria-Go
´mora L and
Newsome SD (2022) Sex- and
age-specic migratory strategies
of blue whales in the northeast
Pacic Ocean.
Front. Mar. Sci. 9:944918.
doi: 10.3389/fmars.2022.944918
COPYRIGHT
© 2022 Blevins, Busquets-Vass, Pardo,
Gendron, Jacobsen, Go
´mez-Dı
´az,
Pe
´rez-Puig, Ortega-Ortiz, Heckel,
Urba
´n R., Viloria-Go
´mora and
Newsome. This is an open-access
article distributed under the terms of
the Creative Commons Attribution
License (CC BY). The use, distribution
or reproduction in other forums is
permitted, provided the original author
(s) and the copyright owner(s) are
credited and that the original
publication in this journal is cited, in
accordance with accepted academic
practice. No use, distribution or
reproduction is permitted which does
not comply with these terms.
TYPE Original Research
PUBLISHED 02 September 2022
DOI 10.3389/fmars.2022.944918
females, intra-specic competition among adult males, and inexperience in
locating prey in juveniles. We also describe baleen d
15
N patterns in recently
weaned whales (<16.5m) that reect switching from the consumption of milk to
solid food (krill). In addition, baleen d
13
C data suggest that weaned whales
continue to use stored nutrients (blubber) acquired during the nursing period
long after they are weaned. These results broaden our understanding of habitat
selection in this species, highlight the importance of nursing for the critical
period after weaning, and indicate that the Costa Rica Dome is an important
calving region for this endangered population.
KEYWORDS
blue whales, migratory strategies, feeding ecology, stable isotopes, baleen plates,
intraspecic competition, nutrient transfer, northeast Pacic ocean
Introduction
For many species, a single habitat does not provide enough
resources throughout the annual life cycle to survive and
reproduce (Dingle and Drake, 2007;Bauer et al., 2009;
Chapman et al., 2014). Migration, the periodic and directional
movement among different geographic areas, is a behavior that
evolved in a variety of invertebrate and vertebrate taxonomic
groups. It is a common ecological phenomenon that increases
the probability of survival and reproductive success because
animals can take advantage of seasonal pulses in resource
availability and/or utilize habitats that provide protection from
predators (Dingle and Drake, 2007;Bauer et al., 2009;Shaw and
Couzin, 2013;Chapman et al., 2014). Migration is often linked to
the reproduction strategies used by animals, which can be
generally divided into income breeding and capital breeding.
Income breeders continuously ingest nutrients throughout
migration for survival and reproduction, while capital breeders
use stored resources to reproduce (Jönsson, 1997;Langin et al.,
2006). While understanding the relationship between migratory
patterns and breeding strategies is a fundamental aspect of a
speciesecology, our ability to study animal migration and
habitat use has logistical limitations, including the high cost of
satellite tags to track individual movement and the low temporal
residency of tags on whale bodies, difculty of obtaining in situ
observations, and the lack of long-term databases that describe
inter-individual variability in migratory patterns. These
limitations are especially common in wide-ranging and cryptic
marine organisms.
Resources in marine pelagic ecosystems are generally
patchily distributed. In particular areas and seasons, however,
oceanographic conditions can generate consistent and reliable
primary production that is targeted by large aggregations of
consumers. Consequently, some income breeding species with
high energetic demands migrate long distances to access these
productive foraging areas. For example, the population of blue
whales (Balaenoptera musculus) in the northeast Pacic Ocean
migrates seasonally and feeds year round in highly productive
ecosystems like the California Current Ecosystem (summer-fall)
(Palacios et al., 2019;Rockwood et al., 2020), the Gulf of
California (winter-spring) (Gendron, 1992;Gendron, 2002;
Sears et al., 2013;Busquets-Vass et al., 2021), and the Costa
Rica Dome (winter-spring) (Mate et al., 1999) where seasonal
aggregations of their primary prey (euphausiids) occur in high
abundance (Gendron, 1992;Fiedler et al., 1998;Fiedler, 2002;
Croll et al., 2005;Lluch-Cota et al., 2007;Matteson, 2009). In
contrast to strict capital breeders that may fast for months on the
wintering/breeding grounds (i.e., southern right whales,
Eubalaena australis,Carroll et al., 2021), blue whales likely fast
for short periods of time while transiting between summer and
winter foraging grounds (Bailey et al., 2009). This strategy makes
blue whales particularly vulnerable to changes in resource
availability because of their high energetic requirements
(Acevedo-Gutierrez et al., 2002), and whales in poor body
condition are frequently observed during years characterized
by low primary productivity (Casillas-Lo
pez, 2016;
Wachtendonk et al., 2022). Studies that address individual
migratory and dietary strategies of this species are needed to
better understand habitat use, and how this varies among age
and sex categories, which in turn would provide information on
population dynamics that are critical to their management
and conservation.
Studying the migratory and dietary strategies of baleen
whales is challenging due to their wide range distribution and
long dive patterns, which limit observation. The development of
satellite tagging technology (Mate et al., 1999;Palacios et al.,
2019) and analysis of intrinsic biomarkers (Busquets-Vass et al.,
2017;Busquets-Vass et al., 2021) have emerged in response to
the growing need for data on migratory marine mammal
populations (Hobson, 1999;Newsome et al., 2010).
Blevins et al. 10.3389/fmars.2022.944918
Frontiers in Marine Science frontiersin.org02
Specically, the use of stable isotope analysis (SIA) has increased
exponentially in the past three decades to study the foraging
ecology (Bentaleb et al., 2011;Witteveen et al., 2012;Fleming
et al., 2016;Busquets-Vass et al., 2021), habitat use (Gendron
et al., 2001;Gaufer et al., 2020), migratory patterns (Lee et al.,
2005;Busquets-Vass et al., 2017), and physiology (Schell et al.,
1989;Busquets-Vass et al., 2017) of this elusive taxonomic
group. Several factors inuence variation in carbon (d
13
C) and
nitrogen (d
15
N) isotope values of animals, including: (1) spatial
and temporal variation in the isotopic composition of the base of
the food web can cascade up food chains to top consumers like
marine mammals; (2) physiologically-mediated isotopic
discrimination that occurs between a consumer and its diet;
and (3) physiological controls on isotopic incorporation and
growth rates for metabolically active and inactive tissues,
respectively. Metabolically active tissues record the diet
ingested from minutes/hours (CO
2
), weeks (blood), months
(skin, muscle) to years (bone collagen) (Hobson and Clark,
1993;Hobson, 1999;Newsome et al., 2010). In contrast,
metabolically inert but continuously growing tissues (e.g.,
whiskers, baleen) can be sub-sampled to create a longitudinal
ecological and eco-physiological record for a single individual
animal (Hobson and Schell, 1998;Hobson, 1999;Wunder, 2012;
Busquets-Vass et al., 2017).
