Fantastic beasts and what they ate: Revealing feeding habits and ecological niche of late Quaternary Macraucheniidae from South America

Quaternary Science Reviews 231 (2020) 106178

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Fantastic beasts and what they ate: Revealing feeding habits and ecological niche of late Quaternary Macraucheniidae from South America
a, c, Karoliny de Oliveira a, b, c, *, Thaísa Araújo a, c, Alline Rotti a, Dimila Mothe d , e, f a, b, c , Leonardo S. Avilla Florent Rivals
rio de Mastozoologia, Instituto de Bioci^ Laborato encias, Universidade Federal do Estado do Rio de Janeiro. Avenida Pasteur, 458, Sala 501, Urca., 22290-240, Rio de Janeiro, RJ, Brazil ~o em Biodiversidade Neotropical, Universidade Federal do Estado do Rio de Janeiro. Avenida Pasteur, 458, Sala 506A, Urca.,
s-graduaça Programa de Po 22290-240, Rio de Janeiro, RJ, Brazil c ~o em Biodiversidade e Biologia Evolutiva (PPGBBE), Universidade Federal do Rio de Janeiro, Centro de Ci^
s-graduaça Programa de Po encias da Saúde, Pr
edio
ria, 21941-902, Rio de Janeiro, RJ, Brazil
s-graduaço ~es do Instituto de Biologia, Interbloco B/C, Cidade Universita das Po d ICREA, Pg. Lluís Companys 23, 08010, Barcelona, Spain e  de Paleoecologia Humana i Evolucio
Social (IPHES), Zona Educacional 4, Campus Sescelades URV (Edifici W3), 43007, Tarragona, Spain Institut Catala f  ria, Avinguda de Catalunya 35, 43002, Tarragona, Spain Universitat Rovira i Virgili (URV), Area de Prehisto a

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 8 June 2019 Received in revised form 27 December 2019 Accepted 18 January 2020 Available online xxx

The extinction of the Quaternary megafauna stands out among the evolutionary history of Cenozoic mammals. In South America, nearly 80% of the megamammals went extinct, including the native ungulates Macrauchenia patachonica and Xenorhinotherium bahiense. Little is known about the causes of the macraucheniids’ extinction and their paleobiology. Here, we have reconstructed the dietary habits of M. patachonica and X. bahiense using enamel microwear and occlusal enamel index analyses, and also inferred their niches using species distribution modeling and stable isotope paleoecology, in addition to enamel microwear and occlusal enamel index data. We found that both macraucheniids had grazerfeeding habits, although their environmental requirements were different. M. patachonica could live in colder temperatures and arid, subtropical/temperate ecosystems, while X. bahiense was adapted to warmer temperatures and more humid, semi-arid tropical environments. Thus, despite similar feeding habits, these macraucheniids had distinct environmental requirements and ecological niches, which might explain the disjunction in the South American records. © 2020 Elsevier Ltd. All rights reserved.

Keywords: Last Glacial Maximum Middle Holocene Species niche modeling Enamel microwear Occlusal enamel complexity Macraucheniidae Pleistocene Paleogeography South America Stable isotopes

1. Introduction The South American native Quaternary mammals stand out for their morphological characteristics, which many specialists consider bizarre and unique, for example, the native ungulate


rio de Mastozoologia, Instituto de Biocie ^ncias, * Corresponding author. Laborato Universidade Federal do Estado do Rio de Janeiro. Avenida Pasteur, 458, sala 501, Urca., 22290-240, Rio de Janeiro, RJ, Brazil. E-mail addresses: [email protected] (K. de Oliveira), thaisa. [email protected] (T. Araújo), [email protected] (A. Rotti), dimothe@hotmail.
), fl[email protected] (F. Rivals), [email protected] com (D. Mothe (L.S. Avilla). https://doi.org/10.1016/j.quascirev.2020.106178 0277-3791/© 2020 Elsevier Ltd. All rights reserved.

Macrauchenia patachonica Owen, 1838 wich had nostrils at the top of its skull, posterior to the orbits. In 1834, Charles Darwin collected in Puerto San Juli
an, southern Patagonia Argentina, the first fossil remains of Macrauchenia patachonica (Paula-Couto, 1979). After its initial identification, this macraucheniid was also recorded in Paraguay, Peru, Chile, Brazil, Bolivia and Uruguay, as well as in several other locations in Argentina (Ochsenius, 1979; Bond, 1999; Scherer et al., 2009). A few decades ago, a new macraucheniid genus and species were recognized from the South American Pleistocene, Xenorhinotherium bahiense Cartelle and Lessa, 1988. Both X. bahiense and M. patachonica have similar size, although their morphological differences rely on rostral anatomy, and on the

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K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

robustness of vertebrae and appendicular skeleton (Lessa, 1992; Silva, 2008). After this classification, all the records from the
rin northeastern region of Brazil were assigned to X. bahiense. Gue and Faure (2004) described 50 specimens of macraucheniids (dental and post-cranial elements) from Piauí and concluded that X. bahiense might be a junior synonym of M. patachonica. However,
rin and this taxonomic proposition was not widely accepted, as Gue Faure (2004) did not compare Piauí specimens with the type materials described by Cartelle and Lessa, 1988 (Scherer et al., 2009). However, these taxa did not overlap their records, resulting in disjunct geographic distributions (Scherer et al., 2009). As ecological competition is expected between closely related taxa sharing the same habitat, the extinction of one of these taxa could have been caused by competition (Begon et al., 2007). Essentially, species diverge due to ecological competition. However, our primary hypothesis is that the disjunct distributions of Macrauchenia patachonica and Xenorhinotherium bahiense prevented their ecological competition and, possibly, the extinction of one of these species, leading them to pursue different diets and to occupy distinct environments. This study aimed to identify the ecological niches of Macrauchenia patachonica and Xenorhinotherium bahiense and to infer the dietary patterns of these species by analyzing the enamel microwear (EM) and the occlusal enamel index (OEI). We also estimated the potential distributions of these species during the Last Glacial Maximum and the Middle Holocene using species distribution modeling (SDM). We discuss the paleobiology of these species and the possible causes of their extinction at the late Pleistocene/Holocene boundary. Tooth EM analysis involves the qualitative and quantitative identification of scars made by food items and exogenous grit on the occlusal surface of tooth enamel during mastication. EM is used to identify or infer the dietary habits of herbivore mammals, such as the consumption of fruits, tree barks, leaves, branches and grasses (Grine, 1986; Solounias and Semprebon, 2002; Rotti et al., 2018). Solounias and Semprebon (2002) developed this method using a low-magnification technique that allowed the direct quantification of the scars on epoxy casts through a stereomicroscope (with 35x magnification). The microwear scars on a piece of enamel were made during the mastication of the animal’s last meals and provide a record of its dietary patterns (Solounias and Semprebon, 2002). Various refractive properties and scars morphology define different types of scars, including scratches, gouges and pits. Scratches are elongated marks, with continuous and parallel margins, and can be fine (thin, shallow scratches with a high refraction) or coarse (wide, deep and less refractive). The tooth enamel may also exhibit crossscratches, which are scratches that are oriented approximately perpendicular to the main scratches. Pits are circular scars and can be small (relatively shallow and highly refractive/bright) or large (broader and deeper than the small pits and less refractive/dark). The largest and deepest perforations are the gouges, which have irregular borders (Solounias and Semprebon, 2002; Rotti et al., 2018). The OEI, developed by Famoso et al. (2013), quantifies the occlusal enamel surface complexity of herbivorous mammals, a factor that is related to their feeding habits, and allows for paleoecological inferences (Famoso and Davis, 2014, 2016; Famoso et al., 2016). Since the OEI is an index, it results in a dimensionless unit that decreases the isometric effects of the animal’s body size, providing a more accurate interpretation of the data. The analysis of stable isotopes in fossil specimens is an excellent tool to understand the dietary habits of extinct megamammals, as this procedure does not rely on tooth morphology and indirectly reflects the animal’s feeding ecology. This analysis is related to an

