Journal of Paleontology, page 1 of 8 Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. 0022-3360/21/1937-2337 doi: 10.1017/jpa.2021.113 New fossil remains of the commensal barnacle Cryptolepas rhachianecti provide evidence of gray whales in the prehistoric South Pacific Larry Taylor,1,2* Juan Abella,3,4* and Jorge Manuel Morales-Saldaña5 1 Department of Integrative Biology and University of California Museum of Paleontology, University of California, Berkeley, Berkeley, CA 94720, USA 2 Helena College, University of Montana, Helena, MT 59601, USA 3 Institut Català de Paleontologia Miquel Crusafont, Edifici Institut de Ciència i Tecnologia Ambientals - Institut Català de Paleontologia (ICTA-ICP), Universitat Autònoma de Barcelona, Barcelona, Spain < juan.abella@icp.cat> 4 Instituto Nacional de Biodiversidad, Quito, Ecuador 5 Smithsonian Tropical Research Institute, Balboa, Republic of Panama Abstract.—We report the finding of two partial specimens of Cryptolepas rhachianecti (Cirripedia, Coronulidae), a cor- onulid barnacle known only to inhabit the skin of gray whales (Eschrichtius robustus), in Pleistocene-aged sediments from the Canoa Basin, Ecuador. While the historical range of gray whales includes the North Pacific and North Atlantic, to our knowledge this is the first inferred evidence of a gray whale population having resided within the South Pacific. We describe the two Cryptolepas rhachianecti fossils, use isotopic analysis to investigate evidence of migration in their host whales, and discuss their implications for our understanding of gray whale evolutionary history. Introduction C. rhachianecti previously has been known only from the Nor- thern Hemisphere, both in the present day and within the fossil Coronuloidea consists of a superfamily of commensal barnacles record. While fossil whale barnacles usually exist in small num- adapted to live on a remarkable variety of organisms, including bers wherever they are found, an exception to this general rule is manatees, crabs, mollusks, sea snakes, sea turtles, and cetaceans the Canoa Basin of Ecuador, where dozens of coronulid fossils (Hayashi, 2013). The whale-living barnacles, or coronulids have been collected, previously all assigned to the genus Coro- (family Coronulidae), are the most recently derived lineage, hav- nula (Bianucci et al., 2006a, b). ing diverged from the other commensal barnacles within the past Here we report finding two partial shells of the gray whale five million years (Hayashi et al., 2013). This timing coincides barnacle Cryptolepas rhachianecti in Pleistocene-aged deposits with the onset of gigantism in baleen whales (Slater et al., from the Canoa Basin, Ecuador. To our knowledge, these are the 2017), and most coronulids make their home on the modern oldest known fossil specimens of Cryptolepas, the first occur- giants, although some species are occasionally seen on delphi- rences of the genus in the Southern Hemisphere, and the first nids (Seilacher, 2005; Hayashi, 2012). evidence of a gray whale population regularly living in or As a group, the coronulids are relatively abundant through- migrating through the southern Pacific Ocean. out the modern oceans. The most abundant coronulid species in the oceans today is Coronula diadema (Linnaeus, 1767), which Geological setting lives attached to the skin of humpback whales (Megaptera novaeangliae Borowski, 1781). Where whale barnacle fossils Specimens were collected in Pleistocene-aged sediments of the are found, they belong nearly exclusively to the genus Coronula Canoa Basin in the Cabo San Lorenzo area of the Manabi Prov- (Fleming, 1959; Zullo, 1969; Beu, 1971; Buckeridge, 1983; ince, Ecuador (1.1821°S, 80.8622°W). During the Plio- Bianucci et al., 2006a, b; Dominici et al., 2011; Collareta Pleistocene, the Cabo San Lorenzo area was an uplifting island et al., 2016; Taylor et al., 2019). The genus Cryptolepas is repre- separated from mainland Ecuador by a shallow, narrow strait. sented by a single extant species, Cryptolepas rhachianecti, Continued uplift eventually connected this island to mainland which is a host-specific inhabitant of the skin of gray whales Ecuador via a land bridge. Glacial-interglacial oscillations (Eschrichtius robustus Lilljeborg, 1861) (Newman and Ross, caused the shoreline to advance and retreat multiple times, 1976; Newman and Abbott, 1980; Seilacher, 2005; Bradford extending west of present-day La Plata Island during glacial per- et al., 2011; Hayashi, 2012; Swartz, 2018). Like its host, iods, when sea level was lower (Di Celma et al., 2002, 2005; Cantalamessa and Di Celma, 2004). During warmer intergla- cials, rising sea levels resulted in the shoreline retreating east- *Corresponding author. ward to create a southwesterly facing coastal embayment, the 1 Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 2 Journal of Paleontology:1–8 Figure 1. (1) A map showing the location of the Canoa Basin sediments in relation to the range of modern-day gray whales, with inset showing greater detail of the region surrounding the field site. (2) During glacial lowstands, the Canoa coastline extended west past present-day Isla de la Plata. (3) During past interglacial high- stands, the coastline moved east, creating a small coastal embayment, the Canoa Basin. Canoa Basin (Fig. 1). Over time, the basin has been progres- 2004). Each sequence is bound below by an erosional surface, sively filled by ∼120 m of cyclically stacked shallow marine above which lies a basal hiatal shell bed followed by several strata (Di Celma et al., 2002, 2005). meters of sparsely fossiliferous sediment (Di Celma et al., Stratigraphic, sedimentological, paleoecological, and 2005). While the lowermost shell bed is quite taxa-rich and taphonomic studies of the entire succession indicate it is com- densely packed, whale