Isotopes from fossil coronulid barnacle shells record
evidence of migration in multiple Pleistocene
whale populations
Larry D. Taylora,1, Aaron O’Deab, Timothy J. Bralowerc, and Seth Finnegana
aDepartment of Integrative Biology, University of California, Berkeley, CA 94720; bSmithsonian Tropical Research Institute, Balboa, Republic of Panama;
and cDepartment of Geosciences, Pennsylvania State University, University Park, PA 16802
Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved February 15, 2019 (received for review May 22, 2018)
Migration is an integral feature of modern mysticete whale
ecology, and the demands of migration may have played a key
role in shaping mysticete evolutionary history. Constraining when
migration became established and assessing how it has changed
through time may yield valuable insight into the evolution of
mysticete whales and the oceans in which they lived. However,
there are currently few data which directly assess prehistoric
mysticete migrations. Here we show that calcite δ18O profiles of
two species of modern whale barnacles (coronulids) accurately re-
flect the known migration routes of their host whales. We then
analyze well-preserved fossil coronulids from three different loca-
tions along the eastern Pacific coast, finding that δ18O profiles
from these fossils exhibit trends and ranges similar to modern
specimens. Our results demonstrate that migration is an ancient
behavior within the humpback and gray whale lineages and that
multiple Pleistocene populations were undertaking migrations of
an extent similar to those of the present day.
cetacean | barnacle | migration | evolution | fossil
Most modern mysticete whales undertake annual migrationsthat allow them to feed in cool, seasonally productive,
high-latitude waters in summer before returning to warm, trop-
ical waters where they breed in winter. In the northeast Pacific,
migration routes span from breeding areas in Central America,
Mexico, and Hawaii to feeding areas in the Gulf of Alaska,
Bering Sea, and California Current system (1, 2). These migra-
tions link mysticete ecology to the processes which shape ocean
productivity patterns, and short-term disruptions to these pat-
terns induce corresponding changes in mysticete migratory be-
havior and distribution (3). During the Pliocene and Pleistocene
the world’s oceans became characterized by increasingly strong
seasonal upwelling and patchy productivity distributions, and
long-distance migrations are thought to have first become se-
lectively favored at this time (4–8). The Plio-Pleistocene was also
a pivotal time in mysticete evolution: Taxonomic diversity and
morphological disparity decreased, most small-bodied forms
disappeared, and gigantism became established across the clade
(6, 7). Whether these evolutionary trends were driven by
changing patterns of ocean productivity and selection for mi-
gratory adaptations remains an open question. Understanding
when migration first became established, which ancient pop-
ulations were migrating, and how stable the behavior has been
through time may resolve questions of the significance of mi-
gration to mysticete evolution. However, we currently have little
direct data regarding the migratory behaviors of prehistoric
whale populations. Stable isotope systems can be useful in
reconstructing animal movements (9), but these methods require
a continuously growing tissue that has a high preservation po-
tential and is resistant to diagenetic alteration. Tooth enamel has
been used to reconstruct the movements of extinct odontocetes
(10), but edentulous mysticetes have no comparable tissue.
Several mysticete lineages play host to commensal barnacles,
however, and δ18O profiles collected from fossil whale barnacles
may offer insight into ancient mysticete behaviors (11).
Coronulid barnacles belong to the superfamily Coronuloidea,
which includes species adapted to live on turtles, manatees,
crabs, and snakes (12). These barnacles live enclosed within a
shell of six calcite plates and grow by depositing new material at
the shell base, with the δ18O values of each new growth in-
crement determined primarily by the temperature and isotopic
composition of the surrounding seawater (refs. 13 and 14 and SI
Appendix, Fig. S1). A continuously growing barnacle can thus
preserve an oxygen isotope signature of its host whale’s move-
ments, with a year’s worth of shell growth recording an entire
annual migration. This approach has been used to reconstruct
the migration of modern-day turtles and California gray whales
(14, 15). While several fossil specimens of the gray whale bar-
nacle (Cryptolepas rhachianecti) are known, a more promising
system to investigate in the fossil record is that of the humpback
whale lineage and their common barnacle, Coronula diadema, as
this coronulid species is much more common in the fossil record
and is known from more than a dozen sites worldwide (16–21).
