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Faunal isotope records reveal trophic and nutrient dynamics in twentieth century Yellowstone grasslands

DOI:10.1098/rsbl.2012.0321
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Kena Fox-Dobbs
Kena Fox-Dobbs
Kena Fox-Dobbs
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Abigail A Nelson at Montana Fish Wildlife and Parks
Abigail A Nelson
  • Montana Fish Wildlife and Parks
Paul L Koch at University of California, Santa Cruz
Paul L Koch
Jennifer A Leonard at Spanish National Research Council
Jennifer A Leonard
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Abstract and Figures

Population sizes and movement patterns of ungulate grazers and their predators have fluctuated dramatically over the past few centuries, largely owing to overharvesting, land-use change and historic management. We used δ(13)C and δ(15)N values measured from bone collagen of historic and recent gray wolves and their potential primary prey from Yellowstone National Park to gain insight into the trophic dynamics and nutrient conditions of historic and modern grasslands. The diet of reintroduced wolves closely parallels that of the historic population. We suggest that a significant shift in faunal δ(15)N values over the past century reflects impacts of anthropogenic environmental changes on grassland ecosystems, including grazer-mediated shifts in grassland nitrogen cycle processes.
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Fox-Dobbs et 12 BioLet 8-suppl
Data
April 2014
Kena Fox-Dobbs · Abigail A Nelson · Paul L Koch · Jennifer A Leonard
... Given that many species, especially predators, impact ecosystems through their diet, we suggest that one way of doing this is to compare the volume and overlap of dietary niches of extinct taxa and their potential ecological replacements. Stable isotope ratios in the tissues of consumers predictably reflect those in their food (Phillips et al., 2014) so one indirect but tractable way of doing this is to quantify isotopic niche volume and overlap using modern and historical tissue samples (Chamberlain et al., 2005;Fox-Dobbs, Nelson, Koch, & Leonard, 2012;Newsome et al., 2010). ...
... Previous studies have compared past to present day isotopic niches of members of the same or similar species (Chamberlain et al., 2005;Fox-Dobbs et al., 2012;Newsome et al., 2010) but as far as we are aware, this is the first study to explicitly compare isotopic niches between an extinct species and a potential ecological replacement. Given the burgeoning interest in ecological replacement as a conservation tool (Falcón & Hansen 2018;Griffiths et al., 2011;Seddon et al., 2014), we foresee that similar studies will become more common. ...
... Prior to the introduction of sheep, upland geese were the primary terrestrial grazers in the Falklands, so limits on their distribution by FIWs were likely to have had cascading effects on vegetation, nutrient cycling, avian nesting habitat, and so on. (Fox-Dobbs et al., 2012). We presume that SAGFs may have similar effects on those islands where they are present but further study would be required to confirm this. ...
A wolf in fox's clothing? Using stable isotopes to quantify ecological replacement
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  • Feb 2021
Ecological replacement as a conservation tool presupposes that nonnative taxa can restore degraded ecosystems by performing the ecological functions of extinct taxa. This assumption is rarely tested however, largely because it is difficult to quantify the functions of species extirpated long ago. Here, we test whether feral South American grey foxes (SAGF), introduced to the Falkland Islands ∼90 years ago, act as unintended ecological replacements for endemic Falkland Islands wolves (FIW), extirpated during the 19th century. Using hair stable isotope ratios as proxies for diet, we show that the isotopic niche space of modern SAGFs almost completely encompasses that of archaic FIWs. However, the former's niche is larger so while SAGFs may play similar ecological roles to FIWs, they probably perform additional functions, which may or may not be desirable. In so doing, we illustrate a generalized framework for using comparative isotopic niche analysis to test for ecological replacement objectively.
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... B: Comparison of nitrogen isotope ratios (d 15 N col. , in ‰) measured in the bone collagen of the large mammals from Amboseli Game Reserve, Kenya (data from Koch et al., 1991), Yellowstone National Park, USA (data from Fox-Dobbs et al., 2012), Kasungu National Park, Malawi (data from Sealy et al., 1987) and VM in GBD (data from Palmqvist et al., 2008a). Values of mean annual precipitation (MAP, in mm) are provided for the three natural parks. ...
... Koch et al., 1991) and even Yellowstone (2.4e9.8‰; Fox-Dobbs et al., 2012), where MAP (590 mm) is~1.7 times higher than today in Orce (Fig. 1B). In contrast, it is very similar to that of Kasungu (1.6e8.0‰; ...
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... This approach relies on the fact that isotope ratios of organismal tissues (e.g., teeth, hair, and bone collagen) are strongly related to dietary inputs and the animals' physiological condition over the period of tissue growth (West et al. 2006;Ehleringer et al. 2008;Cerling et al. 2009;Cryan et al. 2014). Further, the collective analysis of isotope ratios from specimens archived in natural history collections can be used to infer movement patterns (e.g., Cryan et al. 2004;Fox-Dobbs et al. 2012), foraging and habitat preferences (e.g., Clementz and Koch 2001;Cerling et al. 2009), and long-term variation in resource use (e.g., Blight et al. 2015). ...