barnacles are rare in the lowest two posed of a series of glacio-eustatically driven parasequences sequences and become more abundant thereafter. The upper capturing recurring periods of rising and falling sea levels, Canoa and Tablazo formations are interpreted to be a continuous exposed along ∼10 km of coastline between Punta Canoa and sedimentary record of two and six depositional sequences created Rio Callejón (Di Celma et al., 2002, 2005). The succession under the control of 100 kyr-long sea level fluctuations (Di Celma has been divided into the lower Canoa and upper Tablazo forma- et al., 2005). Shell beds are found basally and mid-cycle, separated tions, with the Canoa Formation being further divided by an by sparsely fossiliferous siliciclastics, and exhibit within-habitat angular unconformity (Sheppard, 1930; Pilsbry and Olsson, time averaging (Bianucci et al., 2006a). The Tablazo Formation 1941; Marchant, 1961; Savoyat, 1971; Baldock, 1982; Tsuchi was described and is best known from the Santa Elena Province et al., 1988; Whittaker, 1988; Di Celma et al., 2005). Older sedi- (∼120 km to the south of this site), and has yielded mostly contin- ments in the basin have yielded Oligo-Miocene fossils, and the ental fossils (Hoffstetter, 1952; Edmund, 1965; Ficcarelli et al., Miocene-aged Tosagua Formation lies just below the lower 2003; Lindsey and Lopez, 2015; Cadena et al., 2017), but also Canoa (Cadena et al., 2018). The lower Canoa rests unconform- marine remains (Edmund, 1965; Flores, 2018; Flores et al., 2020). ably atop the Tosagua, and is composed of fine-grained, bluish- The Canoa and Tablazo formations previously have yielded gray, silty to sandy shales (Di Celma et al., 2005). Above, the dozens of whale barnacles belonging to the species Coronula upper Canoa consists of gray-brown silts to sands, overlain by diadema, which lives on the skin of humpback whales, leading the brown sands of the Tablazo Formation. Sediments in both to the conclusion that the Canoa Basin was visited by migrating formations are rich in fossils (bivalves, gastropods, echinoids, whales in the Pleistocene (Bianucci et al., 2006a, b). crustaceans, corals, and occasional vertebrate remains) (Bia- nucci et al., 2006a; Flores et al., 2018). Materials and methods The lower Canoa consists of four depositional sequences formed under the control of 40 kyr-long sea level fluctuations Fossils were collected in September 2018 from sediments of the (Di Celma et al., 2002, 2005; Cantalamessa and Di Celma, upper Canoa Formation in the Canoa Basin, Ecuador, Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 Taylor et al.—Fossil whale barnacles suggest ancient gray whale population 3 coordinates 1.1821°S, 80.8622°W. For isotopic analysis, a small Specimen UCMP 116132 is also represented by a single Dremel handheld drill was used to collect calcite samples of 50– compartment, but is more complete, with many of the radial 100 micrograms from along the primary (vertical) growth axis of lamellae still intact (Fig. 2). Taken together, several characters the shell. Samples were analyzed at the Center for Stable Isotope identify the specimens as Cryptolepas rhachianecti; these Biogeochemistry at the University of California, Berkeley with a include a transversely grooved sheath, the presence of four GV IsoPrime mass spectrometer with Dual-Inlet and MultiCarb lamellar folds plus two half (sutural) folds on each systems. Several replicates of one international standard NBS19 compartment, irregularly branching radial lamellae where and two lab standards CaCO3-I and II were measured along with many branches fail to reach the periphery, and the absence of every run of samples. Overall external analytical precision is terminal flanges uniting the radial lamellae into a solid outer ±0.07‰ for δ18O and ±0.05‰ for δ13C. wall (Pilsbry, 1916; Davis, 1972). Transverse grooving of the Barnacle calcite δ18O is determined by both the temperature sheath is present in both UCMP 116131 and UCMP 116132. and δ18O of the seawater in which it forms, as described by the The eroded lamellar folds are clear on the outward-facing balanomorph-barnacle paleotemperature equation of Killingley walls of UCMP 116131. In UCMP 116132, many of the and Newman (1982): lamellar folds are well-preserved and display the species’ characteristic irregular branching pattern, the failure of several of these branches to reach the periphery, and the absence of t(◦ C) = 22.14 − 4.37(dC − dW) + 0.07(dC − dW)2 the wall-forming terminal flanges found in some other coronulids (Fig. 2). UCMP 116131 bears a strong resemblance where δC denotes barnacle calcite δ18O and δW denotes to a (sub)fossil Cryptolepas rhachianecti specimen from the seawater δ18O. Because of latitudinal differences in the whale’s Netherlands reported by Bosselaers and Collareta (2016), and feeding and breeding regions, the barnacle experiences the cold- closely resembles a worn shell depicted by Pilsbry (1916, pl. est waters in the summer feeding season. Although this will also 66, fig. 2). generally correspond with the lowest seawater δ18O, the temperature-dependent fractionation in barnacles (and other cal- Remarks.—Specimens UCMP 116131 and UCMP 116132 cifying organisms) generates an enriched shell calcite δ18O in were both collected from the upper Canoa Formation. The cold temperatures and a depleted δ18O in warm temperatures. features described above distinguish Cryptolepas from Coronula—a coronulid found in much greater abundance in the Repositories and institutional abbreviations.