Article

Cabrera's Vole Microtus cabrerae Thomas, 1906 and the subgenus Iberomys during the Quaternary: Evolutionary implications and conservation

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Abstract

The corological evolution of the species of the subgenus Iberomys and, specifically, of Microtus cabrerae, are described. Iberomys appeared in the Iberian Peninsula during the Lower Pleistocene and then reached southern France and Italy during the Middle Pleistocene. M. cabrerae established itself as an Iberian endemic during the final glacial period and subsequently occupied South-Eastern France. This latter population and those found along the Mediterranean coast survived until the Subatlantic period. Thus, it is concluded that Iberomys is endemic to the European sector of the western Mediterranean Basin, but once was found over much more of the Iberian Peninsula, Italy and France. The Iberian Peninsula is, nevertheless, fundamental in its life history as its evolutionary centre and the origin of expansions into other areas. On the other hand, it is possible to locate the centre of origin of the subgenus Iberomys at a regional scale (the Iberian Peninsula) and adapt its evolutionary cycle to a Symmetrical Model. The contraction of the range of M. cabrerae during the Holocene is not related to the Subboreal climatic crisis; rather, it took place during the Subatlantic and could be related to the expansion of agriculture, which probably destroyed many of its habitats. Thus, this reduction in its range is anthropic in origin and could be corrected by means of appropriate management and conservation policies.

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... M. (I.) brecciensis es originario de la Península Ibérica donde se registra desde el final del Pleistoceno Inferior en los yacimientos mencionados más arriba, y durante todo el Pleistoceno Medio en numerosos yacimientos (Sesé, 1994;Sesé & Sevilla, 1996;Garrido-García y Soriguer-Escofet, 2012;, dando lugar en el Pleistoceno Superior a la especie actual M. (I.) cabrerae (Ayarzaguena & López Martínez, 1976;Cabrera-Millet et al., 1982). M. (I.) brecciensis se extendió por la mitad sureste de Francia e Italia posiblemente desde el comienzo del Pleistoceno Medio, periodo en el que Iberomys alcanzó su mayor distribución geográfica, mientras que M. (I.) cabrerae en el Pleistoceno Superior nunca ocupó Italia, estando restringida a la región mediterránea de Francia, de dónde desapareció en tiempos históricos recientes, y a la Península Ibérica, donde sigue habitando actualmente (aunque en áreas fragmentadas e inconexas que según Garrido-García et al., 2013 son, a grandes rasgos, la Luso-Carpetana, Montibérica, Bética y Prepirenaica), habiendo desaparecido actualmente de algunas regiones en las que, sin embargo, hay registro fósil de Iberomys hasta avanzado el Holoceno, como Cataluña (Ayarzaguena & López Martínez, 1976;Garrido-García & Soriguer-Escofet, 2012;. López-García et al. (2015), en su estudio sobre la distribución de Iberomys en Italia durante el Pleistoceno, refieren su hallazgo en Spessa, aunque con escaso material, y en Rifreddo, yacimientos que atribuyen biostratigráficamente al Pleistoceno Inferior (aunque la asociación faunística de este último yacimiento Masini et al., 2005 lo sitúan al comienzo del Pleistoceno Medio), y señalan que, en todo caso, sería de una edad más reciente que los hallazgos de Iberomys de los niveles del Pleistoceno Inferior de Atapuerca, por lo que la expansión de Iberomys fuera de la Península Ibérica podría haber tenido lugar al final del Pleistoceno Inferior o bien en el tránsito del Pleistoceno Inferior al comienzo del Pleistoceno Medio. ...
... Garrido-García & Soriguer-Escofet (2012) apuntan a que su reducción en épocas recientes fue debida a otras causas como la influencia humana, al destruir los hábitats húmedos en los que vive por la expansión de la agricultura desde el periodo Subboreal. Ambas hipótesis, climática y antrópica, tal como señalan , y en nuestra opinión, no son excluyentes, ya que la retracción del área de distribución de Iberomys podría deberse, como se ha dicho, a causas climáticas, con la consecuente reducción de sus hábitats húmedos preferenciales, acelerada en tiempos recientes por la destrucción intensiva de los mismos por la acción humana que hacen necesaria la búsqueda de medidas para prevenir su extinción (Garrido-García & Soriguer-Escofet, 2012;Garrido-García et al., 2013;Fuentes et al., 2013;Pita et al., 2014;Cuenca-Bescós et al., 2014). ...
... El clima por tanto podría haber sido de tipo mediterráneo similar o incluso algo más benigno que el actual por la presencia de taxones que actualmente parecen estar en regresión o casi desparecidos de la región. Con respecto a esto último, hay que tener en cuenta no solo los cambios climáticos acaecidos desde el Pleistoceno Medio que han podido estar en el origen de los cambios en la distribución geográfica de algunos micromamíferos, sino también el hecho de que la reducción o desaparición actualmente de algunos taxones de muchas zonas en las que sin embargo habitaron durante el Pleistoceno Medio, Pleistoceno Superior y gran parte del Holoceno, como parece que está documentado por el registro fósil de Microtus (I.) brecciensis y su descendiente Microtus (I.) cabrerae (Garrido-García & Soriguer-Escofet, 2012;, ha podido estar influida también por la presencia humana, especialmente en tiempos recientes, al modificar el entorno haciendo desparecer sus biotopos preferenciales, en este caso los humedales. ...
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The micromammal association established in this work is the following: Lagomorpha: Oryctolagus cuniculus; Eulipotyphla: Crocidura cf. russula, cf. Sorex sp., Neomys sp., Soricidae indet. and Talpa sp.; and Rodentia: Eliomys quercinus, Apodemus cf. sylvaticus, Cricetulus (Allocricetus) bursae, Arvicola aff. sapidus, Microtus (Iberomys) brecciensis and Microtus (Terricola) duodecimcostatus. This association is characteristic of the Middle Pleistocene. The morphological state of Cricetulus (A.) bursae, Arvicola aff. sapidus and Microtus (I.) brecciensis allows to place it in the advanced, but not final, Middle Pleistocene, which agrees with the numerical data of the site (243-337 ka) that places it in the MIS 8 or 9. The micromammals indicate the predominance of the open spaces with abundant vegetation mainly of herbaceous and bushes but also with some areas with trees. The climate would be of Mediterranean type, similar to the actual or perhaps a little milder and more humid. © 2016 CSIC. This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial (by-nc) Spain 3.0 License.