Here we investigate the potential of using fossil coronulid δ18
O values to gain insight into the migratory behaviors of pre-
historic mysticete whales. Because the majority of the coronulid
fossil record belongs to C. diadema, an important first step is to
establish the reliability with which δ18O profiles from this species
accurately reflect a host whale’s migration; we address this by
analyzing modern C. diadema shells collected from whales
with known migration routes. We then analyze Pleistocene-aged
Significance
Migration has long been hypothesized to have played a critical
role in baleen whale evolution, but fossil constraints on the
history of migration are sparse. Here we provide evidence that
the oxygen isotope composition of modern whale barnacle
shells reliably records migration pathways. We also analyze
fossil whale barnacle shells from three Pleistocene localities
and show that they display isotope profiles similar to those of
modern specimens. Our results indicate the presence of mi-
gration among all three ancient whale populations studied and
point to the possibility of reconstructing changes in migratory
behaviors from the Pliocene to the present.
Author contributions: L.D.T. designed research; L.D.T., A.O., T.J.B., and S.F. performed
research; L.D.T., T.J.B., and S.F. analyzed data; and L.D.T., A.O., T.J.B., and S.F. wrote
the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Published under the PNAS license.
1To whom correspondence should be addressed. Email: larry.taylor@berkeley.edu.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1808759116/-/DCSupplemental.
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coronulids from three unlithified, shallow-sediment sites along
the eastern Pacific coast.
Results
Modern coronulid δ18O profiles show absolute values, ranges,
and trajectories that are consistent with expectations given the
known migratory pathways of their hosts. UCMP 221031 is a C.
diadema shell collected from a humpback whale that washed
ashore on the California coast and is believed to have belonged
to the population which migrates between California and the
southern Baja Peninsula. The δ18O profile recovered from this
specimen is consistent with the whale feeding in the waters off
the California coast during the previous summer before migrat-
ing to the waters surrounding the southern Baja Peninsula (Fig.
1). CAS MAM 21691 is a C. diadema collected from a humpback
whale that washed ashore near Sitka, Alaska. The δ18O profile
recovered is consistent with the host whale’s feeding in the wa-
ters near southeast Alaska the previous year before migrating to
Hawaii, where the majority of Alaskan humpbacks spend their
winters (ref. 2 and Fig. 1). Both of these barnacles are quite large
(and therefore presumably old) and appear to record an entire
migratory cycle. CAS MAM 21149 is a C. rhachianecti shell
collected from a gray whale that washed ashore in northern
California. Its δ18O profile is consistent with the whale’s having
died while heading southward from the Bering Sea (California
gray whales migrate from the Bering, Chukchi, and Beaufort
Seas to breeding grounds along the Baja Peninsula; SI Appendix,
Fig. S2).
To test δ18O variability across plates within individual barna-
cles we sampled two shell plates of UCMP 221031; both plates
show very similar profiles (SI Appendix, Fig. S3). To test δ18O
variability across barnacles from a single whale we sampled three
small Coronula specimens (UCMP 221032, 221033, and 221034)
that were collected from a single young whale with an unknown
migration route. δ18O profiles from these specimens do not re-
cord a full migratory cycle but exhibit generally consistent trends
(SI Appendix, Fig. S3).
We examined fossil coronulids from Pleistocene-aged sedi-
ments of the San Pedro Formation and Bay Point Formation
of California and from sediments previously assigned to the
Pliocene-aged Burica Formation of Panama, but which we
herein assign a Middle to Late Pleistocene age based on the
presence of Emiliana huxleyi (refs. 22–25 and SI Appendix, Fig.
S4). δ18O profiles from four large C. diadema specimens from
the Burica Peninsula (UCMP 221022, 221028, 221029, and
221030) exhibit trends and ranges similar to modern specimens
but average ∼0.96‰ more enriched, as would be expected if
these barnacles grew during a glacial (Fig. 2 and SI Appendix,
Fig. S5 and Table S1). Stationary mollusks collected from the
same beds yield notably smaller δ18O ranges (Fig. 2D and SI
Appendix, Fig. S5). Bay Point fossils (SDSNH 102564, 111656,
and 114317, all Coronula, and 134747, Cryptolepas) and San
Pedro fossils (SDSNH 50195, Coronula, and 30462, Cryptolepas)
are all small shell fragments and thus yield truncated δ18O pro-
files. Nevertheless, δ18O ranges and trajectories are comparable
to those from modern specimens and are on average enriched by
∼1.02‰ (Bay Point fossils) and 1.64‰ (San Pedro fossils) (Fig.