In the northeast Pacic Ocean, blue whales generally use the
California Current Ecosystem (CCE) (Figure 1) in summer and
fall (Mate et al., 1999;Etnoyer et al., 2006;Calambokidis et al.,
2009a), which is considered the main foraging ground for this
population. Most whales migrate south to spend the winter and
spring in one of two regions: a well-described calving ground in
the Gulf of California (GC) (Gendron, 2002;Sears et al., 2013),
or the Costa Rica Dome (CRD) (Mate et al., 1999;Matteson,
2009), where calves have also been observed, but less is known
about this potentially important breeding area. These three
FIGURE 1
Map showing the twelve stranding locations (black dots) from which blue whale baleen plates were collected. Note that the exact stranding
location for whale F was not available, although it was conrmed that the stranding occurred somewhere in California, USA, in the 80s. The map
also shows the regions that blue whale typically visit in the northeast Pacic Ocean, including the California Current Ecosystem (CCE), Gulf of
California (GC), and Costa Rica Dome (CRD).
Blevins et al. 10.3389/fmars.2022.944918
Frontiers in Marine Science frontiersin.org03
ecosystems exhibit contrasting baseline d
15
N values, which are
recorded in blue whale tissues (i.e., skin and baleen) and their
primary prey (i.e., krill and lanternsh) found in these areas
(Busquets-Vass et al., 2017;Busquets-Vass et al., 2021). These
baseline differences have been used to assess blue whale
migratory strategies and quantify the relative importance of
prey from different regions to the diet of blue whales
(Busquets-Vass et al., 2017;Busquets-Vass et al., 2021). For
example, adult females migrated seasonally among ecosystems,
whereas some males remained within the CCE during at least the
~4 years represented in baleen records (Busquets-Vass et al.,
2017). Furthermore, mixing models based on isotope analysis of
skin and potential prey that most whales forage in the CCE, but
there are subgroups of whales that forego migration and remain
within the CRD or the GC for at least a year (Busquets-Vass
et al., 2021). Collectively, these studies provide strong evidence
that blue whales exhibit individual migratory and foraging
strategies that are likely sex- and age-specic. Further analysis
of serially sub-sampled baleen plates collected from different age
and sex categories could provide additional information on how
blue whales use different regions in the northeast Pacic Ocean,
which could help identify critical foraging and breeding grounds
for this endangered species (Cooke, 2018).
The aim of this study was to characterize the individual
migratory patterns and dietary strategies of blue whales of
different sex and age categories via d
13
Candd
15
Nanalysisof
sub-sampled baleen plates collected from thirteen stranded blue
whales in the northeast Pacic Ocean. We analyzed oscillations in
both isotope systems at seasonal and interannual scales, estimated
the isotopic niche size of each whale, and used mixing models to
quantify the relative contribution of different foraging regions to
each whales diet. Our results suggest that whales of different sex
and age classes generally showed different migratory strategies;
however, we found some degree of individual variation within
these categories. We also identied how d
13
Candd
15
Npatternsin
recently weaned blue whales provide insights into the critical
transition from the consumption of milk to solid foods, and show
that nutrients obtained during nursing are essential for the
survival of young whales long after they are weaned. Overall,
these results provide novel information on the ecology of this
endangered cetacean that can contribute to the further renement
of management plans.
Materials and methods
Sample collection
Baleen plates were collected directly from dead whales or
obtained from museums and stranding networks (Table 1) under
special permits issued by Mexican (Secretarı
a de Medio Ambiente
y Recursos Naturales-SEMARNAT) and U.S. (National Oceanic
and Atmospheric Administration-National Marine Fisheries
Service- NOAA/NMFS) government agencies. Samples were
transported via the Convention on International Trade in
Endangered Species of Wild Fauna and Flora (CITES) permits
(CITES import permit-19US774223/9 and export permit-
MX102653). A total of 13 baleen plates from 4 adult males, 3
adult females, 1 juvenile female, 1 juvenile male, 3 recently
weaned whales, one male of unknown age, but likely an adult,
were analyzed for this study. Whale L (Table 1) was submerged in
water when sampling occurred and the entire plate could not be
collected, so only a portion of the distal section of the plate was
available for analysis. These plates were collected over 33 years
(1985-2019) and represent the largest collection of baleen plates
from a single blue whale population in the world (Figure 1).
TABLE 1 Baleen plates collected from dead blue whales in the northeast Pacic Ocean.
Code Sex Length (m) Age Stranding Date Stranding Location Lat Long
AF 25.9 A 28/03/2007 Baja California Sur, MEX 25.3 -112.1
BF 22.3 A 19/10/2009 California, USA 39.4 -123.8
CF 24.3 A 25/05/2017 California, USA 37.9 -122.7
DM 20.7 A 23/06/1986 California, USA 36.3 -121.9
EM 26.5 A 03/09/1988 California, USA 37.7 -122.5
FM ND ND ND (~1980s) California, USA ND ND
GM 21.3 A 01/11/2015 Oregon, USA 42.5 -124.4
HM 22.2 A 05/02/2019 Sonora, MEX 29.2 -112.3
IF 19.5 J 23/06/2019 Baja California Sur, MEX 26.3 -112.5
JM 19.5 J 26/10/2016 California, USA 37.7 -122.5
KF 14.0 W 01/04/2013 Baja California Sur, MEX 26.7 -113.6
LM 16.0 W 23/04/2019 Colima, MEX 19.0 -104.3
MND 15.9 W 05/08/2016 Baja California, MEX 29.8 -114.3
Age categories include adult (A), juvenile (J), and recently weaned (W); ND denotes no data available.
Blevins et al. 10.3389/fmars.2022.944918
Frontiers in Marine Science frontiersin.org04
Sample preparation
Multiple adjacent plates were collected from each individual
and a knife was used to cut through the soft tissue that binds
them together. Soft tissue was scraped from the top of each plate
using a scalpel or removed by hand. To remove surface
contaminants, baleen plates were rinsed with a 2:1 chloroform
methanol solvent solution. Plates were then dried and covered in
aluminum foil to avoid contamination before sub-sampling for
stable isotope analysis.