... M. (I.) brecciensis es originario de la Península Ibérica donde se registra desde el final del Pleistoceno Inferior en los yacimientos mencionados más arriba, y durante todo el Pleistoceno Medio en numerosos yacimientos (Sesé, 1994;Sesé & Sevilla, 1996;Garrido-García y Soriguer-Escofet, 2012;, dando lugar en el Pleistoceno Superior a la especie actual M. (I.) cabrerae (Ayarzaguena & López Martínez, 1976;Cabrera-Millet et al., 1982). M. (I.) brecciensis se extendió por la mitad sureste de Francia e Italia posiblemente desde el comienzo del Pleistoceno Medio, periodo en el que Iberomys alcanzó su mayor distribución geográfica, mientras que M. (I.) cabrerae en el Pleistoceno Superior nunca ocupó Italia, estando restringida a la región mediterránea de Francia, de dónde desapareció en tiempos históricos recientes, y a la Península Ibérica, donde sigue habitando actualmente (aunque en áreas fragmentadas e inconexas que según Garrido-García et al., 2013 son, a grandes rasgos, la Luso-Carpetana, Montibérica, Bética y Prepirenaica), habiendo desaparecido actualmente de algunas regiones en las que, sin embargo, hay registro fósil de Iberomys hasta avanzado el Holoceno, como Cataluña (Ayarzaguena & López Martínez, 1976;Garrido-García & Soriguer-Escofet, 2012;. López-García et al. (2015), en su estudio sobre la distribución de Iberomys en Italia durante el Pleistoceno, refieren su hallazgo en Spessa, aunque con escaso material, y en Rifreddo, yacimientos que atribuyen biostratigráficamente al Pleistoceno Inferior (aunque la asociación faunística de este último yacimiento Masini et al., 2005 lo sitúan al comienzo del Pleistoceno Medio), y señalan que, en todo caso, sería de una edad más reciente que los hallazgos de Iberomys de los niveles del Pleistoceno Inferior de Atapuerca, por lo que la expansión de Iberomys fuera de la Península Ibérica podría haber tenido lugar al final del Pleistoceno Inferior o bien en el tránsito del Pleistoceno Inferior al comienzo del Pleistoceno Medio. ...
... Garrido-García & Soriguer-Escofet (2012) apuntan a que su reducción en épocas recientes fue debida a otras causas como la influencia humana, al destruir los hábitats húmedos en los que vive por la expansión de la agricultura desde el periodo Subboreal. Ambas hipótesis, climática y antrópica, tal como señalan , y en nuestra opinión, no son excluyentes, ya que la retracción del área de distribución de Iberomys podría deberse, como se ha dicho, a causas climáticas, con la consecuente reducción de sus hábitats húmedos preferenciales, acelerada en tiempos recientes por la destrucción intensiva de los mismos por la acción humana que hacen necesaria la búsqueda de medidas para prevenir su extinción (Garrido-García & Soriguer-Escofet, 2012;Garrido-García et al., 2013;Fuentes et al., 2013;Pita et al., 2014;Cuenca-Bescós et al., 2014). ...
... El clima por tanto podría haber sido de tipo mediterráneo similar o incluso algo más benigno que el actual por la presencia de taxones que actualmente parecen estar en regresión o casi desparecidos de la región. Con respecto a esto último, hay que tener en cuenta no solo los cambios climáticos acaecidos desde el Pleistoceno Medio que han podido estar en el origen de los cambios en la distribución geográfica de algunos micromamíferos, sino también el hecho de que la reducción o desaparición actualmente de algunos taxones de muchas zonas en las que sin embargo habitaron durante el Pleistoceno Medio, Pleistoceno Superior y gran parte del Holoceno, como parece que está documentado por el registro fósil de Microtus (I.) brecciensis y su descendiente Microtus (I.) cabrerae (Garrido-García & Soriguer-Escofet, 2012;, ha podido estar influida también por la presencia humana, especialmente en tiempos recientes, al modificar el entorno haciendo desparecer sus biotopos preferenciales, en este caso los humedales. ...
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Resumen: La asociación de micromamíferos determinada en este trabajo es la siguiente: Lagomorpha: Oryctolagus cuniculus; Eulipotyphla: Crocidura cf. russula, cf. Sorex sp., Neomys sp., Soricidae indet. y Talpa sp.; y Rodentia: Eliomys quercinus, Apodemus cf. sylvaticus, Cricetulus (Allocricetus) bursae, Arvicola aff. sapidus, Microtus (Iberomys) brecciensis y Microtus (Terricola) duodecimcostatus. Es una asociación característica del Pleistoceno Medio. El estadio evolutivo de Cricetulus (A.) bur¬sae, Arvicola aff. sapidus y Microtus (I.) brecciensis le aproximan a las poblaciones de dichas especies de algunos yacimientos de la Península Ibérica del Pleistoceno Medio avanzado, pero no final, lo que es acorde con las dataciones numéricas obtenidas en el yacimiento (243-337 ka) que le sitúan en el MIS 8 o 9. Los micromamíferos indican la predominancia de los espacios abiertos con abundante vegetación herbácea y arbustiva, en los que podría haber también alguna zona arbolada. El clima que indican es de tipo mediterráneo, similar al actual en la zona o quizás algo más benigno y más húmedo. Abstract: The micromammal association established in this work is the following: Lagomorpha: Oryctolagus cuniculus; Eulipotyphla: Crocidura cf. russula, cf. Sorex sp., Neomys sp., Soricidae indet. and Talpa sp.; and Rodentia: Eliomys quercinus, Apodemus cf. sylvaticus, Cricetulus (Allocricetus) bursae, Arvicola aff. sapidus, Microtus (Iberomys) brecciensis and Microtus (Terricola) duodecimcostatus. This association is characteristic of the Middle Pleistocene. The morphological state of Cricetulus (A.) bur¬sae, Arvicola aff. sapidus and Microtus (I.) brecciensis allows to place it in the advanced, but not final, Middle Pleistocene, which agrees with the numerical data of the site (243–337 ka) that places it in the MIS 8 or 9. The micromammals indicate the predomi¬nance of the open spaces with abundant vegetation mainly of herbaceous and bushes but also with some areas with trees. The climate would be of Mediterranean type, similar to the actual or perhaps a little milder and more humid.