—Specimens Canoa deposits. Coronula has an ungrooved sheath, fewer collected and described in this study are deposited at the lamellar folds, fewer branches arising from the folds (all of University of California Museum of Paleontology (UCMP), which reach the periphery), and a solid outer wall formed by Berkeley, California, and in the California Academy of the uniting of T-shaped terminal flanges of the folds. Sciences (CAS), San Francisco, California. While fossils of the genus Cryptolepas are sparse, two spe- cies are now recognized in the fossil record. The first is C. rha- Systematic paleontology chianecti, reported here and as a (sub)fossil from the Netherlands (Bosselaers and Collareta, 2016). The second is Class Maxillopoda Dahl, 1956 C. murata, reported by Zullo (1961) from late Pleistocene Subclass Cirripedia Burmeister, 1834 deposits of California. Cryptolepas traditionally has been sug- Superorder Thoracica Darwin, 1854 gested to have derived from the lineage that includes Coronula Order Sessilia Lamarck, 1818 and Cetopirus, with the major differences in shell morphology Suborder Balanomorpha Pilsbry, 1916 seen in Cryptolepas interpreted as degenerative changes related Superfamily Coronuloidea Leach, 1817 to the more embedded, protected station of the shell in the host’s Family Coronulidae Leach, 1817 skin (Pilsbry, 1916; Monroe, 1981). A primary feature distin- Genus Cryptolepas Dall, 1872 guishing Cryptolepas rhachianecti from Coronula and Ceto- pirus is the absence of a complete outer wall to the shell, Type species.—Cryptolepas rhachianecti Dall, 1872, from which in the latter two genera is formed by the merging of beached whale, Monterey, CA, U.S.A., by original designation. T-shaped flanges at the ends of the lamellar folds and which serves to create coring chambers that envelop prongs of the Other species.—Cryptolepas murata Zullo, 1961, from host’s skin. Zullo (1961) interpreted C. murata as being an inter- Pleistocene deposits of San Quentin Bay, CA, U.S.A., by mediate form, possessing many of the distinguishing features of original designation. C. rhachianecti while retaining an outer wall to the shell (Zullo, 1961, 1969). Bosselaers and Collareta (2016) have questioned Cryptolepas rhachianecti Dall, 1872 whether Cryptolepas murata should be reassigned to the Figure 2 genus Cetopirus, but the rarity of Cryptolepas fossils makes answering that question difficult. While C. murata shares with Holotype.—Shell collected from beached whale, Monterey, CA, Cetopirus an outer wall formed by terminal flanges of the lamel- U.S.A., (Dall, 1872, p. 300). lar folds, it also shares with C. rhachianecti a grooved sheath, less symmetrical internal branching of the lamellar folds, and Description.—Specimen UCMP 116131 is a single the presence of internal branches that fail to reach the periphery compartment, with the radial lamellae mostly missing. of the shell (Fig. 2). Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 4 Journal of Paleontology:1–8 Figure 2. Fossil Cryptolepas rhachianecti shells UCMP 116131 (1, 2) and UCMP 116132 (3, 4) from Pleistocene sediments of the Canoa Basin, Ecuador, along- side modern C. rhachianecti shell UCMP 34678 (5–7) and fossil C. murata shell UCMP 34677 (8–10). Fragile folds of shell are supported by whale skin in life (dark material seen in 5, 7) and will easily crumble when dislodged; the folds of UCMP 116132 survived by support from fine-grained sediment (3, 4). The grooved sheath (2, 4, 6, 9) can be seen in all specimens, and several display the blind-ended folds, which do not reach the periphery (4, 7, 10). In C. rhachianecti, the terminal ends of the primary folds do not connect to neighboring folds (4, 7), while in C. murata, the terminal ends of the folds fuse to form a rudimentary outer wall (8, 10), similar to that of the genus Coronula. Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 Taylor et al.—Fossil whale barnacles suggest ancient gray whale population 5 Results Oxygen isotope ratios of coronulid shells have been shown to record the movements of their host whales (Killingley, 1980; Collaretta et al., 2018; Taylor et al., 2019). Isotopic analysis of fossil Cryptolepas rhachianecti shells UCMP 116131 and UCMP 116132 revealed δ18O ranges of 1.93‰ and 2.14‰ (Fig. 3), which is less than the 2.61–3.28‰ range measured in a modern-day C. rhachianecti shells of similar size (Fig. 3; Tay- lor et al., 2019, fig. S2). The fossils also have lower δ18O max- ima than their modern counterparts. Fossil shell δ13C is likewise depleted relative to that of modern shells, and δ13C is only loosely correlated with δ18O (Fig. 3; Taylor et al., 2019, fig. S2). Discussion To our knowledge, these specimens represent the oldest known occurrence of Cryptolepas rhachianecti, and the first report of the species in the southern hemisphere. The oldest previously reported specimen of C. rhachianecti is a single compartment from late Quaternary deposits in the Netherlands (Bosselaers and Collareta, 2016). The gray whale lineage has a geological and historical presence in much of the North Atlantic, and it is reasonable to expect that C. rhachianecti also once ranged throughout the North Atlantic as well (Bisconti and Varola, 2006; Noakes et al., 2013; Alter et al., 2015; Bosselaers and Col- lareta, 2016; Hufthammer et al., 2018; Rodrigues et al., 2018). Overharvesting led to the final collapse of this population by sometime in the 18th century, however, and today C. rhachia- necti is found only in the North Pacific, where it is a host-specific symbiont of the gray whale (Newman and Ross, 1976; Newman and Abbott, 1980; Scarff, 1986; Bradford et al., 2011; Hayashi, Figure 3. δ18O (1) and δ13C (2) profiles collected from along the primary 2012). Modern gray whales live in two distinct populations in growth axis of UCMP 116131, UCMP 116132, and CAS MAM 21149. CAS the western and eastern North Pacific, although some interchange MAM 21149 is a modern C. rhachianecti shell collected from a gray whale that beached in northern California, likely while migrating south from its summer between these populations does