Fig. 1. δ18O profiles from UCMP 221031 (A) and CAS MAM 21691 (B), both modern C. diadema. UCMP 221031 was collected from a humpback whale that
migrated between summer feeding areas along the coast of California and winter breeding areas near the southern Baja Peninsula. Shaded regions of the
δ18O profile (A) correspond with shaded regions of plausibility for the whale’s location during each season (C). CAS MAM 21691 was attached to a humpback
whale that migrated between southeast Alaska and Hawaii; shaded regions in B align with regions of plausibility in D. Analytical precision for this and all
other isotopic analyses is ±0.07‰.
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3 and SI Appendix, Fig. S5 and Table S1). The exact shape of a
δ18O profile depends on the completeness of the specimen and
the direction the host whale was moving in (California fossils, for
example, may have come from whales feeding on the California
coast, or possibly from those which were only passing by on
northward or southward phases of a longer migration).
We examined all specimens for macroscopic indications of
possible alteration. Textural and color abnormalities of CASG
78449, a C. diadema of poorly constrained age from Mexico,
suggest substantial alteration. The δ18O profile from this speci-
men is notably depleted relative to all other specimens we ana-
lyzed (SI Appendix, Fig. S6), which is consistent with open-system
alteration in the presence of meteoric waters (26). We used in-
ductively coupled plasma optical emission spectroscopy (ICP-
OES) to evaluate trace metal concentrations in four modern
coronulids, CASG 78449, and the Burica fossils. Fossil trace
metal concentrations are generally not substantially different
from the ranges seen in modern coronulids, but some fossils do
show modest elevations in iron and manganese (SI Appendix, Fig.
S7). Scanning electron microscopy of modern coronulids, CASG
78449, and the Burica fossils revealed microscopic indications of
alteration in CASG 78449, but not in the other fossils (SI Ap-
pendix, Fig. S8).
Discussion
J. S. Killingley first recognized the potential of coronulid shell
oxygen isotopes to track whale migration, showing that the δ18O
profile of a modern C. rhachianecti shell was consistent with
expectations based on the migration of its host, a California gray
whale (Eschrichtius robustus). Here we extend this work by
showing that modern δ18O profiles from the barnacle C. diadema
reliably reflect the migration paths of host humpback whales
(Megaptera novaeangliae) and that fossils of both Cryptolepas and
Coronula exhibit δ18O profiles similar to those of modern
individuals.
Interpreting coronulid shell δ18O begins with understanding
their life history. Coronulid growth rates, lifespan, and re-
productive strategies are poorly understood due to their unusual
habitat. Coronulids are thought to reproduce while their host
whales are clustered together for their own breeding (27), and
newly settled larvae will eventually grow shells that anchor into
mysticete skin so securely that shells may remain attached for
some time after the barnacle has died (28). The shells erode at
their apex during life (the barnacle retreats downward in
response) and thus a shell may not record the barnacle’s entire
lifespan (28). The largest modern C. diadema shells we analyzed
record less than 2 y of growth as inferred from progressions
between the δ18O profile’s most enriched (corresponding to the
whale’s feeding season) and most depleted (whale’s breeding
season) values (Fig. 1); this is in agreement with previous esti-
mates that coronulids live between 1 and 3 y (27, 29).
The largest fossils we analyzed are those from the Burica
Peninsula, all of which are relatively complete shells or shell
plates. Like modern coronulids, these fossils yield δ18O profiles
with clear signatures of the summer feeding season and winter
breeding season (Fig. 2). δ18O ranges recovered from these
fossils equal or exceed those of modern specimens and sub-
stantially exceed δ18O ranges observed in stationary mollusks
collected from the same beds (Fig. 2 and SI Appendix, Fig. S5).
This suggests that the migrations of prehistoric whales was sim-
ilar in extent to those of today, although a current lack of data on
Pleistocene seawater isotopic composition prohibits us from
specifying the exact migration paths of these whales. It is notable,
however, that the range of δ18O values seen in these fossils is
quite variable (from 1.37‰ to 3.79‰). One possible explana-
tion for this is that Pleistocene whales visiting the Burica
Peninsula utilized a variety of different migratory routes. In the
present day, whales that winter off the coast of Panama migrate
north to feeding grounds which spread from southern California
all the way to the northernmost Gulf of Alaska (1, 2). During the
southern hemisphere winter, some whales which feed off the
coast of Antarctica also migrate to Panama (30, 31). Our results
therefore support the interpretation that Panamanian waters
have served as a meeting point for whales from a variety of
subpopulations for at least the last 270,000 y.
