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Extinction of North American Cuvieronius (Mammalia: Proboscidea: Gomphotheriidae) driven by dietary resource competition with sympatric mammoths and mastodons

Published online by Cambridge University Press:  26 February 2020

Gregory James Smith Open the ORCID record for Gregory James Smith [Opens in a new window]  and
Larisa R. G. DeSantis Open the ORCID record for Larisa R. G. DeSantis [Opens in a new window]
Gregory James Smith
Affiliation:
Department of Earth and Environmental Sciences, Vanderbilt University, Nashville, Tennessee 37240, U.S.A. E-mail: gxs258@gmail.com
Larisa R. G. DeSantis
Affiliation:
Department of Biological Sciences, Vanderbilt University, Nashville, Tennessee 37232, U.S.A.; and Department of Earth and Environmental Sciences, Vanderbilt University, Nashville, Tennessee 37240, U.S.A. E-mail: larisa.desantis@vanderbilt.edu
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Abstract

The gomphotheres were a diverse and widespread group of proboscideans occupying Eurasia, North America, and South America throughout the Neogene. Their decline was temporally and spatially heterogeneous, and the gomphotheres ultimately became extinct during the late Pleistocene; however, the genus Cuvieronius is rarely represented in late Pleistocene assemblages in North America. Two alternative hypotheses have been invoked to explain this phenomenon: (1) competitive exclusion by sympatric mammoths and mastodons or (2) ecologic displacement due to an environmental transition from closed forests to open grasslands. To test whether competition for resources contributed to the demise of North American Cuvieronius, we present herein a large collection of stable isotope and dental microwear data from populations occupying their Pleistocene refugium in the Atlantic Coastal Plain. Results suggest that Cuvieronius consumed a wide range of resources with variable textural and photosynthetic properties and was not specialized on either grasses or browse. Further, we document evidence for the consumption of similar foods between contemporaneous gomphotheres, mammoths, and mastodons. The generalist feeding strategy of the gomphotheres likely facilitated their high Miocene abundance and diversity. However, this “jack of all trades and master of none” feeding strategy may have proved challenging following the arrival of mammoths and likely contributed to the extirpation of Cuvieronius in North America.

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Articles
Information
Paleobiology , Volume 46 , Issue 1 , February 2020 , pp. 41 - 57
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Copyright © The Paleontological Society. All rights reserved 2020

Introduction

Gomphotheres (subfamily Gomphotheriinae sensu lato) are temporally and spatially prolific; the clade became dominant in North America in the Miocene and emigrated to South America from North America after the closure of the Isthmus of Panama between 2.5 and 0.125 Ma (Webb Reference Webb, Stehil and Webb1985; Reguero et al. Reference Reguero, Candela and Alonso2007; Woodburne Reference Woodburne2010; Mothé et al. Reference Mothé, Avilla, Asevedo, Borges-Silva, Rosas, Labarca-Encina, Souberlich, Soibelzon, Roman-Carrion, Ríos, Rincon, Oliveira and Lopes2017). Their dietary flexibility is hypothesized to have facilitated their successful migration in contrast to mammoths and mastodons, which remained in Central and North America despite the continental connection (Pérez-Crespo et al. Reference Pérez-Crespo, Prado, Alberdi, Arroyo-Cabrales and Johnson2016). On the other hand, gomphothere abundance, diversity, and geographic range in North America rapidly drops off after the arrival of mammoths, and the gomphotheres are rarely represented in Rancholabrean faunal assemblages (ca. 0.3–0.012 Ma sensu Bell et al. Reference Bell, Lundelius, Barnosky, Graham, Lindsay and Woodburne2004) (Carrasco et al. Reference Carrasco, Kraatz, Davis and Barnosky2005). The success of the mammoth radiation and its temporal correlation with the demise of the gomphotheres in North America has led some to argue that competition from early mammoths caused the extirpation of the gomphotheres (i.e., competitive exclusion; Kurtén and Anderson Reference Kurtén and Anderson1980). However, others have argued that cooling climates and the emergence of steppe/prairie habitats would have displaced the gomphotheres from North America even in the absence of competition (i.e., ecological displacement; Dudley Reference Dudley, Shoshani and Tassy1996). These two competing hypotheses have yet to be fully tested or resolved.

The competitive exclusion principle attests that when closely related species with similar niches coexist, one of these taxa will either outcompete the other or they will partition their niches to exploit different resources (Hardin Reference Hardin1960). Niche partitioning studies in fossil ungulates are commonly carried out through a reconstruction of diet using methods similar to those implemented here and often show the alteration of dietary preference by one or multiple organisms to facilitate coexistence with other organisms (e.g., in bovids, camelids, and horses; MacFadden et al. Reference MacFadden, Solounas and Cerling1999; Bibi Reference Bibi2007; DeSantis et al. Reference DeSantis, Feranec and MacFadden2009; Yann and DeSantis Reference Yann and DeSantis2014). Similarly, studies of proboscidean dietary niche partitioning often indicate high dietary flexibility among focal taxa (e.g., Calandra et al. Reference Calandra, Göhlich and Merceron2008; Rivals et al. Reference Rivals, Mol, Lacombat, Lister and Semprebon2015; Pérez-Crespo et al. Reference Pérez-Crespo, Prado, Alberdi, Arroyo-Cabrales and Johnson2016). Most paleoecological studies on gomphotheres suggest that they were already highly flexible in their dietary choices, capable of fluctuating between grazing, browsing, and mixed-feeding habits (e.g., MacFadden and Cerling Reference MacFadden and Cerling1996; Koch et al. Reference P. L., Hoppe and Webb1998, Reference Koch, Diffenbaugh and Hoppe2004; MacFadden Reference MacFadden2000; Fox and Fisher Reference Fox and Fisher2001, Reference Fox and Fisher2004; Sánchez et al. Reference Sánchez, Prado and Alberdi2004; Calandra et al. Reference Calandra, Göhlich and Merceron2008; DeSantis et al. Reference DeSantis, Feranec and MacFadden2009; Rivals et al. Reference Rivals, Mol, Lacombat, Lister and Semprebon2015; Pérez-Crespo et al. Reference Pérez-Crespo, Prado, Alberdi, Arroyo-Cabrales and Johnson2016; Zhang et al. Reference Zhang, Wang, Janis, Goodall and Purnell2017; González-Guarda et al. Reference González-Guarda, Petermann-Pichincura, Tornero, Domingo, Agustí, Pino, Abarzúa, Capriles, Villavicencio, Labarca, Tolorza, Sevilla and Rivals2018). However, on a smaller spatial and temporal scale, gomphotheres tended to restrict their dietary preferences due to abiotic (climatic) or biotic (competitive) factors; for example, South American populations of Notiomastodon showed an adaptive trend toward either grazing or browsing habits in the late Pleistocene due to habitat differentiation (Sánchez et al. Reference Sánchez, Prado and Alberdi2004; Mothé and Avilla Reference Mothé and Avilla2015), South China populations of Sinomastodon were restricted to the consumption of browse due to competition with co-occurring Stegodon (Zhang et al. Reference Zhang, Wang, Janis, Goodall and Purnell2017), and the East Asian gomphotherid Protanancus was competitively displaced by the amebelodont Platybelodon (Wang et al. Reference Wang, Deng, Tang, Xie, Zhang and Wang2015). Recognizing this pattern of dietary restriction in smaller populations, we therefore limit our analysis herein to Pleistocene populations of gomphothere (Cuvieronius hyodon), mammoth (Mammuthus columbi), and mastodon (Mammut americanum) occupying the Atlantic Coastal Plain (ACP) physiogeographic province of North America (Fig. 1A).