Baleen plates are comprised of keratin, a metabolically inert
tissue that continuously grows transversally and can be sub-
sampled to create a longitudinal ecological and eco-physiological
record of each whale over the course of ~4-5 years prior to death,
depending on the baleen length. A previous study estimated the
mean ( ± SD) growth rate of baleen for eastern Pacic blue
whales to be 15.5 ± 2.2 cm yr
-1
(Busquets-Vass et al., 2017), and
similar values have been estimated for North Atlantic blue
whales (~13.5 cm yr
-1
;Trueman et al., 2019). Baleen plates
were sub-sectioned into ~1 cm intervals using a measuring tape
positioned along the outer edge of each plate. Samples of keratin
powder were collected from each centimeter using a Dremel
rotary drill on the outer edge of the plate. This sampling strategy
integrates the cortex and the medulla of the baleen (Rita et al.,
2019) into a single integrated sample and follows the
methodology previously used for sampling blue whale baleen
plates (Busquets-Vass et al., 2017). We started at the proximal
edge that was embedded in the whale´s gum, which represents
the most recently synthesized tissue. Due to the uniform growth
of baleen, this sampling strategy yielded samples that
approximately represent equal time intervals (Busquets-Vass
et al., 2017). Plates and equipment were cleaned between
collection of each sub-sample with ethanol. Each powdered
sub-sample was stored in sterilized and labeled plastic
microcentrifuge tubes. Previous studies have shown that
adjacent baleen plates in gray whales (Eschrichtius robustus;
Caraveo-Patiño and Soto, 2005) and plates from opposing
sides of the mouth in bowhead whales (Balaena mysticetus;
Schell et al., 1989) exhibit consistent isotope values, therefore we
assumed that each baleen plate yields a reliable multi-year record
of the foraging history of each blue whale. Moreover, the growth
rate of baleen located in different sections of the rack (ltering
apparatus) of Balaenopterids is constant, thus we assumed the
isotope values of baleen plates collected from different sections of
the rack are comparable (Garcı
a-Vernet et al., 2018;Aguilar and
Borrell, 2021).
Stable isotope analysis
Approximately 0.50.6 mg of each baleen sub-sample was
weighed into tin capsules. Carbon (d
13
C) and nitrogen (d
15
N)
isotope values were measured with a Costech 4010 elemental
analyzer (Valencia, CA) coupled to Delta V Plus isotope ratio
mass spectrometer (Bremen, Germany) at the University of New
Mexico Center for Stable Isotopes (Albuquerque, NM). Isotope
data are reported as delta (d) values, which are calculated with
the formula: d
13
Cord
15
N = 1000 [(Rsample/Rstandard)1],
where R =
13
C/
12
Cor
15
N/
14
N ratio of sample and standard.
Values are in units of parts per thousand, or per mil (). The
internationally accepted standards are Vienna-Pee Dee
Belemnite limestone (V-PDB) for d
13
C and atmospheric N
2
for d
15
N. Within-run analytical precision (SD) was estimated via
analysis of two proteinaceous internal reference materials, which
was ±0.2for both d
13
C and d
15
N. We also measured the
weight percent carbon and nitrogen concentration of each
sample and used the C/N ratio as a proxy of sample
macromolecular composition (Logan et al., 2008). We
analyzed isotope values of seven baleen plates (Table 1:CM)
and used published values from Busquets-Vass et al. (2017) for
six whales (Table 1:A,B,DG). To organize the entire collection
of baleen plates by age class, the letter codes used by Busquets-
Vass et al. (2017) were modied to complement the larger
dataset reported here.
Analysis of temporal oscillations in
isotope values of adult and
juvenile whales
Temporal variation in isotope values along baleen plates was
evaluated by estimating interannual and seasonal Bayesian
random effects on each time series of d
13
C (Suess Corrected
d
13
C, see section below) or d
15
N using an integrated nested
Laplace approximation (INLA; Rue et al., 2009) with the package
R-INLA for the R language (R Core Team, 2021). The
longitudinal nature of the data, and therefore the lack of
independency between consecutive values, was acknowledged
by introducing a random walk effect (RW) of the Julian day as
the main process (Rue and Held, 2005;Gomez-Rubio, 2020). We
tested for rst and second order random walks and chose the one
with lowest Watanabe-Akaike Information Criterion (WAIC;
Rue and Held, 2005;Gomez-Rubio, 2020). The default precision
of the intercept was set to the analytical precision of d
13
Cord
15
N
measurements (SD = 0.2). The aim of this analysis was to
characterize the temporal trends in each isotope system,
separating the interannual and the seasonal signals, which
would show the migration consistency and amplitude between
contrasting foraging regions. A higher hyper-standard deviation
(HSD) of the random effects would mean a stronger effect of that
scale on that animal, and that such temporal scale explains a
high proportion of the variability (Rue and Held, 2005;Rue et al.,
2009;Gomez-Rubio, 2020). In this case, HSD values would be
comparable only between whales within the same isotope system
and in the same temporal scale. The latter condition is because
the seasonal and interannual scales are independent signals and
Blevins et al. 10.3389/fmars.2022.944918
Frontiers in Marine Science frontiersin.org05
therefore, it is possible that an animal has a strong consistent
seasonal variation, but very low interannual variation, and
vice versa.
For tting these models, the length (cm) of each baleen plate
was converted into a temporal axis by using the date of stranding
as the initial reference to infer the specic months and years
contained in each plate. We used the available estimation of blue
whale baleen growth rate (15.5 ± 2.2 cm y
-1
;Busquets-Vass et al.,
2017) and converted each sequential sampling point into a Julian
day. We tted the interannual and seasonal models only for
adult and juvenile whales with stranding date information (nine
baleen plates total). We did not have stranding information for
whale F, which exhibited isotopic oscillations that were like those
of adult males (see Results), thus we assume this animal was an
adult male. Therefore, for whale F, we could only estimate the
number of years represented by the baleen plate, but not
specic dates.
