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Life History and Ecology of Late Miocene Hipparionins from the Circum-Mediterranean Area

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Life History and Ecology of Late Miocene Hipparionins from the Circum-Mediterranean Area ADVERTIMENT. Lʼaccés als continguts dʼaquesta tesi queda condicionat a lʼacceptació de les condicions dʼús establertes per la següent llicència Creative Commons: http://cat.creativecommons.org/?page_id=184 ADVERTENCIA. El acceso a los contenidos de esta tesis queda condicionado a la aceptación de las condiciones de uso establecidas por la siguiente licencia Creative Commons: http://es.creativecommons.org/blog/licencias/ WARNING. The access to the contents of this doctoral thesis it is limited to the acceptance of the use conditions set by the following Creative Commons license: https://creativecommons.org/licenses/?lang=en PhD Thesis Doctorate in Biodiversity Life History and Ecology of Late Miocene Hipparionins from the Circum-Mediterranean Area Guillermo Orlandi Oliveras Supervisor Dra. Meike Köhler Institut Català de Paleontologia Miquel Crusafont Universitat Autònoma de Barcelona 2019 PhD Thesis – 2019 Life History and Ecology of Late Miocene Hipparionins from the Circum-Mediterranean Area Guillermo Orlandi Oliveras Dissertation presented by Guillermo Orlandi Oliveras in fulfillment of the requirements for the degree of Doctor in the Universitat Autònoma de Barcelona, doctorate program in Biodiversity of the Departament de Biologia Animal, Biologia Vegetal i d’Ecologia. Under the supervision of: - Dra. Meike Köhler, ICREA at Institut Català de Palaeontologia Miquel Crusafont and teacher of the Departament de Biologia Animal, Biologia Vegetal i d’Ecologia at Universitat Autònoma de Barcelona. Doctoral candidate Guillermo Orlandi Oliveras Supervisor Dra. Meike Köhler Abstract Hipparionins are a clade of tridactyl equids that greatly diversified during the late Miocene throughout the circum-Mediterranean area, with some taxa undergoing dwarfing. Due to their abundance, they have been the subject of several paleoecological studies and constitute a key mammalian group for exploring evolutionary patterns, although more research is necessary to better understand their ecology. One central aspect of an organism’s biology is its life history, which can be inferred from the analysis of bone and dental microstructure. In addition, since a species’ life history evolves relative to ecological conditions, its study can provide environmental information. Feeding ecology, another feature of an organism’s biology and an important link to its environment, can be inferred from dental microwear. With this in mind, the central aim of this thesis is to elucidate the ecological conditions and mechanisms that accompanied dwarfing in western and eastern Mediterranean hipparionins. Therefore, I (i) reconstruct the growth patterns of metapodials and molars in different-sized hipparionins using bone and dental histology, (ii) make inferences regarding their life histories, and (iii) examine their diets by studying dental microwear textures to test the ecological inferences obtained from life history analyses. Metapodial histology confirms the usefulness of metapodials for reconstructing the entire ontogenetic growth and establishing a relative maturity attainment. Therefore, the identification of different timings of metapodial growth cessation demonstrate distinct growth strategies within the hipparionins analyzed. For the first time among ungulates, the analysis of daily enamel laminations reveals higher growth rates in first/second molars compared to later-formed third molars, which suggests a link between dental development and somatic growth. Thus, the slower dental growth rates and the relatively late eruption timings (correlated with life history traits) in hipparionins indicate slower paces of life compared to Equus. This challenges previous assumptions that hipparionins have faster life histories due to their generally smaller body size. Western dwarf hipparionins, moreover, show an even slower dental development than larger forms, and a relatively late skeletal maturity, pointing to a slower life history than expected for their size. Conforming with life history theory, this evidences that dwarfing in these western hipparionins was led by lower resource availability. Conversely, the eastern small-sized form shows an advanced relative maturity, which indicates that its size decrease was triggered by higher extrinsic mortalities (predation). This scheme suggests that paleoenvironmental differences accounted for the distinct ecological pressures inferred: forested habitats in the western Mediterranean likely provided increased cover against predation but less resources for the hipparionins, while the more open habitats further east were riskier, but richer in resources. Dietary reconstructions reveal mixed-feeding