occur (LeDuc et al., 2002; Cooke feeding areas. δ18O of barnacle shells is determined by the temperature and iso- et al., 2007; IWC, 2011). While the fossil record clearly attests to topic composition of the seawater in which the barnacle was located during each the presence of the gray whale lineage in the North Pacific, there growth interval. Shell δ13C is affected by several factors and is best interpreted in conjunction with δ18O, where positive correlations may indicate changes in tem- are no historical or fossil records of gray whale populations living perature or salinity, while depleted δ13C coupled with enriched δ18O may be a in the equatorial Pacific or southern hemisphere (Tsai et al., 2014; signal of upwelling. Analytical precision is ±0.07‰ for δ18O and ±0.05‰ for Tsai and Boessenecker, 2015; Kimura et al., 2018). δ13C. Besides the Netherlands specimen, no other fossils of C. rhachianecti are known, most likely due to the fragile nature while host whales are in their winter breeding areas, and accu- of the shell. Due to this fragility, much of the fine structure of mulations of fossil whale barnacle shells have been interpreted UCMP 116132 was damaged during isotopic sampling (images as representing ancient whale breeding areas (Monroe, 1981; in Fig. 2 were taken prior to sampling). Whereas other whale Bianucci et al., 2006a, b; Taylor et al., 2019). Our finding of barnacles extrude far above the host’s skin and consequently Cryptolepas rhachianecti fossils raises the possibility that a are constructed robustly, C. rhachianecti lives deeply buried Pleistocene gray whale population used the Canoa Basin as a in the skin of gray whales, with the shell being largely supported winter breeding area. by the skin of the host interweaving between the radial lamellae Extant gray whales in the eastern North Pacific spend their (Fig. 2). This embedded, low-profile lifestyle of C. rhachianecti summer months feeding in cold, poleward waters, primarily in may be related to the suction-feeding habit of gray whales, the Bering and Chukchi Seas, before migrating southward to which causes the whales to rub their skin on the seafloor. If warm, shallow, and sheltered waters along the coast of Baja C. rhachianecti shells protruded much more above the skin, California Sur to breed and raise their calves (Swartz et al., they would risk being dislodged or destroyed via abrasion. 2006; Mate et al., 2015). The Pleistocene Canoa Basin would The fragility of C. rhachianecti shells and their resulting have offered conditions similar to the lagoons and bays where scarcity in the fossil record suggests that the barnacles’ host modern gray whales overwinter, and the large number of Coro- whales must have been a common visitor of the ancient Canoa nula diadema fossils found in the region suggests that the region Basin, considering we found two specimens in only three days at least served as an ancient breeding area for humpback whales of fieldwork. Whale barnacles are thought to be shed mostly (Bianucci et al., 2006a). While humpback and gray whales do Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 6 Journal of Paleontology:1–8 not typically winter together, they do sometimes seek out similar 2007; Capella et al., 2008; Felix and Olavarria, 2012; Hucke- water depths and temperatures (Martins et al., 2000), and winter- Gaete et al., 2013). It is known that small numbers of modern ing populations of both species can be found only a few miles gray whales do not migrate (Pyenson and Lindberg, 2011), but apart along the coast of present-day Baja California. the δ18O ranges of these fossils are difficult to explain via annual If a Pleistocene gray whale population once inhabited the variation in the immediate area, suggesting that the whales did South Pacific, it has not survived to the present day. Humpback migrate to some extent. The δ18O maxima are less enriched whales, on the other hand, still breed off the modern Ecuadorian than would be expected if the host whales were traveling to Ant- coast. Compared to humpbacks, gray whales are less numerous, arctica, but the δ18O ranges are similar to those of some barna- less ubiquitous, and more selective about areas where they will cles collected from modern, migrating humpback whales feed or breed. These differences may have made prehistoric gray (Taylor et al., 2019). It is plausible these ancient whales may whales comparatively rarer and more sensitive to change. While have migrated to the Chilean coast, as some modern humpbacks they are capable of generalist filter feeding like the other baleen do (Gibbons et al., 2003; Acevedo et al., 2007; Capella et al., whales, gray whales primarily prey on shallow, benthic inverte- 2008; Felix and Olavarria, 2012; Hucke-Gaete et al., 2013), brate communities via suction feeding. This feeding habitat was but they also may have migrated to any number of unknown greatly reduced during glacial maxima, however, reducing car- ancient feeding grounds. rying capacity for the species (Pyenson and Lindberg, 2011). Interpreting shell δ13C is less straight forward because δ13C It is plausible that one of these disruptions could have winnowed may be affected by the incorporation of metabolic carbon, a southern population beyond recovery, and that an intolerance kinetic disequilibrium effects, temperature-dependent fraction- for crossing warm equatorial waters coupled with the fidelity ation, and the effects of upwelling or freshwater input on δ13C of whale mothers to their natal lagoons has kept the species of dissolved inorganic carbon. Interpretation of shell δ13C is from recolonizing these areas in the modern day (Lindberg, best done in conjunction with corresponding shell δ18O, where 1991; Goerlitz et al., 2003; IWC, 2011). depletion of both δ13C and δ18O may be a signal of freshwater At least