Spatial baseline gradients among the ecosystems that blue
whales use in the northeast Pacic have been reviewed in
previous papers and show that the GC has higher d
15
N values
(14.416.9) than the CCE (11.912.9), while the CRD (9.2
11.4) has the lowest baseline d
15
N values of the three regions
(Williams et al., 2014;Busquets-Vass et al., 2017;Busquets-Vass
et al., 2021). We used published prey isotope data to assign
sections of each baleen plate to a specic foraging region,
corrected for trophic discrimination (see Materials and
Methods:Isotope Mixing Models), and estimate the expected
isotope values of baleen if the tissue was isotopically equilibrated
to each foraging region (Busquets-Vass et al., 2017;Busquets-
Vass et al., 2021). This was only possible for d
15
N data because of
the extensive overlap in d
13
C values of potential prey among
regions (Busquets-Vass et al., 2017;Busquets-Vass et al., 2021).
We used previously published d
15
N data of all recognized
primary prey for blue whales from each foraging region
(Busquets-Vass et al., 2017;Busquets-Vass et al., 2021). Blue
whale diets have been described in the northeast Pacicvia in
situobservations and analysis of fecal samples collected in the
GC, CCE, and CRD. In the CCE, blue whales primarily feed on
dense aggregations of two temperate krill species (Thysanoessa
spinifera and Euphausia pacica)(Fiedler et al., 1998;Croll et al.,
2005;Nickels et al., 2018). In the GC, blue whales feed on a
combination of dense aggregations of the subtropical krill
(Nyctiphanes simplex)(Gendron, 1992;Del Angel-Rodrı
guez,
1997) and lanternsh (Family: Myctophidae) (Jimenez-Pinedo,
2010), whereas in the CRD whales have been observed feeding
on krill of unknown species (Matteson, 2009).
To characterize the migratory strategies of blue whales, we
assumed that the spatial gradients in potential blue whale prey
among foraging regions were relatively stable through time. This
assumption has been addressed in previous papers (Busquets-
Vass et al., 2017;Busquets-Vass et al., 2021). Briey, blue whale
prey isotope values in the CCE are consistent between sites
(Monterey Bay, Northern California Current, British Columbia)
and across decades (1994, 2000-2001, 2013) (Sydeman et al.,
1997;Miller, 2006;Becker et al., 2007;Hipfner et al., 2010;Carle,
2014). Previous work has also shown that zooplankton d
15
N
values in the CCE are consistent over decadal scales (Rau et al.,
2003). In the GC, there are marked latitudinal baseline gradients
in d
15
N north and south of Midriff Islands (Dı
az-Gamboa et al.,
2018), which produces a large range in krill d
15
Nvalues
(Busquets-Vass et al., 2017;Busquets-Vass et al., 2021). In
addition, the opportunistic consumption of lanternsh also
results in higher values in blue whale tissues in this region
compared to the CCE and CRD. Therefore, baleen d
15
N values
as low as ~14and as high as ~17indicate foraging within
the GC (Figure 2). Krill collected in the CRD have lower d
15
N
values compared to the GC and CCE (Williams, 2013;Williams
et al., 2014), and d
15
N data from blue whale individuals that
forage in this region are consistently lower in comparison to
whales that forage in the GC and CCE (Busquets-Vass et al.,
2017;Busquets-Vass et al., 2021).
Suess effect corrections
We used the SuessR package for R language to correct baleen
d
13
C values for the Suess Effect (Clark et al., 2021). This package
was designed specically for regional Suess Effect corrections for
marine organisms. Blue whales in the northeast Pacicare
distributed as far north as the Gulf of Alaska (Calambokidis
et al., 2009a), therefore we selected the corrections for this region
and assumed they remained constant at lower latitudes. For
adult whales of known stranding date, we used the sequential
Julian day calculated for modeling purposes; see Analysis of
Temporal Oscillations in Isotope Values of Adult and Juvenile
Whales in the Materials and Methods section. For whale F, we
did not know the exact stranding date, but this individual died in
the 1980s, so we used the mean Suess effect corrections applied
to whales D and E that died in the same decade. In the case of
recently weaned whales, we only had information on stranding
year, which ranged from 20132019, so we used a mean
correction of 1.1based on the SuessR package corrections
for each stranding year. All temporal models and statistical
analysis used Suess corrected baleen d
13
C values.
Nursing period versus weaning period in
weaned whales
Whales K, L, and M were identied as recently weaned
animals since they were less than 16.5 m in total length
(Table 1). We identied a steep decrease in d
15
N located after
the oldest section of the baleen plates, likely reecting the
weaning period (Hobson and Schell, 1998;Caraveo-Patiño
et al., 2007;Lysiak, 2009). Baleen growth rates decrease with
age in gray whales (Sumich, 2001) and southern right whales
Blevins et al. 10.3389/fmars.2022.944918
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(Best and Schell, 1996). In the case of blue whales, there are no
estimates of baleen growth rates for young animals, therefore we
were unable to estimate the temporal resolution contained within
the baleen of this age group. Instead, we analyzed the oscillations
along the baleen in reference to length in centimeters, where zero
represents the section of the baleen plate that was embedded in
the gum and represents the most recently formed tissue. We
estimated the magnitude of the decrease in nitrogen isotope
values associated with weaning by comparing the posterior
means of d
15
Nvaluesinthesectionofthebaleenbefore
(potential nursing period) and after the steep decrease (weaning
section) (see Results) with a one-way Bayesian analysis of
variance (ANOVA
B
)(Kery, 2010).
Comparison of sex and age classes
Global isotopic variation among sex and age classes was
evaluated by comparing mean Suess corrected d
13
C and d
15
N
values with ANOVA
B
for each isotope system separately. Age
class categorization of adult and juvenile whales was based on
the total length compiled from stranding records, while the
recently weaned category was identied using both the length of
the whale and the presence of the d
15
N patterns described above.
We excluded whale F as no age class data were available for this
individual. The analysis estimates the posterior distributions of
each sex and age class means from normal likelihoods. We then
estimated the posterior distributions of the differences between
all possible sex and age group pairs. From those posteriors, we
estimated the proportion of iterations below and above zero and
the highest of those two values represents the probability that a
given age class pair is different (Gelman et al., 2014).
Isotopic niche estimates
The isotopic niche width of each individual whale was
estimated via standard ellipse areas (SEA in
2
units) that
BC
DE F
GHI
J
A
FIGURE 2
Interannual random effects on d
15
N values along nine individual blue whale baleen plates as a function of time. The hyper-standard deviation
(HSD) of the random-effect likelihoods is reported for each whale. Colors represent females (red), and males (blue). Colored dots and lines are
the medians of the random effects, and colored shaded areas are the 95%-credible intervals. Gray shading represents the expected d
15
N values
of baleen of blue whales foraging in the Gulf of California (GC), California Current Ecosystem (CCE), and the Costa Rica Dome (CRD). Figure
shows whales (AJ). HSD could not be estimated for whale (F) given the lack of information on stranding date, so the temporal scale
corresponds to the number of years reected in the baleen record.