herbivore’s d13C values, which are obtained from ingested plants. These d13C values are related to the ingested plants’ photosynthetic pathways and environmental factors, such as humidity and vegetation density (MacFadden et al., 1999; Scherler et al., 2014). In large herbivorous mammals, the d13C is retained in the tissues and is indicated by a specific isotopic shift of 14.1 ± 0.5 (Cerling and Harris, 1999; MacFadden et al., 1999). In previous studies, this value was frequently applied to herbivorous mammals, regardless of their body size, phylogenetic affinities or primary diet source (Passey et al., 2005). However, a recent study argued that an animal’s body mass affects the interpretation of the isotopic data (TejadaLara et al., 2018). The estimated d13C values for exclusive C3 feeders vary depending on their habitats (dense forest,
22‰ to
16‰; forest,
16‰ to
11‰; and bushy to arid grasslands,
11‰ to
8‰). For C4 feeders, the estimated d13C values are
3‰ to þ5‰. Values between
8‰ and
3‰ represent mixed C3 and C4 feeders (Domingo et al., 2012). SDM is a useful tool for evaluating potential species distribution and ecological niches (Gregorini et al., 2007; Costa et al., 2012; Feng et al., 2017). SDM preferably uses data of presence (species record by localities), since absence data is generally limited and suspect (especially for extinct species due to a fossil record bias, Amaro and Morais, 2013). SDM generates a map of suitability, i.e., the potential distribution of an extinct species, by indicating the geographic areas with more favorable conditions for their occurrence and acknowledging their ecological requirements based on previous records (Silva Lopes et al., 2007; Coelho et al., 2016; Varela et al., 2017). 2. Materials and methods The specimens used in the EM and OEI analyses are housed at the fossil mammal collections of Museo de La Plata (MLP) and Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” (MACN), in Buenos Aires Province, Argentina; of Museu Nacional (MN)1 and Companhia de Pesquisa e Recursos Minerais, CPRM ^ncias (MCT), in Rio de Janeiro state, Brazil; and at the Museu de Cie
lica de Minas Gerais (MCL), Naturais da Pontifícia Universidade Cato in Minas Gerais state, Brazil. 2.1. Analysis of enamel microwear (EM) We analyzed only upper second molars (M2) in an intermediate wear level to avoid age mixed samples including very young or senile individuals (since they do not preserve all the microwear scars). In this way, 13 M2 of M. patachonica and 8 M2 of X. bahiense were suitable for microwear analysis. The steps of cleaning, molding and production and examination of casts followed the methods of Solounias and Semprebon (2002). The identification and quantification of the microwear patterns were performed on a 0.16 mm2 area of the paracone second band (Fig. 1) with a stereomicroscope with 35X magnification. We also calculated the percentage of individuals with low scratch values (0e17%), distinguishing traditional browsers and grazers by the number of scratches. The higher the consumption of abrasive grasses, the lower the percentage of scratches with values between 0 and 17 (Semprebon and Rivals, 2007; Semprebon et al., 2015). The scar counting was performed three times on each tooth analyzed, and the values were averaged for each scar type (total of

1 Currently, these specimens are lost or destroyed due to the fire incident that occurred in September 2018, at the Museu Nacional - UFRJ main building and fossil collections (after specimen analysis).

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

Fig. 1. Occlusal view of the upper molars (M3-M2-M1) of Macrauchenia patachonica (MACN 11361), with highlights on the M2 occlusal structures, where: 1-paracone, 2metacone, 3-hypocone, 4-protocone, a-disto-lingual fosset, b-medial fosset, c-mesiobuccal fosset, d-mesio-lingual fosset. Based on Lobo et al. (2015). Schematic drawing by
sar Ferreira Junior. Scale bar: 1 cm. Júlio Ce

the values/3), to avoid bias and misidentification of the marks. All the microwear analysis was performed by a single observer (KO) to avoid inter-observer error. 2.2. Occlusal enamel index (OEI) The analysis of the tooth occlusal surface complexity was conducted using the Occlusal Enamel Index (OEI ¼ OEL/√occlusal total area) (Famoso et al., 2013). In total, 58 upper molars of macraucheniids, in loci and isolated, were analyzed (28 of Macrauchenia patachonica and 30 of Xenorhinotherium bahiense). This analysis was conducted using scaled photographs of the occlusal surface, which were taken using a Nikon D60 camera, and edited and measured on the free software ImageJ 1.5 (available at https:// imagej.nih.gov/ij/). Each tooth had its total occlusal area and OEL measurements applied to the OEI formula, obtaining the index values for the sampled macraucheniids.

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collections mentioned above. These maps are generated using the maximum entropy algorithm -MaxEnt v.3.3.3k (Phillips et al., 2006). This software has better performance than other modeling methods, such as BIOCLIM, Garp and GLM, besides being highly efficient with small samplings (Amaro and Morais, 2013). It uses an algorithm that estimates species’ distributions through the maximum entropy probability, i.e., as close as possible to the uniform distribution, searching for the statistical model that infers the highest possible precision to the observed data (Varela et al., 2017). In this study, 10,000 background points were used and 25% of the points from the original presence data set were randomly selected to test predictions and evaluate model performance. Besides these, five replicas were also used to generate the final model. The value threshold used was Maximum training sensitivity plus specificity and ROC - AUC statistical methods to evaluate Maxent performance and model validation, cross-validation was used. The environmental variables for Last Glacial Maximum (LGM model, about 22 ka) and Middle Holocene (HM projection, 6 ka) were used, examining the changes in these macraucheniids’ potential distributions during the Pleistocene/Holocene transition, a period of significant climatic-environmental changes and extinction of megafauna all over the world. Bioclimatic variable layers are obtained from the Worldclim Project platform version 1.4 (Hijmans et al., 2005), where 19 variables are provided in various circulation models, known as Global Climate Models (GCM’s). Pearson’s correlation was used to verify the multicollinearity between the climatic data and to choose the ones with the lowest correlation, since the variables come from temperature and precipitation only, generating a high degree of correlation between the bioclimatic layers, the environmental variables selected for both species were as follows: isothermality (bio3), the average temperature during the hottest trimester (bio10), annual precipitation (bio12) and precipitation during the hottest trimester (bio18). The AUC value, related to the model sensitivity, ranges from 0 to 1, with AUC <0.5 (model is random and unreliable), AUC between 0.5 and 0.7 (acceptable model), and AUC> 0.7 (excellent model; Lobo et al., 2008). 3. Results and discussion

2.3. Calibration of d13C values

3.1. Recognition of dietary patterns

We reviewed the isotope values from the literature for both macraucheniids following the study of Tejada-Lara et al. (2018). Those authors tested if a single enrichment pattern is valid for all herbivorous mammals, and they demonstrated that body mass and d13C enrichment are highly correlated in these animals. The correlation becomes higher, according to the different types of herbivore digestive systems. Thus, some equations were suggested to calibrate these enrichment differences. Previous studies were used to estimate body mass of South American Quaternary macraucheniids, indicating that these species would weigh approximately one ~ a et al., 1998; Farin ~ a et al., 2005; França et al., 2015). At ton (Farin first, the calibration equation indicated for all mammals (e* ¼ 2.4 þ 0.034 (BM)), where BM is body mass in kg, was used for the macraucheniids, not considering their type of digestive system, since they belong to an extinct mammalian lineage and their digestive apparatus are not known.

The EM analysis of M. patachonica and X. bahiense identified all known enamel microscars, such as fine scratches (Fs), cross scratches (Cs), coarse scratches (CoS), small pits (Sp), large pits (Lp) and gouges (G). The absolute values are present in Tables 1 and 2 (Fig. 2). The specimens of M. patachonica showed scratch values of 23.7 ± 5.1 and pit values of 16.3 ± 9.7, in which the first is more homogeneous than the later (Table 1; Fig. 3). Xenorhinotherium bahiense showed values for scratches of s 26 ± 5.9 and 19.7 ± 6.1 for pits, with similar values for both microscopic scars(Table 2; Fig. 3), which positioned this macraucheniid in the ecospace of traditional grazers. Scratches values suggest that X. bahiense, as well as M. patachonica, would also have been a grazer. Additionally, the presence of pits indicates some ingestion of abrasive particles or “dirt” attached to the food. Three broad dietary habits for herbivorous mammals are recognized: grazers, browsers, and mixed feeders (e.g., Hofmann, 1989; Solounias and Semprebon, 2002). The browsers include in their diet both woody and soft portions of dicots; the grazers ingest exclusive or mostly, monocotyledonous (grasses); and the mixed feeders consume elements from both grazing and browsing habits (Ramdarshan et al., 2016). Comparisons with extant and extinct herbivorous mammals

2.4. Species distribution modeling (SDM) The geographic distribution of Macrauchenia patachonica and Xenorhinotherium bahiense were reviewed based on published literature and data from Paleobiology Database (https://paleobiodb. org/), in addition to museum records from visiting paleontological

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Fig. 2. Enamel microscars found in the Macrauchenia patachonica and Xenorhinotherium bahiense microwear analysis: 1 - large pits, 2 - small pits, 3 - coarse scratches, 4 - fine scratches. Scale bar: 1 mm.

Table 1 Absolute number of scars found in specimens of Macrauchenia patachonica: Fine scratches (Fs), coarse scratches (Cs), cross scratches (CoS), small pits (Sp), large pits (Lp) and gouges (G).

Table 2 Absolute number of scars found in specimens of Xenorhinotherium bahiense: Fine scratches (Fs), coarse scratches (Cs), cross scratches (CoS), small pits (Sp), large pits (Lp) and gouges (G).

