1 This is the peer reviewed version of the following article: Tsai C-H, Collareta A, Fitzgerald
2 EMG, et al. (2017) Northern pygmy right whales highlight Quaternary marine mammal
3 interchange. Current Biology, 27, R1058-R1059, which has been published in final form at
4 http://www.cell.com/current-biology/fulltext/S0960-9822(17)31096-5.
5
6 Northern pygmy right whales highlight Quaternary marine
7 mammal interchange
8
9 Cheng-Hsiu Tsai1,2,†, Alberto Collareta3,4,†, Erich M. G. Fitzgerald5,6, Felix G.
10 Marx5,7,8,*, Naoki Kohno1,9, Mark Bosselaers8,10, Gianni Insacco11, Agatino Reitano11,
11 Rita Catanzariti12, Masayuki Oishi13,14 and Giovanni Bianucci3
12
13
14 The pygmy right whale, Caperea marginata, is the most enigmatic living whale.
15 Little is known about its ecology and behaviour, but unusual specialisations of visual
16 pigments [1], mitochondrial tRNAs [2], and postcranial anatomy [3] suggests a
17 lifestyle different from that of other extant whales. Geographically, Caperea
18 represents the only major baleen whale lineage entirely restricted to the Southern
19 Ocean. Caperea-like fossils, the oldest of which date to the Late Miocene, are
20 exceedingly rare and likewise limited to the Southern Hemisphere [4], despite a more
21 substantial history of fossil sampling north of the equator. Two new Pleistocene
22 fossils now provide unexpected evidence of a brief and relatively recent period in
23 geological history when Caperea occurred in the Northern Hemisphere.
24 The new material, referable to Caperea sp. and cf. Caperea, respectively,
25 consists of a fragmentary skull with ear bones (USNM 358972) from the upper
26 portion of the Naha Formation of Okinawa-jima, Japan, dating to 0.9–0.5 Ma; and a
27 tympanic bulla (MSNC 4451) from an unnamed deposit on Penisola Maddalena, near
28 Syracuse (Sicily, Italy), dating to 1.9–1.7 Ma (Supplemental Information). The
29 tympanic bullae of both specimens are highly diagnostic, and identifiable based on
30 their (i) rectangular Eustachian outlet; (ii) flattened involucrum lacking any sign of an
31 inner posterior prominence; (iii) broadly convex medial margin; (iv) prominent,
32 angular anteromedial corner; and (v) L-shaped dorsal profile of the involucrum
33 (Figure 1). USNM 358972 furthermore shares with extant Caperea the presence of
34 (vi) an elongate squamosal fossa; (vii) a foramen pseudovale enclosed entirely by the
35 pterygoid; (viii) a narrow, sulcus-like Eustachian notch; (ix) a delicate connection
36 between the anterior process and the body of the periotic; (x) an anteriorly directed
37 anteroexternal sulcus on the anterior process of the periotic; and (xi) a robust, conical
38 and externally exposed compound posterior process of the tympanoperiotic (Figure 1;
39 Supplemental Information). In features (vii) and (ix), USNM 358972 differs from the
40 only named extinct relative of Caperea, Miocaperea pulchra, from the Late Miocene
41 of Peru [5]. MSNC 4451 and Miocaperea currently cannot be compared as the bulla
42 morphology remains unknown for the latter. Nevertheless, the notable similarity of
43 MSNC 4451 and living pygmy right whales justifies referral to cf. Caperea.
44 The Northern Hemisphere material of Caperea could conservatively be
45 interpreted as extralimital occurrences of the living species, yet it also provides 40%
46 of the total putative fossil record of the family, two thirds of the undisputed record,
47 and the only fossil evidence of Caperea itself [4]. Considering the vagaries of fossil
48 preservation, the occurrence of two geologically young northern specimens is thus
49 likely more than a chance event. Instead, the striking absence of Caperea in
50 comparatively well-studied northern Miocene–Pliocene fossil assemblages suggests a
51 Pleistocene ecological regime change. The latter was presumably glacially-driven,
52 e.g. via changes in seasonal nutrient distributions, and temporarily allowed localised
53 marine mammal species to disperse across the normally impermeable tropics.