Figure 1. Geography, body size, and phylogeny related to the study material. A, Overview of the study area, with the Atlantic Coastal Plain shaded (orange online) and sites delineated by their geologic ages. B, Average body size and shoulder height of the focal proboscideans with enrichment factor (ɛ*) obtained using body-size estimates. Ch, Cuvieronius hyodon; Ma, Mammut americanum; Mc, Mammuthus columbi. C, UF 80004, left m3. Scale bar, 10 cm. Cross-hatching represents area where dental microwear texture analysis (DMTA) mold was sampled, with 3D surface model of wear facet (higher-resolution images available in the Dryad repository for this manuscript). D, TMM 47200-172, right m3. E, UF 86825, right m1. F, Temporal ranges of North American proboscidean taxa (modified from Fisher Reference Fisher2018). Thick bars show known range of taxa; thin bars show uncertain range extensions.

While both the mastodon and the gomphothere families were present in the ACP since the middle Miocene, the earliest mammoths did not arrive until the early Pleistocene (Hulbert Reference Hulbert and Hulbert2001). Mastodons, represented by the genus Zygolophodon, and gomphotheres, including the genus Gomphotherium, have been recovered from Miocene sites in both Florida and Texas (Lambert and Shoshani Reference Lambert, Shoshani, Janis, Scott and Jacobs1998). Later representatives of these clades, including the mastodon Mammut and the gomphothere Rhynchotherium, are found extensively in the southern latitudes of North America and Central America beginning in the early Pliocene (Lambert and Shoshani Reference Lambert, Shoshani, Janis, Scott and Jacobs1998; Lucas and Alvarado Reference Lucas and Alvarado2010; Pasenko Reference Pasenko2012). Cuvieronius—the only gomphothere genus found in North America, South America, and Central America—appears in Florida by ca. 2 Ma (Arroyo-Cabrales et al. Reference Arroyo-Cabrales, Polaco, Laurito, Johnson, Alberdi and Zarmora2007; Lucas Reference Lucas2008; Lucas and Alvarado Reference Lucas and Alvarado2010). The mammoth specimens recovered from the ACP are coeval with some of the earliest Mammuthus records in North America from the Rio Grande valley of southern New Mexico (Lucas et al. Reference Lucas, Morgan, Love and Connell2017). Cuvieronius is known in Florida until ca. 0.5 Ma (Lucas Reference Lucas2008); however, some of the youngest Cuvieronius records known in North America come from the Big Cypress Creek site of east Texas (Lundelius et al. Reference Lundelius, Bryant, Mandel, Thies and Thomas2013, Reference Lundelius, Thies, Graham, Bell, Smith and DeSantis2019). Mammuthus and Mammut are last known from North America in late Pleistocene sites between 14 and 10 ka (Bell et al. Reference Bell, Lundelius, Barnosky, Graham, Lindsay and Woodburne2004; Barnosky et al. Reference Barnosky, Holmes, Kirchholtes, Lindsey, Maguire, Poust, Stegner, Sunseri, Swartz, Swift, Villavicencio and Wogan2014). Thus, the samples used in this study include some of the earliest and latest examples of these proboscidean taxa in the ACP.

This study aims to fill an important spatial and temporal gap in the paleoecological record of proboscideans. In this paper, we present a quantitative analysis of dietary differences among Pleistocene proboscideans in North America using the integration of stable isotope geochemistry and dental microwear texture analysis (DMTA). The design of this study allows for both a regional comparison over time (from the early to late Pleistocene) and local, site-based assessments. Specifically, multiproxy data are used to test the following hypotheses: (1) North American Cuvieronius consumed similar resources as sympatric Mammuthus and/or Mammut; and (2) Cuvieronius, Mammuthus, and Mammut altered their dietary habits in the ACP throughout the Pleistocene. Evidence for the consumption of similar resources by Cuvieronius and Mammuthus or Mammut, as inferred via stable isotopes and dental microwear textures, may suggest that competition was a primary driver of the extirpation of North American gomphotheres.

