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Web Resource Partitioning Among Top Predators in a Miocene Food Downloaded from rspb.royalsocietypublishing.org on December 2, 2013 Resource partitioning among top predators in a Miocene food web M. Soledad Domingo, Laura Domingo, Catherine Badgley, Oscar Sanisidro and Jorge Morales Proc. R. Soc. B 2013 280, 20122138 first published online 7 November 2012 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2012/11/03/rspb.2012.2138.DC1.h tml References This article cites 51 articles, 5 of which can be accessed free http://rspb.royalsocietypublishing.org/content/280/1750/20122138.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections ecology (1477 articles) palaeontology (148 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on December 2, 2013 Resource partitioning among top predators in a Miocene food web M. Soledad Domingo1, Laura Domingo2, Catherine Badgley1, Oscar Sanisidro3 and Jorge Morales3 rspb.royalsocietypublishing.org 1Museum of Paleontology, University of Michigan, 1109 Geddes Avenue, Ann Arbor, MI 48109, USA 2Department of Earth and Planetary Sciences, University of California, 1156 High Street, Santa Cruz, CA 95064, USA 3Departamento de Paleobiolog´ıa, Museo Nacional de Ciencias Naturales CSIC, C/Jose´ Gutie´rrez Abascal 2, 28006 Madrid, Spain Research The exceptional fossil sites of Cerro de los Batallones (Madrid Basin, Spain) con- Cite this article: Domingo MS, Domingo L, tain abundant remains of Late Miocene mammals. From these fossil Badgley C, Sanisidro O, Morales J. 2013 assemblages, we have inferred diet, resource partitioning and habitat of three Resource partitioning among top predators in a sympatric carnivorous mammals based on stable isotopes. The carnivorans Miocene food web. Proc R Soc B 280: include three apex predators: two sabre-toothed cats (Felidae) and a bear dog (Amphicyonidae). Herbivore and carnivore carbon isotope (d13C) values 20122138. from tooth enamel imply the presence of a woodland ecosystem dominated http://dx.doi.org/10.1098/rspb.2012.2138 13 by C3 plants. d C values and mixing-model analyses suggest that the two sabre-toothed cats, one the size of a leopard and the other the size of a tiger, consumed herbivores with similar d13C values from a more wooded portion of the ecosystem. The two sabre-toothed cats probably hunted prey of different Received: 11 September 2012 body sizes, and the smaller species could have used tree cover to avoid encoun- Accepted: 16 October 2012 ters with the larger felid. For the bear dog, d13C values are higher and differ significantly from those of the sabre-toothed cats, suggesting a diet that includes prey from more open woodland. Coexistence of the sabre-toothed cats and the bear dog was likely facilitated by prey capture in different portions of the habitat. This study demonstrates the utility of stable isotope analysis for Subject Areas: investigating the behaviour and ecology of members of past carnivoran guilds. palaeontology, ecology Keywords: carnivoran, stable carbon isotopes, Miocene, 1. Introduction resource partitioning Apex predators occupy the peak of the trophic pyramid and, from that position, they are important regulators of the food web because they are partly respon- sible for limiting their prey populations, commonly herbivores, and, by Author for correspondence: controlling herbivory, they indirectly regulate vegetation [1]. The propagation M. Soledad Domingo of impacts by consumers on their prey through food webs was formalized in e-mail: [email protected] the concept of ‘trophic cascades’ [2]. The removal of apex predators from eco- systems, either from natural or anthropogenic causes, triggers reactions that cascade to the lowest trophic levels [3]. An intrinsic characteristic of species at the top of the consumer food web in terrestrial ecosystems is that they occur in low densities. In the fossil record, the common pattern is that herbivore remains far outnumber carnivoran remains [4]. Consequently, the scarce carni- voran remains have a particularly high value in systematic studies, and analyses that require destructive sampling (such as stable isotope analyses) are rarely permitted. Accordingly, ancient predator–prey systems remain understudied from the perspective of stable isotope geochemistry and this fact is more evident for older systems. Yet, in terms of stable isotope ecology, apex predators are particularly useful because their isotopic values typically represent multiple species of prey and, therefore, have the potential to convey Electronic supplementary material is available an integrated environmental signal [5]. at http://dx.doi.org/10.1098/rspb.2012.2138 or Exceptionally rich fossil sites present a unique opportunity to investigate via http://rspb.royalsocietypublishing.org. trophic interactions in ancient ecosystems. The fossil sites of Cerro de los Batallones (Madrid Basin, Spain; figure 1a) contain abundant, diverse and well-preserved remains of Late Miocene vertebrates (approx. 