ID

Fs

Cs

CoS

Sp

Lp

G

ID

Fs

Cs

CoS

Sp

Lp

G

MACN 14857 MLP 5167 MACN 0002 MLP 121428 MACN 18191 MLP 121425 MLP 122465 MACN 11361 MACN 2384 MLP 1214271 MLP 1214272 MACN 10051 MACN 2381

24 16 18 15 24 19 27 21 27 17 20 22 24

0 5 0 1 0 3 0 6 0 3 2 1 4

0 3 2 2 4 1 0 0 1 1 0 0 2

5 2 3 8 15 6 17 15 21 17 23 31 15

0 0 4 4 0 1 2 0 0 4 13 3 2

4 1 0 0 0 0 2 0 0 0 3 0 0

MN 4.167-V MN 4.168-V MN 3624- V MCT 4094-M MCL 3696 MCL 3601 MCL 3572 MCL 3650

31 28 26 26 23 16 26 18

6 1 0 9 1 0 0 0

0 0 0 2 3 0 5 1

21 19 17 29 30 11 13 15

0 0 0 0 3 2 0 1

3 1 0 0 1 0 1 0

Fig. 3. Bivariate plot of the average numbers of pits and scratches for M. patachonica (red star) and X. bahiense (yellow star). Error bars correspond to the standard deviation of the mean for the fossil samples. Based on Solounias and Semprebon, 2002: dark gray ¼ browser ecospace, and light gray ¼ grazer ecospace.

(Solounias and Semprebon, 2002) allow positioning M. patachonica in the traditional grazer ecospace, due to the high number of scratches. These data and the individual scratch values suggest that M. patachonica was a grazer, with high/exclusive ingestion of grasses. However, the presence of pits and fine scratches may also indicate the significant ingestion of “dirt” particles together with food items, since grazers feed close to the soil, and eventually ingest sedimentary particles (Jardine et al., 2012). The percentage of M. patachonica individuals with low scratch values (0e17) is 7.6%, while for X. bahiense, it is 12.5%, an expected pattern for traditional grazers that consume grasses (Rivals and Semprebon, 2011; Semprebon et al., 2015, Fig. 4). Famoso et al. (2013, 2016) recognized differences in the OEI values of artiodactyls and perissodactyls, and these may be related to the different digestive strategies between the ruminants (artiodactyls) and cecum fermenters (perissodactyls). The lower OEI values of the artiodactyls may be associated with reduced oral processing of food, as they invest in a higher chewing frequency (ruminants). On the other hand, the higher OEI values of perissodactyls may be related to comparatively higher oral processing of food, since they chew the food only once, later fermented at the posterior part of the digestion tract by the symbiotic microorganisms that live at the intestinal cecum. The OEI analysis resulted in average values of 5.30 and 5.40 and median values of 5.51 and 5.39 (Table 3) for M. patachonica and X. bahiense, respectively. Thus, the results show that the molar complexity of these two species are quite similar, both being able to eat abrasive foods. Thus, we compared the OEI values of macraucheniids from this

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

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Fig. 5. Occlusal Enamel Index values for Macrauchenia patachonica, Xenorhinotherium bahiense (this study), Perissodactyla, and Artiodactyls (from Famoso et al., 2016).Black band: median; whiskers: maximum and minimum variability and white circles: outliers. Fig. 4. Percentage of individuals with scratch values (0e17) of M. patachonica (red star) and X. bahiense (yellow star). Diagram based on and modified from Semprebon et al. (2015), where black boxes represent results for living ungulates.

study with those presented by Famoso et al. (2016) for ungulates (Artiodactyla and Perissodactyla). Nevertheless, they are represented by a limited diversity of ungulates, including only the Equinae from Middle Miocene to Recent (Perissodactyla), and modern ruminants and Lamini (Artiodactyla), all feeding on abrasive food, predominantly grasses. We recognized here that the OEI might help to infer the efficiency of oral processing, in addition to the complexity of enamel on the occlusal surface. The Equinae from Famoso et al. (2016) showed the highest OEI values (Fig. 5) among the sample, and selection probably favored a more efficient strategy of oral processing, which occurs in a single step in Equinae. On the contrary, the ruminants and the Lamini frequently alternate between the oral (mastication) and chemical processing of food in the stomach, which improves the digestion without further mastication. Thus, even having a diet as abrasive as the Perissodactyla, the

oral processing of ruminants and Lamini does not require a high complexity of occlusal enamel (Fig. 5). In this way, we inferred that macraucheniids may have an accessory digestive apparatus for fermentation, such as the Artiodactyla. This feature is not exclusive to Artiodactyla among the mammals; kangaroos, sloths and some rodents also have digestive systems with an accessory apparatus for fermentation (Pough et al., 2012). Previous isotopic analyses suggested a mixed diet based on C3/ C4 plants with a higher frequency of C3 for these macraucheniids. Studies of M. patachonica specimens from the southern Brazil and Pampean regions indicate a mixed diet, based on C3 and C4 plants in open environments, despite the difference of d13C values found which have an average of
12.16‰ (Domingo et al., 2012; França et al., 2015; Bocherens et al., 2016). Omena (2015) found for X. bahiense higher d13C values (±
12.31‰), suggesting that it would exclusively consume C3 plants. However, when these values are calibrated following Tejada-Lara et al. (2018), the average values of d13C for M. patachonica and X. bahiense shifts to
10.36‰

Table 3 Absolute values of the Occlusal Enamel Complexity Index (OEI) for Macrauchenia patachonica e Xenorhinotherium bahiense. TA: Total Area. M. patachonica M1 M1 M1 M1 M1 M1 M1 M1 M1 M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M3 M3 M3 M3 M3 M3 M3 M3 M3

e e e e e e e e e e e e e e e e e e e e e e e e e e e e

MACN 11361 MACN 18137 MACN 2372 MACN 581 MLP 121427 MLP 121427 MLP 211425 MLP 211425 MLP 2565 MACN 11361 MACN 14857 MACN 18137 MACN 2384 MACN 5167 MLP 121425 MLP 121427 MLP 121427 MLP 1425 MLP 2565 MACN 10051 MACN 11361 MACN 18137 MLP 121425 MLP 121427 MLP 121427 MLP 121427 MLP 1425 MLP 2565

OEL

TA

OEI

X. bahiense

OEL

TA

OEI

20,677 20,799 20,739 18,509 16,535 14,272 13,896 13,896 13,172 24,839 18,439 21,791 22,475 20,249 21,339 17,887 15,977 20,793 22,824 20,941 15,882 18,055 17,343 12,73 13,079 12,73 17,683 21,439

12,487 12,897 13,954 11,148 10,26 8794 8,61 8,61 11,152 14,729 9106 14,255 13,584 12,761 12,639 10,622 9776 12,745 13,833 13,098 10,065 11,013 10,741 8499 8742 8499 10,765 13,418

5,85 5,79 5,55 5,54 5,16 4,81 4,73 4,73 3,94 6,47 6,11 5,77 6,09 5,66 6 5,48 5,1 5,82 6,13 5,78 5 5,44 5,29 4,36 4,42 4,36 5,38 5,85

M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M1 M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M2 M3 M3 M3

26,753 25,584 24,252 24,59 19,707 21,874 21,814 19,041 20,483 20,195 21,355 24,514 19,614 16,196 17,422 17,88 20,53 17,47 29,528 21,272 22,331 29,532 20,753 21,659 23,513 23,157 16,422 20,351 25,482

17,803 17,297 15,531 17,138 12,859 15,104 11,962 11,549 12,670 12,698 13,719 15,046 12,998 11,062 11,052 10,3 14,17 10,984 19,273 15,507 14,875 19,456 13,850 13,994 15,813 12,936 9446 14,723 15,998

6,34 6,15 6,15 5,93 5,49 5,62 6,3 5,6 5,75 5,66 5,76 6,31 5,44 4,86 5,24 5,57 5,45 5,27 6,72 5,4 5,79 6,69 5,57 5,78 5,91 6,43 5,34 5,3 6,37

-

MCL 2644 - 01 MCL 3458 MCL 3459 MCL 3551 MCL 3575 MCL 3600 MCL 3603 MCL 3622 MCL 3649 MCL 3656 MCL 3658 MCL 3660 MCL 3693 MCL 3732 MCL 3823 MN 1467 - V MN 1477 - V MN 4170 - V MCL 2644 - 01 MCL 3454 MCL 3457 MCL 3548 MCL 3572 MCL 3650 MCL 3670 MCL 3598 MN 4168 - V MCL 2644 - 01 MCL 3454

