Abstract
We tested the validity of Bergmann’s rule and Rosenzweig’s hypothesis through an analysis of the geographical variation of the skull size of Otaria flavescens along the entire distribution range of the species (except Brazil). We quantified the sizes of 606 adult South American sea lion skulls measured in seven localities of Peru, Chile, Uruguay, Argentina, and the Falkland/Malvinas Islands. Geographical and environmental variables included latitude, longitude, and monthly minimum, maximum, and mean air and ocean temperatures. We also included information on fish landings as a proxy for productivity. Males showed a positive relationship between condylobasal length (CBL) and latitude, and between CBL and the six temperature variables. By contrast, females showed a negative relationship between CBL and the same variables. Finally, female skull size showed a significant and positive correlation with fish landings, while males did not show any relationship with this variable. The body size of males conformed to Bergmann’s rule, with larger individuals found in southern localities of South America. Females followed the converse of Bergmann’s rule at the intraspecific level, but showed a positive relationship with the proxy for productivity, thus supporting Rosenzweig’s hypothesis. Differences in the factors that drive body size in females and males may be explained by their different life-history strategies. Our analyses demonstrate that latitude and temperature are not the only factors that explain spatial variation in body size: others such as food availability are also important for explaining the ecogeographical patterns found in O. flavescens.
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References
Aldrich JW, James FC (1991) Ecogeographic variation in the American robin (Turdus migratorius). Auk 108:230–249
Amano M, Miyazaki N (1992) Ecographic variation and sexual dimorphism in the skull of Dall’s porpoise, Phocoenoides dalli. Mar Mammal Sci 8:240–261
Ashton KG (2001) Body size variation among mainland populations of the western rattlesnake (Crotalus viridis). Evolution 55:2523–2533
Ashton KG (2004) Are there general intraspecific patterns of body size variation in relation to latitude (and temperature) for tetrapod vertebrates? Integr Comp Biol 44:401–412
Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415
Beddington J (1995) The primary requirements. Nature 374:213–214
Berta A, Sumich JL (1999) Marine mammals. Evolutionary biology. Academic, San Diego
Blanckenhorn WU, Demont M (2004) Bergmann and converse Bergmann latitudinal clines in arthropods, two ends of a continuum? Integr Comp Biol 44:413–424
Blois JL, Feranec RS, Hadly EA (2008) Environmental influences on spatial and temporal patterns of body-size variation in California ground squirrels (Spermophilus beecheyi). J Biogeogr 35:602–613
Boyce MS (1978) Climatic variability and body size variation in the muskrats (Ondatra zibethicus) of North America. Oecologia 36:1–19
Brunner S, Shaughnessy PD, Bryden MM (2002) Geographic variation in skull characters of fur seals and sea lions (family Otariidae). Aust J Zool 50:415–438
Campagna C, Le Boeuf BJ (1988) Reproductive behaviour of Southern sea lions. Mar Mammal Sci 104:233–261
Cappozzo HL, Perrin WF (2009) South American sea lion Otaria flavescens. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Elsevier, Amsterdam, pp 1076–1079
Case TJ (1978) A general explanation for insular body size trends in terrestrial vertebrates. Ecology 59:1–18
Cruwys E, Friday AE (1995) A comparative review of condylobasal lengths and other craniometric characters in 30 species of pinniped. Polar Rec 31:45–62
Dayan T, Simberloff D, Tchernov E, Yom-Tov Y (1991) Calibrating the paleothermometer: climate, communities, and the evolution of size. Paleobiology 17:189–199
FAO (2003) Yearbook of fisheries statistics. FAO, Rome