The Bay Point and San Pedro fossils are small shell fragments,
with only one of these specimens appearing to capture a full
migratory cycle (Fig. 3). The majority instead display a one-way
trend in δ18O values that is interpreted as capturing a portion of
the host whale’s migration. Even these one-way δ18O profiles
display δ18O ranges that are too large to be accounted for by
annual changes within the region and are therefore taken as
reflecting migratory movements of the host whales. While the
incompleteness of these profiles makes them more difficult to
interpret, they nonetheless display a variety of δ18O ranges and
values. Whales off the California coast include individuals that
spend the entire summer feeding in the regional upwelling zones
as well as those which pass through on their way to the Pacific
Northwest, Alaska, or (in the case of gray whales) even the
Bering and Chukchi Seas. The specimen that seems to record a
relatively complete migration, a C. diadema shell fragment
Fig. 2. δ18O profiles from four Pleistocene-aged C. diadema fossils from the
Burica Peninsula of Panama. Specimens are UCMP 221029 (A), 221030 (B),
221022 (C), and 221028 (D). Blue bar in the right of D indicates the range of
δ18O recorded in immobile bivalve shells from the same bedding plane as
UCMP 221028. The variety of δ18O profiles suggests that the whales were
migrating to several different feeding regions. This is similar to the modern,
where whales that winter off the coast of Panama migrate north to feeding
areas from southern California to the Bering Sea and south to the Southern
Ocean.
Fig. 3. δ18O profiles from six Pleistocene-aged coronulid fossils from Cal-
ifornia. Four are Coronula (A–D) and two are Cryptolepas (E and F). Speci-
mens come from the Bay Point Formation (A–C and F) and San Pedro
Formation (D and E). Specimens are SDSNH 102564 (A), 111656 (B), 114317
(C), 50195 (D), 30462 (E), and 134747 (F).
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(SDSNH 102564), yields a δ18O range of 2.26‰, similar to the
modern California C. diadema shell (UCMP 221031) which
yielded a δ18O range of 1.95‰ (SI Appendix, Table S1). Taken
together, our analysis of the Burica and California fossils con-
firms the presence of migratory behavior in multiple eastern
Pacific mysticete populations belonging to both the humpback
and gray whale lineages from three different Pleistocene time
points.
Both the modern and fossil coronulids yield δ18O profiles with
a continuous progression between the most enriched and de-
pleted values (noting that smaller fossils do not appear to record
the full migratory cycle). These progressions sometimes display
excursions from the primary δ18O trend, which may be caused by
the whale’s passing through waters that locally depart from the
route’s overall seawater temperature or δ18O gradients. For ex-
ample, positive δ18O excursions against the δ18O profile’s pri-
mary trends can occur if the whale passes through either a region
of temporarily lower temperature (such as a localized upwelling
zone) or a region of high evaporation (preferential evaporation
of 16O leaves the water enriched in 18O). Negative δ18O excur-
sions may occur if the whale’s route passed through locally
warmer regions or into coastal settings influenced by freshwater
runoff, which can create localized depletions of 1 to 3‰ in
seawater δ18O values extending more than a dozen kilometers
offshore (32).
Low-Mg calcite is less prone to diagenetic alteration than
other biogenic carbonates, and our fossils come from shallow,
unlithified sediments, but some fossils nonetheless show modest
enrichments in Fe and Mn (SI Appendix, Fig. S7), which can be
indicators of diagenetic alteration (33, 34). Although this suggests
that they may have experienced some diagenetic alteration in the
presence of reducing groundwaters, there is little indication that
δ18O profiles are pervasively altered (with the exception of
CASG 78449). While recrystallization in the presence of mete-
oric waters typically causes depletions in bulk δ18O, the Burica,
Bay Point, and San Pedro fossils all have δ18O values which are
enriched relative to modern coronulid values, which is an un-
likely outcome of independent diagenetic histories. These δ18O
profiles are also coherent and fall within ranges compatible with
growth during the glacial Pleistocene, which is hard to reconcile
with any major alteration. SEM imaging revealed homogenous,
comparable external shell structure between modern coronulids
and the Burica fossils (SI Appendix, Fig. S8). In contrast, CASG
78449 displays textural and color indications of alteration, has
considerable loss or morphing of delicate shell structure, and has
a δ18O profile substantially depleted relative to all other coro-
nulids analyzed (SI Appendix, Fig. S6). SEM imaging of CASG
78449 displays evidence of dissolution, pitting, and crystalline
overgrowth (SI Appendix, Fig. S8).