Materials and Methods

Fossil Populations

Our study uses specimens recovered from numerous fossil mammal sites in the ACP of the United States (Fig. 1A). We first compiled all published bulk stable isotope data (MacFadden and Cerling Reference MacFadden and Cerling1996; Koch et al. Reference P. L., Hoppe and Webb1998; Feranac and MacFadden Reference Feranac and MacFadden2000; Hoppe Reference Hoppe2004; Koch et al. Reference Koch, Diffenbaugh and Hoppe2004; DeSantis et al. Reference DeSantis, Feranec and MacFadden2009; Yann and DeSantis Reference Yann and DeSantis2014; Yann et al. Reference Yann, DeSantis, Koch and Lundelius2016; Smith and DeSantis Reference Smith and DeSantis2018; Lundelius et al. Reference Lundelius, Thies, Graham, Bell, Smith and DeSantis2019) and DMTA data previously analyzed on the confocal microscope located at Vanderbilt University (Green et al. Reference Green, DeSantis and Smith2017; Smith and DeSantis Reference Smith and DeSantis2018) for proboscideans from this area (Supplementary Table 1). Focusing on localities from below 35°N limits the possible inclusion of C3 grass, which increases in abundance in more northern and western regions with decreased growing season temperatures (Teeri and Stowe Reference Teeri and Stowe1976; Stowe and Teeri Reference Stowe and Teeri1978; Still et al. Reference Still, Berry, Collatz and DeFries2003). All late Pleistocene samples in this study come from sites in east Texas and Florida. These regions likely had similar plant communities due to physiogeographic similarities; comparable precipitation amounts, mean annual temperatures, and moisture sources; and low abundances of C3 grasses and C4 shrubs, as reflected in 13C-enriched enamel in mammals from both regions. New targeted samples of primarily undersampled Cuvieronius and co-occurring Mammuthus and/or Mammut from the same locality were added to published data, resulting in a total of 248 bulk stable isotope samples and 241 DMTA samples.

Stable Isotope Geochemistry

Geochemical bulk samples of the carbonate portion of enamel hydroxyapatite were removed from well-preserved proboscidean samples from the Texas Memorial Museum (TMM) in Austin, Texas, and the Florida Museum of Natural History (FLMNH) in Gainesville, Florida. All sampled teeth were drilled by hand using a variable-speed rotary drill with carbide dental burrs (1 mm burr width), which was used to create a 1 cm × 1 mm sample transect oriented parallel to the growth axis of the tooth. Because sampling was not automated, the depth to which each sample was drilled varied, but was typically ~1–2 mm. Due to the nature of enamel growth in proboscidean teeth, this averages the dietary and environmental signal accrued in enamel tissue across multiple seasons (Dirks et al. Reference Dirks, Bromage and Agenbroad2012; Metcalfe and Longstaffe Reference Metcalfe and Longstaffe2012). While prior work has shown that stable isotope values differ significantly in mammoth, mastodon, and gomphothere teeth due to seasonal changes in diet and environment (summarized in Metcalfe Reference Metcalfe2017), the use of large sample size for each time bin should overcome these deviations and better capture the average dietary tendencies in each organism.

The collected enamel powder was pretreated with 30% H2O2 to remove organics, rinsed with distilled water, treated with 0.1 N acetic acid for 18 hours to remove secondary carbonates (similar to Koch et al. Reference Koch, Tuross and Fogel1997), and rinsed with distilled water again. Samples were left to air dry, and 1 mg per sample was analyzed on a VG Prism stable isotope ratio mass spectrometer with an in-line ISOCARB automatic sampler in the Department of Geological Sciences at the University of Florida. The standard deviation (1σ) of the laboratory standard included with these samples was <0.05‰ for both carbon and oxygen. The analytical precision is ± 0.1‰, based on replicate analyses of samples and standards. Stable isotope data were normalized to NBS-19 and are reported in conventional delta notation.

Stable carbon isotopes recorded in mammalian enamel reflect the photosynthetic signature of foods consumed (e.g., Cerling et al. Reference Cerling, Harris, MacFadden, Leakey, Quade, Eisenmann and Ehleringer1997). Carbon values from enamel (δ13Cenamel) are reported relative to VPDB (Coplen Reference Coplen1994). Consumer δ13Cenamel values were converted to the carbon isotope value of vegetation consumed (δ13Cveg) using enrichment factors (ɛ*) of 15.1‰, 15.0‰, and 14.6‰ for Mammuthus columbi, Mammut americanum, and Cuvieronius hyodon, respectively. These enrichment factors were obtained using the regression equation for hindgut fermenters from Tejada-Lara et al. (Reference Tejada-Lara, MacFadden, Bermudez, Rojas, Salas-Gismondi and Flynn2018): ln ɛ* = 2.42 + 0.032 * (BM), where BM is body mass in kilograms and is log-transformed. Average body mass for each proboscidean taxon was derived from volumetric method estimates reported by Larramendi (Reference Larramendi2016); the body-mass values we used are 9500 kg for M. columbi, 8000 kg for M. americanum, and 3500 kg for C. hyodon (Fig. 1B). To correct for the effects of differing atmospheric carbon isotope (δ13Catm) values over time on δ13Cveg values, we used estimates of past δ13Catm values from benthic foraminifera (Tipple et al. Reference Tipple, Meyers and Pagani2010) to convert paleodietary vegetation to their modern equivalent values (δ13Cvmeq) based on an A.D. 2000 δ13Catm of −8‰ (following methods outlined in Kohn Reference Kohn2010). Sample age came from site age estimates (see section on biochrons); we used the estimates of minimum and maximum site age (Supplementary Table 1) to calculate average δ13Catm value over the age range of the sample. This value was inserted into eq. 3 from Kohn (Reference Kohn2010) and used to calculate Δ. We then calculated δ13Cvmeq using the following linear regression equation, obtained using the data set in the supplemental material from Kohn (Reference Kohn2010): δ13Cvmeq = −0.9543 * Δ − 8.3617. The δ13Cvmeq values reported here reflect isotopic values of C3 shrubs/trees and C4 grasses, respectively, and are thus indicative of browsing, grazing, and mixed-feeding habits. Here we assume that δ13Cvmeq values less than −25.1‰ indicate diets of at least 85% C3 vegetation while values greater than −16.0‰ indicate at least 85% C4 vegetation; values in between suggest a mix of both C3 and C4 resources (Cerling et al. Reference Cerling, Harris, MacFadden, Leakey, Quade, Eisenmann and Ehleringer1997; Kohn Reference Kohn2010; also see Supplementary Appendix 1).

Stable oxygen isotopes reflect environmental factors, including temperature and precipitation, and are useful for identifying spatially or temporally mixed assemblages or for separating glacial and interglacial periods. The oxygen isotopes reported here (δ18Oenamel) are those recorded in enamel and reflect multiple compounding factors impacting each individual proboscidean, including temperature, humidity, altitude, and latitude (Dansgaard Reference Dansgaard1964; also see Supplementary Appendix 1). Oxygen isotope values are reported relative to VSMOW. Previously published δ18Oenamel values reported relative to VPDB were converted using the following equation: δ18OVSMOW = 1.03086 * δ18OVPDB + 30.86 (Friedman and O'Neil Reference Friedman and O'Neil1977).

