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Micromammal diversity loss in central-eastern Patagonia over the last 400 years
Journal of Arid Environments 85 (2012) 71e75
Contents lists available at SciVerse ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Short communication
Micromammal diversity loss in central-eastern Patagonia over the last 400 years U.F.J. Pardiñas, D.E. Udrizar Sauthier*, P. Teta Unidad de Investigación Diversidad, Sistemática y Evolución, Centro Nacional Patagónico-CONICET, Boulevard Brown 2915, Casilla de Correo 128, 9120 Puerto Madryn, Chubut, Argentina
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 July 2011 Received in revised form 24 April 2012 Accepted 29 May 2012 Available online 13 July 2012
Through the study of a late Holocene sample of small mammal remains from central Patagonia (Chubut province, Argentina) we document the regional extinction of four sigmodontines and one fossorial caviomorph rodent. This diversity loss is discussed in the light of two potential causes: Little Ice Age and human impact. We conclude that probably the latter was the main reason behind the current structure of small mammal communities. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Extinctions Little Ice Age Sheep grazing Small mammals
Changes in micromammal diversity and assemblage structure during the last thousands to hundreds of years represent a powerful tool to infer recent environmental modifications including those attributed to climate phenomena such as global warming (e.g. Avery, 1992; Blois et al., 2010; Moritz et al., 2008; Terry, 2010). In Patagonian drylands, a region poor in classical proxies (i.e. pollen, insects, varves), stratigraphical sequences composed of micromammal remains are valuable sources of evidence in order to reflect Holocene environments (e.g. Pardiñas et al., 2011; Pearson, 1987 and the references therein). Paleoecological reconstructions usually have been based on presence-absence data or changes in the relative abundance of some climate-indicator species (e.g. Teta et al., 2005). Recently, we made a concerted effort to create a complete database of extant rodent and marsupial assemblages for central Patagonia (Pardiñas et al., 2011). In turn, the recent processes that drive the Patagonian communities to their modern structural composition, especially during the last millennium, remain unexplored. This is not a minor issue; this time period was marked by the occurrence of two important climatic anomalies, the Medieval Climatic Anomaly and the Little Ice Age (Villalba, 1990). In addition and partially coupled with the latter, Patagonian ecosystems have been degraded due to human land-use change and livestock introduction around 1890 (e.g. Aagesen, 2000).
* Corresponding author. Tel.: þ54 280 4473 853, þ54 280 4451024/4450401/ 4451301/4451375; fax: þ54 280 4451 543. E-mail address: [email protected] (D.E. Udrizar Sauthier). 0140-1963/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2012.05.009
Here we make a first approximation of the factors causing recent faunal changes in central arid Patagonia. We based our study on the fossil content of the paleontological site “Las Plumas” rockshelter (LPR, hereafter). Even though this is a single sample, its geographic emplacement and specific richness offer an opportunity to explore the small mammal community composition prior to the European settlement. LPR is located 7.5 km southwest Las Plumas (43 470 2500 S, 67180 0800 W, 207 m) in central Chubut province (Fig. 1). The site is placed in the ecotone between the shrub steppes of Nassauvia spp. and Chuquiraga aurea (locally known as “eriales”) and the shrubby steppes of Junellia tridens from the Central District of the Patagónica Phytogeographic Province (sensu León et al., 1998). This is one of the driest sectors in Patagonia with an average annual rainfall up to 200 mm, mostly concentrated in the cooler months from April to September (Paruelo et al., 1998). LPR is a large rockshelter formed by volcanic rocks of the Lonco Trapial formation (Mesozoic). A rock step of 4 m in height served as a perch for owls, generated an unstratified deposit, approximately 20 cm thick consisting of owl pellets and disaggregated skeletal remains of microvertebrates indurated with raptor feces. This shelf collapsed, partly burying the osseous assemblage and protecting them from possible alterations. The studied sample was recovered using a brush and a small shovel, extracting about 15 kg of sediments and skeletal remains. Later, in the laboratory, we pulled out a small amount of organic material for radiocarbon-dating (including ca. 350 g of owl feces and complete owl pellets, because no other organic materials were available); the remaining materials were sieved (0.2 mm), washed with hot water and dried.