diets and opportunistic feeding behaviors in most hipparionins, although some western large-sized forms were grazers. Dental microwear textures of western hipparionins, therefore, provide evidence of distinct diets between the size classes. In this case, dwarfs had broader browse-dominated feeding spectra supporting the idea that they dwelt in more forested habitats and/or that their resources were more limited. Conversely, eastern hipparionins do not show significantly different microwear textures, thus indicating similar dietary preferences in a resource-rich environment that precluded resource partitioning. Contrary to expectations for more open habitats, eastern hipparionins seem to have included less grass in their diets than western forms, which could be related to a higher consumption of browse during droughts and/or the presence of grit affecting microwear texture. In summary, this thesis provides evidence that the dwarfing process and the mechanisms behind it are not uniform, but that they depend on the specific ecological context. The results represent a further step toward the understanding of the life histories and ecologies of extinct equids. iii iv Resum Els hipparionins eren uns èquids tridàctils molt diversificats durant el Miocè superior a l’àrea circummediterrània, on alguns van esdevenir nans. Per la seva abundància, aquests són un grup clau en la recerca paleoecològica i l’anàlisi de patrons evolutius, tot i que encara cal conèixer millor la seva ecologia. Un dels aspectes més importants de la biologia d’un organisme és la seva història de vida, la qual pot ser reconstruïda a partir de la microestructura òssia i dental, i ens proporciona informació sobre el context ambiental. Així mateix, la dieta, una altra característica de la biologia d’un organisme i un important vincle amb l’ambient, es pot inferir a través del microdesgast dental. En aquesta tesi, l’objectiu principal és dilucidar les condicions ecològiques i els mecanismes relacionats amb la disminució de mida que van patir alguns hipparionins de l’est i oest del Mediterrani. Amb aquesta finalitat, es (i) reconstrueixen els patrons de creixement de metàpodes i molars d’hipparionins de diferent mida, (ii) s’infereixen les seves històries de vida, i (iii) s’exploren les seves dietes a través del microdesgast per testar les inferències ecològiques obtingudes de l’anàlisi de les històries vitals. L’estudi de la histologia dels metàpodes permet reconstruir el creixement ontogenètic i establir l’assoliment d’una maduresa relativa. La identificació de diferents edats de maduració, doncs, evidencia diferents estratègies de creixement en els hipparionins analitzats. L’estudi de laminacions diàries en l’esmalt revela, per primer cop en ungulats, taxes de creixement en primeres/segones molars més elevades que en terceres molars de formació més tardana, suggerint un vincle entre el desenvolupament dental i el somàtic. Així, les taxes de creixement dental més lentes i les erupcions relativament posteriors (correlacionades amb trets d’història de vida) indiquen ritmes de creixement més lents en hipparionins comparat amb Equus. Això contrasta amb la idea d’històries de vida ràpides en hipparionins pel fet de ser generalment més petits. A més, els hipparionins nans occidentals mostren un desenvolupament dental més lent que el de les formes grans i una maduresa relativament tardana, indicant també una història vital més lenta de l’esperada per la seva mida. D’acord amb la teoria de les històries de vida, això assenyala que la menor disponibilitat de recursos és la causa del nanisme en aquests hipparionins. Per contra, les formes petites orientals mostren una maduresa relativa avançada, el que suggereix que la disminució de mida va ser causada per una major mortalitat extrínseca (depredació). Diferències paleoambientals explicarien les pressions ecològiques contraposades: ambients més tancats a l’oest del Mediterrani proporcionaven més cobertura contra la depredació però menys recursos pels hipparionins, mentre a l’est els hàbitats més oberts eren arriscats però rics en recursos. L’anàlisi del microdesgast dental indica un tipus d’alimentació mixta i oportunista en la majoria dels hipparionins, encara que algunes formes occidentals grans pasturaven. D’altra banda, els hipparionins occidentals nans tenien espectres tròfics més amplis i brostejaven, el que avala que habitessin ambients més boscosos i/o tinguessin recursos més limitats. En canvi, els hipparionins orientals petits no difereixen dels grans en les seves textures de microdesgast, suggerint dietes similars en un entorn ric en recursos que evitaria la necessitat del seu repartiment. Contràriament al que s’esperaria en ambients més oberts, els hipparionins orientals menjaven menys gramínies que els occidentals, cosa que es podria relacionar amb canvis de dieta durant sequeres i/o la presència de sorra alterant
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