Dental Microwear Texture Analysis

Microwear molds were collected from the jaws and isolated teeth of proboscidean fossils held at TMM (n = 13) and FLMNH (n = 104). Sampling methods for DMTA followed procedures outlined in prior studies (Green et al. Reference Green, DeSantis and Smith2017; Smith and DeSantis Reference Smith and DeSantis2018). Briefly summarized here, the wear facets of mammoth, mastodon, and gomphothere molars were cleaned with acetone and then sampled with Regular Body President's Jet to create a mold. We prioritized sampling the central enamel bands for all specimens (Fig. 1C–E) to maintain consistency with past studies of DMTA in proboscideans (Green et al. Reference Green, DeSantis and Smith2017; Zhang et al. Reference Zhang, Wang, Janis, Goodall and Purnell2017; Smith and DeSantis Reference Smith and DeSantis2018) and because sampling these areas reduces the amount of variation in microwear features attributable to differences in the direction of the power stroke during mastication (e.g., Laub Reference Laub, Stewart and Seymour1996; Todd et al. Reference Todd, Falco, Silva and Sanchez2007; von Koenigswald Reference von Koenigswald2016). The molds were then cast at Vanderbilt University using a high-resin epoxy (Epotek 301) and dried in a fume hood for at least 72 hours before analysis.

All specimens were scanned in three dimensions in four adjacent fields of view for a total sampled area of 204 × 276 μm2 using the Plu NEOX white-light microscope with confocal capabilities at Vanderbilt University. Scans were analyzed using scale-sensitive fractal analysis software (ToothFrax and SFrax, Surfract Corporation, www.surfract.com), which characterizes wear surfaces according to variables including complexity (Asfc), anisotropy (epLsar), textural fill volume (Tfv), and heterogeneity of complexity (HAsfc). Complexity is a quantification of the change in surface roughness with increasing scale and is used to distinguish taxa that consume hard/brittle foods from those that eat softer/tougher foods (Ungar et al. Reference Ungar, Brown, Bergstrom and Walker2003, Reference Ungar, Merceron and Scott2007; Scott et al. Reference Scott, Ungar, Bergstrom, Brown, Grine, Teaford and Walker2005; Prideaux et al. Reference Prideaux, Ayliffe, DeSantis, Schubert, Murray, Gagan and Cerling2009; Scott Reference Scott2012; DeSantis Reference DeSantis2016). Anisotropy is the degree to which surface features share a similar orientation, such that a predominance of parallel striations leads toward highly anisotropic surfaces—typical in grazers and other consumers of tough food items (Ungar et al. Reference Ungar, Brown, Bergstrom and Walker2003, Reference Ungar, Merceron and Scott2007; Prideaux et al. Reference Prideaux, Ayliffe, DeSantis, Schubert, Murray, Gagan and Cerling2009; Scott Reference Scott2012; DeSantis Reference DeSantis2016; Hedberg and DeSantis Reference Hedberg and DeSantis2017). Textural fill volume is a measure of the total volume of square cuboids of a given scale that fill surface features and is useful for distinguishing deeper microwear features (such as gouges from pits), which has the potential to distinguish between consumption of foods with different fracture properties (e.g., leaves vs. fruit pits) (Scott et al. Reference Scott, Ungar, Bergstrom, Brown, Childs, Teaford and Walker2006; Ungar et al. Reference Ungar, Merceron and Scott2007, Reference Ungar, Grine and Teaford2008). Heterogeneity of complexity is calculated by splitting individual scanned areas into smaller sections with equal numbers of rows and columns (from 2 × 2 up to 11 × 11) and comparing Asfc values between subregions (Scott et al. Reference Scott, Ungar, Bergstrom, Brown, Childs, Teaford and Walker2006). Low values in heterogeneity have been shown to be indicative of either high grit loads or grass consumption (Scott Reference Scott2012; Merceron et al. Reference Merceron, Ramdarshan, Blondel, Boisserie, Brunetiere, Francisco, Gautier, Milhet, Novello and Pret2016). We report heterogeneity at two scales, 3 × 3 (HAsfc 3×3) and 9 × 9 (HAsfc 9×9), as has been the practice in previous studies (e.g., Green et al. Reference Green, DeSantis and Smith2017; Smith and DeSantis Reference Smith and DeSantis2018).

Assignment to Biochronologic Intervals (“Biochrons”)

Each proboscidean individual sampled for stable isotopes or DMTA was referred to a specific locality (Supplementary Table 1). For published samples, the minimum and maximum ages for that locality were inferred from the publication that contained the sample reference. For new samples, the age of the site was either determined from the literature or in consultation with the collections manager of the FLMNH (R. Hulbert personal communication 2019). DeSoto Shell Pit, Devil's Elbow, Haile 7C, and Brighton Canal were all considered to date to the late Blancan (Bl5). Following Lucas (Reference Lucas2008), we consider all gomphotheriids from Florida from Bl5 or younger to be C. hyodon. We therefore include the samples originally referred to Rhynchotherium in MacFadden and Cerling (Reference MacFadden and Cerling1996) and refer them to C. hyodon. Site ages were used to bin samples to the following biochrons, with ages from Bell et al. (Reference Bell, Lundelius, Barnosky, Graham, Lindsay and Woodburne2004): Bl5 (late Blancan), minimum age = 1.6 Ma, maximum age = 2.5 Ma; Ir1 (early Irvingtonian), minimum age = 0.85 Ma, maximum age = 1.6 Ma; Ir2 (late Irvingtonian), minimum age = 0.3 Ma, maximum age = 0.85; Ra (Rancholabrean), minimum age = 0.010 Ma, maximum age = 0.3 Ma.