in the Canoa region, however, a primary cause of input, and where depletion of δ13C corresponding to enriched the loss of gray whales must have been the continual uplift of δ18O may be a signal of upwelling (Killingley and Berger, the Ecuador coast, which has eliminated the shallow embay- 1979; Killingley and Lutcavage, 1983; Bemis and Geary, ments suitable for gray whale breeding. Gray whales only 1996; Sadler et al., 2012). There is some indication of depletion raise calves in sheltered lagoons and embayments, typically in of δ13C where δ18O is most enriched in modern C. rhachianecti waters of 10 m depth or less (Gardner and Chavez-Rosales, shells (Fig. 3; Taylor et al., 2019, fig. S2), but in both modern 2000; Goerlitz et al., 2003; IWC, 2011). While previous periods and fossil shells δ13C and δ18O are either not correlated or of high sea level would have created such a suitable breeding show a slight positive correlation over the majority of the cap- habitat within the Canoa Basin, uplift of the Ecuadorian coast tured signal, indicating that freshwater input and other factors has resulted in the modern Canoa coast being dominated by cliffs, may be exerting a strong influence on shell δ13C. while Andean uplift has further eliminated shallow embayments With only a handful of Cryptolepas fossils known, our find- along the South American coast (Lindberg, 1991). Humpback ing of C. rhachianecti fossils in the Canoa Basin makes the whales, in contrast, will breed in a wider variety of water depths, region a promising area for further study. Collecting and isotop- and so may have been undisturbed by this loss of shallow habitat ically analyzing more C. rhachianecti fossils from the Canoa (Felix and Botero-Acosta, 2011; Pack et al., 2017). Basin may offer more insight into the behavior of this prehistoric An alternative explanation is that C. rhachianecti once whale population. commonly occurred on a different host whale species. However, there is little to support this hypothesis. Settlement of coronulid Acknowledgments larvae seems to be initiated by chemical cues from the preferred host’s skin (Nogata and Matsumura, 2005), while contact with Specimens were collected using excavation permit number other hosts initiates an immune response capable of shedding a bar- M-JA-2018-82. Thank you to F. Flores and X. Guncay, our nacle (Ridgeway et al., 1997). Consequently, the most parsimonious undergraduate research assistants during field work. We also explanation for the occurrence of C. rhachianecti fossils within the thank D. Strauss and S. Kahanamoku of the UCMP for their deposits is the prior presence of gray whales in the area. work in photographing the specimens. We thank J. Jijón (Insti- The δ18O range of the Canoa Basin fossils is smaller than tuto Nacional de Patrimonio Cultural, Ecuador) for his support that collected from modern C. rhachianecti specimens, which and help before, during, and after fieldwork. This study was sup- may reflect the fragmentary nature of the shells, or it may reflect ported by the Generalitat de Catalunya (CERCA Programme, real differences in the migratory extent of the host whales as and Beatriu de Pinós contract 2017 BP 00223 from AGAUR compared to their modern counterparts. If there was once a to JA), by the Geological Society of America, by the UC Berke- population of gray whales visiting the coast of Ecuador, then ley Department of Integrative Biology, by the University of those whales have no directly comparable modern counterpart, California Museum of Paleontology, by the American Society but some insight may come from looking at the behavior of of Naturalists, and by the Paleontological Society. humpback whales that breed off the modern Ecuador coast References (Sheidat et al., 2000; Felix and Botero-Acosta, 2011). These modern humpbacks are known to migrate to feeding areas Acevedo, J., Rasmussen, K., Felix, F., Castro, C., Llano, et al., 2007, Migratory along the coast of Chile, within the Magellan Strait, and along destinations of humpback whales from the Magellan Strait feeding ground, the Antarctic Peninsula (Gibbons et al., 2003; Acevedo et al., southeast Pacific: Marine Mammal Science, v. 23, p. 453–463. Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 Taylor et al.—Fossil whale barnacles suggest ancient gray whale population 7 Alter, S.E., Meyer, M., Post, K., Czechowski, P., Gravlund, P., Gaines, C., Di Celma, C., Ragaini, L., Cantalamessa, G., and Curzio, P., 2002, Shell con- Rosenbaum, H.C., Kaschner, K., Turvey, S.T., van der Plicht, J., Shapiro, centrations as tools in characterizing sedimentary dynamics at sequence- B., and Hofreiter, M., 2015, Climate impacts on transocean dispersal and bounding unconformities: examples from the lower unit of the Canoa habitat in gray whales from the Pleistocene to 2100: Molecular Ecology, Formation (late Pliocene, Ecuador): Geobios, v. 35, p. 72–85. v. 24, p. 1510–1522. Di Celma, C., Ragaini, L., Cantalamessa, G., and Landini, W., 2005, Basin Baldock, J.W., 1982, Geología del Ecuador: Boletín de la explicación del mapa physiography and tectonic influence on sequence architecture and stacking geológico nacional de la República del Ecuador, Dirección de Investigación pattern: Pleistocene succession of the Canoa Basin (central Ecuador): Geológico-Minera. Geological Society of America Bulletin, v. 117, p. 1226–1241. Bemis, B.E., and Geary, D.H., 1996, The usefulness of bivalve stable isotope Dominici, S., Bartalini, M., Benvenuti, M., and Balestra, B., 2011, Large kings profiles as environmental indicators: data from the eastern Pacific Ocean with small crowns: a Mediterranean Pleistocene whale barnacle: Bollettino and the southern Caribbean Sea: Palaios, v. 11, p. 328–339. della Societa Paleontologica Italiana, v. 50, p. 95–101. Beu, A.G., 1971, Further fossil whale