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Fig. 1. a) Central Patagonia showing the location of the paleontological site Las Plumas rockshelter, (LPR; locality #3, arrow) and recent owl pellet samples of micromammals (the brown shaded area correspond to the Monte Phytogeographic Province); b) UPGMA clustering of Jaccard values among studied samples. For each figure numbers are according to Table 1; c) Rarification curves; d) Histograms illustrating contrast in taxonomic structure between LPR (above) and a recent sample (locality #4); þ and e symbols on histogram columns highlighted the main differences; y ¼ locally extinct; other abbreviations are as follow: Abrothrix longipilis (Al); Akodon iniscatus (Ai); Calomys musculinus (Cm); Ctenomys sp. (Cte); Eligmodontia sp. (Elig); Graomys griseoflavus (Gg); Loxodontomys micropus (Lm); Microcavia australis (Ma); Notiomys edwardsii (Ne); Oligoryzomys longicaudatus (Ol); Phyllotis xanthopygus (Px); Reithrodon auritus (Ra); Thylamys pallidior (Tp); Tympanoctomys barrerae (Tb). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Taphonomically, the frequency of skeletal parts, degree of digestion, size and form of pellets, and the fact that the sample was found under a rockshelter strongly suggest that the bony accumulation resulted from the predatory foraging habits of a mediumsized owl, perhaps Tyto alba (cf. Andrews, 1990; Reed, 2005). The obtained material mostly consisted of skull and dentaries, postcranial bones and teeth of rodents and marsupials. For each taxon recognized, the minimum number of individuals (MNI) was calculated as a measure of raw abundance in the sample (Grayson, 1984). Taxonomic identifications were made through specific keys and comparative material; studied samples are housed in the Colección de Material de Egagrópilas y Afines “Elio Massoia” of the Centro Nacional Patagónico, Puerto Madryn, Chubut (acronym CNP-E). The radiocarbon date (conventional radiocarbon age) gave a calibrated age of 410 80 yr B P (LP-1956, Laboratorio de Tritio y Radiocarbono, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata; calibration for the Southern Hemisphere: McCormac et al., 2004. CALIB 5.0.1 program, used in conjunction with Stuiver and Reimer, 1993). LPR fossil content was compared against a database of more than 300 small mammal samples from central Patagonian localities; however, for comparative purposes we used only those samples of freshly owl pellets produced by T. alba and located near the Chubut river (like LPR) in a radio of ca. 75 km (Fig. 1a; Table 1). As has been discussed by other authors, Barn owl pellet samples accurately represents the living micromammal communities at a regional scale (Andrews, 1990). Rarefaction curves were calculated for each sample in order to
explore specific richness variation. A cluster analysis was performed on a standardized by octave-scale method data matrix of abundances (%MNI) and used to evaluate the general similarity (Jaccard coefficient) among studied samples (Gauch, 1982). The number of species represented in LPR reached 13, while in the recent samples we find from 8 to 11 (Table 1). Rarefaction curves show that specific richness is not a sample size artifact; at comparable smaller sizes the expected number of species in LPR is 12 whereas the remainder samples ranged between 8 and 10 (Fig. 1c). It is also noteworthy that several of the species registered in LPR are regionally extirpated. These include four sigmodontines (Fig. 2), the long-clawed semifossorial Notiomys edwardsii, two typical Andean elements, Abrothrix longipilis and Loxodontomys micropus, and the colilargo Oligoryzomys longicaudatus, and one caviomorph, the red vizcacha rat Tympanoctomys barrerae. A remarkable finding is the absence in the LPR sample of the currently widespread pericote Graomys griseoflavus (Fig. 1d). In overall terms, modern samples also showed a decrease in the relative abundances of Reithrodon auritus and Ctenomys sp. (Fig. 1c, Table 1). The former is a typical sigmodontine rodent of open habitats with high herbaceous cover, whereas the latter is a subterranean caviomorph widely distributed in Patagonian arid lands (Pearson, 1995). The sigmodontine rodents A. longipilis, L. micropus, and O. longicaudatus have strong affinities to moist microenvironments with dense vegetation cover (Pearson, 1995); these three species are currently sympatric in the Subandean district and Nothofagus forests,
U.F.J. Pardiñas et al. / Journal of Arid Environments 85 (2012) 71e75
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Table 1 Minimum number of individuals (MNI) for each sample of small mammals studied, Central Patagonia (Chubut province). Assemblages are arranged by longitude and taxa by alphabetic order. Numbers between parentheses refer to those used in Fig. 1.
Abrothrix longipilis Abrothrix olivacea Akodon iniscatus Calomys musculinus Ctenomys sp. Eligmodontia sp. Euneomys chinchilloides Galea musteloides Graomys griseoflavus Loxodontomys micropus Microcavia australis Notiomys edwardsii Oligoryzomys longicaudatus Phyllotis xanthopygus Reithrodon auritus Thylamys pallidior Tympanoctomys barrerae Total MNI Species
Peligro cave (1)
De la viborita cave (2)
Las Plumas rockshelter (3)
9.5 km W las Plumas (4)
Cañadón Carbón 3 (5)
Conj. RP 25 and 27 (6)
20 km E los Altares (7)
22 km E los Altares (8)
e e 137 237 3 335 e 6 725 e 9 e e 213 16 140 e 1848 10
e e 4 22 11 235 e 1 52 e 33 e 2 31 8 15 e 414 11
1 e 6 6 36 115 e e e 1 3 1 2 3 15 5 9 203 13
e e 2 23 6 85 e e 42 e 3 e e e 4 2 e 167 8
e e 12 3 5 84 e e 132 e 6 e e 64 1 35 e 342 9
e e 13 9 5 227 1 1 38 e 7 e e 10 10 14 e 336 11
e e 12 41 8 99 e e 8 e 2 e e 9 9 2 e 191 9
e 1 9 36 4 78 e e 22 e 2 e e 2 9 1 e 164 10
more than 300 km west to LPR (Pardiñas et al., 2003; Fig. 2). In turn, N. edwardsii is often found in shrubby and herbaceous steppes and basaltic rocky plateaus (Pardiñas et al., 2011). Finally, T. barrerae is a Monte caviomorph rodent specialist in saline and sandy environments with patches of the shrub Atriplex (Udrizar Sauthier et al., 2009). The only species not recorded in the fossil sample, G. griseoflavus, is loosely linked to the Monte desert and Patagonian river valleys, where it occupies shrubby habitats with sandy and rocky soils and scarce vegetation cover (Udrizar Sauthier et al., 2011). Summarizing, the record of LPR and its comparison with modern samples shows an important decrease of the specific