Statistical Analyses

All published and new data were combined for statistical comparisons. We carried out two statistical comparisons of δ13Cvmeq, δ18Oenamel, and DMTA attributes for each genus: first, within each biochron to test for consumption of similar foods in sympatric populations; and second, across biochrons to assess whether dietary niche was conserved over time for each taxon. Our tests for the late Pleistocene combined samples from Florida and east Texas based on the assumption that the paleoenvironment was broadly similar in the two regions at that time; however, we also excluded samples from Texas and reran statistical comparisons between δ13Cvmeq and δ18Oenamel to ensure that this was a valid assumption. When comparing between normally distributed attributes, parametric tests (e.g., t-test or analysis of variance) were employed; otherwise, nonparametric equivalent tests (e.g., Mann-Whitney U or Kruskal-Wallis) were used. For all tests, the Bonferroni correction factor was withheld, as it can result in an increase in type II errors (Cabin and Mitchell Reference Cabin and Mitchell2000; Nakagawa Reference Nakagawa2004). p-Values of <0.05 were considered significant.

Results

Stable Isotope Ecology

Mammut δ13Cvmeq values are indistinguishable through time in contrast to Mammuthus, which exhibits higher δ13Cvmeq values during the Rancholabrean as compared with the late Irvingtonian, and Cuvieronius, which has significantly lower mean δ13Cvmeq values during the Rancholabrean than the early Irvingtonian (Table 1, all statistical comparisons in Supplementary Table 2). Further, Mammut consistently has lower δ13Cvmeq values than both Cuvieronius and Mammuthus through time, while Mammuthus has significantly greater δ13Cvmeq values than Cuvieronius during the Rancholabrean (note, δ13Cvmeq values are indistinguishable when compared with the early Irvingtonian values).

Table 1. Stable isotope summary statistics for all proboscidean samples analyzed. n, number of specimens; Min, minimum; Max, maximum; SD, 1 standard deviation (1σ); SE, standard error of the mean (σ/√n); p-value is that associated with a Shapiro-Wilk test (bold values indicate a nonnormal distribution); δ13Cvmeq, modern equivalent vegetation stable carbon isotope signature of paleodiet; δ18Oenamel, stable oxygen isotope signature of enamel; Bl5, late Blancan (2.6–1.8 Ma); Ir1, early Irvingtonian (1.8–0.85 Ma), Ir2, late Irvingtonian (0.85–0.3 Ma); Ra, Rancholabrean (0.3–0.011 Ma).

Oxygen isotope values of Cuvieronius are significantly greater during the early Irvingtonian than both the late Blancan and Rancholabrean (Table 1). In contrast, Mammut has significantly higher δ18Oenamel values during the late Irvingtonian than both the early Irvingtonian and Rancholabrean. Mammuthus has the highest δ18Oenamel values during the late Irvingtonian followed by the early Irvingtonian and Rancholabrean (all significantly different from one another, Supplementary Table 2). Overall, all proboscideans examined have indistinguishable δ18Oenamel values from one another during the late Irvingtonian and Rancholabrean, with only Cuvieronius yielding significantly higher δ18Oenamel values than both Mammut and Mammuthus during the early Irvingtonian.

Results are statistically unchanged when excluding Rancholabrean specimens from Texas from the analysis. The total range of δ13Cvmeq values for Cuvieronius (11.2‰) and Mammuthus (8.0‰) during the Rancholabrean (Table 1) remain similar (10.0‰ and 7.3‰, respectively) after excluding specimens from Texas. When Texas specimens are excluded, the average δ13Cvmeq value for Cuvieronius changes from −22.3‰ to −23.4‰, and the average δ13Cvmeq value for Mammuthus changes from −18.6‰ to −20.7‰. Cuvieronius samples from Florida remain significantly lower in δ13Cvmeq than Mammuthus samples from Florida (p = 0.001). Moreover, Rancholabrean Mammuthus and Cuvieronius δ18Oenamel values remain statistically indistinguishable from one another when Texas samples are removed (p = 0.072). In short, the results of this study hold whether looking at the ACP as a whole or at Florida alone.

Textural Properties of Food Resources

Cuvieronius and Mammut both have Asfc, epLsar, Tfv, and HAsfc (HAsfc 3×3 and HAsfc 9×9) values that are statistically indistinguishable within each taxon over time (Table 2, Supplementary Table 2). Only Mammuthus exhibits significantly greater Tfv during the early Irvingtonian as compared with both the late Irvingtonian and Rancholabrean. During the early Irvingtonian, Cuvieronius has significantly higher Asfc values than Mammut, while Mammuthus has significantly higher Tfv than Cuvieronius. Mammut and Mammuthus have Asfc, epLsar, Tfv, and HAsfc (HAsfc 3×3 and HAsfc 9×9) values that are indistinguishable from one another during the late Irvingtonian. During the Rancholabrean, Mammuthus has significantly higher Asfc values than Mammut, Cuvieronius has significantly lower epLsar values than both Mammut and Mammuthus, and Mammuthus has significantly higher Tfv values than Cuvieronius and Mammut.

Table 2. Dental microwear texture analysis (DMTA) summary statistics for all proboscideans analyzed, broken down by biochronologic interval. Asfc, area-scale fractal complexity; epLsar, anisotropy; Tfv, textural fill volume; HAsfc 3×3, HAsfc 9×9, heterogeneity of complexity in a 3 × 3 and 9 × 9 grid, respectively. See Table 1 for definitions of other abbreviations. Bold values indicate a nonnormal distribution (Shapiro-Wilk; p < 0.05 is significant).