54 Evidence of such dispersal exists among living cetaceans and pinnipeds in the form of
55 antitropical species pairs, such as Eubalaena, Lissodelphis and Mirounga
56 (Supplemental Discussion).
57 The new Caperea fossils from the Northern Hemisphere demonstrate that
58 there was likely a greater degree of marine faunal interchange during the Pleistocene
59 than hitherto assumed, and that it affected even highly localised specialists. In light of
60 our findings, other highly unusual occurrences, even southern walruses and northern
61 penguins, should be anticipated. The fact that the two fossils are separated by as much
62 as one million years raises the tantalising possibility that a separate long-lived
63 population, or even species, of Caperea may once have inhabited northern seas.
64 Given the sparseness of available material, it is equally likely, however, that Caperea
65 crossed the equator more than once during successive glacial periods (Supplementary
66 Material), and then disappeared again as interglacial conditions interrupted the
67 connection with the south.
68 Together, extant antitropical species pairs and sudden range extensions like
69 that of Caperea emphasise that, at times, physical and biotic barriers play a major role
70 in marine mammal evolution [6, 7]. The Pleistocene with its constant change between
71 glacial and interglacial conditions is a prime example, with the relaxation and
72 subsequent re-establishment of an equatorial barrier driving range extensions,
73 speciations and, in the case of Caperea, local extinctions. A globally poor Pleistocene
74 fossil record likely obscures the true extent of this Quaternary marine interchange.
75 Nevertheless, faunal interchange during the Pleistocene had a pronounced effect on
76 marine mammal richness and community structure, and can be seen as the last major
77 step in the emergence of modern marine mammal assemblages. This adds a new layer
78 on to previous studies, which suggested that faunal modernisation primarily occurred
79 in response to a related, yet independent (Late) Pliocene turnover event (Supplemental
80 Discussion).
81 While Pliocene turnover was likely driven by the onset of Northern
82 Hemisphere glaciation (resulting in the loss of coastal habitats) [8], the Quaternary
83 marine interchange is related to the change between glacial and interglacial periods,
84 and as such still ongoing – albeit now with a human dimension. Just as glacial-
85 interglacial dynamics affect marine barriers to dispersal, anthropogenic climate
86 change may ultimately drive a reorganisation of current marine mammal ranges, with
87 implications for future speciation and, crucially, extinction. For example, a warmer
88 world might see poleward range shifts among extant marine mammals [9] and the
89 establishment of a ‘permanent’ El Niño state in the tropics [10], thereby cementing
90 the impassability of the equator and further restricting (or obliterating) gene flow
91 between existing populations.
92
93 SUPPLEMENTAL INFORMATION
94 Supplemental Information including further details on morphology and stratigraphic
95 context can be found with this article online at XXX
96
97 AUTHOR CONTRIBUTIONS
98 A.R. discovered and G.I. collected MSNC 4451. M.O., A.C. and M.B. first identified
99 the fossils. A.C., R.C., N.K., C.-H.T. and F.G.M. established their provenance and
100 age. F.G.M, E.M.G.F. and G.B. organised the collaborative project. All authors
101 discussed and wrote the paper.
102
103 ACKNOWLEDGEMENTS
104 C.-H.T. was funded by a University of Otago Doctoral Scholarship and a postdoctoral
105 fellowship from the Japan Society for the Promotion of Science (P15329). E.M.G.F.
106 was supported by a postdoctoral fellowship from the Smithsonian Institution, and
107 funding from the Harold Mitchell Foundation and Museums Victoria. F.G.M. was
108 funded by an EU Marie Skłodowska-Curie Global Postdoctoral fellowship (656010/
109 MYSTICETI) and by a postdoctoral fellowship from the Japan Society for the
110 Promotion of Science (P13505). N.K. was funded by a JSPS Grant-in-Aid for
111 Scientific Research C (15K05333). M.O. was funded by an Oversea Dispatch
112 Training for Curators of the Ministry of Education, Japan and Kamei Social-
113 Education Promotion Foundation. N. Pyenson, D. Bohaska, the late F. Whitmore, J.
114 Mead, C. Potter, J. Ososky, K. Date, K. Roberts, O. Lambert and S. Bruaux provided
115 access to museum collections. Thanks to O. Lambert and two anonymous reviewers
116 for their helpful comments, as well as C. Buell for his illustration.