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and
10.51‰, respectively. These results would indicate consumption of C3 plants from forested to arid grasslands (according to Domingo et al., 2012). However, as previously argued here, the macraucheniids M. patachonica and X. bahiense possibly have an accessory digestive apparatus, maybe similar to that of ruminants, but it seems likely they possessed a digestive tract that invested less in oral processing. Thus, when the isotope results are calibrated with the ruminant equation, the new enrichment values for M. patachonica and X. bahiense are
10.96‰ and
11.11‰, respectively, which also indicate the consumption of C3 plants (Domingo et al., 2012). Thus, the recognition of the diet of M. patachonica and X. bahiense through EM, OEI and isotope values, suggested that they were grazers, with high consumption of C3 grasses. Although the ~ a (2015) suggest that morphofunctional study by Varela and Farin M. patachonica would be an open-habitat browser (probably a broad aspect of the expected ecological niche for this species), the difference from our interpretation can be explained by the use of distinct methods. While the broad morphological analyses reflect dietary adaptations of a lineage, being more an evolutionary proxy in terms of diet, microwear and isotopic analyses indicate an immediate diet of the individuals or populations, i.e., their feeding habits. Several studies indicate that that areas of occurrence of M. patachonica and X. bahiense were areas of open grasslands (Ray and Adams, 2001; Vivo and Carmignotto, 2004; Wainer et al., 2005; Arruda et al., 2017). Furthermore, Bocherens et al. (2016, 2017) analyzed the isotopic paleoecology of Pleistocene Pampean region mammals and recognized that they exhibited high values of d13C, ranging from
21.6‰ to
17‰, with M. patachonica showing the highest values (
17‰ and
17.1‰) among the herbivores. In their interpretation (Bocherens et al., 2016, 2017), these values indicate the consumption of C3 plants, and even some C4 plants, and they assume that M. patachonica would live in open environments. Therefore, as M. patachonica and X. bahiense are sister-taxa (Forasiepi et al., 2016) and both had remarkably similar diets, they should avoid ecological competition, so it is expected to them to diverge in some other aspect of their ecological niches. 3.2. Species distribution modeling According to the review of the geographic distribution of South American Quaternary macraucheniids, Macrauchenia patachonica occurred in Uruguay, Argentina, Bolivia, Chile, Peru, Paraguay, and Southern Brazil, while Xenorhinotherium bahiense occurred in the Northeast and Southeast of Brazil and Venezuela (see Fig. 6; Table 4). The results of SDM showed distinct suitabilities for M. patachonica and X. bahiense during the LGM and the HM. Here we intended to define both macraucheniid areas of occurrence (environment niche) and how they respond to the climate change during the Pleistocene/Holocene, having the suitability map for the HM as a projection. Our interpretations are based mainly on areas with occurrences recorded for each species and areas with great suitability, understanding that even with having suitable environmental conditions, some regions still do not have a record of either species. The average AUC test for the replicate runs for Macrauchenia patachonica during the LGM is 0.804, and 0.826 during the HM. For Xenorhinotherium bahiense during LGM the mean AUC is 0.882 and for HM is 0.882. 3.2.1. Last Glacial Maximum (LGM) The LGM was the period when the largest ice cap was present on Earth, and the Amazon, Atlantic Rainforest and other humid forests

may have been drastically reduced, and vast deserts and semidesert areas all were present over South America, mainly in southern regions (Ray and Adams, 2001). Also, South America would have had colder and drier climate/environmental conditions than in the present day; with higher aridity, the decrease in temperature during the LGM could have been from 6 to 7  C or higher, while in other areas it could have been around 3  C, with a noticeable temperature gradient (van der Hammen, 1974). During the LGM, most of the M. patachonica populations would have been better suited to areas in southern Brazil and Patagonia, however Andean areas of Chile, Bolivia, Peru and Ecuador would have also been suitable (Fig. 7a). Behling (2002) indicates that the climate in southern Brazil was markedly drier and about 5e7  C colder during the LGM. Brady et al. (2013) found that the Pampean region and Patagonia would also have had colder conditions with a large thermal amplitude varying seasonally from
10 to 20  C, in addition to a well-marked dry season, when precipitation could reach values close to 0 mm. Hulton et al. (1994) argued that the average annual temperature in Patagonia during the LGM would have been about 3  C colder than the present. Heine (2000) also indicated higher aridity with marked reduction of precipitation for the suitable Andean regions during LGM; an average annual temperature of about 5.6  C colder than the present days. Stevaux (2000) recognized a “first dry episode” for the south-central region of Brazil and northeast of Argentina that would also be related to the LGM. Ray and Adams (2001) indicate that these areas would be composed mainly of temperate deserts and semi-deserts, mainly formed by low vegetation with grassland physiognomy in plains and slightly undulating topographies (Roche et al., 2007). Behling (2002) indicated that grasslands dominated the landscape based on pollen records from the southern region of Brazil, and would extend for 750 km from Southern to Southeast Brazil. Grasslands were also proposed to dominate Bolivian regions with low diversity of woody plants (Behling and Hooghiemstra, 1999). Additionally, Xenorhinotherium bahiense had suitable habitat mainly in areas at the Brazilian Intertropical Region (BIR) and Venezuela during the LGM, but also to a few areas in Colombia and Peru (Fig. 7b). Bush et al. (2001) suggests that the regions suitable to X. bahiense would have had a period of aridity since cooler surface temperatures of the ocean and continent would have reduced evaporation and, consequently, cloud development. Despite the colder temperatures than present days, the BIR could reach almost 30  C at specific periods of the year, and also had a low thermal amplitude and suffered fewer variations when compared to other regions of Brazil (Brady et al., 2013; Arruda et al., 2017). Stute et al. (1995) indicates that the Northeast region cooled about 5.4  C, compared to present days. Arruda et al. (2017) argues that there was a significant precipitation decrease in the northeast region of Brazil. In Venezuela, Colombia and Peru, an average temperature of 5.4 e 6  C lower than the present is estimated, according to Stute et al. (1995) and Heine (2000). Regarding the suitable areas for X. bahiense, two well-defined periods for precipitation are considered: a rainy season that could reach 500 mm and a period of drought (Ray and Adams, 2001; Brady et al., 2013). These vegetation areas were tropical plains and semi-deserts, consisting of low vegetation, small trees, and other woody plants (Ray and Adams, 2001). For the BIR, Arruda et al. (2017) indicates a vegetation gradient composed of areas of Caatingas, deciduous, semi-deciduous and Brazilian savanna (Cerrado) areas that would be characterized by scenarios ranging from dense grasses to shrub-forest species, where the dry period could last more than eight months. Werneck et al. (2012) also indicated that in the Cerrado, several types of vegetation could occur closely, under the same climate, but differ widely in

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

7

Fig. 6. Reviewed occurrence map of Macrauchenia patachonica (red stars) and Xenorhinotherium bahiense (yellow circles) based on reviewed information from the literature. See Table 4 for locations.

floristic and structural composition. The records for the Colombian region suggest a landscape dominated by grasslands (Behling and Hooghiemstra, 1999). Hence, M. patachonica most likely lived in colder environments with greater thermal amplitude and aridity, with typical pasture vegetation with few woody plants. Whereas X. bahiense most likely lived in arid and warmer environments, although still colder than present days conditions. Precipitation had two well-defined periods, and the vegetation most likely consisted of a gradient of open areas, woody plants and forests.

3.2.2. Middle Holocene (HM) When projected to the HM, the potential distribution of these two species remain separated, although both show a decrease in suitable habitat, which could be explained by environmental

changes in the Pleistocene/Holocene transition and the reduction in the continental area of South America. Iglesias et al. (2011) recognized significant seasonality and humidity for South America, also including periods of drought in open areas. Macrauchenia patachonica was more restricted to areas of southern Brazil and Patagonia during the HM (Fig. 8a). The southern region of Brazil would have had warmer and drier climate conditions since it had no increase in precipitation (Arruda et al., 2017). Moro et al. (2004) indicated that a humid climate marked the early Holocene, followed by a long cold and dry period, starting around 8.7 ka, and subsequently by humid periods. Behling et al. (2001) also suggested a drier period for the southern region during the HM, with a predominance of grasslands and small Araucaria forest. Markgraf et al. (2003) indicated that around 6 ka, the Antarctic cold fronts brought moisture to southern

8

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Table 4 Locations with presence of Macrauchenia patachonica e Xenorhinotherium bahiensea. Nº

Specie

Locality

Coordinates

Reference

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense X. bahiense M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica M. patachonica

Taima Taima - VE Jirau - BR Lajedo da Escada - BR Lajedo de Soledade - BR Lagoa de Dentro - BR ~s/Campo Alegre - BR Sítio Curimata
- BR Taperoa Lage Grande BR Fazenda Ovo da Ema - BR Fazenda Paraíso do Talhado - BR Fazenda Elefante - BR Toca dos Ossos - BR Sítio Novo - BR
Aguas de Arax
a - BR Quebrada de Cachimayu - PE Kamac Mayu- CL Tarija Valley - BO Jujuy - AR Riacho Negro - PY Formosa - AR Touro Passo - BR Sanga da Cruz - BR Formaç~ ao Sopas - UY Formaç~ ao El Pamar - AR
- AR Santa Fe San Luis - AR ~ La Quebrada de Nuapua - BO Hermenegildo Beach - BR Lujan - AR La Paz/Casil Quarry - UY Camet Norte - AR Paso Otero - AR
n Salado - AR Queque
Grande - BR Arroyo Naposta Playa del Barco - AR Monte Hermoso - BR Puerto San Julian - AR Ultima Esperanza - CL