... Climatic warming and aridification during the Bronze Age (Middle Sub-Boreal period, about 5.0-2.5 thousand years ago) are possible reasons to explain the subsequent range contraction of M. cabrerae (Cabrera-Millet et al. 1982;Ferna´ndez-Salvador 1998). However, population retraction may have been particularly pronounced from the Iron Age (Sub-Atlantic period, about 2.5 thousand years ago) to present, suggesting that the reduction and fragmentation of the distribution of M. cabrerae may be largely attributed to agricultural expansion since that period (Garrido-Garcı´a and Soriguer-Escofet 2012;Laplana and Sevilla 2013), which has resulted in the destruction of suitable habitats for the species (see ''Conservation''). ...
... Archaeological and paleontological sites with fossils of Iberomys (heuscarensis-brecciensis-cabrerae) were thoroughly inventoried by Garrido-Garcı´a and Soriguer-Escofet (2012) and Laplana and Sevilla (2013). Fossils of M. huescarensis were found at 4 sites in Spain: near Atapuerca (Burgos-Laplana and Cuenca-Besco´s 1998;Cuenca-Besco´s et al. 1999 Fossils of M. brecciensis were found at more than 50 sites from the Iberian Peninsula (including Portugal, Spain, and Britain-Gibraltar), France, and Italy (Garrido-Garcı´a and Soriguer-Escofet 2012). ...
... Archaeological and paleontological sites with fossils of Iberomys (heuscarensis-brecciensis-cabrerae) were thoroughly inventoried by Garrido-Garcı´a and Soriguer-Escofet (2012) and Laplana and Sevilla (2013). Fossils of M. huescarensis were found at 4 sites in Spain: near Atapuerca (Burgos-Laplana and Cuenca-Besco´s 1998;Cuenca-Besco´s et al. 1999 Fossils of M. brecciensis were found at more than 50 sites from the Iberian Peninsula (including Portugal, Spain, and Britain-Gibraltar), France, and Italy (Garrido-Garcı´a and Soriguer-Escofet 2012). In addition, fossils described as H. brecciensis were apparently found in the Balkan Peninsula (Marjan, Croatia-Vuletic 1953), although no information on cranial measurements or molar size and structure is available for confirmation. ...
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Microtus cabrerae Thomas, 1906, or Cabrera's vole, is a medium-sized arvicoline, and one of the largest Microtus species. M. cabrerae is an Iberoccitane endemic, which is currently restricted to the Iberian Peninsula, where it presents a highly fragmented distribution. The species is the sole extant representative of the anagenetic Iberomys lineage with origin in the early Pleistocene. M. cabrerae is primarily restricted to wet habitats dominated by tall grasses, sedges, and rushes. The species has experienced strong population declines mainly during the past 10 years, particularly due to agricultural intensification. M. cabrerae is currently classified by the International Union for Conservation of Nature and Natural Resources as ''Near Threatened,'' and is listed in the Habitats Directive and Bern Convention, thus requiring appropriate conservation measures. FULL TEXT AVAILABLE AT: http://www.asmjournals.org/toc/mmsp//912
... Thus, it suggests that the previously described gradual retraction of its distribution since the Middle Holocene linked to the climatic aridification trend by some authors (López-Martínez 2003), might be in fact an artifact caused by a lack of small mammal studies from the Neolithic onwards. With the updated information, the sharp decline of M. cabrerae records occurs during Iron Age -Roman period and Middle Ages, a fact that is reinforced by the hypothesis that this retraction mainly took place in the last 2,500 years before present and it is still ongoing (Garrido- García and Soriguer-Escofet 2012;Laplana and Sevilla 2013). Although the decrease of records is strongly influenced by the scarcity of studies dealing with microvertebrates at more recent archaeological sites, genetic studies and species distribution modelling data are consistent with this hypothesis Garrido-García et al. 2018). ...
... Concerning the causes triggering this biogeographic dynamic, our results support a major anthropic influence in this process reinforcing previous studies (Cabrera-Millet et al. 1983;Garrido-García and Soriguer-Escofet 2012;López-García and Cuenca-Bescós 2012;Garrido-García et al. 2018). Furthermore, new records of M. cabrerae in localities of south-eastern Iberia (e.g. ...
Article
Postes Cave in SW Spain (Extremadura) displays a Holocene archaeostratigraphic sequence radiocarbondated to between c. 8.5–4 cal kyr BP (Mesolithic-Chalcolithic). The sediments collected at two areas within the cave yielded small mammal remains belonging to eleven species of rodents, ‘insectivores’, lagomorphs and chiropterans. This small mammal fossil assemblage is one of the few known to date in the southwest of the Iberian Peninsula. Preliminary taphonomic analysis and previously published data suggest that the remains were accumulated by the predatory activity of Eurasian eagle owls and small to medium-sized carnivores such as red foxes. The palaeoenvironmental and palaeoclimatic reconstructions performed show stable conditions with slight variations during its time span, suggesting an initial scenario of open forested habitats during the Mesolithic and Neolithic which progressively decreased in favour of more open habitats during the Chalcolithic coinciding with human-induced changes of the landscape and with the aridification trend of this period. The presence of Microtus cabrerae and Crocidura suaveolens in the assemblage is noteworthy since they are now extinct in this region. The plausible causes and the processes of these extirpations are discussed.
... These conditions could have relegated the species' niche to specific habitats which could ensure the necessary environmental requirements that could not be satisfied by climate (e.g. areas of high phreatic level or areas in mountain foothills) 28,38 . ...
... B.P. 52 . Previous studies have reported a historic contraction in the distribution of the species and its disappearance from France as a result of climate, interspecific interactions and/or an intensification of anthropogenic impacts 28,38,53 . Nevertheless, the results suggest that climate is not the main cause of extinction in the French territory. ...