Feijoo M, Lessa EP, Loizaga de Castro R, Crespo EA (2011) Mitochondrial and microsatellite assessment of population structure of South American sea lion (Otaria flavescens) in the Southwestern Atlantic Ocean. Mar Biol 158:1857–1867
Ferguson SH, Lariviere S (2008) How social behaviour links environment and body size in mammalian carnivores. Open Ecol J 1:1–7
Fleischer RC, Johnson RF (1982) Natural selection on body size and proportions in house sparrows. Nature 298:747–749
Futuyma DJ (1998) Evolutionary biology, 3rd edn. Sinauer, Sunderland
Gaston KJ, Blackburn TM (2000) Pattern and process in macroecology. Blackwell, Oxford
Guill JM, Hoo CS, Heins DC (2003) Body shape variation within and among three species of darters (Perciformes: Percidae). Ecol Freshw Fish 12:134–140
Higdon JW (2011) Biogeography and conservation of the pinnipeds (Carnivora: Mammalia) (Ph.D. dissertation). Department of Environment and Geography, University of Manitoba, Winnipeg
James FC (1970) Geographic size variation in birds and its relationship to climate. Ecology 51:365–390
Katti M, Price TD (2003) Latitudinal trends in body size among over-wintering leaf warblers (genus Phylloscopus). Ecography 26:69–79
Khokhlova I, Krasnov BR, Shenbrot GI, Degen A (2000) Body mass and environment: a study in Negev rodents. Isr J Zool 46:1–13
King JE (1983) Seals of the world, 2nd edn. Cornell University Press, New York
Lindenfors P, Tullberg BS, Biuw M (2002) Phylogenetic analyses of sexual selection and sexual size dimorphism in pinnipeds. Behav Ecol Sociobiol 52:188–193
Lindsay SL (1986) Geographic size variation in Tamiasciurus douglasii: significance in relation to conifer cone morphology. J Mammal 67:317–325
Majluf P (1991) El Niño effects on pinnipeds in Peru. Pinniped and El Niño, responses to environmental stress. In: Trillmich F, Ono KA (eds) Animal species and evolution. Springer, Berlin, pp 55–65
Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge
McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52:845–854
Medina AI, Marti DA, Bidau CJ (2007) Subterranean rodents of the genus Ctenomys (Caviomorpha, Ctenomyidae) follow the converse to Bergmann’s rule. J Biogeogr 34:1439–1454
Meiri S (2011) Bergmann’s rule—what’s in a name? Global Ecol Biogeogr 20:203–207
Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351
Meiri S, Dayan T, Simberloff D (2004) Carnivores, biases and Bergmann’s rule. Biol J Linn Soc 81:579–588
Meiri S, Dayan T, Simberloff D (2005) Variability and correlations in carnivore crania and dentition. Funct Ecol 19:337–343
Meiri S, Yom-Tov Y, Geffen E (2007) What determines conformity to Bergmann’s rule? Global Ecol Biogeogr 16:788–794
Neira S, Arancibia H (2004) Trophic interactions and community structure in the Central Chile marine ecosystem (33°S-39°S). J Exp Mar Biol Ecol 312:349–366
Olifiers N, Vieira MV, Grelle CEV (2004) Geographic range and body size in Neotropical marsupials. Global Ecol Biogeogr 13:439–444
Oliveira LR, Malabarba LR, Majluf P (1999) Variação geográfica em crânios do lobo-marinho sul-americano Arctocephalus australis (Zimmermann, 1783) das populações do Brasil e Peru. Comunicações do Museu de Ciências e Tecnologia da PUCRS. Sér zoologia 12:179–192
Oliveira LR, Hoffman JI, Hingst-Zaher E, Majluf P, Muelbert MMC, Morgante JS, Amos W (2008) Morphological and genetic evidence for two evolutionarily significant units (ESUs) in the South American fur seal, Arctocephalus australis. Conserv Genet 9:1451–1466
Pauly D, Christensen V (1995) Primary production required to sustain global fisheries. Nature 374:255–257
Ralls K (1976) Mammals in which females are larger than males. Q Rev Biol 51:245–276
Ralls K, Mesnick SL (2002) Sexual dimorphism. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Elsevier, Amsterdam, pp 1071–1078
Rosenzweig ML (1968) The strategy of body size in mammalian carnivores. Am Midl Nat 80:299–315