Several different factors may influence calcite δ13C, including
the incorporation of metabolic carbon, kinetic disequilibrium
effects, temperature-dependent fractionation, and the δ13C of
dissolved inorganic carbon, which itself can be modified by up-
welling or freshwater input. Interpreting δ13C data is best done
alongside accompanying δ18O values (15, 35–37). Depleted δ13C
values coupled with an enrichment in δ18O may indicate time
spent in an upwelling environment (35, 37), while relatively
enriched δ13C values may correspond to periods spent in more
open ocean environments (15). In our coronulid shells, the most
enriched δ18O values often coincide with some of the most de-
pleted δ13C values, whereas depleted δ18O values are often
paired with relatively enriched δ13C values; this pattern may
signify time that the host whale spent feeding in productive up-
welling zones vs. time spent migrating across open ocean envi-
ronments or in breeding areas with little upwelling. While these
broad patterns describing the relationship between δ18O and δ13C
profiles are true for the majority of the coronulids we ana-
lyzed, they are not true for all of them, indicating that the other
factors are likely playing a large role in determining coronulid
shell δ13C.
It has been suggested that mysticetes first began to migrate in
the Plio-Pleistocene (6–8) as productivity became increasingly
seasonal (5), clustered within high-latitude waters (38, 39), and
repeatedly redistributed by glacial–interglacial cycles (40–42),
possibly providing a selective advantage for migration as a means
of reliably accessing ephemeral and far-flung resources. Gigan-
tism became established at the same time, allowing for more
efficient long-distance travel and enabling mysticetes to better
utilize pulses of intense productivity followed by long periods of
fasting (6, 43, 44). Our findings demonstrate that migration has
been established across multiple whale populations for at least
the last several hundred thousand years. Isotopic analysis of
other fossil coronulids—which are known from more than a
dozen sites across six continents and from sediments dating
back to the late Pliocene—provides a promising approach for
answering long-standing questions about mysticete behavior
and evolution. Combining fossil coronulid δ18O profiles with
paleoceanographic models and emerging proxies that can in-
dependently constrain seawater temperature and isotopic
composition may provide further constraints on prehistoric
migratory pathways.
Materials and Methods
Modern coronulid specimens were previously collected by members of the
National Oceanic and Atmospheric Administration’s Marine Mammal
Stranding Network at the San Diego Natural History Museum (SDNHM) and
the California Academy of Sciences (CAS) before being donated to the Uni-
versity of California Museum of Paleontology; several modern specimens
were also loaned from the existing collections at the CAS. Some fossil speci-
mens were loaned from the SDNHM and the CAS, and more fossil specimens
were collected on the Burica Peninsula of Panama. Modern and fossil speci-
mens from the CAS have specimen labels beginning with “CAS”; SDNHM
fossil labels begin with “SDSNH,” for the San Diego Society of Natural History.
Depending on the size of the shell, a Dremel hand drill or a New Wave
Systems micromill was used to collect calcite samples from along the primary
(vertical) growth axis of the shell. Samples of 50 to 100 μg were collected at
roughly 1-mm intervals then were analyzed at the Center for Stable Isotope
Biogeochemistry at the University of California, Berkeley with a GV IsoPrime
mass spectrometer with Dual-Inlet and MultiCarb systems. Several replicates
of one international standard NBS19 and two laboratory standards CaCO3-I
and II were measured along with every run of samples. Overall external
analytical precision is ±0.07‰ for δ18O. Retrieved oxygen isotope profiles are
interpreted using the balanomorph-specific paleotemperature equation of
Killingley and Newman (13).