richness involving losses of several sigmodontines mainly associated to more densely covered habitats or some habitat specialists. Taking into account temporal (<500 years) and regional (central Patagonia) scales, two not mutually exclusive causes could be suggested in order to explain this faunal change: (1) Little Ice Age: the calibrated age of LPR sample is 1543e1624 AD and largely falls within a cold and moist climatic pulse detected in northern Patagonia and linked with the global anomaly called Little Ice Age (Villalba, 1990). Under this scenario, higher mean annual rainfall and lower mean
Fig. 2. Rodent species regionally extirpated in Central Patagonia. For each taxon recent distribution is showed in green. Blue dot: Las Plumas rockshelter. Red dots are unpublished Late Holocene records: A. Los Altares profile (2.2 ka B.P.-recent); B. De la Virgen cave (5.5 ka B.P.-recent); C. Lonco Trapial crevice (Late Holocene); D. Caolinera Dique Ameghino cave (3.9 ka B.P.-recent). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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temperatures could have allowed the eastward expansion of typically western species associated to more heterogeneous and cold environments, such as A. longipilis, O. longicaudatus and L. micropus (Rebane, 2002). Also, the increase in vegetation cover, especially grasses, could have been favored some steppe species, such as R. auritus and N. edwardsii. By the end of this period, in the mid-nineteenth century, climatic conditions became drier (Villalba, 1990) and Monte floristic formations advanced over the Patagonian steppe, causing the regional extirpation of these western elements and their putative replacement by opportunistic species such as G. griseoflavus and C. musculinus (Pardiñas et al., 2011). (2) Human impact: since the establishment of the first Welsh settlers in the middle to late nineteenth century in central Patagonia, there was a progressive transformation of natural environments, mainly due to a combination of extensive sheep farming and the development of crop fields in river valleys. Farming practices, especially ovine grazing, have caused the loss of herbaceous cover and the increase of shrubs and bare soil patches in central Patagonia (Bisigato and Bertiller, 1997). Furthermore, intense ovine pressure on small wetlands, locally known as “mallines,” favored a variety of desertification processes (Mazzoni and Vazquez, 2009). Both the reduction of herbaceous cover and the dense shrubby microhabitats could be the cause of the disappearance of several species such as A. longipilis, L. micropus or O. longicaudatus and the relative decrease in the abundance of R. auritus. At the same time, Ctenomys sp. and T. barrerae may have also been strongly affected or eradicated by the soil compaction caused by sheep trampling on soft substrates (cf. Osgood, 1943). In turn, G. griseoflavus was surely favored by the increase of disperse shrubs, whereas C. musculinus was benefited by the development of crop fields along the Chubut river valley (cf. Pardiñas et al., 2000). Dissecting climate and human signals in a faunal change process is not an easy task; a large amount of data about biotic communities previous to the recent antrophic impact is usually required as well as the existence of undisturbed, large control areas (Moritz et al., 2008; Terry, 2010). Regrettably, both are lacking for Patagonia, where the knowledge on micromammals is still incipient (see Lessa et al., 2010). However, several facts and primary observations (Pardiñas et al., 2000, 2011) reinforce our perception of the major role of the recent human impact on driving small mammal assemblages to their current structure. First, extensive micromammal sequences in several regions of Patagonia covering the entire Holocene showed that communities were basically conservative despite the occurrence of strong climatic fluctuations (e.g. Pearson, 1987). Even when some variation in relative abundances has been widely documented through Patagonia (e.g. Teta et al., 2005), local extirpation involving several small mammal species over relatively large areas, or drastic increments of generalist taxa are both restricted to the last hundred years (Pardiñas et al., 2000, 2011). This scenario is in accordance with the historical information. European settlement in central Patagonia took place ca. 1865, affecting specially river valleys areas, where the native vegetation was almost replaced by pastures and cultivate fields in <50 years (Matthews, 2005). Secondly, the rodents extirpated according to the LPR record include species linked both to western and eastern Patagonian environments, under different climatic conditions. These species-specific responses are more in accordance with what is expected from stressed ecosystems such as those affected by human disturbance (Gray, 1989). For the lower valley of the Chubut river East LPR, Pardiñas et al. (2000) documented a strong reduction in rodent diversity during
the latest Holocene. In this area, an impressive increase of the local abundance of the small and versatile sigmodontine Calomys can be linked with the rapid conversion of natural habitats to pasture and cultivated fields. Under the same argument, Udrizar Sauthier et al. (2009) recorded the Late Holocene occurrence of several Tympanoctomys populations along the Chubut river valley that are now extinct. Micromammal diversity loss in the late Holocene is not a feature exclusive of Patagonian dryland assemblages. Several sigmodontine species were extirpated during the last hundred years at Pampean mid latitudes in Argentina (e.g. Scheifler et al., in press). More importantly, impoverishment of species assemblages attributed to a variety of human activities was inferred from the Holocene record in several places in the southern hemisphere, including Chile (Simonetti and Saavedra, 1998), South Africa (Avery, 1992), or Australia (Bilney et al., 2010). Under the present scenario of increasing desertification in Patagonia (Mazzoni and Vazquez, 2009) a clear understanding of the relative influences of