10–9 Ma; & 2012 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from rspb.royalsocietypublishing.org on December 2, 2013 (a) 2 (b) rspb.royalsocietypublishing.org Proc R Soc B 280: 20122138 FRANCE IBERIAN RANGE L A SPAIN G U T R O P Segovia CENTRAL 0 300 km Guadalajara E SISTEMA G Madrid N A R A R MADRID I Cerro de los M BASIN O Batallones T L A Toledo 4 cm TOLEDO MOUNTS sedimentary fill Cenozoic carbonate rocks Mesozoic N metamorphic rocks Paleozoic 0 50 km granites Figure 1. (a) Location of Cerro de los Batallones within the Madrid Basin. (b) Skull and mandible of Machairodus aphanistus (B-5445) from the fossil locality Batallones-1. Vallesian European Land Mammal Age [6,7]). The nine fossil By extension, d13C values from mammalian fossil enamel sites discovered thus far are concentrated in an area of 16 ha. are an important tool for reconstructing the type(s) of habitat Fossil remains occur in marls and siliciclastic sediments that where the animals lived. discordantly cut across the three sedimentary units defined In modern ecosystems with diverse carnivorous mammals, in the ridge, indicating that the fossil assemblages were the apex predators compete intensively over prey and carcasses deposited in cavities. Several independent chambers formed [16]. Differential use of resources (i.e. resource partitioning) by erosion of the clay matrix [8]. facilitates coexistence. Coexistence of predators is achieved The most remarkable feature of these fossil sites is that through numerous strategies, such as targeting different types two of the nine assemblages are overwhelmingly dominated of prey in terms of species, size and age classes, temporal sep- by mammalian carnivores [8]. In the other fossil sites, aration of predatory activity (diurnal versus nocturnal herbivore remains are far more abundant than carnivoran predators), mutual avoidance or differences in habitat use fossils. More than 92 per cent of the large-mammal specimens [17–19]. Here, we use stable isotope analyses to evaluate the (n 18 000) recovered from the lower-level assemblage of the predator–prey relationships and habitat partitioning of the locality Batallones-1 belong to 10 carnivoran taxa. These three largest carnivores and their potential ungulate prey include four species of Felidae (cats): two sabre-toothed cats species in Late Miocene Cerro de los Batallones localities. (Promegantereon ogygia and Machairodus aphanistus; figure 1b) We use a mixing-model for d13C values of the predators and and two felines (Styriofelis vallesiensis and an undescribed eight potential prey species to infer which herbivores were feas- species). In addition, a bear dog (Magericyon anceps)from ible prey for each predator. Because sample sizes of the three the extinct family Amphicyonidae, a primitive hyaena carnivorans are relatively large, we also use the variance in (Protictitherium crassum), an early relative of the red panda d13C values as a measure of the versatility of habitat use by (Simocyon batalleri), a marten (Martes sp.) and two relatives the predators. d13C values of the mammals are used to estimate of modern skunks (Proputorius sp. and Sabadellictis sp.) have gradients from open to closed habitats within the original Mio- been recovered [8–10]. Geological and taphonomic evidence cene ecosystem. Compared with analyses of mammalian suggests that the dominance of carnivorans resulted from herbivores, stable isotope analyses of modern and Pleistocene preferential entrapment of these taxa in the chambers [8,11]. carnivores are infrequent (although increasing; [20–29]). The three carnivorans analysed here, the two sabre- Cerro de los Batallones localities offer a view into carnivore toothed cats and the amphicyonid, were apex predators in guilds that is rarely available and, to the best of our knowledge, this ecosystem (i.e. taxa with virtually no predators of their this study constitutes the first stable isotope analysis of own, except possibly each other). We evaluated their diet mammalian predator–prey relationships for a Miocene fauna. through comparison of their carbon isotopic values to those of relevant herbivore prey. Also, stable carbon isotope (d13C) analyses permitted us to investigate how these Miocene carnivorans partitioned the resources
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