barnacles from New Zealand: New Zea- Edmund, A.G., 1965, A Late Pleistocene Fauna from the Santa Elena Peninsula, land Journal of Geology and Geophysics, v. 14, p. 898–904. Ecuador: Toronto, Royal Ontario Museum, Life Sciences Division, 350 p. Bianucci, G., Di Celma, C., Landini, W., and Buckeridge, J., 2006a, Palaeoecol- Felix, F., and Botero-Acosta, N., 2011, Distribution and behaviour of humpback ogy and taphonomy of an extraordinary whale barnacle accumulation from whale mother-calf pair during the breeding season off Ecuador: Marine the Plio-Pleistocene of Ecuador: Palaeogeography, Palaeoclimatology, Ecology Progress Series, v. 426, p. 277–287. Palaeoecology, v. 242, p. 326–342. Felix, F., and Olavarria, C., 2012, Genetic diversity and population structure of Bianucci, G., Landini, W., and Buckeridge, J., 2006b, Whale barnacles and humpback whales (Megaptera novaeangliae) from Ecuador based on mito- Neogene cetacean migration routes: New Zealand Journal of Geology and chondrial DNA analyses: Journal of Cetacean Research and Management, Geophysics, v. 49, p. 115–120. v. 12, p. 71–77. Bisconti, M., and Varola, A., 2006, The oldest eschrichtiid mysticete and a new Ficcarelli, G., Coltorti, M., Moreno-Espinosa, M., Pieruccini, P.L., Rook, L., and morphological diagnosis of Eschrichtiidae (gray whales): Rivista Italiana di Torre, D., 2003, A model for the Holocene extinction of the mammal mega- Paleontologia e Stratigrafia, v. 112, p. 447–457. fauna in Ecuador: Journal of South American Earth Sciences, v. 15, p. 835–845. Borowski, G.H., 1781, Gemeinnüzzige Naturschichte des Tierreichs: Berlin and Fleming, C.A., 1959, A Pliocene whale barnacle from Hawke’s Bay, New Zea- Stralsund, G.L. Lange, v. 2, 196 p. land: New Zealand Journal of Geology and Geophysics, v. 2, p. 242–247. Bosselaers, M., and Collareta, A., 2016, The whale barnacle Cryptolepas rha- Flores, F.F., 2018, Estudio Poblacional del Tiburón Blanco (Carcharodon chianecti (Cirripedia: Coronulidae), a phoront of the grey whale Eschrich- carcharias, Linnaeus, 1758), del Yacimiento Pleistoceno de Quebrada tius robustus (Cetacea: Eschrichtiidae) from a sandy beach in The Tiburón (Atahualpa, Santa Elena, Ecuador) [Graduate thesis]: La Libertad, Netherlands: Zootaxa, v. 4145, p. 331–338. Ecuador, Universidad Estatal Península de Santa Elena, Ecuador. Bradford, A.L., Weller, D.W., Burdin, A.M. and Brownell, R.L., Jr., 2011, Flores, F.F., Guncay, X., Carrillo-Briceño, J., Taylor, L.D., Morales, J., and Using barnacle and pigmentation characteristics to identify gray whale calves Abella, J., 2018, Nuevos restos fósiles de peces condrictios y actinopteri- on their feeding grounds: Marine Mammal Science, v. 27, p. 644–651. gios de la Formación Canoa y Tablazo (Cantón Montecristi, Manabí, Ecua- Buckeridge, J.S., 1983, Fossil barnacles (Cirripedia: Thoracica) of New Zealand dor). XLII Jornados Nacionales de Biologia: Santa Elena, Ecuador, and Australia: New Zealand Geology Survey Paleontological Bulletin, Universidad Estatal Península de Santa Elena. v. 50, p. 1–151. Flores, F.F., Carrillo-Briceño, J.D., Guncay, X., and Abella, J., 2020, A great Burmeister, H., 1834, Beiträge zur Naturgeschichte der Rankenfüser (Cirri- white shark (Carcharodon carcharias Linnaeus, 1758) paleopopulation pedia): Berlin, G. Reimer, 60 p. from the Pleistocene of the Santa Elena Peninsula, Ecuador: 2nd Palaeonto- Cadena, E., Abella, J., and Gregori, M., 2017, New findings of Pleistocene fossil logical Virtual Congress, p. 169. https://www.uv.es/palaeovc/Documentos turtles (Geoemydidae, Kinosternidae and Chelydridae) from Santa Elena %20/2nd%20PVC/2nd_PVC_Book_of_Abstracts.pdf. Province, Ecuador: PeerJ, 5:e3215. https://doi.org/10.7717/peerj.3215. Gardner, S.C., and Chavez-Rosales, S., 2000, Changes in the relative abundance Cadena, E., Abella, J., and Gregori, M., 2018, The first Oligocene sea turtle and distribution of gray whales (Eschrichtius robustus) in Magdalena Bay, (Pan-Cheloniidae) record of South America: PeerJ, 6:e4554. https://doi. Mexico during and El Nino event. Marine Mammal Science, v. 16, org/10.7717/peerj.4554. p. 728–738. Cantalamessa, G., and Di Celma, C., 2004, Origin and chronology of Pleisto- Gibbons, J., Capela, J.J., and Valladares, C., 2003, Rediscovery of a humpback cene marine terraces of Isla de la Plata and of flat, gently dipping surfaces whale (Megaptera novaeangliae) feeding ground in the Straits of Magellan, of the southern coast of Cabo San Lorenzo (Manabi, Ecuador): Journal of Chile: Journal of Cetacean Research and Management, v. 5, p. 203–208. South American Earth Sciences, v. 16, p. 633–648. Goerlitz, D.S., Urban, J., Roja-Bracho, L., Belson, M., and Schaeff, C.M., Capella, J.J., Gibbons, J., Florez-Gonzalez, L., Llano, M., Valladres, C., Sabaj, 2003, Miochondrial DNA variation among Eastern North Pacific gray V., and Vilina, Y.A., 2008, Migratory round-trip of individually identified whales (Eschrichtius robustus) on winter breeding grounds in Baja Califor- humpback whales at the Strait of Magellan: clues on transit times and phy- nia: Canadian Journal of Zoology, v. 81, p. 1965–1972. lopatry to destinations: Revista Chilena de Historia Natural, v. 81, Hayashi, R., 2012, Atlas of the barnacles on marine vertebrates in Japanese p. 547–560. waters including taxonomic review of superfamily Coronuloidea (Cirri- Collareta, A., Margiotta, S., Varola, A., Catanzariti, R., Bosselaers, M., and Bia- pedia: Thoracica): Journal of the Marine Biological Association of the Uni- nucci, G., 2016, A new whale barnacle from the early Pleistocene of Italy ted Kingdom, v. 92, p. 107–127. suggests an ancient right whale breeding ground in the Mediterranean: Hayashi, R., 2013, A checklist of turtle and whale barnacles (Cirripedia: Thor- Comptes Rendus Palevol, v. 15, p. 473–481. acica: Coronuloidea): Journal of the Marine Biological Association of the Collareta, A., Regattieri, E., Zanchetta, G., Lambert, O., Catanzariti, R., Bosse- United Kingdom, v. 93, p. 143–182. laers, M., Covelo, P., Varola, A., and Bianucci, G., 2018, New insights on Hayashi, R., Chan, B.K.K., Simon-Blecher, N., Watanabe, H., Guy-Haim, T., ancient cetacean movement patterns from oxygen isotope analyses of a Yonezawa, T., Levy, Y., Shuto, T., and Achituv, Y., 2013, Phylogenetic Mediterranean Pleistocene whale barnacle: Neues Jahrbuch für Geologie position and evolutionary history of the turtle and whale barnacles (Cirri- und Paläontologie—Abhandlungen, v. 288, p. 143–159. pedia: Balanomorpha: Coronuloidea): Molecular Phylogenetics and Evolu- Cooke, J.G., Weller, D.W., Bradford, A.L., Burdin, A.M., and Brownell, R.L., tion, v. 67, p. 9–14. 