Discussion

Despite the oft-mentioned view that the extinction of gomphotheres was tied to competition with other megaherbivores, particularly mammoths (Kurtén and Anderson Reference Kurtén and Anderson1980; Cerling et al. Reference Cerling, Harris, Leakey, Leakey and Harris2003; Sanders Reference Sanders2007; Lucas et al. Reference Lucas, Aguilar and Spielmann2011; Lister Reference Lister2013), there are few studies that have assessed competition between these taxa in the fossil record. Interspecific competition is notoriously difficult to verify when examining fossil populations, as paleoecologists can neither directly observe interference competition (e.g., male–male combat or other acts of aggression toward a competitor) nor precisely quantify the magnitude of resource limitation leading toward exploitative competition (e.g., consumption of similar resources by two potential competitors). Because of these limitations, evidence of interspecific competition in the fossil record is usually either modeled using phylogenetic hypotheses (e.g., Rabosky Reference Rabosky2013) or inferred from character displacement (Schluter Reference Schluter2000; Grant and Grant Reference Grant and Grant2006). However, the paleontological record offers a potential strength in documenting the signs of exploitative and interference competition over geologic timescales if one makes a few assumptions about how competition between megaherbivores could manifest in the fossil record. First, if one assumes via the principle of limiting similarity that there is a limit to how similar species can be and still coexist (MacArthur and Levins Reference MacArthur and Levins1967; May and MacArthur Reference May and MacArthur1972; May Reference May1974), then it follows that there is an upper limit of shared niche space that would facilitate coexistence between two species. Above this limit, it becomes more likely that one species will exclude the other through competition for resources. Second, if one assumes that competition promotes the use of different resources (as opposed to complete exclusion) (Schoener Reference Schoener1974, Reference Schoener1982; Pianka Reference Pianka and May1976), then shifting dietary habits over geologic timescales may be correlated with the intensity of interspecific competition. In this case, demonstrating such shifts in response to the presence of a potential competitor can be considered evidence of competition (Pianka Reference Pianka and May1976). Finally, if we assume that where mammoths are abundant, they may be considered keystone competitors (sensu Bond Reference Bond, Schulze and Mooney1993), then mammoths should limit large herbivore abundances via monopolizing resource utilization in their local communities (Fritz Reference Fritz1997; Fritz et al. Reference Fritz, Duncan, Gordon and Illius2002). Bearing these assumptions in mind, we elaborate below on the evidence for interspecific competition between sympatric megaherbivores in Pleistocene North America with relevance to the extirpation and eventual extinction of Cuvieronius.

Although we are unable at present to generalize beyond the southeastern United States, our results comprise two lines of evidence that support the competitive exclusion hypothesis (as opposed to the ecological displacement hypothesis [Dudley Reference Dudley, Shoshani and Tassy1996]). First, data presented here support the hypothesis that Columbian mammoth (M. columbi) and gomphothere (C. hyodon) populations consumed foods of similar geochemical and textural properties during the early Irvingtonian (1.6–1.0 Ma), when mammoths first appear in North America. Specifically, mean δ13Cvmeq values of −19.2‰ and −18.6‰ for Cuvieronius and Mammuthus, respectively, indicate a predominately C4 grazing signature supplemented with C3 resources (Table 1), while moderate Asfc and epLsar values that both have a high range similarly suggest a highly generalized mixed-feeding signature for both proboscideans (Table 2). All of these proxy data (i.e., δ13Cvmeq, Asfc, and epLsar) are statistically indistinguishable for gomphotheres and mammoths. We interpret these results to show that, upon arriving in the ACP, Mammuthus began to exploit similar resources as endemic Cuvieronius.

All early Irvingtonian samples in our data set come from two assemblages from Florida—the Leisey Shell Pit Local Fauna (LSPLF) (Morgan and Hulbert Reference Morgan and Hulbert1995) and the Punta Gorda Local Fauna (PGLF) (Webb Reference Webb and Webb1974). The LSPLF was deposited during an interglacial period ca. 1.6–1.0 Ma, as supported by magnetic polarity dates; strontium isotope values on marine bivalves; stratigraphic evidence of a high-stage sea-level stand; vertebrate chronology, including the presence of warm-adapted vertebrates such as alligators; and 18O-enriched values in mammalian herbivore enamel, consistent with a drier climate (Morgan and Hulbert Reference Morgan and Hulbert1995; DeSantis et al. Reference DeSantis, Feranec and MacFadden2009). Our data show no statistically significant difference in δ18Oenamel values between LSPLF and PGLF Cuvieronius (mean δ18Oenamel = 31.5‰ and 31.4‰, respectively; p = 0.867) or Mammuthus (mean δ18Oenamel = 30.1‰ and 29.9‰, respectively; p = 0.534). This may indicate that a similar climatic setting was experienced by both faunas, which would support the inference by Morgan and Hulbert (Reference Morgan and Hulbert1995) that the two sites are of similar ages. DeSantis et al. (Reference DeSantis, Feranec and MacFadden2009) reported significant differences in the δ13C signatures of browsers (Palaeolama, Tapirus, Mammut, Odocoileus), mixed feeders (Mylohyus, Platygonus, Hemiauchenia), and grazers (Equus, Mammuthus, Cuvieronius) of the LSPLF, but noted no significant differences when browsers were compared with one another or when grazers were compared with one another. The authors suggested that the high degree of niche partitioning among the mammalian community, facilitated by the abundance of C4 grass and the diversity of C3 dietary resources, may have contributed to the high mammalian diversity of the LSPLF (DeSantis et al. Reference DeSantis, Feranec and MacFadden2009). Our results corroborate this suggestion and specifically indicate that Cuvieronius and Mammuthus were able to coexist during the early Irvingtonian despite consuming foods of similar geochemical and textural properties. This suggests that there must have been an abundance of dietary resources in the ACP, as both proboscideans were large monogastric-caecalid grazers with high dietary resource intake requirements (Guthrie Reference Guthrie, Martin and Klein1984). As large mammalian herbivores are primarily food limited (Sinclair Reference Sinclair1975) (as opposed to predator limited [e.g., Sinclair et al. Reference Sinclair, Mduma and Brashares2003; Fritz et al. Reference Fritz, Loreau, Chamaille-Jammes, Valeix and Clobert2011]), warm climates and long growing seasons likely produced a diverse floral habitat with considerable local heterogeneity needed to support such a high abundance of closely related and ecologically similar taxa (a “vegetative mosaic” [Guthrie Reference Guthrie, Martin and Klein1984]).