climatic and human factors in mammal communities’ configurations must be a priority. The longer temporal perspective provided through the fossil record produced by owls raised the importance of not only this kind of proxy data but if not also of the occurrence of very recent and overlooked key ecological events such as regional extinctions. Acknowledgments This contribution was partially supported by PICT 32405 and PICT 2008-0547 from Agencia Nacional de Promoción Científica y Tecnológica, Argentina. Walter Udrizar Sauthier, Joaquín Pardiñas, Anahí Formoso, and Adela Bernardis assisted us during field and laboratory works. The observations made by two anonymous reviewers greatly improved an early version of this work. References Aagesen, D., 2000. Crisis and conservation at the end of the world: sheep ranching in Argentine Patagonia. Environmental Conservation 27, 208e215. Andrews, P., 1990. Owls, Caves and Fossils. Natural History Museum Publications, London. Avery, D.M., 1992. Man and/or climate? Environmental degradation and micromammalian community structure in South Africa during the last millennium. Siud-Afrikaanse Tydskrif vir Wetenskap 88, 483e489. Bilney, R.J., Cooke, R., White, J.G., 2010. Underestimated and severe: small mammal decline from the forests of south-eastern Australia since European settlement, as revealed by a top-order predator. Biological Conservation 143, 52e59. Bisigato, A.J., Bertiller, M.B., 1997. Grazing effects on patchy dryland vegetation in Northern Patagonia. Journal of Arid Environments 36, 639e653. Blois, J.L., McGuire, J.L., Hadly, E.A., 2010. Small mammal diversity loss in response to late-Pleistocene climatic change. Nature 465, 771e774. Gauch, H.G., 1982. Multivariate Analysis in Community Ecology. Cambridge University Press, New York, 298 pp. Gray, J.S., 1989. Effects of environmental stress on species rich assemblages. Biological Journal of the Linnean Society 37, 19e32. Grayson, D.K., 1984. Quantitative Zooarchaeology. Topics in the Analysis of Archaeological Faunas. In: Studies in Archaeological Science. Academic Press, Inc., New York, 202 pp. León, R.J.C., Bran, D., Collantes, M., Paruelo, J.M., Soriano, A., 1998. Grandes unidades de vegetación de la Patagonia extra andina. Ecología Austral 8, 75e308. Lessa, E.P., D’Elía, G., Pardiñas, U.F.J., 2010. Genetic footprints of late Quaternary climate change in the diversity of Patagonian-Fueguian rodents. Molecular Ecology 19, 3031e3037. Matthews, A., 2005. Crónica de la colonia galesa. Editores el Regional, Gaiman, Chubut, Argentina. Mazzoni, E., Vazquez, M., 2009. Desertification in Patagonia. In: Latrubesse, E. (Ed.), Natural Hazards and Human-Exacerbated Disasters in Latin America: Special Volumes of Geomorphology. Elsevier, pp. 351e377. McCormac, F.G., Hogg, A.G., Blackwell, P.G., Buck, C.E., Higham, T.F.G., Reimer, P.J., 2004. SHCal04 Southern Hemisphere Calibration 0e11.0 cal KYR BP. Radiocarbon 46, 1087e1092. Moritz, C., Patton, J.L., Conroy, C.J., Parra, J.L., Withe, G.C., Beissinger, S.R., 2008. Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261e264. Osgood, W.H., 1943. The mammals of Chile. Field Museum of Natural History, Zoological Series 30, 1e268.
U.F.J. Pardiñas et al. / Journal of Arid Environments 85 (2012) 71e75 Pardiñas, U.F.J., Moreira, G., García-Esponda, C., De Santis, L.J.M., 2000. Deterioro ambiental y micromamíferos durante el Holoceno en el nordeste de la estepa patagónica (Argentina). Revista Chilena de Historia Natural 72, 541e556. Pardiñas, U.F.J., Teta, P., D’Elía, G., Lessa, E.P., 2011. The evolutionary history of sigmodontine rodents in Patagonia and Tierra del Fuego. Biological Journal of the Linnean Society 103, 495e513. Pardiñas, U.F.J., Teta, P., Cirignoli, S., Podesta, D.H., 2003. Micromamíferos (Didelphimorphia y Rodentia) de norpatagonia extra andina, Argentina: taxonomía alfa y biogeografía. In: Mastozoología Neotropical, vol. 10, pp. 69e113. Paruelo, J.M., Beltrán, A., Jobbágy, E.G., Sala, O.E., Golluscio, R., 1998. The climate of Patagonia: general patterns and controls on biotic processes. Ecología Austral 8, 85e101. Pearson, O.P., 1987. Mice and the Postglacial history of the Traful valley of Argentina. Journal of Mammalogy 68, 469e478. Pearson, O.P., 1995. Annotated keys for identifying small mammals living in or near Nahuel Huapi National Park or Lanín National Park, southern Argentina. Mastozoología Neotropical 2, 99e148. Rebane, K. 2002. The Effects of Historic Climatic Change and Anthopogenic Disturbance on Rodent Communities in Patagonia, Argentina. Unpublished Honors thesis, Stanford University, Stanford, CA. Reed, D.N., 2005. Taphonomic implications of roosting behavior and trophic habits in two species of African owl. Journal of Archaeological Science 32, 1669e1676.
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Scheifler, N.A., Teta, P., Pardiñas, U.F.J. Small mammals (Didelphimorphia and Rodentia) of the archaeological site Calera (Pampean region, Buenos Aires Province, Argentina): taphonomic history and Late Holocene environments. Quaternary International, in press Simonetti, J.A., Saavedra, B., 1998. Holocene variation in the small mammal fauna of central Chile. Zeitschrift für Säugetierkunde 63, 58e62. Stuiver, M., Reimer, P.J., 1993. Extended 14C database and revised CALIB 3.0 14C Age calibration program. Radiocarbon 35, 215e230. Terry, R.C., 2010. The dead do not lie: using skeletal remains for rapid assessment of historical small-mammal community baselines. Proceedings of the Royal Society B 277, 1193e1201. Teta, P., Andrade, A., Pardiñas, U.F.J., 2005. Micromamíferos (Didelphimorphia y Rodentia) y paleoambientes del Holoceno tardío en la Patagonia noroccidental extra-andina (Argentina). Archaeofauna 14, 183e197. Udrizar Sauthier, D.E., Formoso, A.E., Teta, P., Pardiñas, U.F.J., 2011. Enlarging the knowledge on Graomys griseoflavus (Rodentia: Sigmodontinae) in Patagonia: distribution and environments. Mammalia 75, 185e193. Udrizar Sauthier, D.E., Pardiñas, U.F.J., Tonni, E.P., 2009. Tympanoctomys (Mammalia: Rodentia) en el Holoceno de Patagonia, Argentina. Ameghiniana 46, 203e207. Villalba, R., 1990. Climatic fluctuations in northern Patagonia during the last 1000 years as inferred from tree-ring records. Quaternary Research 34, 346e360.