To assess if coronulid shells reliably record an isotopic signature of whale
movements we compared isotope profiles from modern coronulids against
expectations based on their host whales’ known migratory route. To do this,
we created gridded maps which predict what the average δ18O of barnacle
calcite formed at any point in the ocean should be during each month of the
year. Barnacle calcite δ18O is determined by both the temperature and δ18O
of the seawater in which it forms, as described by Killingley and Newman’s
equation (13):
tð°CÞ=   22.14− 4.37ðδC − δWÞ+   0.07ðδC − δWÞ2,
where δC denotes barnacle calcite δ18O and δW denotes seawater δ18O. We
downloaded global seawater δ18O (45) and monthly seawater tempera-
ture (46) data derived from direct observations coupled with oceano-
graphic models then merged these datasets in R (47). National Oceanic and
Atmospheric Administration (NOAA)_Optimum Interpolation (OI)_Sea Sur-
face Temperature (SST) data provided by the NOAA Office of Oceanic and
Atmospheric Research, Earth System Research Laboratory, Physical Sciences
Division, Boulder, CO (https://www.esrl.noaa.gov/psd/). With the two vari-
ables determining barnacle shell δ18O thus known, we then used the pale-
otemperature equation to back out predicted barnacle calcite δ18O for each
unit of a map. We created a series of maps indicating the expected δ18O of
barnacle calcite produced in each unit of the map grid; we generated these
maps for each month of the year (SI Appendix, Fig. S8). We then used these
maps to assess whether the δ18O profiles recovered from modern coronulid
shells aligned with expectations based on the host whale’s migration route.
We used the δ18O profile’s three to four most enriched and most depleted
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consecutive values as expectations of where the whale should be during the
summer feeding season and winter breeding season, respectively. Because
our temperature data are monthly, the number of data points used was
chosen so as to represent 1 mo assuming constant growth rates of the
barnacle. Because of the latitudinal difference in the whale’s feeding and
breeding regions, the barnacle experiences the coldest waters in the summer
feeding season. Although this will also generally correspond with the lowest
seawater δ18O, the temperature-dependent fractionation in barnacles (and
other calcifying organisms) generates an enriched shell calcite δ18O in cold
temperatures and a depleted δ18O in warm temperatures.
Fossils analyzed from California museum collections come from the
Pleistocene-aged San Pedro Formation and Bay Point Formation of southern
California (23–25), along with one specimen from an unrecorded location in
mainland Mexico. Further fossil specimens were collected from shallow
marine sediments in the eastern Burica Peninsula of Panama, which were
previously believed to belong to the Pliocene-aged Burica Formation (22);
bulk samples from this unit were collected for analysis of calcareous nan-
noplankton assemblages to further constrain ages. Smear slides were pre-
pared using standard techniques and viewed at a magnification of 1250
using a Zeiss Axioskop light microscope. Samples were also observed in a FEI
Nova NanoSEM 630 FE scanning electron microscope in the Pennsylvania
State University Materials Characterization Laboratory. δ18O profiles re-
covered from all fossil coronulids were qualitatively compared against the
modern profiles to assess evidence of migration.
All fossil specimens were examined for macroscopic indications (color and
texture) of alteration. External shell samples frommodern coronulids and the
Burica fossils were also imaged with a Hitachi TM-1000 scanning electron
microscope for microscopic indications of alteration. We used ICP-OES to
compare the trace metal concentrations in the Burica fossils and CASG 78449.
The smaller Bay Point and San Pedro fossils, loaned by the San Diego Natural
History Museum, were not large enough to be subjected to these analyses
without destroying the specimens.
ACKNOWLEDGMENTS. We thank Tom Demere and Kesler Randall (San
Diego Natural History Museum), Moe Flannery, Christina Piotrowski, and the
late Jean Demouthe (California Academy of Sciences), and Nick Pyenson
(Smithsonian National Museum of Natural History) for contributing speci-
mens to this study; Paul Taylor, Ethan Grossman, and Abigail Kelly for their
help in the field; Wenbo Yang, Todd Dawson, and Stefania Mambelli (Center
for Stable Isotope Biogeochemistry) for their help with all isotope analysis;
the staff at the University of California, Berkeley Electron Microscope
Laboratory for advice and assistance in electron microscopy sample prepa-
ration and data collection; and Valerie and Bill Anders for their generous
support. This study was supported by NSF Grant EAR-1325683 and the
National System of Investigators (National Secretariat for Science, Technol-
ogy and Innovation) (to A.O.), by the David and Lucile Packard Foundation
(S.F.), and by funding from the Paleontological Society, the Geological
Society of America, Sigma Xi, and the University of California Museum of
Paleontology (L.D.T.).
1. Calambokidis J, Steiger G, Straley J, Herman L, Cerchio S (2001) Movements and
population structure of humpback whales in the North Pacific. Mar Mamm Sci 17:
769–794.