2007, Population assessment of the western gray whales in 2007. Paper Hoffstetter, R., 1952, Les Mammifères Pleistocenes de la Republique de l’Equa- SC/59/BRG41 Presented to the International Whaling Commission Scien- teur: Mémoires de la Société Géologique de France, nouv. sér., v. 66, p. 1– tific Committee, Anchorage, AK: Publications, Agencies and Staff of the 391. U.S. Department of Commerce, 69. https://digitalcommons.unl.edu/cgi/ Hucke-Gaete, R., Haro, D., Torres-Florez, J.P., Montecinos, Y., Viddi, F., viewcontent.cgi?article=1068&context=usdeptcommercepub. Bedrinana-Romano, L., Nery, M.F., and Ruiz, J., 2013, A historical feeding Dahl, E., 1956, Some crustacean relationships, in Wingstrand, K.G., ed., Bertil ground for humpback whales in the eastern South Pacific revisited: the case Hanström, Zoological Papers in Honour of 65th Birthday: Lund, Zoological of northern Patagonia, Chile: Aquatic Conservation: Marine and Freshwater Institute, p. 138–147. Ecosystems, v. 23, p. 858–867. Dall, W.H., 1872, On the parasites of the cetaceans of the N.W. coast of Amer- Hufthammer, A.K., Arntsen, L., Kitchener, A.C., and Buckley, M., 2018, Grey ica, with descriptions of new forms: Proceedings of the California Academy whale (Eschrichtius robustus) in Norwegian waters 2000 years ago: Palaeo- of Sciences v. 4, p. 299–301. geography, Palaeoclimatology, Palaeoecology, v. 495, p. 42–47. Darwin, C.R., 1854, A Monograph on the Sub-Class Cirripedia, with Figures of IWC [International Whaling Commission], 2011, Report of the Scientific Com- All Species: The Balanidae (or Sessile Cirripedia); the Verricidae, etc., etc., mittee, Annex F: Sub-Committee on Bowhead, Right and Gray Whales: etc.: London, The Ray Society, 684 p. Tromso, Norway, 30 May to June 11 2011. Davis, C.W., 1972, Studies on the Barnacles Epizoic on Marine Vertebrates [MA Killingley, J.S., 1980, Migrations of California gray whales tracked by thesis]: San Francisco, California State University, San Francisco, 60 p. oxygen-18 variations in their epizoic barnacles: Science, v. 207, p. 759–760. Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113 8 Journal of Paleontology:1–8 Killingley, J.S., and Berger, W.H., 1979, Stable isotopes in a mollusk shell: Pyenson, N.D., and Lindberg, D.R., 2011, What happened to gray whales dur- detection of upwelling events: Science, v. 205, p. 186–188. ing the Pleistocene? The ecological impact of sea-level change on benthic Killingley, J.S., and Lutcavage, M., 1983, Loggerhead turtle movements recon- feeding areas in the North Pacific Ocean: PLOS One, v. 6, e21295. structed from 18O and 13C profiles from commensal barnacle shells: Estuar- https://doi.org/10.1371/journal.pone.0021295. ine, Coastal, and Shelf Science, v. 16, p. 345–349. Ridgeway, S.H., Lindner, E., Mahoney, K.A., and Newman, W.A., 1997, Gray Killingley, J.S., and Newman, W.A., 1982, 18O fractionation in barnacle calcite: whale barnacles Cryptolepas rhachianecti infest white whales, Delphinap- a barnacle paleotemperature equation: Journal of Marine Research, v. 40, terus leucas, housed in San Diego Bay: Bulletin of Marine Science, v. 61, p. 893–902. p. 377–385. Kimura, T., Hasegawa, Y., and Kohno, N., 2018, A new species of the genus Rodrigues, A.S.L., Charpentier, A., Bernal-Casasola, D., Gardeisen, A., Nores, Eschrichtius (Cetacea: Mysticeti) from the early Pleistocene of Japan: Pale- C., Millán, J.A.P., McGrath, K., and Speller, C.F., 2018, Forgotten Medi- ontological Research, v. 22, p. 1–19. terranean calving grounds of grey and North Atlantic right whales: evidence Lamarck, J.B., 1818, Histoire Naturelle des Animaux sans Vertèbres 5: Paris, from Roman archaeological records: Proceedings of the Royal Society B, Verdière, Libraire, quai des Augustins, 612 p. 285, 20180961. https://doi.org/10.1098/rspb.2018.0961. Leach, W.E., 1817, Distribution systématique de la classedes Cirripèdes: Jour- Sadler, J., Carre, M., Azzoug, M., Schauer, A.J., Ledesma, J., et al., 2012, nal de Physique de Chimie et d’Histoire Naturelle, v. 85, p. 67–69. Reconstructing past upwelling intensity and the seasonal dynamics of pri- LeDuc, R.G., Weller, D.W., Hyde, J., Burden, A.M., Rosel, P.E., Brownell, R.L., mary productivity along the Peruvian coastline from mollusk shell stable Wursig, B., and Dizon, A.E., 2002, Genetic differences between western isotopes: Geochemistry, Geophysics, Geosystems, v. 13, Q01015. https:// and eastern gray whales (Eschrichtius robustus): Journal of Cetacean doi.org/10.1029/2011GC003595. Research and Management, v. 4, p. 1–5. Savoyat, E., 1971, Leyenda explicativa de la hoja de Montecristi, 1/100.000: Lilljeborg W., 1861, Hvalben funna ijorden på Gräsön I Roslagen i Sverige: Forhan- Quito, Ecuador, Departamento de Investigacion Geologica, Ministero de dlinger ved de skandinaviske Naturforskeres, Kopenhagen, v. 8, p. 599–616. Recursos Naturales y Turismo, Direccion General de Geologia y Minas, 6 p. Lindberg, D.L., 1991, Marine biotic interchange between the northern and Scarff, J.E., 1986, Occurrence