Article
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Climate change is not only evident, but its implications on biodiversity are already patent. The scientific community has delved into the limitations and capabilities of species to face changes in climatic conditions through experimental studies and, primarily, Species Distribution Models (SDMs). Nevertheless, the widespread use of SDMs comes with some intrinsic assumptions, such as niche conservatism, which are not always true. Alternatively, the fossil record can provide additional data to solve the uncertainties of species' responses to climate change based on their history. Using a combined environmental (niche overlap indices) and geographical approach (temporal transferability of SDMs), we assessed the niche conservatism of Microtus cabrerae throughout its evolutionary history: the Late Pleistocene and the Holocene. The set of analyses performed within this timeframe provides a broad view pointing to a shift in the realized climatic niche of the species. Specifically, M. cabrerae exhibited a broader niche during glacial times than interglacial times, expanding towards novel conditions. Hence, the species might have developed an adaptive ability, as a consequence of mechanisms of local adaptation or natural pressures, or just be preadapted to cope with the novel environment, due to expansion into an unfilled portion of the niche. Nevertheless, the more restricted realized niche during last interglacial times reveals that the species could be close to its physiological limits.
... This distribution suggests a trend of contraction of a previously widespread species into increasingly isolated populations, possibly driven by climatic factors Mestre et al. 2015). Likewise, the excellent fossil record of the Cabrera vole indicates that its past distribution has fluctuated throughout the climatic oscillations of the Late Pleistocene, with colonisation-extinction-recolonisation dynamics (Garrido-García & Soriguer-Escofet 2012;Laplana & Sevilla 2013). In any case, it is postulated that climate induced aridification would have been enhanced by anthropogenic activities that gradually decreased forest area, impacting the Iberian Peninsula more intensely ...
... There was, however, a subsequent cold period -the Younger Dryas (YD) (c. 13 to 11.4 kya) -that marked the end of the Pleistocene. At this point, the Cabrera vole's favoured habitat would have become scarcer once again for a short period of time as fossil abundance from this period is low (Robinson et al. 2006;Garrido-García & Soriguer-Escofet 2012;Laplana & Sevilla 2013;Bañuls-Cardona et al. 2014). Such conditions might have favoured further subdivision within each geographic nucleus, as reflected by the high mitochondrial haplotype diversity ( Figure 2). ...
... The extant Microtus cabrerae Thomas, 1906 is an Iberoccitanian endemism. It is actually distributed along an arch, from the southwest to the center to the south-east of the Iberian Peninsula, in Spain and Portugal, including also some isolated nuclei in the Pyrenean foothills (Ayarzagüena & López-Martínez 1976;Cabrera Millet 1980;Cabrera Millet et al. 1982;Madureira & Ramalhinho 1985;Gisbert & García-Perea 1988Gisbert & Fernández-Salvador 1998;Ventura et al. 1998;Palomo & Gisbert 2002;Fernández-Salvador et al. 2005a,b;Mira et al. 2006;Pita et al. 2006Pita et al. , 2011aGarrido-García et al. 2008;Garrido-García & Soriguer-Escofet 2012;among others). Late Holocene populations persist in France in the site of Chauve-Souris, Donzère, situated to the south of the Rhodanian Valley (Jeannet & Vital 2009). ...
... The proposition of a new common name aims to the conservation of this endangered rodent, as it may be confused with the 'topillo' (Microtus arvalis Pallas, 1778), which causes periodical damage to crops. The reduction of the populations of Iberomys cabrerae is anthropic (Fernández-Salvador 2007;Gisbert & García-Perea 2009Jeannet & Vital 2009;Garrido-García & Soriguer-Escofet 2012); hence, the change of name may help in raising funds for and drawing attention to the conservation of the Cabrera's vole. ...
Article
Full-text available
The extant Cabrera’s vole, Microtus cabrerae, differs in morphology and evolutionary history from the other species of Microtus. This arvicoline has unique, derived features in the cranium, mandible and dentition. Probably its most conspicuous features are its large size, the high skull in lateral view, the long and distally broad nasals, and the triangle-shape of the anteroconid complex, with a marked labio-lingual asymmetry of the occlusal surface of the first lower molars. In this study, we propose a phylogenetic lineage that includes Cabrera’s vole in what until now has been the Microtus subgenus Iberomys. Paleontological information and several life history traits support the elevation of Iberomys to the rank of genus. Genus Iberomys comprises species, which have appeared in succession during the Quaternary: in the Early Pleistocene, the extinct I. huescarensis; in the Middle Pleistocene, the extinct I. mediterraneus; and in the Late Pleistocene, the extant I. cabrerae. Interestingly, the extant species shows several biological singularities, such as multiple polymorphic copies of the SRY male-specific gene in both males and females, and the lowest basal metabolic rate in relation to weight among arvicoline species. Likewise, its habitat requirement is unique among the Iberian arvicolines. Accordingly, the biological and paleontological data that we present in this work support the elevation of its taxonomic rank to that of genus. This study also suggest a modification of nomenclature: Microtus (Iberomys) brecciensis is replaced with Iberomys mediterraneus and the common name of the extant M. (I.) cabrerae changed from ‘topillo’ to ‘iberon’ in order to improve conservation and protection actions.
... The extant Microtus cabrerae Thomas, 1906 is an Iberoccitanian endemism. It is actually distributed along an arch, from the southwest to the center to the south-east of the Iberian Peninsula, in Spain and Portugal, including also some isolated nuclei in the Pyrenean foothills (Ayarzagüena & López-Martínez 1976;Cabrera Millet 1980;Cabrera Millet et al. 1982;Madureira & Ramalhinho 1985;Gisbert & García-Perea 1988Gisbert & Fernández-Salvador 1998;Ventura et al. 1998;Palomo & Gisbert 2002;Fernández-Salvador et al. 2005a,b;Mira et al. 2006;Pita et al. 2006Pita et al. , 2011aGarrido-García et al. 2008;Garrido-García & Soriguer-Escofet 2012;among others). Late Holocene populations persist in France in the site of Chauve-Souris, Donzère, situated to the south of the Rhodanian Valley (Jeannet & Vital 2009). ...