The second line of evidence in support of the competitive exclusion hypothesis is niche plasticity in Cuvieronius populations occupying the ACP. While stable isotope and dental microwear data do support the hypothesis of shifting dietary habits over time, the magnitude and direction of this shift varies by taxon. Mammut exhibits the narrowest dietary niche of the three proboscideans, with the smallest range in δ13Cvmeq values of all taxa in each NALMA (Table 1) and statistically unchanging DMTA attribute values for all NALMAs (Table 2, Supplementary Table 2). Further, Mammut δ13Cvmeq values are consistently significantly lower than either Cuvieronius or Mammuthus values, implying a persistent preference for C3 dietary resources over time—interpreted here as woody-browse. Because of the high abundance of Mammut remains recovered in the ACP, our interpretation of these data is that mastodons successfully dominated the “large monogastric browser” niche up until the end-Pleistocene, even during periods of resource limitation. Similarly, Mammuthus δ13Cvmeq, Asfc, and epLsar values do not change significantly from the early Irvingtonian to the Rancholabrean, suggesting a similar dietary niche of C4 grazing supplemented with C3 resources of varying textural properties; thus, mammoths are interpreted as having occupied the “large monogastric grazer” niche. Because mammoths lacked a rumen (and could therefore not avoid absorbing toxic plant defenses including alkaloids and cyanogens into the bloodstream [Guthrie Reference Guthrie, Martin and Klein1984]), they likely would have required a diet consisting of grass as a staple and supplemented by other plant species with complementary nutrients and less toxic defenses. In contrast to mammoths and mastodons, Cuvieronius populations show a statistically significant decrease in δ13Cvmeq values from the early Irvingtonian to the Rancholabrean while more than doubling the standard deviation of mean δ13Cvmeq values (Table 1). During the Rancholabrean, Cuvieronius populations in the ACP consumed a diet that was geochemically intermediate between Mammut and Mammuthus diets and texturally indistinguishable from either (Fig. 2). Rancholabrean gomphothere δ13Cvmeq values are statistically equitable to their late Blancan δ13Cvmeq values. Our interpretation of these data is that late Pleistocene gomphotheres in the ACP were mixed-feeding C3/C4 generalists (similar to gomphotheres in the early Pleistocene, before the arrival of mammoths), covering a dietary spectrum that was overlapped by mammoths on the grazing end and mastodons on the browsing end.

Figure 2. Bivariate plots of stable isotope values and dental microwear attributes for proboscidean samples from the Atlantic Coastal Plain. Circles (blue online), Cuvieronius hyodon; triangles (brown online), Mammut americanum; squares (green online), Mammuthus columbi. Mean values for each population are shown with error bars for the standard deviation; individual sample values are slightly transparent. Convex hulls overlay the range of values for each taxon.

During the Pleistocene, rapid climate changes may have disturbed vegetative mosaics and led to floral community restructuring, resulting in periodic resource scarcity and affecting niche partitioning among large mammalian herbivores. Pleistocene glacial–interglacial dynamics became especially pronounced beginning ca. 70–60 ka, with the onset of 2–3 kyr warm–cool oscillations (Dansgaard-Oescher, or D-O, events) punctuated by abrupt (~1 kyr) cool phases characterized by Heinrich events (i.e., the fracturing of ice shelves into the North Atlantic) (Heinrich Reference Heinrich1988; Dansgaard et al. Reference Dansgaard, Johnsen, Clausen, Dahl-Jensen, Gundenstrup, Hammer, Hvidberg, Steffensen, Sveinbjörnsdottir, Jouzel and Bond1993; Bond and Lotti Reference Bond and Lotti1995; Elliot et al. Reference Elliot, Labeyrie, Bond, Cortijo, Turon, Tisnerat and Duplessy1998; Alley et al. Reference Alley, Marotzke, Nordhaus, Overpeck, Peteet, Pielke, Pierrehumbert, Rhines, Stocker, Talley and Wallace2003). These climatic changes likely led to phenological shifts in plant communities (e.g., earlier flowering or emergence dates) and individualistic shifts in the reproductive habits and geographic ranges of mammals, as is currently occurring in modern biotas (Graham Reference Graham2005; Post Reference Post and Post2013). Further, there is evidence from an ~60 kyr palynological record from south Florida that ACP pollen changes and the warming effects of D-O events were out of sync with the rest of North America (Grimm et al. Reference Grimm, Jacobson, Watts, Hansen and Maasch1993, Reference Grimm, Watts, Jacobson, Hansen, Almquist and Diffenbacher-Krall2006; Arnold et al. Reference Arnold, Diefendorf, Brenner, Freeman and Baczynski2018). Heterogeneous climatic and environmental changes in North America served to break down the Pleistocene vegetative mosaics that had supported the coevolution of a high diversity of specialized groups of organisms (Graham and Lundelius Reference Graham, Lundelius, Martin and Klein1984; Graham and Grimm Reference Graham and Grimm1990). As seasonal mixed feeders, proboscideans depend on the right composition of low-quality grass and high-quality (but chemically defended) browse emerging at the right time of year (e.g., Janzen and Martin Reference Janzen and Martin1982; Guthrie Reference Guthrie, Martin and Klein1984; Owen-Smith Reference Owen-Smith1988; Teale and Miller Reference Teale and Miller2012; Metcalfe Reference Metcalfe2017); disruption of this timing would have limited the abundance of these dietary resources at critical times, potentially leading to increased intra- and interspecific competition.