66.879745,10.163583
39.705971,-3.356789
37.617287,-5.080387
37.831734,-5.589280
35.363379,-6.669846
36.130436,-7.127180
36.050330,-7.183739
36.722559,-8.424581
37.504511,-9.313476
37.900376,-9.502921
37.093675,-10.011259
41.057044,-10.931539
42.8498419,-13.909890
46.941277,-19.593247
13.454722,-71.473889
22.441667,-68.911111
21.510000,-64.725556
24.181667,-65.299722
25.344722,-57.597222
26.181944,-58.176111
29.785000,-57.060833
29.568889,-55.709167
30.404167,-56.480833
31.416389,-58.033333
31.605556,-60.697222
33.297222,-66.337778
20.758333,-63.072500
33.518889,-53.369444
34.554167,-57.125000
34.746111,-56.233889
37.825000,-57.490278
38.207500,-59.107500
38.748333,-60.603333
38.5333,-62.0833
39.002500,-61.581111
38.985833,-61.287500
49.297222,-67.732500
50.820278,-73.467222

Socorro, 2006 Araújo-Junior, 2015 Barbosa, 2013 Porpino et al., 2004 Kinoshita et al., 2005 Araújo-Junior, 2015 Bergqvist et al., 1997 Araújo-Júnior et al., 2013 Silva, 2008 Lima and Silva, 2016 França et al., 2015 Lobo et al., 2015 Lobo et al., 2015 Melo et al., 2005 Scherer et al., 2009 Cartajena et al., 2010 Tonni et al., 2009 Scherer et al., 2009 Scherer et al., 2009 Scherer et al., 2009 Scherer et al., 2009 Kerber and Oliveira, 2008 Ubilla, 2004 Ferrero et al., 2007 Scherer et al., 2009 Scherer et al., 2009 Scherer et al., 2009 Scherer et al., 2009 Tonni et al., 1985 Corona et al., 2012/Alvarenga et al., 2010 Bocherens et al., 2016 Tonni et al., 1985 Tonni et al., 1985 Deschamps and Tonni, 1992* Tomassini et al, 2010 Aramayo et al., 2005 Scherer et al., 2009 Villavivencio et al., 2016

a Localities with presence of M. patachonica and X. bahiense in South America, according with the literature used in this study. References with * are from Paleobiology Database.

Patagonia, and after this period, there was a change in humidity patterns, being more or less seasonally variable. For Glasser et al. (2004) the period of 6e3.6 ka would also have been colder and more humid than the present. Around 6 ka, southern Brazil, Uruguay, and NE Argentina would have been slightly more humid and colder, especially in summer (Silva Dias et al., 2009). The Province of Buenos Aires presented climatic fluctuations between arid and cold, and warm and humid intervals in the period of 9e3 ka. Temperature and humidity would have reached their maximum peaks in this region during the HM, which would be associated with grasses revealing more temperate or locally humid conditions (Quattrocchio et al., 2008). Part of the BIR and Venezuela continued to be X. bahiense suitable areas during the HM (Fig. 8b), though the suitable area clearly decreases in Venezuela. The BIR would have had an increase in temperature and decrease of precipitation (Arruda et al., 2017), although Pessenda et al. (2005) showed an intermediate situation in its southern region, starting with dry periods between 10e7 ka and becoming more humid after seven ka. Later, a humid transition occurred around 6 ka, and Cerrado expansion areas would have occurred (Werneck, 2011). Enters et al. (2009) also indicated open savanna vegetation (Cerrado) and gallery forests at approximately 6.9 ka at the BIR. Regarding Venezuela, a humid early Holocene is suggested (Leal et al., 2011), with decreasing humidity between 8e7 ka, corresponding to the “Middle Holocene drought,” which reached the Amazon Basin. Silva Dias et al. (2009) indicated a

landscape formed by dry forests and savannas for the region of Venezuela. Macrauchenia patachonica occupied environments with lower temperatures during the HM. Despite the general temperature increase in the Pleistocene/Holocene transition, these regions also had alternating higher humidity and dry periods, in a low vegetation scenario. Xenorhinotherium bahiense persisted in warmer areas, with denser vegetation, but still open lands, with high precipitation. South American megafauna went extinct during the Pleistocene/Holocene transition, but the causes for this evolutionary event are still poorly known. The most accepted/discussed hypotheses are related to climate/environmental changes that occurred after the LGM (around 21-18 ma, Koch and Barnoski, 2006; Roche et al., 2007). The SDM results suggest that Macrauchenia patachonica had environmental suitability for temperate areas with higher aridity and lower temperatures, while Xenorhinotherium bahiense had suitability for tropical semi-arid regions with comparable episodes of higher humidity and warmer temperatures. The principle of competitive exclusion, or the principle of Gause (1934), argues that when species in the same community explore very similar niches, a competition for resources is established (Giacomini, 2007). Thus, different environmental preferences may have been one of the pillars in niche differentiation necessary to avoid competition for resources between the two species, since diet reconstruction resulted in similar feeding habits. Due to their

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

Fig. 7. Suitability map during Last Glacial Maximum for A: Macrauchenia patachonica and B: Xenorhinotherium bahiense.

Fig. 8. Suitability map projection for Middle Holocene for A: Macrauchenia patachonica and B: Xenorhinotherium bahiense.

9

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K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178

specific environmental preferences, environmental changes during the late Pleistocene may have been significant factors in the extinction of Macrauchenia patachonica and Xenorhinotherium bahiense. Even though their known geographic distributions (based on fossil records) were disjunct, the reduction of the suitability areas from the LGM model to the HM projection is recognized for both macraucheniids. The increase in temperature and humidity or the change in vegetation caused by such climatic changes probably affected their niches, possibly leading them to extinction. 4. Conclusions We found that the Quaternary macraucheniids Macrauchenia patachonica and Xenorhinotherium bahiense had grazing dietary habits, which does not support the hypothesis that they had distinct geographical distributions mainly due to differences in their dietary patterns. Their occurrences suggest that their habitat preferences were distinct, which separated their geographic distributions, resulting in distinct ecological niches. Therefore, if climatic conditions were decisive for the imposition of distinct niches, and both species vanished simultaneously, it is possible that changes in climatic conditions and suitable environments were the main drivers of their negative selection during late Pleistocene/early Holocene. A synergy of climate change and human action is not ruled out, but this study supports that climate change was an important piece of the South American megafauna extinction “puzzle” in the Quaternary. Declaration of competing interest None. Acknowledgements The authors thank all curators of the collections who allowed access to the specimens studied here during 2017 and 2018: A. Kramarz (Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires), M.A. Reguero (Museo de La Plata, La ^ncias Naturais of PUC-MINAS, Minas Plata), C. Cartelle (Museu de Cie Gerais), U. Cabral (Museu Nacional/UFRJ, Rio de Janeiro) and R. da
gico do Brasil e CPRM, Rio de Janeiro). We also Silva (Serviço Geolo
sar Ferreira Junior (PPGBIO - UNIRIO) for the art of the thank Júlio Ce molars in Fig. 1, we also thank Dr. Nicholas A. Famoso for grammar review. This study was funded by Conselho Nacional de Desen
gico (CNPq) (DM process number volvimento Científico e Tecnolo ~o de PDJ 153536/2016e0, TA and AR PIBIC scholarships), Fundaça Amparo  a Pesquisa do Estado do Rio de Janeiro (FAPERJ) (DM process numbers 202.375/2018 and 202.376/2018, AR process number E-26/203.086/2019) and Coordenaç~ ao de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (KO process number 001). References Alvarenga, H., Jones, W., Rinderknecht, A., 2010. The youngest record of phorusrhacid birds (Aves, Phorusrhacidae) from the late Pleistocene of Uruguay. €ont. Abh. 256, 229e234. N. Jb. Geol. Pala ~o geogra
fica potential do a
caro Amaro, G.C., Morais, E. G. F. De, 2013. Distribuiça
rica do Sul. Boletim de Pesquisa e Desenvolvermelho-das-palmeiras na Ame vimento, Embrapa, pp. 5e29.
rrez, T., Schillizzi, R.A., 2005. Sedimentologic and paleontologic Aramayo, S.A., Gutie study of the southeast coast of Buenos Aires province, Argentina: a late PleistoceneeHolocene paleoenvironmental reconstruction. J. S. Am. Earth Sci. 20, 65e71. https://doi.org/10.1016/j.jsames.2005.05.002. ^ mico para vertebrados de depo
sitos de Araújo-Junior, H.I., 2015. Modelo tafono
s-graduaça ~o tanque do nordeste do Brasil. Tese de Doutorado. Programa de Po em Geologia. Universidade Federal do Rio de Janeiro, Rio de Janeiro, 208pp. Araújo-Júnior, H.I., Porpino, K.O., Ximenes, C.L., Bergqvist, L.P., 2013. Unveiling the