... The proposition of a new common name aims to the conservation of this endangered rodent, as it may be confused with the 'topillo' (Microtus arvalis Pallas, 1778), which causes periodical damage to crops. The reduction of the populations of Iberomys cabrerae is anthropic (Fernández-Salvador 2007;Gisbert & García-Perea 2009Jeannet & Vital 2009;Garrido-García & Soriguer-Escofet 2012); hence, the change of name may help in raising funds for and drawing attention to the conservation of the Cabrera's vole. ...
Article
Full-text available
The extant Cabrera's vole, Microtus cabrerae, differs in morphology and evolutionary history from the other species of Microtus. This arvicoline has unique, derived features in the cranium, mandible and dentition. Probably its most conspicuous features are its large size, the high skull in lateral view, the long and distally broad nasals, and the triangle-shape of the anteroconid complex, with a marked labio-lingual asymmetry of the occlusal surface of the first lower molars. In this study, we propose a phylogenetic lineage that includes Cabrera's vole in what until now has been the Microtus subgenus Iberomys. Paleontological information and several life history traits support the elevation of Iberomys to the rank of genus. Genus Iberomys comprises species, which have appeared in succession during the Quaternary: in the Early Pleistocene, the extinct I. huescarensis; in the Middle Pleistocene, the extinct I. mediterraneus; and in the Late Pleistocene, the extant I. cabrerae. Interestingly, the extant species shows several biological singularities, such as multiple polymorphic copies of the SRY male-specific gene in both males and females, and the lowest basal metabolic rate in relation to weight among arvicoline species. Likewise, its habitat requirement is unique among the Iberian arvicolines. Accordingly, the biological and paleontological data that we present in this work support the elevation of its taxonomic rank to that of genus. This study also suggest a modification of nomenclature: Microtus (Iberomys) brecciensis is replaced with Iberomys mediterraneus and the common name of the extant M. (I.) cabrerae changed from ‘topillo’ to ‘iberon’ in order to improve conservation and protection actions. This article is protected by copyright. All rights reserved
... We aim to reconstruct the biogeographic history of Microtus cabrerae from its fossil record in archaeological and palaeontological sites. Previous research has highlighted changes in the species' distribution over time but was based on few data (Ayarzagüeña & López Martínez 1976, Cabrera-Millet et al. 1983, López-Martínez 2009, Garrido-García & Soriguer-Escofet 2012. We used every available record of the species found in the literature, throughout its whole geographic range and from its first appearance to the present, as well as a number of unpublished records from Spanish localities. ...
... While some authors (e.g. López -Martínez 2003) linked the contraction of the area occupied by Microtus cabrerae with the climatic change towards aridification that occurred from the middle Holocene onwards, other authors see the contraction as a consequence of anthropic changes in the environment (mainly the expansion of agriculture; Cabrera-Millet et al. 1983, Garrido-García & Soriguer-Escofet 2012. In our opinion, it seems likely to be the combined result of both climatic and anthropic factors. ...
Article
1. Microtus cabrerae is an Iberian endemic vole species with specific adaptations to the subhumid Mediterranean climate. Its living populations are under a regressive trend. The earliest known records of Microtus cabrerae date from the late Middle Pleistocene, and it originated from Microtus brecciensis. 2. We describe changes in the geographic distribution of Microtus cabrerae throughout its history based on its palaeontological record, and link them to environmental changes that have taken place since the appearance of Microtus cabrerae. 3. A series of successive chronological intervals comprising the recorded existence of the species was established, so that the majority of the published fossil records of Microtus cabrerae could be used for analysis. For each interval, a map with the inferred distribution of the species was created. The maps were used to establish variations in the species’ distribution through time. 4. A first regression in the extent of the distribution of Microtus cabrerae took place in Marine Isotope Stage 2, when the species abandoned south-eastern France and central Spain, where it had been present since the beginning of the Late Pleistocene. This range contraction was probably due to the global decline in temperatures and rainfall that took place in this period. After a rapid recolonization of most of the previously abandoned areas at the beginning of the Holocene and a remarkable increase in records during the Neolithic, a new gradual decrease of records is observed from the Neolithic to the Roman period, intensifying from c. 2000 years ago onwards and ending with the final disappearance of the species from south-western France and north-eastern Iberia. This second decline is linked to the aridification of the Mediterranean entourage that started in the mid- Holocene and has been enhanced by human modification of the landscape. The species is shown to be sensitive to climate change.
... Iberomys cabrerae debe ser considerado un endemismo ibérico, con un área de distribución fragmentada (Ayarzagüena et al. 1976, Palomo 1999. Según los datos paleobiológicos ( Fig. 2; Garrido- García & Soriguer 2012, Laplana & Sevilla 2013, esta situación se configuró a lo largo del Holoceno, debido a extinciones que habrían reducido la extensión del área de distribución original y desconectado los núcleos actuales entre sí. Así, su desaparición en Cataluña y el sureste de Francia habría separado los actuales núcleos Prepirenaico y Montibérico, y la pérdida de las poblaciones de los tercios central y occidental de las cordilleras Béticas habría reducido mucho el núcleo Bético. ...
Article
In this article, we provide a map representing the whole distribution area of Iberomys cabrerae, displayed in UTM System, at a scale of 10x10 km squares. Our results show that a) the records are included in 420 squares, which are grouped in four large, disjunct nuclei: Luso-Carpetanian, Montiberian, Baetic and Prepyrenean, the Luso-Carpetanian grouping the largest number of populations, and the Prepyrenean (isolated and threatened) including the smallest number of populations; b) it is necessary to conduct surveys in certain poorly explored areas; and c) available data on the population status are unbalanced in quality and geographic distribution, providing an inaccurate picture of the global conservation status, and preventing the development of global strategies for an adequate conservation and management of the species.
... Los lugares arqueológicos y paleontológicos con fósiles de Iberomys (heuscarensisbrecciensis-cabrerae) han sido inventariados exhaustivamente en Garrido-García y Soriguer-Escofet (2012) Vuletic, 1953), aunque no se dispone de información sobre las medidas craneales o del tamaño y estructura de los molares para su confirmación. Los subfósiles de topillo de Cabrera son relativamente comunes en muchos depósitos del Pleistoceno-Holoceno tardío en la Península Ibérica y sur de Francia. ...