Blevins et al. 10.3389/fmars.2022.944918
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contained 95% of the data using the SIBER package for R
language (Jackson et al., 2011). SEA were estimated using the
Suess corrected d
13
C and d
15
N covariance matrix. For inter-
individual comparisons, we estimated the Bayesian SEA (SEA
B
)
tted using Bayesian approximations within SIBER, and we also
determined the percent overlap among ellipses of
different whales.
Isotope mixing models
Foraging strategies of each individual blue whale were
characterized using isotope mixing models based on d
15
N data
and analyzed in a Bayesian framework with the package
MixSIAR for R language (Stock and Semmens, 2018). Suess
corrected d
13
C data were not used because of lack of differences
in the carbon isotope composition of potential prey (Busquets-
Vass et al., 2021). We excluded the nursing period from the
model for recently weaned whales K, L, and M (see Results). The
variables used in the mixing models included: d
15
N of the baleen
plates from each individual whale, prey d
15
N from previously
published literature (Busquets-Vass et al., 2017;Busquets-Vass
et al., 2021), and mean ( ± SD) d
15
N trophic (tissue-diet)
discrimination factor (D
15
N) previously estimated to be 1.8 ±
0.3for blue whales (Busquets-Vass et al., 2017). Model
parameters had non-informative priors and posterior
distributions were generated with a Markov Chain Monte-
Carlo (MCMC) set as follows: chains = 5, chain length =
1,000,000 iterations, burn-in phase = 300,000 iterations,
thinning = one iteration retained each 50. The error structure
chosen for all models (process multiplied by residual error) was
selected based on analysis by Stock and Semmens (2016). For
model selection, we compared six different model structures
using Watanabe-Akaike Information Criterion (WAIC) and
Leave-One-Out (LOO) Cross-Validation Information
Criterion. Models with low LOO values have a better t while
theAkaikeWeightsbasedonWAICscoresindicatethe
probability of the model given the data (Burnham et al., 2002;
Stock and Semmens, 2016). Model structure was set as follows:
(1) null model in which no factors were evaluated, (2) individual
whale set as xed effect, (3) sex and/or age set as a xed effect, (4)
individual whale set as a random effect, (5) sex and/or age class
set as a random effect, and (6) individual whale set as a random
effect and sex and/or age nested into individual whale.
Results
Temporal trends in baleen Suess
corrected d
13
C and d
15
N
The interannual and seasonal random effects in d
15
N along
baleen plates showed variability between whales of different sex
and age classes (Figures 2,3) based on HSD values. Adult female
A exhibited the highest interannual (12.3) and seasonal (2.3)
HSD, and the oscillations in d
15
N along its baleen suggest
this whale visited all three regions, GC, CCE, and CRD
(Figures 2A,3A). Interannually, this whale showed a
consistent decline in d
15
N between 2003 and 2007, suggesting
a gradual increasing tendency to use the CRD (Figure 2A).
Interestingly, the seasonal d
15
N peak occurred typically during
early boreal summer, suggesting this individual was visiting the
GC mostly during summer (Figure 3A). Adult male H had the
second highest interannual and seasonal HSD, however, this
whale only visited the GC and CCE in a seasonal pattern
(Figure 2H). The seasonal peak in d
15
N occurred in December
and January, indicating that this whale visited the GC mainly
during the boreal winter (Figure 3H). Adult females B and C had
intermediate interannual and seasonal HSD (Figures 2B,C,3B,
C). Adult female B typically visited the CCE and CRD in a
relatively consistent seasonal pattern (Figure 2B), whereas
female C used all three regions in a less predictable pattern
(Figure 2C). Adult whale B exhibited lower d
15
N values during
September and October, indicating that this whale typically
visited the CRD during these months (Figure 3B). Female C
had lower values in January and July (Figure 3C), suggesting this
whale did not follow consistent seasonal migratory patterns, and
thus visited the CRD in different months (Figure 2C). It is
important to note that adult females A and B skipped migration
during 20032004 and 20082009, respectively (Figures 2A,B).
Adult males D and E had intermediate interannual HDS and
the lowest seasonal HSD (Figures 2D,E,3D,E). d
15
N values
along the baleen of these males were surprisingly consistent and
remained within a 1range, indicating both males remained
within the CCE during 34 years prior to death (Figures 3D,E).
For male whale F (unknown stranding date), we were unable to
run the interannual and seasonal models, however, this whale
showed near identical patterns to adult males D and E
(Figure 2F). Adult whale G exhibited intermediate interannual
HSD and relatively high seasonal HSD (Figures 2G,3G). The
patterns in d
15
N indicate this whale migrated at least twice to the
CRD, and typically remained within the CCE (Figure 2G). The
seasonally lower d
15
N values occurred in February and March,
suggesting that this whale visited the CRD during the boreal
winter (Figure 3G). Juvenile whales migrated among foraging
regions, but no clear patterns were observed (Figures 2I,J), and
they exhibited intermediate interannual and seasonal HSD in
comparison to the adult whales (Figures 2I,J,3I,J). The juvenile
female I remained several months in the CCE (2016-2017) and
in the CRD (2018-2019) (Figure 2I), whereas Juvenile male J
remained mostly within the GC (Figure 2J).
Although less pronounced or consistent, Suess corrected
d
13
C values also exhibited some temporal variation among
individuals, both interannually and seasonally (Figures 4,5)
which in general matched those of d
15
N(Figures 2,3), but
with lower variation in the values. The ranges in Suess corrected
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d
13
C values observed in whales that moved among different
foraging regions (Figures 4AC,G,H), overlapped with those
of the whales that remained in the CCE (Figures 4DF) based
on oscillations (or lack thereof) in d
15
N(Figure 2). In
comparison to adults, juvenile and recently weaned whales had
lower Suess corrected d
13
C values (Figures 4,6) (see Results,
Ontogenetic Comparisons).