117
118 REFERENCES
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131 5. Bisconti, M. (2012). Comparative osteology and phylogenetic relationships of 132 Miocaperea pulchra, the first fossil pygmy right whale genus and species 133 (Cetacea, Mysticeti, Neobalaenidae). Zool J Linn Soc Lond 166, 876-911. 134 6. Davies, J.L. (1963). The antitropical factor in cetacean speciation. Evolution 135 17, 107-116. 136 7. Lindberg, D.R. (1991). Marine biotic interchange between the northern and 137 southern hemispheres. Paleobiology 17, 308-324. 138 8. Pimiento, C., Griffin, J.N., Clements, C.F., Silvestro, D., Varela, S., Uhen, 139 M.D., and Jaramillo, C. (2017). The Pliocene marine megafauna extinction 140 and its impact on functional diversity. Nature Ecology & Evolution. 141 9. Kaschner, K., Tittensor, D.P., Ready, J., Gerrodette, T., and Worm, B. (2011). 142 Current and future patterns of global marine mammal biodiversity. PLOS 143 ONE 6, e19653. 144 10. Fedorov, A.V., Dekens, P.S., McCarthy, M., Ravelo, A.C., deMenocal, P.B., 145 Barreiro, M., Pacanowski, R.C., and Philander, S.G. (2006). The Pliocene 146 paradox (mechanisms for a permanent El Niño). Science 312, 1485-1489. 147
148 †These authors contributed equally to the work; 1Department of Geology and
149 Palaeontology, National Museum of Nature and Science, Tsukuba, Japan.
150 2Department of Geology, University of Otago, Dunedin, New Zealand. 3Dipartimento
151 di Scienze della Terra, Universitá di Pisa, Pisa, Italy. 4Dottorato Regionale in Scienze
152 della Terra Pegaso, Pisa, Italy. 5Geosciences, Museums Victoria, Melbourne, Vic.,
153 Australia. 6National Museum of Natural History, Smithsonian Institution,
154 Washington, DC, USA. 7School of Biological Sciences, Monash University, Clayton,
155 Vic., Australia. 8D.O. Terre et Histoire de la Vie, Institut Royal des Sciences
156 Naturelles de Belgique, Brussels, Belgium. 9Graduate School of Life and
157 Environmental Sciences, University of Tsukuba, Tsukuba,
158 Japan. 10Koninklijk Zeeuwsch Genootschap der Wetenschappen, Middelburg, The
159 Netherlands. 11Museo Civico di Storia Naturale di Comiso, Comiso, Ragusa, Italy.
160 12Istituto di Geoscienze e Georisorse, IGG-CNR, Pisa, Italy. 13Iwate Prefectural
161 Museum, Morioka, Japan. 14Tohoku University Museum, Sendai, Japan. *E-mail:
163
164 Figure 1. Pygmy right whales in the Northern and Southern hemispheres. (A)
165 Global map showing the presumed distribution of extant Caperea marginata (in blue),
166 Caperea fossils from the Northern Hemisphere (red squares), and Caperea-like fossils
167 from the Southern Hemisphere (green squares). (B) Global sea level change over time
168 compared to the age of the fossils shown in (A). See Supplemental Information for
169 data sources. Note the clustering of Northern Hemisphere specimens during the
170 Pleistocene. (C) Right periotic and compound posterior process of extant Caperea
171 marginata, NMV C28531, compared to Caperea sp., USNM 358972. (D) Tympanic
172 bulla of extant Caperea marginata, NMNZ MM002119 (right bulla, mirrored
173 horizontally for comparison), compared to (E) Caperea sp., USNM 358972 and (F)
174 cf. Caperea, MSNC 4451. Drawing of Caperea by Carl Buell.
175
176 eTOC blurb
177 Tsai et al. show that pygmy right whales, Caperea marginata, occurred in the
178 Northern Hemisphere during the Pleistocene. Glacial cooling allowed marine
179 mammals to cross the tropics and disperse across both hemispheres, leading to range
180 extensions, antitropical speciation and, at times, local extinctions that shaped the
181 modern marine mammal fauna.