Contents lists available at SciVerse ScienceDirect
Journal of Arid Environments journal homepage: www.elsevier.com/locate/jaridenv
Short communication
Micromammal diversity loss in central-eastern Patagonia over the last 400 years U.F.J. Pardiñas, D.E. Udrizar Sauthier*, P. Teta Unidad de Investigación Diversidad, Sistemática y Evolución, Centro Nacional Patagónico-CONICET, Boulevard Brown 2915, Casilla de Correo 128, 9120 Puerto Madryn, Chubut, Argentina
a r t i c l e i n f o
a b s t r a c t
Article history: Received 25 July 2011 Received in revised form 24 April 2012 Accepted 29 May 2012 Available online 13 July 2012
Through the study of a late Holocene sample of small mammal remains from central Patagonia (Chubut province, Argentina) we document the regional extinction of four sigmodontines and one fossorial caviomorph rodent. This diversity loss is discussed in the light of two potential causes: Little Ice Age and human impact. We conclude that probably the latter was the main reason behind the current structure of small mammal communities. Ó 2012 Elsevier Ltd. All rights reserved.
Keywords: Extinctions Little Ice Age Sheep grazing Small mammals
Changes in micromammal diversity and assemblage structure during the last thousands to hundreds of years represent a powerful tool to infer recent environmental modifications including those attributed to climate phenomena such as global warming (e.g. Avery, 1992; Blois et al., 2010; Moritz et al., 2008; Terry, 2010). In Patagonian drylands, a region poor in classical proxies (i.e. pollen, insects, varves), stratigraphical sequences composed of micromammal remains are valuable sources of evidence in order to reflect Holocene environments (e.g. Pardiñas et al., 2011; Pearson, 1987 and the references therein). Paleoecological reconstructions usually have been based on presence-absence data or changes in the relative abundance of some climate-indicator species (e.g. Teta et al., 2005). Recently, we made a concerted effort to create a complete database of extant rodent and marsupial assemblages for central Patagonia (Pardiñas et al., 2011). In turn, the recent processes that drive the Patagonian communities to their modern structural composition, especially during the last millennium, remain unexplored. This is not a minor issue; this time period was marked by the occurrence of two important climatic anomalies, the Medieval Climatic Anomaly and the Little Ice Age (Villalba, 1990). In addition and partially coupled with the latter, Patagonian ecosystems have been degraded due to human land-use change and livestock introduction around 1890 (e.g. Aagesen, 2000).
* Corresponding author. Tel.: þ54 280 4473 853, þ54 280 4451024/4450401/ 4451301/4451375; fax: þ54 280 4451 543. E-mail address: [email protected] (D.E. Udrizar Sauthier). 0140-1963/$ e see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jaridenv.2012.05.009
Here we make a first approximation of the factors causing recent faunal changes in central arid Patagonia. We based our study on the fossil content of the paleontological site “Las Plumas” rockshelter (LPR, hereafter). Even though this is a single sample, its geographic emplacement and specific richness offer an opportunity to explore the small mammal community composition prior to the European settlement. LPR is located 7.5 km southwest Las Plumas (43 470 2500 S, 67180 0800 W, 207 m) in central Chubut province (Fig. 1). The site is placed in the ecotone between the shrub steppes of Nassauvia spp. and Chuquiraga aurea (locally known as “eriales”) and the shrubby steppes of Junellia tridens from the Central District of the Patagónica Phytogeographic Province (sensu León et al., 1998). This is one of the driest sectors in Patagonia with an average annual rainfall up to 200 mm, mostly concentrated in the cooler months from April to September (Paruelo et al., 1998). LPR is a large rockshelter formed by volcanic rocks of the Lonco Trapial formation (Mesozoic). A rock step of 4 m in height served as a perch for owls, generated an unstratified deposit, approximately 20 cm thick consisting of owl pellets and disaggregated skeletal remains of microvertebrates indurated with raptor feces. This shelf collapsed, partly burying the osseous assemblage and protecting them from possible alterations. The studied sample was recovered using a brush and a small shovel, extracting about 15 kg of sediments and skeletal remains. Later, in the laboratory, we pulled out a small amount of organic material for radiocarbon-dating (including ca. 350 g of owl feces and complete owl pellets, because no other organic materials were available); the remaining materials were sieved (0.2 mm), washed with hot water and dried.