2. Calambokidis J, et al. (2009) SPLASH: Structure of populations, levels of abundance
and status of humpback whales in the North Pacific. Final report for contract AB133F-
03-RP-0078 (Cascadia Research, Olympia, WA).
3. Benson SR, Croll DA, Marinovic BB, Chavez FP, Harvey JT (2002) Changes in the ce-
tacean assemblage of a coastal upwelling ecosystem during El Nino 1997–98 and La
Nina 1999. Prog Oceanogr 54:279–291.
4. Marlow JR, Lange CB, Wefer G, Rosell-Mele A (2000) Upwelling intensification as part
of the Pliocene-Pleistocene climate transition. Science 290:2288–2291.
5. Ravelo AC, Andreasen DH, Lyle M, Olivarez Lyle A, Wara MW (2004) Regional climate
shifts caused by gradual global cooling in the Pliocene epoch. Nature 429:263–267.
6. Slater GJ, Goldbogen JA, Pyenson ND (2017) Independent evolution of baleen whale
gigantism linked to Plio-Pleistocene ocean dynamics. Proc Biol Sci 284:20170546.
7. Marx FG, Fordyce RE (2015) Baleen boom and bust: A synthesis of mysticete phylog-
eny, diversity and disparity. R Soc Open Sci 2:140434.
8. Berger WH (2007) Cenozoic cooling, Antarctic nutrient pump, and the evolution of
whales. Deep Sea Res Part II Top Stud Oceanogr 54:2399–2421.
9. McMahon KW, Hamady LL, Thorrold SR (2013) A review of ecogeochemistry ap-
proaches to estimating movements of marine animals. Limnol Oceanogr 58:697–714.
10. Matthews CJD, Longstaffe FJ, Ferguson SH (2016) Dentine oxygen isotopes (δ (18)O)
as a proxy for odontocete distributions and movements. Ecol Evol 6:4643–4653.
11. Collareta A, et al. (2018) New insights on ancient cetacean movement patterns from
oxygen isotope analyses of a Mediterranean Pleistocene whale barnacle. Neues Jahrb
Geol Palaontol Abh 288:143–159.
12. Hayashi R, et al. (2013) Phylogenetic position and evolutionary history of the turtle
and whale barnacles (Cirripedia: Balanomorpha: Coronuloidea). Mol Phylogenet Evol
67:9–14.
13. Killingley JS, Newman WA (1982) 18O fractionation in barnacle calcite: A barnacle
paleotemperature equation. J Mar Res 40:893–902.
14. Killingley JS (1980) Migrations of California gray whales tracked by oxygen-18 vari-
ations in their epizoic barnacles. Science 207:759–760.
15. Killingley JS, Lutcavage M (1983) Loggerhead turtle movements reconstructed from
18O and 13C profiles from commensal barnacle shells. Estuar Coast Shelf Sci 16:
345–349.
16. Fleming CA (1959) A Pliocene whale barnacle from Hawke’s Bay, New Zealand. N Z J
Geol Geophys 2:242–247.
17. Bianucci G, Di Celma C, Landini W, Buckeridge J (2006) Palaeoecology and taphonomy
of an extraordinary whale barnacle accumulation from the Plio-Pleistocene of Ecua-
dor. Palaeogeogr Palaeoclimatol Palaeoecol 242:326–342.
18. Buckeridge JS (1983) Fossil barnacles (Cirripedia: Thoracica) of New Zealand and
Australia. N Z Geol Surv Paleontol Bull 50:1–151.
19. Zullo VA (1969) Thoracic Cirripedia of the San Diego formation, San Diego County,
California. Contrib Sci 159:1–25.
20. Beu AG (1971) Further fossil whale barnacles from New Zealand. N Z J Geol Geophys
14:898–904.
21. Dominici S, Bartalini M, Benvenuti M, Balestra B (2011) Large kings with small crowns:
A Mediterranean Pleistocene whale barnacle. Boll Soc Paleontol Ital 50:95–101.
22. Moore GW, Kennedy MP (1975) Quaternary faults at San Diego Bay, California. J Res
US Geol Surv 3:589–595.
23. Wehmiller JF, et al. (1977) Correlation and chronology of Pacific Coast marine terrace
deposits of continental United States by fossil amino acid stereochemistry technique
evaluation relative ages kinetic model ages and geologic implications. Open-File
Report 77-680 (US Geological Survey, Reston, VA).