taphonomy of elusive natural tank deposits: a study case in the Pleistocene of northeastern Brazil. Palaeogeogr. Palaeoclimatol. Palaeoecol. 378, 52e74. https://doi.org/10.1016/j.palaeo.2013.04.001. Arruda, D.M., Schaefer, C.E.G.R., Fonseca, R.S., Solar, R.R.C., Fernandes-Filho, E.I., 2017. Vegetation cover of Brazil in the last 21 ka: new insights into the Amazonian refugia and Pleistocenic arc hypotheses. Global Ecol. Biogeogr. 1e10. https://doi.org/10.1111/geb.12646.
lise paleopatolo
gica em megafauna pleistoce ^nica do Barbosa, F.H.S., 2013. Ana Lajedo da Escada, Baraúna, Rio Grande do Norte, Brasil. Dissertaç~ ao de Mes
s-Graduaça ~o em Geocie ^ncias, Universidade Federal de trado. Programa de Po Pernambuco, Pernambuco, p. 99p. ~o Interespecifica. Ecologia Begon, M., Townsend, C.R., Harper, J.L., 2007. Competiça De individuos a ecossistemas. Artmed Editora S.A. Behling, H., 2002. South and southeast Brazilian grasslands during Late Quaternary times: a synthesis. Palaeogeogr. Palaeoclimatol. Palaeoecol. 177, 19e27. https:// doi.org/10.1016/s0031-0182(01)00349-2. Behling, H., Hooghiemstra, H., 1999. Environmental history of the Colombian savannas of the Llanos Orientales since the last glacial maximum from lake records el pinal and Carimagua. J. Paleolimnol. 21, 461e476. https://doi.org/ 10.1023/A:1008051720473. Behling, H., Bauermann, S.G., Neves, P.C.P., 2001. Holocene environmental changes in the S~ ao Francisco de Paula region, Southern Brazil. J. S. Am. Earth Sci. 14, 631e639. https://doi.org/10.1016/s0895-9811(01)00040-2. Bergqvist, L.P., Gomide, M., Cartelle, C., Capilla, R., 1997. Faunas-locais de mamíferos ^nicos de Itapipoca/Ceara
,Taperoa
/Paraíba e Campina Grande/Paraíba. pleistoce ^ mico e paleoambiental, 6. Revista da UniEstudo comparativo, biostratino ^ncias, pp. 23e32. versidade de Guarulhos, Geocie Bocherens, H., Cotte, M., Bonini, R., Scian, D., Straccia, P., Soibelzon, L., Prevosti, F.J., 2016. Paleobiology of sabretooth cat Smilodon populator in the pampean region (Buenos Aires province, Argentina) around the last glacial maximum: insights from carbon and nitrogen stable isotopes in bone collagen. Palaeogeogr. Palaeoclimatol. Palaeoecol. 449, 463e474. https://doi.org/10.1016/ j.palaeo.2016.02.017. Bocherens, H., Cotte, M., Bonini, R., Scian, D., Straccia, P., Soibelzon, L., Prevosti, F.J., 2017. Isotopic insight on paleodiet of extinct Pleistocene megafaunal Xenarthrans from Argentina. Gondwana Res. 48, 7e14. https://doi.org/10.1016/ j.gr.2017.04.003. Bond, M., 1999. Quatenary native ungulates of Southern South America. A synthesis. In: Rabassa, J., Salemme, M. (Eds.), Quaternary of South America and Antarctic Peninsula, A.A. Balkema Publishers, pp. 177e205. Brady, E.C., Otto-Bliesner, B., Kay, J.E., Rosenbloom, N., 2013. Sensitivity to glacial Forcing in the CCSM4. Commun. Clim. Syst. Model CCSM4 26, 1901e1925. Bush, M.B., Stute, M., Ledru, M.-P., Behling, H., Colinvaux, P.A., De Oliveira, P.E., Grimm, E.C., Hooghiemstra, H., Haberle, S., Leyden, B.W., Salgado-Labouriau, M.L., Webb, R., 2001. Paleotemperature Estimates for the Lowland Americas Between 30o S and 30o N at the Last Glacial Maximum. Interhemispheric Climate Linkages, 4a. Academic Press, pp. 293e304.
pez, P., Martínez, I., 2010. New camelid (Artiodactyla: Camelidae) Cartajena, I., Lo record from the late Pleistocene of Calama (Second Region, Chile): a morphological and morphometric discussion. Rev Mex Cienc Geol. 27, 197e212. ~o de um novo ge ^nero e espe
cie de MacrauCartelle, C., Lessa, G., 1988. Descriça cheniidae (Mammalia, Litopterna) do Pleistoceno do Brasil. Paula-Coutiana 3, 3e26. Cerling, T.E., Harris, J.M., 1999. Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347e363. https://doi.org/10.1007/ s004420050868. Coelho, G.L.N., Carvalho, L. M. T. de, Gomide, L.R., 2016. Modelagem preditiva de
cies pioneiras no Estado de Minas Gerais. Pesqui. Agrodistribuiç~ ao de espe
ria Bras. 51, 207e214. pecua ~ o, P., Goso, C., 2012. Taphonomy, sedimentology and Corona, A., Perea, D., Torin chronology of a fossiliferous outcrop from the continental Pleistocene of Uruguay. Rev. Mex. Ciencias Geol. 29, 514e525.
ticas e seus Costa, T.R.N., Carnaval, A.C.O.Q., Toledo, L.F., 2012. Mudanças clima impactos sobre os anfíbios brasileiros. Rev. Biol. 8, 33e37. Deschamps, C.M., Tonni, E.P., 1992. Los vertebrados del pleistoceno tardio del Arroyo
Grande, provincia de Buenos Aires: aspectos paleoambientais. AmeNaposta ghiniana 29, 201e221. Domingo, L., Prado, J.L., Alberdi, M.T., 2012. The effect of paleoecology and paleobiogeography on stable isotopes of Quaternary mammals from South America. Quat. Sci. Rev. 55, 103e113. https://doi.org/10.1016/j.quascirev.2012.08.017. Enters, D., Behling, H., Mayr, C., Dupont, L., Zolitschka, B., 2009. Holocene environmental dynamics of south-eastern Brazil recorded in laminated sediments of Lago Aleixo. J. Paleolimnol. 44, 265e277. https://doi.org/10.1007/s10933009-9402-z. Famoso, N.A., Davis, E.B., 2014. Occlusal enamel complexity in middle Miocene to Holocene equids (equidae: Perissodactyla) of North America. PloS One 9, e90184. https://doi.org/10.1371/journal.pone.0090184. Famoso, N.A., Davis, E.B., 2016. On the relationship between enamel band complexity and occlusal surface area in Equids (Mammalia, Perissodactyla). Peer J. 4, e2181 https://doi.org/10.7717/peerj.2181. Famoso, N.A., Feranec, R.S., Davis, E.B., 2013. Occlusal enamel complexity and its implications for lophodonty, hypsodonty, bodymass, and diet in extinct and extant ungulates. Palaeogeogr. Palaeoclimatol. Palaeoecol. 387, 211e216. https://doi.org/10.1016/j.palaeo.2013.07.006.