Ross GJB, Cockcroft VC (1990) Comments on Australian bottlenose dolphins and the taxonomic status of Tursiops aduncus (Ehrenberg, 1832). In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic, New York, pp 101–128
Sivertsen E (1954) A survey of the eared seals (family Otariidae) with remarks on the Antarctic seals collected by M/K “Norvegia” in 1928–1929 (scientific results of the Norwegian Antarctic expeditions). Det Norske Videnskaps-Akademi, Oslo, pp 1927–1928
Soto KH, Trites AW (2011) South American sea lions in Peru have a lek-like mating system. Mar Mammal Sci 27:306–333
Szapkievich VB, Capozzo HL, Crespo EA, Bernabeu RO, Comas C, Mudry M (1999) Genetic relatedness in two Southern sea lion (Otaria flavescens) rookeries in Southwestern Atlantic. Zeitschrift für Säugetierkunde 64:1–5
Thompson D, Duck CD, McConnell BJ, Garrett J (1998) Foraging behaviour and diet of lactating female southern sea lions (Otaria flavescens) in the Falkland Islands. J Zool 246:135–146
Vaz-Ferreira R (1982) South American sea lion, Otaria flavescens. In: Ridgway SH, Harrison RJ (eds) Handbook of marine mammals: the walrus, sea lions, fur seal and sea otters, vol 1. Academic, London, pp 39–65
Wiggington JD, Dobson FS (1999) Environmental influences on geographic variation in body size of western bobcats. Can J Zool 77:802–813
Yom-Tov Y, Geffen E (2006) Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 148:213–218
Yom-Tov Y, Yom-Tov S, Baagøe H (2003) Increase of skull size in the red fox (Vulpes vulpes) and Eurasian badger (Meles meles) in Denmark during the twentieth century: an effect of improved diet? Evol Ecol Res 5:1037–1048
Yom-Tov Y, Yom-Tov S, Wright J, Thorne CJR, Du Feu R (2006) Recent changes in body weight and wing length among some British passerine birds. Oikos 112:91–101
Acknowledgments
We thank Ana Avalos for providing access to the otariid skull collection at Museo de Historia Natural de Valparaíso in 1980. We also thank Enrique González of the Museo Nacional de Historia Natural in Montevideo, and Roberto Portela, Mammal Section Curator, British Museum (National History), London, for providing access to specimens, and Javier Sánchez for help with the measurements. This study was supported by DIPUV Project NO. 44/2005 and CIGREN Project DIPUV-CID NO 01/03. We are indebted to many people from the Laboratorio de Mamíferos Marinos of the Centro Nacional Patagónico for their assistance in the field collecting specimens for the last 40 years. Institutional support for skull collection in Chubut was given by the Centro Nacional Patagónico (CONICET, Argentina). Permits were provided by the Secretaría de Áreas Protegidas y Turismo and Dirección de Fauna y Flora Silvestre, Chubut Province (Argentina). SNP and EAP acknowledge support from ANPCYT (PICT9801-04025), Conservación de la Diversidad Biológica Marina y Prevención de la Contaminación en Patagonia (GEF/PNUD ARG 02/018), Estudio de las amenazas para la conservación de mamíferos marinos de Patagonia (BBVA, BIOCON 04), and the South American Sea Lion Conservation Program of Amnéville Zoo, France. RNP Goodall’s research in Ushuaia, Tierra del Fuego (TdF), has been supported mainly by grants from the Committee for Research and Exploration (CRE) of the National Geographic Society. She is very grateful for the support of the coastal estancias (farms) in TdF and for the research assistance of many assistants and interns over the years.
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Communicated by Helene Marsh.
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Sepúlveda, M., Oliva, D., René Duran, L. et al. Testing Bergmann’s rule and the Rosenzweig hypothesis with craniometric studies of the South American sea lion. Oecologia 171, 809–817 (2013). https://doi.org/10.1007/s00442-012-2462-1
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DOI: https://doi.org/10.1007/s00442-012-2462-1