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Fig. 1. a) Central Patagonia showing the location of the paleontological site Las Plumas rockshelter, (LPR; locality #3, arrow) and recent owl pellet samples of micromammals (the brown shaded area correspond to the Monte Phytogeographic Province); b) UPGMA clustering of Jaccard values among studied samples. For each figure numbers are according to Table 1; c) Rarification curves; d) Histograms illustrating contrast in taxonomic structure between LPR (above) and a recent sample (locality #4); þ and e symbols on histogram columns highlighted the main differences; y ¼ locally extinct; other abbreviations are as follow: Abrothrix longipilis (Al); Akodon iniscatus (Ai); Calomys musculinus (Cm); Ctenomys sp. (Cte); Eligmodontia sp. (Elig); Graomys griseoflavus (Gg); Loxodontomys micropus (Lm); Microcavia australis (Ma); Notiomys edwardsii (Ne); Oligoryzomys longicaudatus (Ol); Phyllotis xanthopygus (Px); Reithrodon auritus (Ra); Thylamys pallidior (Tp); Tympanoctomys barrerae (Tb). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Taphonomically, the frequency of skeletal parts, degree of digestion, size and form of pellets, and the fact that the sample was found under a rockshelter strongly suggest that the bony accumulation resulted from the predatory foraging habits of a mediumsized owl, perhaps Tyto alba (cf. Andrews, 1990; Reed, 2005). The obtained material mostly consisted of skull and dentaries, postcranial bones and teeth of rodents and marsupials. For each taxon recognized, the minimum number of individuals (MNI) was calculated as a measure of raw abundance in the sample (Grayson, 1984). Taxonomic identifications were made through specific keys and comparative material; studied samples are housed in the Colección de Material de Egagrópilas y Afines “Elio Massoia” of the Centro Nacional Patagónico, Puerto Madryn, Chubut (acronym CNP-E). The radiocarbon date (conventional radiocarbon age) gave a calibrated age of 410 80 yr B P (LP-1956, Laboratorio de Tritio y Radiocarbono, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata; calibration for the Southern Hemisphere: McCormac et al., 2004. CALIB 5.0.1 program, used in conjunction with Stuiver and Reimer, 1993). LPR fossil content was compared against a database of more than 300 small mammal samples from central Patagonian localities; however, for comparative purposes we used only those samples of freshly owl pellets produced by T. alba and located near the Chubut river (like LPR) in a radio of ca. 75 km (Fig. 1a; Table 1). As has been discussed by other authors, Barn owl pellet samples accurately represents the living micromammal communities at a regional scale (Andrews, 1990). Rarefaction curves were calculated for each sample in order to
explore specific richness variation. A cluster analysis was performed on a standardized by octave-scale method data matrix of abundances (%MNI) and used to evaluate the general similarity (Jaccard coefficient) among studied samples (Gauch, 1982). The number of species represented in LPR reached 13, while in the recent samples we find from 8 to 11 (Table 1). Rarefaction curves show that specific richness is not a sample size artifact; at comparable smaller sizes the expected number of species in LPR is 12 whereas the remainder samples ranged between 8 and 10 (Fig. 1c). It is also noteworthy that several of the species registered in LPR are regionally extirpated. These include four sigmodontines (Fig. 2), the long-clawed semifossorial Notiomys edwardsii, two typical Andean elements, Abrothrix longipilis and Loxodontomys micropus, and the colilargo Oligoryzomys longicaudatus, and one caviomorph, the red vizcacha rat Tympanoctomys barrerae. A remarkable finding is the absence in the LPR sample of the currently widespread pericote Graomys griseoflavus (Fig. 1d). In overall terms, modern samples also showed a decrease in the relative abundances of Reithrodon auritus and Ctenomys sp. (Fig. 1c, Table 1). The former is a typical sigmodontine rodent of open habitats with high herbaceous cover, whereas the latter is a subterranean caviomorph widely distributed in Patagonian arid lands (Pearson, 1995). The sigmodontine rodents A. longipilis, L. micropus, and O. longicaudatus have strong affinities to moist microenvironments with dense vegetation cover (Pearson, 1995); these three species are currently sympatric in the Subandean district and Nothofagus forests,
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Table 1 Minimum number of individuals (MNI) for each sample of small mammals studied, Central Patagonia (Chubut province). Assemblages are arranged by longitude and taxa by alphabetic order. Numbers between parentheses refer to those used in Fig. 1.
Abrothrix longipilis Abrothrix olivacea Akodon iniscatus Calomys musculinus Ctenomys sp. Eligmodontia sp. Euneomys chinchilloides Galea musteloides Graomys griseoflavus Loxodontomys micropus Microcavia australis Notiomys edwardsii Oligoryzomys longicaudatus Phyllotis xanthopygus Reithrodon auritus Thylamys pallidior Tympanoctomys barrerae Total MNI Species
Peligro cave (1)
De la viborita cave (2)
Las Plumas rockshelter (3)
9.5 km W las Plumas (4)
Cañadón Carbón 3 (5)
Conj. RP 25 and 27 (6)
20 km E los Altares (7)
22 km E los Altares (8)
e e 137 237 3 335 e 6 725 e 9 e e 213 16 140 e 1848 10
e e 4 22 11 235 e 1 52 e 33 e 2 31 8 15 e 414 11
1 e 6 6 36 115 e e e 1 3 1 2 3 15 5 9 203 13
e e 2 23 6 85 e e 42 e 3 e e e 4 2 e 167 8
e e 12 3 5 84 e e 132 e 6 e e 64 1 35 e 342 9
e e 13 9 5 227 1 1 38 e 7 e e 10 10 14 e 336 11
e e 12 41 8 99 e e 8 e 2 e e 9 9 2 e 191 9
e 1 9 36 4 78 e e 22 e 2 e e 2 9 1 e 164 10
more than 300 km west to LPR (Pardiñas et al., 2003; Fig. 2). In turn, N. edwardsii is often found in shrubby and herbaceous steppes and basaltic rocky plateaus (Pardiñas et al., 2011). Finally, T. barrerae is a Monte caviomorph rodent specialist in saline and sandy environments with patches of the shrub Atriplex (Udrizar Sauthier et al., 2009). The only species not recorded in the fossil sample, G. griseoflavus, is loosely linked to the Monte desert and Patagonian river valleys, where it occupies shrubby habitats with sandy and rocky soils and scarce vegetation cover (Udrizar Sauthier et al., 2011). Summarizing, the record of LPR and its comparison with modern samples shows an important decrease of the specific