24. Bryant ME (1987) Emergent marine terraces and quaternary tectonics, Palos Verdes
Peninsula, California. Geology of the Palos Verdes Peninsula and San Pedro Bay:
Volume and Guidebook, eds Fischer PJ, et al. (Society of Economic Paleontologists
and Mineralogists, Tulsa, OK), pp 63–78.
25. Coates AGC, et al. (1992) Closure of the Isthmus of Panama: The near-shore marine
record of Costa Rica and western Panama. Geol Soc Am Bull 104:814–828.
26. Tucker ME, Wright VP (2008) Carbonate Sedimentology (Blackwell Scientific, Oxford).
27. Best PB (1991) The presence of coronuline barnacles on a southern right whale Eu-
balaena australis. S Afr J Mar Sci 11:585–587.
28. Seilacher A (2005) Whale barnacles: Exaptational access to a forbidden paradise.
Paleobiology 31:27–35.
29. Monroe R (1981) Studies in the Coronulidae (Cirripedia): Shell morphology, growth,
and function, and their bearing on subfamily classification. Mem Queensl Mus 20:
237–251.
30. Acevedo-Gutierrez A, Smultea MA (1995) First records of Humpback whales including
calves at Golfo Dulce and Isla del Coco, Costa Rica, suggesting geographical overlap of
northern and southern hemisphere populations. Mar Mamm Sci 11:554–560.
31. Rasmussen K, et al. (2007) Southern hemisphere humpback whales wintering off
Central America: Insights from water temperature into the longest mammalian mi-
gration. Biol Lett 3:302–305.
32. Khim BK, Krantz DE, Cooper LW, Grebmeier JM (2003) Seasonal discharge of estua-
rine freshwater to the western Chukchi Sea shelf identified in stable isotope profiles
of mollusk shells. J Geophys Res 108:3300–3309.
33. Land LS (1967) Diagenesis of skeletal carbonates. J Sediment Petrol 37:914–930.
34. Brand U, Veizer J (1980) Chemical diagenesis of a multicomponent carbonate system–
1: Trace elements. J Sediment Petrol 50:1219–1236.
35. Sadler J, et al. (2012) Reconstructing past upwelling intensity and the seasonal dy-
namics of primary productivity along the Peruvian coastline from mollusk shell stable
isotopes. Geochem Geophys Geosyst 13:Q01015.
36. Killingley JS, Berger WH (1979) Stable isotopes in a mollusk shell: Detection of up-
welling events. Science 205:186–188.
37. Bemis BE, Geary DH (1996) The usefulness of bivalve stable isotope profiles as envi-
ronmental indicators: Data from the Eastern Pacific Ocean and the Southern Carib-
bean Sea. Palaios 11:328–339.
38. Barron JA, Lyle M, Koizumi I (2002) Late Miocene and early Pliocene biosiliceous
sedimentation along the California margin. Rev Mex Cienc Geol 19:161–169.
39. Barron JA (1998) Late Neogene changes in diatom sedimentation in the North Pacific.
J Asian Earth Sci 16:85–95.
40. Martínez-García A, et al. (2014) Iron fertilization of the Subantarctic ocean during the
last ice age. Science 343:1347–1350.
41. Kumar N, et al. (1995) Increased biological productivity and export production in the
glacial Southern Ocean. Nature 378:675–680.
42. Lisiecki LE, Raymo ME (2007) Plio–Pleistocene climate evolution: Trends and transi-
tions in glacial cycle dynamics. Quat Sci Rev 26:56–69.
43. Goldbogen JA, et al. (2017) How baleen whales feed: The biomechanics of engulf-
ment and filtration. Annu Rev Mar Sci 9:367–386.
44. Williams TM (1999) The evolution of cost efficient swimming in marine mammals:
Limits to energetic optimization. Philos Trans R Soc Lond B Biol Sci 354:193–201.
45. Schmidt GA, Bigg GR, Rohling EJ (1999) Global Seawater Oxygen-18 Database. V1.22.
Available at https://data.giss.nasa.gov/o18data/. Accessed March 1, 2016.
46. Reynolds RW, et al. (2002) An improved in situ and satellite SST analysis for climate. J
Climate 15:1609–1625.
47. R Core Team (2016) R: A language and environment for statistical computing
(R Foundation for Statistical Computing, Vienna). Available at https://www.
R-project.org/. Accessed March 1, 2016.
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