Trophic flexibility within the oldest Cervidae lineage to persist through the Miocene Climatic Optimum

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Abstract

The oldest known Cervidae lineage, Procervulus, is a useful example for understanding the adaptations of mammalian clades to climatic and environmental changes. It appeared in the Lower Miocene (MN3), persisted through the Miocene Climatic Optimum, and became extinct at the onset of the Mid-Miocene general cooling. A combined approach of dental microwear and mesowear is undertaken to reconstruct its feeding behaviour to learn whether and how it responded to new environmental circumstances. None of the Early and Middle Miocene fossil taxa in the Calatayud–Daroca and Rubielos de Mora basins (NE Spain) had a wholly browser or grazer lifestyle, but rather dietary strategies equaling those of extant mixed feeders. However, members of Procervulus were sensitive to changes in the structure of ecosystems and vegetation that occurred during the Middle Miocene, and responded to these by substantially increasing the intake of grasses and abrasives. Despite this, it did not apparently display the sufficiently high trophic flexibility to bring about a change in its feeding style. Two possible, probably interrelated, causes can be pointed out; constraints imposed by both its small body size and its brachydont cheek teeth. If such a change in the feeding style was crucial for its survival, Procervulus disappeared as a consequence of an insufficient response to environmental changes because it may have been unable to compensate for the low nutritional content and abrasiveness of the new food items over a prolonged period. As the last Procervulus and the first bovids in the basin have similar dental wear signals, competition could be another possible explanation for its disappearance. Middle Miocene Procervulus could have been at a clear disadvantage after the advent of Tethytragus, whose teeth present morphologies that suggest better adaptation to grass-eating. Since diets tend to reflect habitats, the wear signals and assignments obtained from the Ramblian and earliest Aragonian cervids are indicative of humid climates and mixed environments, where closed areas were well developed and browse vegetation was abundant. In contrast, data from late Early and Middle Aragonian cervids and bovids reflect dry-seasonal and more open scenarios, with a higher diversity of grasses and abrasives.

Introduction

An important interval in the global climatic and evolution of terrestrial mammalian faunas was the Early to Middle Miocene (Zachos et al., 2001). The cooling and rapid expansion of Antarctic continental ice-sheets that took place in the earliest Oligocene persisted until the latter part of the Oligocene, when a global and gradual warming trend reduced the extent of the ice (the warmest since the late Eocene; Flower and Kennett, 1994). From this point until the Middle Miocene the global ice volume remained low, and bottom water temperatures were slightly higher (Miller et al., 1991a, Wright et al., 1992). This warm and humid period, characterized by tropical and dry conditions in the basins of NE Spain (van der Meulen and Daams, 1992), peaked in the Middle Miocene Climatic Optimum, and was followed by a sudden decrease in temperature, the Mid-Miocene cooling, related to the reestablishment of the east Antarctic ice-sheet (Miller et al., 1991b, Zachos et al., 2001, Shevenell et al., 2004, Lewis et al., 2008).

This succession of events, associated with tectonic processes and sea-level oscillations, had enormous consequences on ecosystems, and therefore, on the further evolution of terrestrial mammalian faunas. Antarctica terrestrial organisms were obviously most affected (Lewis et al., 2008), but the European artiodactyls and perissodactyls also witnessed drastic changes in paleoenvironmental conditions (Zachos et al., 2001), and were some of the groups most significantly affected. Extinction, migration, or adaptation to the new conditions, for example, are some of the most important bioevents commonly attributed to major changes, and are well-known to have occurred during this epoch (Pickford and Morales, 1994).

Therefore, the Early to Middle Miocene is one of the most remarkable and interesting intervals for investigating the influence of global climatic changes on local environments, and the adaptive response of mammals that were highly sensitive to the shifts occurred.

In order to obtain paleoclimatic and paleoenvironmental reconstructions as accurately as possible, we must look for the characterization of taxa that respond to changes in terms of adaptive strategies. Ruminants are particularly suitable for reconstruction, and consequently are among the most frequently utilized paleoecological indicators (Gordon and Illius, 1994). This is due to the fact that they are entirely dependent on different types of plants for nutrition and, therefore, adapted to a wide variety of habitats, and also because of their ubiquity at fossil sites.

Interestingly, we have a well-documented and continuous record (4 Ma) of a ruminant lineage (Procervulus, Cervidae) that persisted through the Miocene Climatic Optimum, but which became extinct at the onset of the Mid-Miocene cooling. We consider this lineage as a useful example for understanding the problems that certain mammalian clades encounter when trying to adapt to new local environmental conditions; perhaps by being unable to sufficiently exhibit the trophic flexibility to respond to a change in the structure of the vegetation. As Procervulus was also coincident with the first bovids in the basin (Tethytragus, Bovidae), both groups should have competed directly, and its disappearance could have also been a consequence of food competition with these new, though better morphologically adapted, taxa.

Since cervids and bovids from northeast Spain witnessed notable paleoenvironmental shifts that other authors have pointed out to have occurred during this temporal interval (van der Meulen and Daams, 1992), the main object of this study is to provide an accurate description of Procervulus feeding habits to learn whether and how this taxon responded to changes (dietary response). It could be expected that potential changes strong enough to promote certain important faunistic events would affect the abundance of vegetation and, consequently, would have an immediate and recordable effect on dietary signals. It is also our aim to better reconstruct the environmental context of northeast Spain during the Early and Middle Miocene by attempting to provide information on aridity and seasonality, how open the habitat was or how widespread grasses were.

Section snippets

Geographical setting and data collection

We studied fossil material housed in the Museo Paleontológico de la Universidad de Zaragoza (Zaragoza, Spain), Museo Nacional de Ciencias Naturales-CSIC (Madrid, Spain) and Instituut voor Aardwetenschappen, Rijksuniv (Utrecht, Holland). The material belongs to the Neogene Calatayud–Daroca and Rubielos de Mora basins, which are located respectively in the north central and eastern Iberian Chain, NE Spain (Fig. 1). The basins of these areas display well exposed Early–Middle Miocene deposits

Results and description

Presented in Table 1 are micro- and mesowear summary results and also the number of specimens measured in the sample and the basin to which they belong.

Paleodietary reconstruction

Both microwear and mesowear analyses resulted in similar feeding assignments for most of the fossil species investigated. PVALT and PMUN1 however had significantly different habits from those of the rest, showing an exclusive specialization on grass and browse, respectively. It must be emphasized that there was no important incongruity, in the sense that no case was classified as a browser in one methodology and as a grazer in the other. The discrepancies between micro- and mesowear patterns

Conclusion

The combined approach of dental microwear and mesowear analysis has successfully reconstructed the feeding behaviour of Procervulus and Tethytragus from NE Spain, and, consequently, the climatic and environmental conditions that took place during the Early and Middle Miocene.

None of the species in the Calatayud–Daroca and Rubielos de Mora basins had a wholly browser or grazer lifestyle, but rather dietary strategies equaling those of extant mixed feeders. However, despite some samples being not

Acknowledgements

Authors wish to thank people who, in one way or another, have contributed to the field work and the study of the material. We also thank M. Fortelius for his help and valuable comments that substantially improved the mesowear analysis. This research was supported by the Spanish Ministerio de Educación y Ciencia (Plan Nacional I + D, projects CGL2004-00400 and CGL2005-03900/BTE, and a FPU predoctoral grant to D.DM.) and by the Government of Aragón (E05). Excavations were funded and supported by

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