Nursing and weaning comparisons
The baleen record from the three recently weaned whales
exhibited a marked decrease in d
15
Nvalues(Figures 6KM), that
we identied as the weaning period, when they switched from
nursing to active foraging (Hobson and Schell, 1998;Caraveo-
Patiño et al., 2007;Lysiak, 2009). As such, we dened the nursing
period as the section of the baleen plate formed before the
observed decrease in d
15
Nvalues(Figures 6KM). During
weaning, all three whales showed a decrease in d
15
N indicating
they were actively feeding on prey in the CRD (Figures 6KM).
Once weaned, whale K migrated to the CCE (Figure 6K), whale M
moved to the CCE and then entered the GC ~2-3 months before
death (Figure 6M), and whale L stayed several months in the CRD
(Figure 6L). It is important to note that for whale L we only had a
portion of the oldest section of the baleen plate (see Materials and
Methods), and therefore lacked isotopic data reecting the
northward migration into the southwestern Mexican coast
where the whale was struck and killed by a cargo ship.
The nursing period was characterized by higher estimates of
d
15
N posterior means (Mean = 12.4;CredibleIntervals:2.5%=
12.3, 97.5% = 12.6) compared to the post-weaning period
(Mean = 11.3, Credible Intervals: 2.5% = 11.2, 97.5% =
11.4). The posterior mean estimate of the difference in d
15
N
values between the nursing and post-weaning periods was 1.1
(Credible Intervals: 2.5% = 0.8, 97.5% = 1.3)with100%
probability of being higher during the nursing period. Suess
corrected d
13
C values also varied along the baleen of recently
weaned whales (Figure 6). All recently weaned whales showed
consistently low Suess corrected d
13
Cvaluesthatremainedwithina
~1range along the entire baleen record prior to death (Figure 6).
BC
DE F
GH I
J
A
FIGURE 3
Seasonal random effects on d
15
N values along nine individual blue whale baleen plates as a function of time. The hyper-standard deviation (HSD)
of the random-effect likelihoods is reported for each whale. Colors represent females (red), and males (blue). Colored dots and lines are the
medians of the random effects, and colored shaded areas are the 95%-credible intervals. Figure shows whales (AJ). This analysis was not
possible for whale (F) given the lack of information on stranding date.
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Ontogenetic comparisons
The posterior mean estimates of d
15
N and Suess corrected
d
13
C for each baleen plate and the posterior estimations of the
difference in d
15
N and Suess corrected d
13
C among baleen plates
from different age classes in the northeast Pacic are shown in
Supplementary Table 1 and Supplementary Table 2.The
probabilities of difference in mean d
15
N values between whales
from different sex and age classes was 82% to 100%, but
differences only ranged from 0.1to 0.8(Supplementary
Table 2). For d
15
N, the largest contrast was between juveniles
and recently weaned whales, with the former having a higher
posterior mean (13.0; range: 12.7 to 13.3) compared to the
latter (12.2; range: 12.0 to 12.4). For Suess corrected d
13
C,
adult females and males had values that were 0.6 to 1.4higher
than juveniles and recently weaned whales, with a probability of
difference of 100(Supplementary Table 1,Supplementary
Table 2). Juvenile whales also had Suess corrected d
13
C values
that were 0.8higher than recently weaned whales
(Supplementary Table 1,Supplementary Table 2). Adult
females and males had similar Suess corrected d
13
C and d
15
N
values that only differed by 0.1for both isotope systems
(Supplementary Table 2).
Isotopic niche
Isotopic niche widths among the thirteen blue whales ranged
from 1.2
2
to 11.1
2
(Supplementary Table 3;Figure 7).
Juveniles whale I (11.1
2
,Figure 7I) and juvenile whale J
(9.0
2,
Figure 7J) had the largest isotopic niches. Three adult
males, whales D, E and G, and weaned whale K (2.3
2
,
Figure 7D;2.1
2
,Figure 7E;3.3
2
,Figure 7G;1.2
2
,
Figure 7K) had smaller isotopic niches. Whale F had the
smallest isotopic niche (2.0
2
,Figure 7F), the age of this
whale was unknown, but isotopic data suggests this whale was
an adult. Three adult whales, A, C, and H (Figures 7A,C,H),
that migrated among all three foraging regions had similar
BC
DEF
GH
I
J
A
FIGURE 4
Interannual random effects on Suess corrected d
13
C values along nine individual blue whale baleen plates as a function of time. The hyper-
standard deviation (HSD) of the random-effect likelihoods is reported for each whale. Colors represent females (red), and males (blue). Colored
dots and lines are the medians of the random effects, and colored shaded areas are the 95%-credible intervals. Figure shows whales (AJ). HSD
could not be estimated for whale (F) given the lack of information on stranding date, so the temporal scale corresponds to the number of years
reected in the baleen record.
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isotopic niche widths (~7.0
2
). Female adult whale B
(Figure 7B), that migrated mainly between the CCE and CRD,
had intermediate isotopic niche width (4.0
2
). Lastly, weaned
whales L and M also exhibited intermediate isotopic niche width
(Figures 7L,M). The overlap among the isotopic niche width of
individual whales varied from 0% to 100% (Supplementary
Table 4). The isotopic niche of recently weaned whale K only
overlapped with whale C (Figures 7K,C;Supplementary
Table 4), whale J (Figure 7;Supplementary Table 4) and with
recently weaned whales L and M (Figures 7L,M;Supplementary
Table 4). It is important to recognize that the degree of overlap
among the isotopic niches of different individuals was driven by
variations in Suess corrected d
13
C (not d
15
N).
Dietary isotopic mixing models
The model with the lowest LOOic and highest probability of
prediction was Model 4 (Supplementary Table 5), which had
whale ID set as a random effect. The second-best model was
Model 6 with whale ID set as a random effect and sex and/or age
nested into whale ID (Supplementary Table 5). The posterior
estimates of the relative contribution of the three foraging
regions (GC, CCE, CRD) to the diet of the thirteen different
blue whales using Model 4, and to the different sex/age classes
using Model 6, are shown in Supplementary Tables 6,7as well as
Figure 7 and Supplementary Figure 1. A common trend
observed in Model 4 and Model 6 was the consistent
intermediate to high dietary contribution of prey from the
CRD to the diets of adult females (~3150%), juveniles (~37
67%), and recently weaned whales (~2653%). In contrast, the
contribution of CRD prey was negligible (48%) for adult males
D, E, F, and G (Supplementary Table 6;Figure 8), and only 17%
when data for all males was combined (Supplementary Table 7,
Supplementary Figure 1). Dietary contributions of prey from the
CCE varied among whales of different sex and/or age categories
(Supplementary Table 7,Supplementary Figure 1). The highest
contributions from the CCE were observed in adult males D, E,
BC
DE F
GH I
J
A
FIGURE 5
Seasonal random effects on Suess corrected d
13
C along nine individual blue whale baleen plates as a function of time. The hyper-standard
deviation (HSD) of the random-effect likelihoods is reported for each whale. Colors represent females (red), and males (blue). Colored dots and
lines are the medians of the random effects, and colored shaded areas are the 95%-credible intervals. Figure shows whales (AJ). HSD could
not be estimated for whale (F) given the lack of information on stranding date, so the temporal scale corresponds to the number of years
reected in the baleen record.