... Iberomys cabrerae debe ser considerado un endemismo ibérico, con un área de distribución fragmentada (Ayarzagüena et al. 1976, Palomo 1999. Según los datos paleobiológicos ( Fig. 2; Garrido- García & Soriguer 2012, Laplana & Sevilla 2013, esta situación se configuró a lo largo del Holoceno, debido a extinciones que habrían reducido la extensión del área de distribución original y desconectado los núcleos actuales entre sí. Así, su desaparición en Cataluña y el sureste de Francia habría separado los actuales núcleos Prepirenaico y Montibérico, y la pérdida de las poblaciones de los tercios central y occidental de las cordilleras Béticas habría reducido mucho el núcleo Bético. ...
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In this article, we provide a map representing the whole distribution area of Iberomys cabrerae, displayed in UTM System, at a scale of 10x10 km squares. Our results show that a) the records are included in 420 squares, which are grouped in four large, disjunct nuclei: Luso-Carpetanian, Montiberian, Baetic and Prepyrenean, the Luso-Carpetanian grouping the largest number of populations, and the Prepyrenean (isolated and threatened) including the smallest number of populations; b) it is necessary to conduct surveys in certain poorly explored areas; and c) available data on the population status are unbalanced in quality and geographic distribution, providing an inaccurate picture of the global conservation status, and preventing the development of global strategies for an adequate conservation and management of the species
... This global radiation is evidenced within the Iberian fossil record by local speciation (e.g. development of the endemic lineage Iberomys within Microtus [62][63][64]) as well as by immigration of new species from other Eurasian regions, being both processes spurred by global environmental change. Overall, such ecological reorganization of assemblages appears to be triggered by global climatic changes and modulated by the differences in ecological specialization of the implied species, similarly to what was observed in earlier periods of faunal replacement in Spain [36,65]. ...
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Open Access: http://www.biomedcentral.com/1471-2148/13/94 BACKGROUND: Several macroevolutionary hypotheses propose a synchrony between climatic changes and variations in the structure of faunal communities. Some of them focus on the importance of the species ecological specialization because of its effects on evolutionary processes and the resultant patterns. Particularly, Vrba's turnover pulse hypothesis and resource-use hypothesis revolve around the importance of biome inhabitation. In order to test these hypotheses, we used the Biomic Specialization Index, which is based on the number of biomes occupied by each species, and evaluated the changes in the relative importance of generalist and specialist rodents in more than forty fossil sites from the Iberian Plio-Pleistocene. RESULTS: Our results indicate that there was a decrease in the specialization degree of rodent faunas during the Pliocene due to the global cooling that triggered the onset of the glacial events of the Cenozoic (around 2.75 Ma). The subsequent faunal transition after this critical paleoenvironmental event was characterized by an increase of specialization related to the adaptation to the new environmental conditions, which was mainly associated with the Pleistocene radiation of Arvicolinae (voles). CONCLUSIONS: The pattern of faunal turnover is correlated with the development of the modern glaciations in the Northern Hemisphere around 2.75 Ma, and represents a reorganization of the rodent communities, as suggested by the turnover pulse hypothesis. Our data also support the resource-use hypothesis, which presumes the role of the degree of specialization in resources specifically related to particular biomes as a driver of differential speciation and extinction rates. These results stress the intimate connection between ecological and evolutionary changes.
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Aim: Reconstructing species' glacial refugial history and demographic changes over time has greatly relied on comparing inferences from multiple methods while not sufficiently acknowledging their limitations. Here, we aim to integrate as fully as possible complementary methods in ecology, genomics and palaeobiology to improve the reconstruction of species biogeographical history. Location: Southwestern Europe. Taxon: Cabrera vole (Microtus cabrerae). Aim Reconstructing species' glacial refugial history and demographic changes over time has greatly relied on comparing inferences from multiple methods while not sufficiently acknowledging their limitations. Here, we aim to integrate as fully as possible complementary methods in ecology, genomics and palaeobiology to improve the reconstruction of species biogeographical history. Location South-western Europe. Taxon Cabrera vole (Microtus cabrerae). Methods We compiled and mapped the raw fossil data of the Cabrera vole for the Last Glacial Maximum (LGM) and Mid-Holocene (MH). Alongside, we projected the calibrated ecological niche model (ENM) of the species' current distribution for the LGM, the Younger Dryas and the MH. Complementarily, we used previously obtained Genotyping-by-Sequencing data to evaluate the demographic history and range expansion patterns of all four Evolutionarily Significant Units of the species, in an integrative framework. Results ENM-inferred refugial areas and genomic modelling consistently supported northern Iberian glacial refugia for the Cabrera vole. This contrasted with the higher fossil abundance of the species in southern and eastern Iberia and southern France from the LGM to the MH. Our results suggest that populations in areas with high fossil abundance went extinct, and were later replaced by northern Iberian populations such that they did not contribute significantly to the current gene pool. Main conclusions Our integrative approach indicates how the range of the Cabrera vole fluctuated in response to environmental change during and following the LGM. Despite methodological limitations, the ENM and genomic approaches produced generally congruent results. Instead, the fossil record may misrepresent the ancestral distribution of this species and should be considered cautiously for ancestral distribution reconstruction, considering that it also reflects the fossilization conditions. Overall, our study supports the idea that integrative approaches are essential to provide an accurate and well-supported picture of historical refugial areas and range dynamics.