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178 Famoso, N.A., Davis, E.B., Feranec, R.S., Hopkins, S.S.B., Price, S.A., 2016. Are hypsodonty and occlusal enamel complexity evolutionarily correlated in ungulates? J. Mamm. Evol. 23, 43e47. https://doi.org/10.1007/s10914-015-9296-7. ~ a, R.A., Vizcaíno, S.F., Bargo, M.S., 1998. Body mass estimation in Lujanian (late Farin pleistocene-early Holocene of south America) mammal. Mastozool. Neotrop. 5, 87e108. ~ a, R.A., Blanco, R.E., Christiansen, P., 2005. Swerving as the escape strategy of Farin Macrauchenia patachonica Owen (Mammalia; Litopterna). Ameghiniana 42, 751e760. Feng, X., Castro, M.C., McBee, K., Papes, M., 2017. Hiding in a cool climatic niche in the tropics? An assessment of the ecological biogeography of Hairy Long-Nosed Armadillos (Dasypus pilosus). Trop. Conserv. Sci. Megafauna 10, 1e13. https:// doi.org/10.1177/1940082917697249. Ferrero, B., Brandoni, D., Noriega, J.I., Carlini, A.A., 2007. Mammals of the El Palmar Formation (Late Pleistocene) from Entre Ríos Province, Argentina, vol. 9. Revista del Museo Argentino de Ciencias Naturales, pp. 109e117.
, C., Forasiepi, A.M., MacPhee, R.D.E., Del Pino, S.H., Schmidt, G.I., Amson, E., Grohe 2016. Exceptional skull of Huayqueriana (Mammalia, Litopterna, Macraucheniidae) from the late Miocene of Argentina: anatomy, systematics, and paleobiological implications. Bull. Am. Mus. Nat. Hist. 404, 1e76. https://doi.org/ 10.1206/0003-0090-404.1.1. França, L.M., Asevedo, L., Dantas, M.A.T., Bocchiglieri, A., Avilla, L.S., Lopes, R.P., Silva, J.L.L., 2015. Review of feeding ecology data of Late Pleistocene mammalian herbivores from South America and discussions on niche differentiation. Earth Sci. Rev. 140, 158e165. https://doi.org/10.1016/j.earscirev.2014.10.006. Gause, G.F., 1934. The Struggle for Existence. Williams and Wilkins, Baltimore. ^ncia de espe
cies como vistos pela Giacomini, H.C., 2007. Os mecanismos de coexiste
gica. Oecologia Brasiliensis 11, 521e543. https://doi.org/10.4257/ teoria ecolo oeco.2007.1104.05. Glasser, N.F., Harrison, S., Winchester, V., Aniya, M., 2004. Late Pleistocene and Holocene palaeoclimate and glacier fluctuations in Patagonia. Global Planet. Change 43, 79e101. https://doi.org/10.1016/j.gloplacha.2004.03.002. ^ndido Jr., J.F., To ^rres, N.M., 2007. Modelagem de Gregorini, M.Z., Rodolfo, A.M., Ca ~o Geogra
fica do tamandua
-bandeira (Myrmecophaga tridactyla) e Distribuiça ^ncia em unidades de conservaça ~o no estado do Paran
sua ocorre a. Anais do VIII Congresso de Ecologia do Brasil. Grine, F.E., 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative analysis of permanent molar microwear. J. Hum. Evol. 15, 783e822. https://doi.org/10.1016/s0047-2484(86)80010-0.
rin, C., Faure, M., 2004. Macrauchenia patachonica Owen (Mammalia, LitopGue
gion de Sa ~o Raimundo Nonato (Piauí, Nordeste bre
silien) et la terna) de la re
des Macraucheniidae ple
istoce nes. Geobios 37, 516e535. https:// diversite doi.org/10.1016/j.geobios.2003.04.006. Heine, K., 2000. Tropical South America during the Last Glacial Maximum: evidence from glacial, periglacial and fluvial records. Quarten. Int. 72, 7e21. https:// doi.org/10.1016/S1040-6182(00)00017-3. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965e1978. https://doi.org/10.1002/joc.1276. Hofmann, R.R., 1989. Evolutionary steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive system. Oecologia 78, 443e457. Hulton, N., Sugden, D., Payne, A., Clapperton, C., 1994. Glacier modeling and the Cclimate of Patagonia during the last glacial maximum. Quat. Res. 42, 1e19. https://doi.org/10.1006/qres.1994.1049. Iglesias, V., Whitlock, C., Bianchi, M.M., Villarosa, G., Outes, V., 2011. Holocene climate variability and environmental history at the Patagonian forest/steppe ecotone. Lago Mosquito 1297e1307 (42 29’37.89’’S, 71 24’14.57’’W) and Laguna
ndor (42 20’47.22’’S, 7117’07.62’’W). The Holocene, 22. del Co Jardine, P.E., Janis, C.M., Sahney, S., Benton, M., 2012. Grit not grass: Concordant patterns of early origin of hypsodonty in Great Plains ungulates and Glires. Palaeogeogr. Palaeoclimatol. Palaeoecol. 365e366, 1e10. https://doi.org/ 10.1016/j.palaeo.2012.09.001.
sseis de Vertebrados para a Sanga da Cruz Kerber, L., Oliveira, E.V., 2008. Novos Fo ^ncias 35, (Pleistoceno Superior), Alegrete, RS, Brasil. Revista Pesquisas em Geocie 39e45. Kinoshita, A., Franca, A.M., Almeida, J. A. C. de, Figueiredo, A.M., Nicolucci, P., Graeff, C.F.O., Baffa, O., 2005. ESR dating at K and X band of northeastern Brazilian Megafauna. Appl. Radiat. Isot. 62, 225e229. https://doi.org/10.1016/ j.apradiso.2004.08.007. Koch, P.L., Barnoski, A.D., 2006. Late quaternary extinctions: state of the debate. Annu. Rev. Ecol. Evol. Syst. 37, 215e250. https://doi.org/10.1146/ annurev.ecolsys.34.011802.132415. Leal, A., Perez, T., Bilbao, B., 2011. Contribution to Early Holocene vegetation and climate history of Eastern Orinoco Llanos, Venezuela, from a paleoecological record of a Mauritia L.f. swamp. Acta Amazonica 41, 513e520. https://doi.org/ 10.1590/S0044-59672011000400009. Lessa, G., 1992. Estudo descritivo de Xenorhinotherium bahiense Cartelle e Lessa, ~o com outras espe
cies de Macraucheniidae (Litopterna, 1988 e comparaça Mammalia) Tese de Mestrado. Universidade Federal do Rio de Janeiro, Rio de Janeiro, p. 264.
sseis pleistoce ^nicos em tanque arenítico no Lima, J.S., Silva, J.L.L., 2016. Mamíferos fo
gicos 26, 77e90. município de Delmiro Gouveia, Alagoas, Brasil. Estudos Geolo https://doi.org/10.18190/1980-8208/estudosgeologicos.v26n2p77-90.
nez-Valverde, A., Real, R., 2008. AUC: a misleading measure of the Lobo, J.M., Jime

11

performance of predictive distribution models. Global Ecol. Biogeogr. 17, 145e151. Lobo, L.S., Scherer, C.S., Dantas, M.A.T., 2015. Megafauna do Pleistoceno final de
tica, cronologia e paleoecologia. Rev. Bras. PalMatina, Bahia, Brasil: sistema aontol. 18, 325e338. https://doi.org/10.4072/rbp.2015.2.11. MacFadden, B.J., Cerling, T.E., Harris, J.M., Prado, J.L., 1999. Ancient latitudinal gradients of C3/C4 grasses interpreted from stable isotopes of New World Pleistocene horse (Equus) teeth. Global Ecol. Biogeogr. 8, 137e149. https://doi.org/ 10.1046/j.1466-822X.1999.00127.x. Markgraf, V., Bradbury, J.P., Schwalb, A., Burns, S.J., Stern, C., Ariztegui, D., Gilli, A., Anselmetti, F.S., Stine, S., Maidana, N., 2003. Holocene palaeoclimates of southern Patagonia: Limnological and environmental history of Lago Cardiel, Argentina. Holocene 134, 581e591. https://doi.org/10.1191/ 0959683603hl648rp. ~o de mamíferos pleisMelo, D.J., Cassab, C. T. R. de, Passos, F. V. dos, 2005. Coleça
^nicos de Aguas
, no Museu de Cie ^ncias da Terra/DNPM-RJ. X toce de Araxa ~o Brasileira Estudos do Quatern
Congresso de Associaça ario (ABEQUA), p. 12. Moro, R.S., Bicudo, C.E.M., Melo, M.S., Schmitt, J., 2004. Paleoclimate of the late
state, southern Brazil. Quat. Pleistocene and Holocene at Lagoa Dourada, parana Int. 114, 87e99. https://doi.org/10.1016/S1040-6182(03)00044-2. Ochsenius, C., 1979. The Neotropical Biogeography of Owen’s Macrauchenia Genus and the Relative Effect of Amazonian Biota as Ecologic Barrier during Upper ~o Paulo, pp. 1e8. Quaternary. Instituto de Geografia Universidade de Sa ~o de iso
topos de C, O e N como ferramenta para avaliar a Omena, E.C., 2015. Utilizaça ^nicos do semia
rido dos estados de Aladieta e habitat de mamíferos Pleistoce goas e Pernambuco, nordeste do Brasil. Dissertaç~ ao de Mestrado, Universidade Federal de Pernambuco, Recife, p. 47p. Owen, R., 1838. Fossil Mammalia. In: Darwin, C.R. (Ed.), Zoology of the Vvoyage of H.M.S. Beagle, under the Command of Captain Fitzroy, during the Years 1832 to 1836, vol. 1. Smith Elder e Co., London, pp. 1e40. Passey, B.H., Robinson, T.F., Ayliffe, L.K., Cerling, T.E., Sponheimer, M., Dearing, M.D., Roeder, B.L., Ehleringer, J.R., 2005. Carbon isotope fractionation between diet, breath CO2, and bioapatite in different mammals. J. Archaeol. Sci. 32, 1459e1470. https://doi.org/10.1016/j.jas.2005.03.015. ^mia Paula-Couto, C. De, 1979. Tratado de Paleomastozoologia: Rio de Janeiro. Acade ^ncias, p. 590. Brasileira de Cie Pessenda, L.C.R., Ledru, M.P., Gouveia, S.E.M., Aravena, R., Ribeiro, A.S., Bendassolli, J.A., Boulet, R., 2005. Holocene palaeoenvironmental reconstruction in northeastern Brazil inferred from pollen, charcoal and carbon isotope records. Holocene 15, 812e820. https://doi.org/10.1191/0959683605hl855ra. Phillips, S.J., Anderson, R.P., Schapire, R.E., 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231e259. https://doi.org/ 10.1016/j.ecolmodel.2005.03.026.
sseis no Porpino, K.O., Santos, M.F.C.F., Bergqvist, L.P., 2004. Registro de mamíferos fo lajedo de Soledade, Apodi, Rio Grande do Norte, Brasil. Rev. Bras. Palaontol. 7, 349e358. Pough, F.H., Janis, C.M., Heiser, J.B., 2012. Vertebrate Life, ninth ed. Pearson, p. 720p. Quattrocchio, M.E., Borromei, A.M., Deschamps, C.M., Grill, S.C., Zavala, C.A., 2008. Landscape evolution and climate changes in the Late PleistoceneeHolocene, southern Pampa (Argentina): evidence from palynology, mammals and sedimentology. Quat. Int. 181, 123e138. https://doi.org/10.1016/ j.quaint.2007.02.018. re, N., Francisco, A., Gautier, D., Surault, J., Ramdarshan, A., Blondel, C., Brunetie Merceron, G., 2016. Seeds, browse, and tooth wear: a sheep perspective. Ecol. Evol. 6, 5559e5569. https://doi.org/10.1002/ece3.2241. Ray, N., Adams, J.M., 2001. A GIS-based vegetation map of the World at the last glacial maximum (25,000-15,000 BP). Internet Archeol. https://doi.org/10. 11141/ia.11.2, 11, 1e44. Rivals, F., Semprebon, G.M., 2011. Dietary plasticity in ungulates: insight from tooth microwear analysis. Quat. Int. 245, 279e284. https://doi.org/10.1016/ j.quaint.2010.08.001. Roche, D.M., Dokken, T.M., Goosse, H., Weber, S.L., 2007. Climate of the Last Glacial Maximum: sensitivity studies and model-data comparison with the LOVECLIM coupled model. Clim. Past 3, 205e224. https://doi.org/10.5194/cpd-2-11052006.
, D., Avilla, L.S., Semprebon, G.M., 2018. Diet reconstruction for an Rotti, A., Mothe extinct deer (Cervidae: Cetartiodactyla) from the quaternary of South America. Palaeogeogr. Palaeoclimatol. Palaeoecol. 497, 244e252. https://doi.org/10.1016/ j.palaeo.2018.02.026. Scherer, C.S., Pitana, V.G., Ribeiro, A.M., 2009. Protherotheriidae and Macraucheniidae (Litopterna, Mammalia) from the Pleistocene of Rio grande do Sul state, Brazil. Rev. Bras. Palaontol. 12, 231e246. https://doi.org/10.4072/rbp.2009.3.06. Scherler, L., Tütken, T., Becker, D., 2014. Carbon and oxygen stable isotope compositions of late Pleistocene mammal teeth from dolines of Ajoie (Northwestern Switzerland). Quat. Res. 82, 378e387. https://doi.org/10.1016/ j.yqres.2014.05.004. Semprebon, G., Rivals, F., 2007. Was grass more prevalent in the pronghorn past? An assessment of the dietary adaptations of Miocene to Recent Antilocapridae (Mammalia: Artiodactyla). Palaeogeogr. Palaeoclimatol. Palaeoecol. 253, 332e347. https://doi.org/10.1016/j.palaeo.2007.06.006. € hlich, U.B., Semprebon, G.M., Rivals, F., Fahlke, J.M., Sanders, W.J., Lister, A.M., Go 2015. Dietary reconstruction of pygmy mammoths from Santa Rosa island of California. Quat. Int. 406, 123e136. https://doi.org/10.1016/j.quaint.2015.10.120. ~o paleoambiental baseada no estudo de Silva, J. L. L. da, 2008. Reconstituiça ^nicos da Maravilha e Poço das Trincheiras, Alagoas, mamíferos pleistoce