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F, G (8994%) and recently weaned whale K (70%)
(Supplementary Table 6;Figure 8). Intermediate contributions
of prey from the CCE were observed in whales B, C, and L (40
50%) (Supplementary Table 6;Figures 8B,C,L), and the lowest
contributions (415%) in whales A, H, I, J, and M
(Supplementary Table 6;Figure 8). Prey from the GC
provided intermediate to high contributions to the diets of
whales A, C, H, J, and M (2559%), and low to negligible
contributions to the diets of whales B, D, E, F, G, K, L (3
11%) (Supplementary Table 6;Figure 8).
Discussion
Age-sex specic migratory and
foraging strategies
Our results suggest that blue whale migratory strategies vary
by sex and age, a nding supported by other lines of evidence
including sex ratios and photographic identications in the GC
as well as acoustic data (Stafford et al., 2001;Gendron, 2002;
Oleson et al., 2007a;Costa-Urrutia et al., 2013;Ugalde de la
Cruz, 2015). We found that adult females potentially migrate
among different foraging regions in a relatively stable
interannual and seasonal pattern (Figures 2A,B), with some
degree of inter-individual variation in the regions they use
during migration (Figure 2C). For example, mixing models
showed that female adult whale C foraged in all regions,
whereas female adult whale A foraged in the GC and CRD,
and whale B foraged predominantly in the CCE and CRD
(Supplementary Table 6;Figures 8AC). These ndings are in
agreement with the high year-to-year site delity of some adult
females but rare sightings of other females in the GC (Gendron,
2002;Ugalde de la Cruz, 2015), which indicates inter-individual
variation in the use of wintering grounds.
Inter-individual variation in seasonal migratory patterns can
increase habitat partitioning among adult females, thus
decreasing intraspecic competition for resources during
periods of high energetic demand associated with reproduction
(pregnancy and nursing). Such seasonal competition for
resources likely inuences differential use of the two
alternative wintering regions, GC or CRD, which can be used
FIGURE 6
d
15
N and Suess corrected d
13
C oscillations along the baleen plates of recently weaned whales. Colors indicate likely periods of potential nursing
(purple), weaning (orange), and active foraging/weaned (green). Figure shows whales K, L and M.
Blevins et al. 10.3389/fmars.2022.944918
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also during the summer (adult female A, Figure 3A). This type of
behavior has also been observed in other migratory mammals.
For example, population size in caribou (Rangifer tarandus) was
a determinant for wintering area selection in two different herds
that undertook long-distance migrations, indicating that
intraspecic competition is a signicant driver of migratory
plasticity in mammals (Le Corre et al., 2020). Another factor
that may play an important role in interannual variation of
migratory patterns is seasonal prey availability within specic
regions. Acoustic data (i.e., local onset and cessation of blue
whale calls) show that blue whales adjust their arrival and
departure in the CCE in response to krill abundance
(Szesciorka et al., 2020), that in turn is directly affected by
climate variability.
An interesting pattern in two adult females (A and B) was
the evidence that these individuals skipped seasonal migration.
Whale A skipped migration in 2003-04 and remained within the
GC, while Whale B skipped migration in 2008-09 and remained
within CCE (Figures 2A,B). A plausible explanation for this
irregular movement pattern is that there were enough resources
in these ecosystems to support adult females for several months.
Interestingly, both Female A and B migrated to the CRD
(Figures 2A,B) after skipping migration, perhaps to give birth.
Calves have been observed in the CRD (Calambokidis et al.,
2009b;Hoyt, 2009), and while it is not currently known how
important this region is for reproduction, our results support the
hypothesis that the CRD is a commonly used calving ground like
the GC (Gendron, 2002;Sears et al., 2013). These results are
supported by studies that described partial migration in
humpback whales (Megaptera novaeangliae;Brown et al.,
1995) and North Atlantic right whales (Eubalaena glacialis;
Gowan et al., 2019), showing that some females may skip
migration because of the high energetic costs associated with
reproduction. Partial migration has also been described in n
BC D
EFGH
IJ KL
M
A
FIGURE 7
Isotopic niche width (solid lines-SEA
2
) of blue whales in the northeast Pacic. d
13
C values were Suess corrected for isotopic niche estimations.
Color indicates sex of the whale: females (red), blue (males), and sex not identied (green); posterior mean estimates of SEA
B
(
2
) are reported
for each whale in the top-left of the panels. Figure shows whales (AM).
Blevins et al. 10.3389/fmars.2022.944918
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whales (Balaenoptera physalus) near Svalbard, Norway. Out of
25 tagged n whales, 10 remained within the tagging region and
15 migrated southwards. Although the sex of the n whales was
not reported, that study noted that southward movements of
some whales could be a consequence of body condition, sex,
resource availability during migration, and breeding condition
(Lydersen et al., 2020).
Adult males exhibited different migratory strategies in
comparison to adult females. Two conrmed adult males (D
and E) and one male (F) of unknown age, but most likely an
adult based on similarity in d
15
N patterns to the other two adult
males, remained within the CCE for at least 3-4 years before
death (Figure 2). Male G remained mostly within the CCE but
migrated twice to the CRD (Figure 2G), whereas whale H
migrated annually among CCE and GC. Mixing models
showed that the resources in the CCE made the largest
contribution (8994%) to the diet of most males, except male
H that had a higher contribution from the GC (49%)
(Supplementary Table 6,Figure 8). Busquets-Vass et al. (2017)
proposed that male blue whales in the eastern Pacic Ocean may
use two distinct migratory strategies, but the potential drivers of
these two strategies were not evaluated. The addition of data for
more individuals reported here suggests that a combination of
energetic requirements and intraspecic competition may
explain individual variation in migratory strategies among
males. Migrating to warmer waters can be energetically
challenging for blue whales, as calculations of their lower
critical temperatures show that they invest substantially more
energy dissipating heat in warmer (i.e., CRD/GC) versus colder
(i.e., CCE) waters (Lavigne et al., 1990). Intraspecic
BCD
EFGH
IJ K L
M
A
FIGURE 8
Standardized posterior probabilities of the relative contribution of prey sources from the California Current Ecosystem (CCE), Gulf of California
(GC), and Costa Rica Dome (CRD) to blue whales in the northeast Pacic Ocean. Each plot shows the mean (black dot), median (white square)
and shaded boxes represent the 50%, 75% and 95% and 95% credible intervals from dark to light blue. Figure shows whales A-M.