The large body size of mammoths and mastodons may have provided these taxa with a competitive advantage over sympatric gomphotheres. Cuvieronius hyodon was the smallest of the three proboscidean taxa in the ACP—on average, between 57% and 68% less massive than M. columbi and 48% to 62% less massive than Mammut based on volumetric estimates of body mass (Larramendi Reference Larramendi2016). Mammut and Mammuthus were also considerably higher at the shoulder than Cuvieronius (Fig. 1B) (Larramendi Reference Larramendi2016). As a result, gomphothere populations were more likely to suffer from both interference competition and exploitative competition with mammoths and mastodons. Modern African elephants (Loxodonta africana) are known to aggressively attack and kill smaller large herbivores such as rhinoceroses, particularly when adult males enter musth (a periodic condition characterized by a sharp rise in aggressive behavior, temporin secretion, and the continuous discharge of urine) (Poole Reference Poole1987; Berger and Cunningham Reference Berger and Cunningham1998; Slotow and van Dyk Reference Slotow and van Dyk2001). Mammoths and mastodons likely engaged in similar violence; fossil evidence of the kind of male-on-male violence typical of musth includes two bull mammoths that died after their tusks became locked during combat (Agenbroad and Mead Reference Agenbroad and Mead1994) and pathologies on the mandible of the holotype of the Pacific mastodon (Mammut pacificus [Dooley et al. Reference Dooley, Scott, Green, Springer, Dooley and Smith2019]) consistent with tusk strikes from another bull. Additionally, low rates of dentin apposition in the tusks of mammoths in the Great Lakes and southern California suggest that some males regularly fasted, as modern elephants do during musth (Fisher Reference Fisher2004; El Adli et al. Reference El Adli, Cherney, Fisher, Harris, Farrell and Cox2015). Exploitative competition was also likely; assuming dietary intake scales with body mass at a rate of BM0.75 (according to the Jarman-Bell principle [Geist Reference Geist1974]), Mammuthus and Mammut would have consumed significantly more food than Cuvieronius. Using regression equations based on modern herbivores (Müller et al. Reference Müller, Codron, Meloro, Munn, Schwarm, Hummel and Clauss2013) and body-mass estimates from Larramendi (Reference Larramendi2016), we estimate that Mammuthus and Mammut consumed roughly twice as much dry matter per day as Cuvieronius (49.9 ± 4.5 kg/day and 43.7 ± 4.9 kg/day for Mammuthus and Mammut, respectively, as compared with ~23.3 kg/day in Cuvieronius). This may have created food scarcity during resource-limited intervals if mammoth and mastodon abundances remained high; for example, modern African elephants with large population densities have been shown to impact the foraging patterns of black rhinoceroses (Diceros bicornis), with rhinos switching from a diet composed of mostly browse to one consisting of mostly grass during seasons of resource scarcity, when elephants have monopolized their food sources (Landman et al. Reference Landman, Schoeman and Kerley2013). This reduced intake of preferred foods and change in diet along the grass–browse continuum may have reduced gomphothere diet quality, causing reduced body mass and/or reduced fecundity (as has been shown to occur in modern ungulates [Simard et al. Reference Simard, Cote, Weladji and Huot2008; Christianson and Creel Reference Christianson and Creel2009]).

Conclusions

In conclusion, dietary proxy data from proboscideans indicate that the early Pleistocene coexistence of mammoths and gomphotheres was potentially made possible by both proboscideans exhibiting a generalist mixed-feeding dietary habit permitted by abundant resources, but that dramatic climatic and ecologic changes in the late Pleistocene may have limited resource availability and led to increased interspecific competition. Gomphotheres were part of a highly coevolved ecological food web that began to experience disruption due to dramatic climatic and ecologic changes in the Pleistocene. The results of this study demonstrate that competition between mammoths, mastodons, and the gomphothere Cuvieronius was prevalent in the ACP of North America throughout the Pleistocene. Cuvieronius may have migrated into South America in the late Pleistocene tracking a preferred environmental habitat (Mothé et al. Reference Mothé, Avilla, Asevedo, Borges-Silva, Rosas, Labarca-Encina, Souberlich, Soibelzon, Roman-Carrion, Ríos, Rincon, Oliveira and Lopes2017), but populations in the ACP of North America experienced heavy competition with Mammuthus and Mammut before disappearing entirely. Using multiple dietary proxies from sympatric megaherbivores, interspecific interactions including niche partitioning and competition can be inferred and here provide compelling evidence for gomphotheres being competitively excluded in North America during the late Pleistocene megafaunal extinctions.

Acknowledgments

Funding included a Geological Society of America student research grant, the Paleontological Society Stephen Jay Gould Award, and the Theodore Roosevelt Memorial Fund to G.J.S., as well as National Science Foundation grant no. 1053839 and Vanderbilt University funds to L.R.G.D. We thank the collections managers and curators of the Texas Memorial Museum and the Florida Museum of Natural History for access to and assistance with the collections, especially R. Hulbert, E. Lundelius, and C. Sagebiel. B. Engh sketched the molars in Figure 1, and J. Curtis analyzed new stable isotope samples at the University of Florida. Thanks to D. Mothé, J. El Adli, and V. A. Pérez-Crespo for providing helpful reviews that greatly improved this article.

Footnotes

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.6djh9w0x1

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Figure 0

Figure 1. Geography, body size, and phylogeny related to the study material. A, Overview of the study area, with the Atlantic Coastal Plain shaded (orange online) and sites delineated by their geologic ages. B, Average body size and shoulder height of the focal proboscideans with enrichment factor (ɛ*) obtained using body-size estimates. Ch, Cuvieronius hyodon; Ma, Mammut americanum; Mc, Mammuthus columbi. C, UF 80004, left m3. Scale bar, 10 cm. Cross-hatching represents area where dental microwear texture analysis (DMTA) mold was sampled, with 3D surface model of wear facet (higher-resolution images available in the Dryad repository for this manuscript). D, TMM 47200-172, right m3. E, UF 86825, right m1. F, Temporal ranges of North American proboscidean taxa (modified from Fisher 2018). Thick bars show known range of taxa; thin bars show uncertain range extensions.

Figure 1

Table 1. Stable isotope summary statistics for all proboscidean samples analyzed. n, number of specimens; Min, minimum; Max, maximum; SD, 1 standard deviation (1σ); SE, standard error of the mean (σ/√n); p-value is that associated with a Shapiro-Wilk test (bold values indicate a nonnormal distribution); δ13Cvmeq, modern equivalent vegetation stable carbon isotope signature of paleodiet; δ18Oenamel, stable oxygen isotope signature of enamel; Bl5, late Blancan (2.6–1.8 Ma); Ir1, early Irvingtonian (1.8–0.85 Ma), Ir2, late Irvingtonian (0.85–0.3 Ma); Ra, Rancholabrean (0.3–0.011 Ma).

Figure 2

Table 2. Dental microwear texture analysis (DMTA) summary statistics for all proboscideans analyzed, broken down by biochronologic interval. Asfc, area-scale fractal complexity; epLsar, anisotropy; Tfv, textural fill volume; HAsfc3×3, HAsfc9×9, heterogeneity of complexity in a 3 × 3 and 9 × 9 grid, respectively. See Table 1 for definitions of other abbreviations. Bold values indicate a nonnormal distribution (Shapiro-Wilk; p < 0.05 is significant).

Figure 3

Figure 2. Bivariate plots of stable isotope values and dental microwear attributes for proboscidean samples from the Atlantic Coastal Plain. Circles (blue online), Cuvieronius hyodon; triangles (brown online), Mammut americanum; squares (green online), Mammuthus columbi. Mean values for each population are shown with error bars for the standard deviation; individual sample values are slightly transparent. Convex hulls overlay the range of values for each taxon.