of the barnacles Coronula diadema, C. reginae, southern hemispheres: Paleobiology, v. 17, p. 308–324. and Cetopirus complanatus (Cirripedia) on right whales: The Scientific Lindsey, E.L., and Lopez, E.X., 2015, Tanque Loma, a new late-Pleistocene Reports of the Whales Research Institute, v. 37, p. 129–153. megafaunal tar seep locality from southwest Ecuador: Journal of South Seilacher, A., 2005, Whale barnacles: exaptational access to a forbidden para- American Earth Sciences, v. 57, p. 61–82. dise: Paleobiology, v. 31, p. 27–35. Linnaeus, C., 1767, Systema Naturae per regna tria naturae, secundum Classes, Sheidat, M., Castro, C., Denkinger, J., Gonzalez, J., and Adelung, D., 2000, A Ordines, Genera, Species, cum characteribus, differentiis, synonymis, locis. breeding area for humpback whales (Megaptera novaeangliae) off Ecuador: Editio Duodecima, Reformata. Tom. I. Pars II: Holmiae, Laurentii Salvii, Journal of Cetacean Research, v. 2, p. 165–171. p. 533–1327. Sheppard, G., 1930, The geology of south western Ecuador: American Associ- Marchant, S., 1961, A photogeological analysis of the structure of the western ation of Petroleum Geologists Bulletin, v. 14, p. 263–309. Guayas Province, Ecuador: with discussion of the stratigraphy and Tablazo Slater, G.J., Goldbogen, J.A., and Pyenson, N.D., 2017, Independent evolution Formation, derived from surface mapping: Geological Society [London] of baleen whale gigantism linked to Plio-Pleistocene ocean dynamics: Pro- Journal, v. 117, p. 215–233. ceedings of the Royal Society B: Biological Sciences, v. 284, 20170546. Martins, C.C.A., Morete, M.E., Engel, M.H., Freitas, A.C., Secchi, E.R., and https://doi.org/10.1098/rspb.2017.0546. Kina, P.G., 2000, Aspects of habitat use patterns of humpback whales in Swartz, S.L., 2018, Gray whale: Eschrictius robustus, in Würsig B., Thewissen, the Abrolhos Bank, Brazil, breeding ground: Memoirs of the Queensland J.G.M., Kovacs, K., eds., Encyclopedia of Marine Mammals, 3rd Edition: Museum, v. 47, p. 563–570. Cambridge, Massachusetts, Academic Press, p. 422–428. Mate, B.R., Ilyashenko, V.Y., Bradford, A.L., Vertyankin, V.V., Tsidulko, G.A., Swartz, S.L., Taylor, B.L., and Rugh, D.J., 2006, Gray whale Eschrichtius Rozhnov, V.V., and Irvine, L.M., 2015, Critically endangered western gray robustus population and stock identity: Mammal Review, v. 36, p. 66–84. whales migrate to the eastern North Pacific: Biology Letters, v. 4, 20150071. Taylor, L.D., O’Dea, A., Bralower, T.J., and Finnegan, S., 2019, Isotopes from https://doi.org/10.1098/rsbl.2015.0071. fossil coronulid barnacle shells record evidence of migration in multiple Monroe, R., 1981, Studies in the Coronulidae (Cirripedia): shell morphology, Pleistocene whale populations: Proceedings of the National Academy of growth, and function, and their bearing on subfamily classification: Mem- Sciences, v. 116, 201808759. https://doi.org/10.1073/pnas.1808759116. oirs of the Queensland Museum, v. 20, p. 237–251. Tsai, C. H., Fordyce, R. E., Chang, C. H., and Lin, L. K., 2014, Quaternary fos- Newman, W.A., and Abbott, D.P., 1980, Cirripedia: the barnacles, in Morris, sil gray whales from Taiwan: Paleontological Research, v. 18, p. 82–93. R.H., Abbot, D.P., and Haderlie, E.C., eds., Intertidal Invertebrates of Cali- Tsai, C. H., and Boessenecker, R. W., 2015, An early Pleistocene gray whale fornia: Palo Alto, California, Stanford University Press, p. 504–535. (Cetacea: Eschrichtiidae) from the Rio Dell Formation of northern Califor- Newman, W.A., and Ross, A., 1976, Revision of the balanomorph barnacles; nia: Journal of Paleontology, v. 89, p. 103–109. including a catalog of the species: San Diego Society of Natural History Tsuchi, R., Shuto, T., Takayama, T., Fujiyoshi, A., Koizumi, I., Ibaraki, M., and Memoir, v. 9, p. 1–108. Tirado, G.R., 1988, Fundamental data on Cenozoic biostratigraphy of the Noakes, S.E., Pyenson, N.D., and McFall, G., 2013, Late Pleistocene gray Pacific coast of Ecuador, in Tsuchi, R., ed., Trans-Pacific Correlation of whales (Eschrictius robustus) offshore Georgia, U.S.A., and the antiquity Cenozoic Geohistory: Shizuoka, Japan, Reports of Andean Studies, Shizu- of gray whale migration in the North Atlantic Ocean: Palaeogeography, oka University Special Volume 2, p. 23–43. Palaeoclimatology, Palaeoecology, v. 392, p. 502–509. Whittaker, J.E., 1988, Benthic Cenozoic Foraminifera from Ecuador: Tax- Nogata, Y., and Matsumura, K., 2005, Larval development and settlement of a onomy and Distribution of Smaller Benthic Foraminifera from Coastal whale barnacle: Biology Letters, v. 2, p. 92–93. Ecuador (Late Oligocene–Late Pliocene): London, British Museum (Natural Pack, A.A., Herman, L.M., Craig, A.S., Spitz, S.S., Waterman, J.O., Hermn, E.Y.K., History), 194 p. Deakos, M.H., Hakala, S., and Lowe, C., 2017, Habitat preferences by individ- Zullo, V.A., 1961, A new whale barnacle from Late Pleistocene deposits at San ual humpback whale mothers in the Hawaain breeding grounds vary with the Quintín Bay, Baja California: The Veliger, v. 4, p. 13–14. age and size of their calves: Animal Behaviour, v. 133, p. 131–144. Zullo, V.A., 1969, Thoracic Cirripedia of the San Diego Formation, San Diego Pilsbry, H.A., 1916, The sessile barnacles (Cirripedia) contained in the collec- County, California: Contributions in Sciences, v. 159, p. 1–25. tions of the U.S. National Museum; including a monograph of the American species: United States National Museum Bulletin, v. 93, p. 1–366. Pilsbry, H.A., and Olsson, A.A., 1941, A Pliocene fauna from Western Ecuador: Proceedings of the Academy of Natural Sciences of Philadelphia, v. 93, Accepted: 1 November 2021 p. 1–80. Downloaded from https://www.cambridge.org/core. IP address: 95.169.224.204, on 14 Jan 2022 at 09:37:26, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/jpa.2021.113