richness involving losses of several sigmodontines mainly associated to more densely covered habitats or some habitat specialists. Taking into account temporal (<500 years) and regional (central Patagonia) scales, two not mutually exclusive causes could be suggested in order to explain this faunal change: (1) Little Ice Age: the calibrated age of LPR sample is 1543e1624 AD and largely falls within a cold and moist climatic pulse detected in northern Patagonia and linked with the global anomaly called Little Ice Age (Villalba, 1990). Under this scenario, higher mean annual rainfall and lower mean
Fig. 2. Rodent species regionally extirpated in Central Patagonia. For each taxon recent distribution is showed in green. Blue dot: Las Plumas rockshelter. Red dots are unpublished Late Holocene records: A. Los Altares profile (2.2 ka B.P.-recent); B. De la Virgen cave (5.5 ka B.P.-recent); C. Lonco Trapial crevice (Late Holocene); D. Caolinera Dique Ameghino cave (3.9 ka B.P.-recent). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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temperatures could have allowed the eastward expansion of typically western species associated to more heterogeneous and cold environments, such as A. longipilis, O. longicaudatus and L. micropus (Rebane, 2002). Also, the increase in vegetation cover, especially grasses, could have been favored some steppe species, such as R. auritus and N. edwardsii. By the end of this period, in the mid-nineteenth century, climatic conditions became drier (Villalba, 1990) and Monte floristic formations advanced over the Patagonian steppe, causing the regional extirpation of these western elements and their putative replacement by opportunistic species such as G. griseoflavus and C. musculinus (Pardiñas et al., 2011). (2) Human impact: since the establishment of the first Welsh settlers in the middle to late nineteenth century in central Patagonia, there was a progressive transformation of natural environments, mainly due to a combination of extensive sheep farming and the development of crop fields in river valleys. Farming practices, especially ovine grazing, have caused the loss of herbaceous cover and the increase of shrubs and bare soil patches in central Patagonia (Bisigato and Bertiller, 1997). Furthermore, intense ovine pressure on small wetlands, locally known as “mallines,” favored a variety of desertification processes (Mazzoni and Vazquez, 2009). Both the reduction of herbaceous cover and the dense shrubby microhabitats could be the cause of the disappearance of several species such as A. longipilis, L. micropus or O. longicaudatus and the relative decrease in the abundance of R. auritus. At the same time, Ctenomys sp. and T. barrerae may have also been strongly affected or eradicated by the soil compaction caused by sheep trampling on soft substrates (cf. Osgood, 1943). In turn, G. griseoflavus was surely favored by the increase of disperse shrubs, whereas C. musculinus was benefited by the development of crop fields along the Chubut river valley (cf. Pardiñas et al., 2000). Dissecting climate and human signals in a faunal change process is not an easy task; a large amount of data about biotic communities previous to the recent antrophic impact is usually required as well as the existence of undisturbed, large control areas (Moritz et al., 2008; Terry, 2010). Regrettably, both are lacking for Patagonia, where the knowledge on micromammals is still incipient (see Lessa et al., 2010). However, several facts and primary observations (Pardiñas et al., 2000, 2011) reinforce our perception of the major role of the recent human impact on driving small mammal assemblages to their current structure. First, extensive micromammal sequences in several regions of Patagonia covering the entire Holocene showed that communities were basically conservative despite the occurrence of strong climatic fluctuations (e.g. Pearson, 1987). Even when some variation in relative abundances has been widely documented through Patagonia (e.g. Teta et al., 2005), local extirpation involving several small mammal species over relatively large areas, or drastic increments of generalist taxa are both restricted to the last hundred years (Pardiñas et al., 2000, 2011). This scenario is in accordance with the historical information. European settlement in central Patagonia took place ca. 1865, affecting specially river valleys areas, where the native vegetation was almost replaced by pastures and cultivate fields in <50 years (Matthews, 2005). Secondly, the rodents extirpated according to the LPR record include species linked both to western and eastern Patagonian environments, under different climatic conditions. These species-specific responses are more in accordance with what is expected from stressed ecosystems such as those affected by human disturbance (Gray, 1989). For the lower valley of the Chubut river East LPR, Pardiñas et al. (2000) documented a strong reduction in rodent diversity during
the latest Holocene. In this area, an impressive increase of the local abundance of the small and versatile sigmodontine Calomys can be linked with the rapid conversion of natural habitats to pasture and cultivated fields. Under the same argument, Udrizar Sauthier et al. (2009) recorded the Late Holocene occurrence of several Tympanoctomys populations along the Chubut river valley that are now extinct. Micromammal diversity loss in the late Holocene is not a feature exclusive of Patagonian dryland assemblages. Several sigmodontine species were extirpated during the last hundred years at Pampean mid latitudes in Argentina (e.g. Scheifler et al., in press). More importantly, impoverishment of species assemblages attributed to a variety of human activities was inferred from the Holocene record in several places in the southern hemisphere, including Chile (Simonetti and Saavedra, 1998), South Africa (Avery, 1992), or Australia (Bilney et al., 2010). Under the present scenario of increasing desertification in Patagonia (Mazzoni and Vazquez, 2009) a clear understanding of the relative influences of climatic and human factors in