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Genetic non-invasive sampling (gNIS) may provide valuable information for population monitoring, as it allows inferences of population density and key behavioural traits such as dispersal, kinship and reproduction. Despite its enormous potential, gNIS has rarely been applied to small mammals, for which live-trapping is still the most commonly used sampling method. Here we evaluated the applicability and cost-effectiveness of gNIS compared with livetrapping, to monitor a metapopulation of an Iberian endemic and elusive rodent: the Cabrera vole (Microtus cabrerae). We compared the genetic diversity, kinship and dispersal movements inferred using both methods. For that, we optimised microsatellite markers for individual identification of M. cabrerae, using both tissue (n = 31) and faecal samples (n = 323) collected from a metapopulation in south-western Iberia. An initial set of 20 loci was optimised for tissue samples, from which 11 were selected to amplify in faecal samples. Overall, gNIS revealed a higher number of identified individuals (65) than live-trapping (31), and the estimated genetic diversity was similar using data from tissues and gNIS. Kinship analysis showed a higher number of inferred relationships and dispersal events when including gNIS, and indicated absence of sex-biased dispersal. The total cost (fieldwork and genetic analysis) of each genotype obtained through live-trapping was three times greater than for gNIS. Our data strongly supports the high potential and cost-effectiveness of gNIS for monitoring populations of elusive and/or threatened small mammals. We also illustrate how this genetic tool can be logistically feasible in conservation.
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Disentangling the relative importance of climatic and anthropogenic factors is crucial in conservation biology but problematic using short-term data only. Long-term (palaeobiological) data are thus increasingly being used to understand taxon history and to identify potential status and baseline (pre-anthropogenic) conditions, which in turn allows the optimization of species conservation plans. We combined species distribution models (SDMs) with current and palaeo-occurrences of Microtus cabrerae, a threatened Mediterranean rodent, to circumvent the limitations of the palaeorecord (e.g. spatio-temporal bias), to characterize this rodent's history (potential status and baseline conditions) since the Mid-Holocene (~6,000 yr BP), and to determine the relative importance of climatic and anthropogenic factors in its decline.
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The occurrence of the genus Iberomys is testified in Italy and the Iberian Peninsula from the Early Pleistocene on. The genus comprises two extinct voles: I. huescarensis from the Early Pleistocene to the early Middle Pleistocene and I. brecciensis (=mediterraneus) from the Middle to the early Late Pleistocene. I. cabrerae, has been present in Spain from the early Late Pleistocene, enduring right through to today. The fossil record of Iberomys in Italy is poor in comparison with those in the Iberian Peninsula and southern France. I. huesca-rensis has been identified in Italy at the Rifreddo and Spessa sites, while I. brecciensis has been recognized at Zoppega 2, Montagnola Senese II, Isernia, Valdemino, Polledrara di Cecanibbio and Paglicci. A revision of the specimens of the genus Iberomys in Italy and a comparison with the fossil records of southern France and the Ibe-rian Peninsula show that the origin of the Early Pleistocene species (I. huescarensis) is clearly in the Iberian Peninsula, where the species having evolved from ancient populations of Allophaiomys nutiensis. The origin of the species I. brecciensis is still unknown. It seems to appear at the same time in Italy and in the Iberian Peninsula, and its extinction occurred during the late Middle Pleistoceneearly Late Pleistocene in Italy, France and Iberia simultaneously.
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Resumen: Se describe la asociación de micromamíferos del yacimiento achelense del Arenero de Arriaga del valle del Manzanares constituida por los soricomorfos: Crocidura sp. y Talpa sp., los roedores: Eliomys quercinus quercinus, Apodemus sp., Microtus brecciensis, Microtus arvalis, Microtus duodecimcostatus y Arvicola aff. sapidus, y el lagomorfo: Oryctolagus cuniculus. La asociación faunística y el estadio evolutivo de Microtus brecciensis y Arvicola aff. sapidus, indican una edad del final del Pleistoceno Medio. La asociación de micromamíferos sugiere la existencia de varios biotopos representados: ripícola, praderas húmedas y secas, y bosque, y un clima templado similar al actual de la Meseta. Abstract: The micromammals from the archaeological site of the Arenero de Arriaga from the Manzanares Valley are here described. They are the Soricomorpha: Crocidura sp. and Talpa sp., the Rodentia: Eliomys quercinus quercinus, Apodemus sp., Microtus brecciensis, Microtus arvalis, Microtus duodecimcostatus and Arvicola aff. sapidus, and the Lagomorpha: Oryctolagus cuniculus. The faunal association and the evolutionary state of Microtus brecciensis and Arvicola aff. sapidus, suggest an age of the end of the Middle Pleistocene. It also indicates the existence of different biotopes: riparian, moist and dry meadows, and forest, and a temperate climate similar to the present-day climate of the Meseta.
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We study the application of the concept ‘centre of origin’ in Historical Biogeography through the predictions of a commonly used biogeographic model, here defined as “symmetric model”: i) local appearance of new species, followed by ii) expansion of the range of the distribution area of the new species. The first prediction occurs only in island species: a) the local appearance of new species has not been documented in not insular regions; b) the centre of origin cannot be accurately located for not insular species, and c) the criteria for infer it do not converge. The second prediction applies only for invasive species, after opening pre-existent barriers, showing their intrinsic capacity for linear expansion of the area at approximately constant speed and not controlled by external factors. The symmetric model assumes a symmetrical biogeographic dynamics: 1st) local origin, 2nd) gradual expansion, 3rd) stasis, 4th) gradual contraction and 5th) extinction. Diverse data refute this symmetrical model: a) the endemic species, the only ones who have a local distribution, show incapacity for expansion of their area; b) the “taxon cycle” in insular species shows that the area of the colonizing species always tend to decrease while differentiation occurs; c) the entries and exits of the guide species in the fossil record show an asymmetric pattern, with very rapid, quasi-synchronic appearance at regional scale and very slow, diachronic extinction along their distribution area; and d) the chronological asymmetry of the paleobiogeographic history of taxa, showing a wide distribution area at the beginning and a slow trend towards area contraction and fragmentation at the end, before extinction. Therefore, the data refute the applicability of the centre of origin concept and point to an asymmetric model of biogeographic dynamics: 1st) sudden appearance of the taxon in a wide area, 2nd) stasis, 3rd) slow contraction and 4th) extinction, frequently after previous fragmentation of the area. En este trabajo se estudia la aplicación del concepto de centro de origen de un taxón en Biogeografía Histórica a través de dos predicciones de un modelo biogeográfico frecuentemente usado, que denominamos “modelo simétrico”: 1º) aparición local de las nuevas especies, seguida de 2º) expansión gradual de su área inicial de distribución. La primera predicción sólo se cumple en especies insulares: a) la aparición local de nuevas especies no ha sido observada hasta ahora en regiones no insulares; b) el centro de origen de especies no insulares no ha podido ser localizado con precisión, y c) los criterios para inferirlo no convergen. La segunda predicción se cumple en especies invasoras, que tras franquear barreras preexistentes expanden el área linealmente, a velocidad aproximadamente constante, mostrando para ello una capacidad intrínseca no ligada a factores externos. El modelo simétrico asume una dinámica biogeográfica simétrica en el tiempo: 1º) origen local, 2º) expansión gradual, 3º) estasis, 4º) contracción gradual, y 5º) extinción. Diversos datos refutan el modelo simétrico: a) las especies endémicas, únicas que muestran una distribución localizada, no muestran capacidad de expansión; b) el “ciclo del taxón” en especies insulares muestra que el área de la especie colonizadora tiende siempre a reducirse según va diferenciándose; c) las entradas y salidas de especies-guías del registro fósil son asimétricas, con pautas de aparición muy rápida a escala regional (cuasi-sincrónica), y de extinción muy lenta y diacrónica a lo largo de su área de distribución; y d) la historia paleobiogeográfica de muchos taxones es asimétrica, con una amplia área de distribución inicial y una tendencia lenta a su contracción y fragmentación antes de la extinción. Por tanto, los datos refutan la aplicabilidad del modelo simétrico y del concepto de centro de origen, y apuntan a un modelo de dinámica biogeográfica asimétrico en el tiempo: 1º) aparición súbita del taxón en una amplia área, 2º) estasis, 3º) lenta contracción, y 4º) extinción, frecuentemente precedida de fragmentación del área.