Blevins et al. 10.3389/fmars.2022.944918
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competition to remain within the CCE could result in larger
(older) males outcompeting smaller (younger) males, which
migrate longer distances and possibly follow adult females to
the wintering grounds in the GC or CRD. This scenario could be
benecial for younger males by increasing the probability of
mating on the wintering grounds. Whale trios consisting of one
female and two males have been observed in the CCE and this
association may indicate reproductive behavior (Schall et al.,
2020). Remarkably, courtship behavior has been observed in the
Loreto Bay National Park and near the Midriff Islands within the
GC in spring (i.e., April) (Gendron pers. comm.; Perez-Puig
pers. comm.). While songs that may be associated with
reproduction are produced by blue whales year-round,
suggesting blue whale mating can occur opportunistically any
time of the year (Stafford et al., 2001;Oleson et al., 2007a;Oleson
et al., 2007b;Schall et al., 2020), the most common mating
season is summer and autumn based on the mating activity
reported in the CCE (Calambokidis et al., 2007;Schall et al.,
2020) and the common observations of calves during the winter
and spring within the GC (Gendron, 2002;Sears et al., 2013).
As mentioned above, climate variability likely impacts whale
migration and distribution. During El Niño Southern Oscillation
(ENSO) events, blue whale population density in the northeast
Pacic Ocean decreases in equatorial areas and the distribution of
whales retracts to more northern waters in the central CCE, the
GC, and north of the Equatorial Countercurrent thermocline
ridge (Pardo et al., 2015). Whales DFstrandedinthe1980s,a
decade that included one of the most severe El Niño Southern
Oscillation (ENSO) events in 19821983. The impact of this
ENSO event, however, was not consistent throughout the
eastern Pacic Ocean. For example, phytoplankton biomass in
the GC did not decline during the 19821983 ENSO (Santamarı
a
del A
ngel et al., 1994), and observations of large aggregations of
cetaceans and seabirds were recorded in the Canal de Ballenas in
the northern GC (Tershy et al., 1991). Assuming productivity
decreased in the CCE during this ENSO event, we would expect
Whales DF to migrate to the GC during the winter, but these
males remained within the CCE. Baleen plates from
contemporaneous adult females are not available, however,
photographic data collected from 1970-2011 in the CCE
(summer-fall) and GC (winter-spring) shows that adult females
are twice as common as adult males (F:M sex ratio 1.8:1.0) during
the peak of the seasonal migration (Gendron, 2002;Costa-Urrutia
et al., 2013;Ugalde de la Cruz, 2015), indicating that migrationis a
more common behavior in females than males. In addition,
acoustic data show year-round detections of vocalizations (or
calls) (Stafford et al., 2001) produced exclusively by males (Oleson
et al., 2007a;Oleson et al., 2007b), which also supports the
hypothesis that males and females potentially use different
movement strategies, and that males may remain in specic
regions for several years without migrating.
Like adult females, juvenile and recently weaned whales also
showed plastic migratory patterns based on measured isotope
values (Figure 2) and mixing models (Figure 7). A common
pattern for these age categories was to remain within the same
region for several months or years (Figures 2I,J), which might
result from inexperience as younger whales must learn
behavioral skills from migratory adults (likely females) to
locate prey. This explanation is supported by previous work
showing that blue whales rely on memory of long-term average
conditions to migrate to specic regions in the northeast Pacic
Ocean (Abrahms et al., 2019), and this would imply that young
whales must learn to follow adults or gradually memorize the
locations of seasonal krill aggregations.
Patterns in isotopic niches of blue whales (Supplementary
Table 3,Supplementary Table 4,Figure 7) further support our
inferences of their migratory and feeding strategies based on
baleen d
15
N. Adult females A and C, adult male H, and both
juveniles exhibited the largest isotopic niches, reecting
movement among different regions in the northeast Pacic
Ocean. The other three adult males, female B, and all recently
weaned whales had the narrowest isotopic niche, likely due to
more restricted movements and feeding within a single region.
Our results also show that signicant latitudinal variation in
baseline d
15
N values across the GC may allow for the
identication of foraging in the northern versus southern areas
of this region. The northern region of the GC located at ~28
latitude has a d
15
N baseline ~2higher than the southern
region (Dı
az-Gamboa et al., 2018). Blue whales typically use the
southern region of the GC (Gendron, 2002), however, whales H
(adult male) and M (recently weaned whale) stranded in the
northern region and the last few subsamples of baleen in both
individuals deposited prior to death had anomalously high d
15
N
values (Figure 2). This baseline gradient in the GC results in a
large range of nearly 3in krill d
15
N values (12.6to 15.4)
across this region (Busquets-Vass et al., 2017;Busquets-Vass
et al., 2021). After application of an appropriate trophic
discrimination factor, baleen d
15
N values as low as 14and
as high as 17likely represents foraging in the GC. These south
to north gradients in d
15
N might be useful to detect small-scale
movement within the GC.
Finally, isotope-based approaches to study the ecology and
eco-physiology of marine mammals must consider seasonal or
interannual variation in baseline isotope values of primary
producers (Newsome et al., 2010). The baleen d
15
N results
from adult males and adult females show that the foraging
regions among which they migrate (GC, CCE and CRD) have
relatively consistent values throughout the seasons and years
(Figure 2). The range in d
15
N values of adult males that
remained within the CCE for at least three years during 1983
1986 (Figure 2D) and 19851988 (Figure 2E) were similar to
baleen from another adult male deposited during 20132016
(Figure 2G) and the adult female baleen plates deposited during
a wider range of years from 2003 to 2017 (Figure 2). A similar
pattern of consistency is also observed in the data for the
CRD (Figure 2).
Blevins et al. 10.3389/fmars.2022.944918
Frontiers in Marine Science frontiersin.org15