mammal communities’ configurations must be a priority. The longer temporal perspective provided through the fossil record produced by owls raised the importance of not only this kind of proxy data but if not also of the occurrence of very recent and overlooked key ecological events such as regional extinctions. Acknowledgments This contribution was partially supported by PICT 32405 and PICT 2008-0547 from Agencia Nacional de Promoción Científica y Tecnológica, Argentina. Walter Udrizar Sauthier, Joaquín Pardiñas, Anahí Formoso, and Adela Bernardis assisted us during field and laboratory works. The observations made by two anonymous reviewers greatly improved an early version of this work. References Aagesen, D., 2000. Crisis and conservation at the end of the world: sheep ranching in Argentine Patagonia. Environmental Conservation 27, 208e215. Andrews, P., 1990. Owls, Caves and Fossils. Natural History Museum Publications, London. Avery, D.M., 1992. Man and/or climate? Environmental degradation and micromammalian community structure in South Africa during the last millennium. Siud-Afrikaanse Tydskrif vir Wetenskap 88, 483e489. Bilney, R.J., Cooke, R., White, J.G., 2010. Underestimated and severe: small mammal decline from the forests of south-eastern Australia since European settlement, as revealed by a top-order predator. Biological Conservation 143, 52e59. Bisigato, A.J., Bertiller, M.B., 1997. Grazing effects on patchy dryland vegetation in Northern Patagonia. Journal of Arid Environments 36, 639e653. Blois, J.L., McGuire, J.L., Hadly, E.A., 2010. Small mammal diversity loss in response to late-Pleistocene climatic change. Nature 465, 771e774. Gauch, H.G., 1982. Multivariate Analysis in Community Ecology. Cambridge University Press, New York, 298 pp. Gray, J.S., 1989. Effects of environmental stress on species rich assemblages. Biological Journal of the Linnean Society 37, 19e32. Grayson, D.K., 1984. Quantitative Zooarchaeology. Topics in the Analysis of Archaeological Faunas. In: Studies in Archaeological Science. Academic Press, Inc., New York, 202 pp. León, R.J.C., Bran, D., Collantes, M., Paruelo, J.M., Soriano, A., 1998. Grandes unidades de vegetación de la Patagonia extra andina. Ecología Austral 8, 75e308. Lessa, E.P., D’Elía, G., Pardiñas, U.F.J., 2010. Genetic footprints of late Quaternary climate change in the diversity of Patagonian-Fueguian rodents. Molecular Ecology 19, 3031e3037. Matthews, A., 2005. Crónica de la colonia galesa. Editores el Regional, Gaiman, Chubut, Argentina. Mazzoni, E., Vazquez, M., 2009. Desertification in Patagonia. In: Latrubesse, E. (Ed.), Natural Hazards and Human-Exacerbated Disasters in Latin America: Special Volumes of Geomorphology. Elsevier, pp. 351e377. McCormac, F.G., Hogg, A.G., Blackwell, P.G., Buck, C.E., Higham, T.F.G., Reimer, P.J., 2004. SHCal04 Southern Hemisphere Calibration 0e11.0 cal KYR BP. Radiocarbon 46, 1087e1092. Moritz, C., Patton, J.L., Conroy, C.J., Parra, J.L., Withe, G.C., Beissinger, S.R., 2008. Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322, 261e264. Osgood, W.H., 1943. The mammals of Chile. Field Museum of Natural History, Zoological Series 30, 1e268.
U.F.J. Pardiñas et al. / Journal of Arid Environments 85 (2012) 71e75 Pardiñas, U.F.J., Moreira, G., García-Esponda, C., De Santis, L.J.M., 2000. Deterioro ambiental y micromamíferos durante el Holoceno en el nordeste de la estepa patagónica (Argentina). Revista Chilena de Historia Natural 72, 541e556. Pardiñas, U.F.J., Teta, P., D’Elía, G., Lessa, E.P., 2011. The evolutionary history of sigmodontine rodents in Patagonia and Tierra del Fuego. Biological Journal of the Linnean Society 103, 495e513. Pardiñas, U.F.J., Teta, P., Cirignoli, S., Podesta, D.H., 2003. Micromamíferos (Didelphimorphia y Rodentia) de norpatagonia extra andina, Argentina: taxonomía alfa y biogeografía. In: Mastozoología Neotropical, vol. 10, pp. 69e113. Paruelo, J.M., Beltrán, A., Jobbágy, E.G., Sala, O.E., Golluscio, R., 1998. The climate of Patagonia: general patterns and controls on biotic processes. Ecología Austral 8, 85e101. Pearson, O.P., 1987. Mice and the Postglacial history of the Traful valley of Argentina. Journal of Mammalogy 68, 469e478. Pearson, O.P., 1995. Annotated keys for identifying small mammals living in or near Nahuel Huapi National Park or Lanín National Park, southern Argentina. Mastozoología Neotropical 2, 99e148. Rebane, K. 2002. The Effects of Historic Climatic Change and Anthopogenic Disturbance on Rodent Communities in Patagonia, Argentina. Unpublished Honors thesis, Stanford University, Stanford, CA. Reed, D.N., 2005. Taphonomic implications of roosting behavior and trophic habits in two species of African owl. Journal of Archaeological Science 32, 1669e1676.
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Scheifler, N.A., Teta, P., Pardiñas, U.F.J. Small mammals (Didelphimorphia and Rodentia) of the archaeological site Calera (Pampean region, Buenos Aires Province, Argentina): taphonomic history and Late Holocene environments. Quaternary International, in press Simonetti, J.A., Saavedra, B., 1998. Holocene variation in the small mammal fauna of central Chile. Zeitschrift für Säugetierkunde 63, 58e62. Stuiver, M., Reimer, P.J., 1993. Extended 14C database and revised CALIB 3.0 14C Age calibration program. Radiocarbon 35, 215e230. Terry, R.C., 2010. The dead do not lie: using skeletal remains for rapid assessment of historical small-mammal community baselines. Proceedings of the Royal Society B 277, 1193e1201. Teta, P., Andrade, A., Pardiñas, U.F.J., 2005. Micromamíferos (Didelphimorphia y Rodentia) y paleoambientes del Holoceno tardío en la Patagonia noroccidental extra-andina (Argentina). Archaeofauna 14, 183e197. Udrizar Sauthier, D.E., Formoso, A.E., Teta, P., Pardiñas, U.F.J., 2011. Enlarging the knowledge on Graomys griseoflavus (Rodentia: Sigmodontinae) in Patagonia: distribution and environments. Mammalia 75, 185e193. Udrizar Sauthier, D.E., Pardiñas, U.F.J., Tonni, E.P., 2009. Tympanoctomys (Mammalia: Rodentia) en el Holoceno de Patagonia, Argentina. Ameghiniana 46, 203e207. Villalba, R., 1990. Climatic fluctuations in northern Patagonia during the last 1000 years as inferred from tree-ring records. Quaternary Research 34, 346e360.