12

K. de Oliveira et al. / Quaternary Science Reviews 231 (2020) 106178


s-graduaça ~o em Geonordeste do Brasil. Tese de Doutorado. Programa de Po ^ncias. Universidade Federal de Pernambuco, Pernambuco, p. 244p. cie Silva Dias, P.L., Turcq, B., Silva Dias, M.A.F., Braconnot, P., Jorgetti, T., 2009. Midholocene climate of tropical south America: a model-data approach. In: Vimeux, F., Sylvestre, F., Khodri, M. (Eds.), Past Climate Variability in South America and Surrounding Regions, 14. França, Paris.
gico e ConSilva Lopes, T., Leite, V.R., Leite, G.R., 2007. Modelagem de Nicho Ecolo
cie Ameaçada de Extinç~ servaç~ ao de Dalbergia nigra, Espe ao. R. Bras. Biosci 5, 438e440.
gicos de Venezuela, el Cuaternario del Socorro, O.A.A., 2006. Tesoros paleontolo
n. Taima Taima. Instituto del Patrimonio Cultura, p. 120p. Estado Falco Solounias, N., Semprebon, G., 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil equids. Am Mus Novit 3366, 1e49. https://doi.org/10.1206/0003-0082(2002)366<0001:AITROU>2.0.CO;2. Stevaux, J.C., 2000. Climatic events during the late Pleistocene and Holocene in the upper parana river: correlation with NE Argentina and South-Central Brazil. Quat. Int. 72, 73e85. https://doi.org/10.1016/S1040-6182(00)00023-9. Stute, M., Forster, M., Frischkorn, H., Serejo, A., Clark, J.F., Schlosser, P., Broecker, W.S., Bonani, G., 1995. Cooling of tropical Brazil (5 C) during the last glacial maximum. Science 269, 379e383. https://doi.org/10.1126/ science.269.5222.379. Tejada-Lara, J.V., MacFadden, B.J., Bermudez, L., Rojas, G., Salas-Gismondi, R., Flynn, J., 2018. Body mass predicts isotope enrichment in herbivorous mammals. P R Soc. B B 285, 20181020. https://doi.org/10.1098/rspb.2018.1020.
mico de los Tomassini, R.L., Montalvo, C.I., Manera, T., Oliva, C., 2010. Estudio tafono mamíferos pleistocenos del yacimiento de Playa del Barco (Pehuen Co), provincia de Buenos Aires, Argentina. Ameghiniana 47, 137e152. Tonni, E.P., Prado, J.L., Menegaz, A.N., Salemme, M.C., 1985. La unidad Mamifero (fauna) Lujanense. Proyeccion de la Estratigrafia Mamaliana al Cuaternario de la Region pampeana. Ameghiniana 22, 255e261.
, G.J.S., Zurita, A.E., Ríos, F.P., Tonni, E.P., Soibelzon, E., Cione, A.L., Carlini, A.A., Yane 2009. Preliminar correlation of the Pleistocene sequences of the Tarija valley

(Bolivia) with the Pampean chronological standard. Quat. Int. 210, 57e65. https://doi.org/10.1016/j.quaint.2009.06.015. Ubilla, M., 2004. Mammalian biostratigraphy of Pleistocene fluvial deposits in northern Uruguay, South America. Proceedings of the Geologists’ Association 115, 347e357. van der Hammen, T., 1974. The Pleistocene Changes of Vegetation and Climate in Tropical South America. J. Biogeogr. 1, 3e26. ~ a, R.A., 2015. Masseter moment arm as a dietary proxy in herbivoVarela, L., Farin rous ungulates. J. Zool. 296, 295e304. https://doi.org/10.1111/jzo.12246. ~ o, S.J., Di Giacomo, M., Farin ~ a, R.A., 2017. Potential Varela, L., Tambusso, P.S., Patin Distribution of Fossil Xenarthrans in South America during the Late Pleistocene: co-Occurrence and Provincialism. J Mammal Evol. https://doi.org/10.1007/ s10914-017-9406-9. Villavivencio, N.A., Lindsey, E.L., Martin, F.M., Borrero, L.A., Moreno, P.I., Marshall, C.R., Barnosky, A.D., 2016. Combination of humans, climate, and vegetation change triggered Late Quaternary megafauna extinction in the Última Esperanza region, southern Patagonia, Chile. Ecography 39, 125e140. https://doi.org/10.1111/ecog.01606. Vivo, M., Carmignotto, A.P., 2004. Holocene vegetation change and the mammal
faunas of South America and Africa. J. Biogeogr. 31, 943e957. https://doi.org/ 10.1111/j.1365-2699.2004.01068.x. Wainer, I., Clauzet, G., Ledru, M.-P., Brady, E., Otto-Bliesner, B., 2005. Last glacial maximum in south America: paleoclimate proxies and model results. Geophys. Res. Lett. 32, 1e4. https://doi.org/10.1029/2004GL021244. Werneck, F.P., 2011. The diversification of eastern South American open vegetation biomes: historical biogeography and perspectives. Quat. Sci. Rev. 30, 1630e1648. https://doi.org/10.1016/j.quascirev.2011.03.009. Werneck, F.P., Nogueira, C., Colli, G.R., Sites Jr., J.W., Costa, G.C., 2012. Climatic stability in the Brazilian Cerrado: implications for biogeographical connections of South American savannas, species richness and conservation in a biodiversity hotspot. J. Biogeogr. 39, 1695e1706. https://doi.org/10.1111/j.13652699.2012.02715.x.