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Faunal remains are basic elements in the analysis of pre- and protohistoríc systems as well as environmental reconstructions as so many studies now amply demonstrate. Because of it, faunal analysis have become a routine of all integral archaeological research. Despite this, the role played by animal associations in the interpretation of human settlements is not free from drawbacks. Not realizing these in each particular case, might cause false interpretations which will eventually damage the theoretical arguments of the discussions. In this work we present some instances of these «damaged theoríes» which have been formulated within the framework of the Iberian Peninsula. Las faunas son elementos fundamentales en la reconstrucción de las economías y de los paisajes de los asentamientos humanos. Esto ha sido ya puesto de manifiesto en numerosos trabajos. Es por ello que actualmente no se concibe un análisis integral de un yacimiento antrópico que no incluya su correspondiente informe faunístico. A pesar de esto, el papel desempeñado por la fauna en la interpretación de un complejo arqueológico no está exento de limitaciones. No reconocer éstas puede inducir a cometer errores interpretativos que acaben lesionando la argumentación teórica. En este trabajo se discuten algunos casos concretos procedentes de estudios llevados a cabo en la Península Ibérica.
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. * Dedicamos este trabajo a la memoria de nuestro inolvidable amigo y compañero Isidoro cuyo entrañable recuerdo e inmensurable sapiencia perdurará para siempre entre nosotros RESUMEN En este trabajo se pretende analizar la situación biogeográfica de los mi-cromamíferos (Roedores, Insectívoros y Lagomorfos) de la Península Ibérica desde dos puntos de vista complementarios; a) desde la perspectiva de un gra-diente latitudinal de diversidad específica y b) su abundancia numérica en dos zonas biogeográficas bien diferenciadas (templada y mediterránea). En un contexto europeo, en cuanto al número de especies de micromamí-feros, la Península Ibérica se encuentra en el extremo más pobre de un gra-diente latitudinal. Dentro ya de la Península Ibérica, la diversidad observada en la zona templada (franja septentrional) es comparable a la de latitudes centroeuropeas y muy superior a la del resto de la Península con influencia claramente mediterránea. Un proceso análogo sucede respecto a la abundan-cia numérica de las especies.
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The Iberian Peninsula was one of the most important Pleistocene glacial refugia in Europe. A number of recent studies have documented the phylogeography of Iberian taxa and their relationship to more widely distributed species that expanded from this southern European refugium. We use a comparative approach to review the literature that challenges the paradigm of Iberia as a single refuge during Pleistocene glacial maxima and instead supports the occurrence of several Iberian refugia for a range of flora and fauna. Some patterns of phylogeo-graphic concordance were found between the refugial areas identified by different case studies and these broadly overlapped with previously recognized areas of high endemism in the Iberian Peninsula. Such patterns help to illustrate the internal complexity of the Iberian Peninsula as a glacial refugium, and show that for many species, populations with a high degree of genetic structure have existed throughout the Pleistocene. Importantly, the occurrence of these ‘refugia-within-refugia’ may confound the interpretation of phylogeographic patterns of European species, and can misleadingly support the occurrence of northern refugia. We discuss these and other consequences, especially when a limited number of samples from the southern Euro-pean refugia are used.
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An improved concept of the best analogs method is used to reconstruct the climate of the last glacial maximum from pollen data in Europe. In order to deal with the lack of perfect analogs of fossil assemblages and therefore to obtain a more accurate climate reconstruction, we used a combination of pollen types grouped according to plant phenology and present climate constraints rather than pollen percentages for each individual taxon. The distribution of pollen taxa into plant functional types (PFTs) is aimed to reflect the vegetation in terms of biomes which have a wider distribution than a species. The climatic variables are then calibrated on these PFTs using an artificial neural network technique. The use of PFTs allowed us to deal with situations where pollen assemblages have only partial modern analogs. The method is applied to the glacial steppic vegetation in Europe, using 15 pollen records. North of the Pyrenees-Alps line, the reconstructed temperatures were lower than today: -30 ± 10°C for the temperature of the coldest month (Tc) and -12 ± 3°C for the annual mean (Tann). South of that line, Tcand Tannanomalies were respectively, -15 ± 5°C and -10 ± 5°C. The available moisture index and annual precipitation were also lower than present: -60 ± 20% north of Mediterranean Sea, (-800 ± 100 mm for precipitation). In Italy and Greece, the available moisture was 20% lower, with a precipitation anomaly of ca. -600 ± 200 mm. Southward, the moisture index was close to that at present (±20%), and precipitation was lower (-300 ± 300 mm). Copyright 1998 University of Washington
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