Isotope values of California vole (Microtus californicus) hair relate to historical drought and land use patterns in California, USA
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Increased drought frequency and intensity and agricultural intensification have been key stressors to ecological systems over the past century. Biological proxies (e.g., pollen, tree rings) have been used to track this environmental change; however, linking these changes to the ecology of organisms remains challenging. Here, we link historical drought records to conditions of high water-stress in grassland habitats through the stable isotope analysis of California vole museum specimens (Microtus californicus). Using museum collections spanning 118-years (1891–2009), isotope values of dated hair tissues were associated with statewide drought metrics on the Palmer Drought Severity Index. We observed a positive correlation between δ¹⁵N and δ¹⁸O values and drought severity. The range in δ¹⁵N values (~ 18‰) is greater than what would be expected as a result of dietary shifts across the landscape (~ 3‰), and is likely attributed to the combined effects of physiological responses of M. californicus and isotopic shifts in plant resources with increased water-stress. Geospatial patterns in δ³⁴S values of hair tissues reflect higher baseline isotope values in coastal habitats. However, comparably high δ³⁴S values in the southern-most inland localities suggest sulfur fertilization of croplands and subsequent transfer to surrounding grassland habitats in ³⁴S enriched forms. A broad δ¹³C range (− 28.7 to − 14.3‰) further suggests the consumption of C3 and C4 plant-based dietary proteins. As shown here, stable isotope analysis of museum collections can provide a climate and land use record based on the physiological performance and ecology of a study species in a region affected intensely by anthropogenic activities.
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... 209) international con cerns within wildlife ecology, and is the subject of what is currently the longest palaeodi etary study using isotope analysis of animal tissue (Codron et al., 2012). Although this chapter is specific to African elephants, it is possible to apply the methodology and ap proach to other species and in different landscapes across the world (Fox-Dobbs et al., 2012;Jennings et al., 2002;Koch et al., 2009;Moss et al., 2006;Szpak et al., 2012). ...
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... Within the Philippines, the δ 15 N values of O. megalotis (mean: 7.04 ± 2.3‰) were ca. 2.22‰ greater than those of T. syrichta (mean: 4.82 ± 1.9‰), indicating significant 15 N-enrichment (Wilcoxon W = 239, p = 0.008; Figure 5); however, the samples from T. syrichta collected in 2010 exhibited systematically low δ 15 N values, perhaps due to recent anthropogenic changes to the landscape (e.g., Fox-Dobbs et al., 2012). When we calculated the mean of these samples, log-transformed all δ 15 N values, and controlled for specimen year in a general model, there was no statistical difference between O. megalotis and T. syrichta (t = -0.28, ...
Niche convergence suggests functionality of the nocturnal fovea
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  • Jul 2014
The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (Tarsius) and scops owls (Otus), taxa united by numerous anatomical homoplasies, including foveate vision. A functional interpretation of these homoplasies predicts dietary convergence. We tested this prediction by analyzing stable isotope ratios that integrate dietary information. In Borneo and the Philippines, the stable carbon isotope compositions of Tarsius and Otus were indistinguishable, whereas the stable nitrogen isotope composition of Otus was marginally higher than that of Tarsius. Our results indicate that species in both genera consumed mainly ground-dwelling prey. Taken together, our findings support a functional interpretation of the many homoplasies shared by tarsiers and scops owls, including a retinal fovea. We suggest that the fovea might function similarly in tarsiers and scops owls by calibrating the auditory localization pathway. The integration of auditory localization and visual fixation during prey detection and acquisition might be critical at low light levels.
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Stable isotope analysis of carnivores from the Turkana Basin, Kenya: Evidence for temporally-mixed fossil assemblages
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Stable isotope palaeoecology of fossil mammals is a key research tool for understanding the environmental context of hominin evolution in the Plio-Pleistocene of Africa. Well studied mammal groups include bovids, suids, equids, proboscideans and primates, but to date there has been no in-depth study of modern and fossil carnivores. Here we produce an Africa-wide oxygen and carbon enamel isotope dataset for modern carnivores and compare it with fossil carnivore data sampled from the Plio-Pleistocene Omo Group of the Turkana Basin, Kenya. Comparison of modern carnivore carbon isotopes with satellite images of land cover indicates that carnivore δ¹³C is related to the proportion of woody cover in the local environment. Modern carnivore oxygen isotopes are strongly influenced by the δ¹⁸O of meteoric water, through drinking from standing water and through prey body fluids. Carbon isotope data from fossil carnivores shows close agreement with palaeovegetation reconstructions from δ¹³C of palaeosol carbonates from the same geological Members, and a similar long-term trend in δ¹³C values through time (4 Ma to 1 Ma), reflecting a gradual increase in the proportion of C4 grasses in the Turkana Basin. This increase in the δ¹³C of large carnivores is consistent with the evidence from other mammalian groups for an increase in the proportion of grazers compared to browsers and mixed feeders during this time interval. Two distinct trends within oxygen versus carbon isotope space indicates that the fossil carnivores lived during two distinct climatic regimes – one in which palaeo-lake Turkana was freshwater, and one in which the lake resembled its modern-day hyperalkaline state. These two climatic states most likely represent the end-members of precessionally-driven rainfall extremes over the Ethiopian Highlands. This indicates that each studied faunal assemblage from the Omo Group is a time- and climate-averaged palimpsest; this has significant implications for the interpretation of environmental signals and community palaeoecology derived from Turkana Basin fossil mammals, including early hominins.
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Human paleoecological integration in subarctic eastern Beringia
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We contribute to the understanding of megafauna extinction and human dispersal in subarctic eastern Beringia by focusing on changes in the trophic dynamics of the large mammal community as well as the ecological role of humans as a predator and competitor. We reconstruct habitat use by megafauna and humans throughout the Pleistocene-Holocene boundary based on zooarchaeological data and stable isotope ratios of collagen. Our results are consistent with habitat heterogeneity and availability being important factors in the changing abundance of large herbivores. We argue that an increase in herbivore diversity and biomass at the beginning of the Bølling-Allerød interstadial and a relative lack of competitors favored the initial human colonization of subarctic eastern Beringia. As herbivore resources dwindled later in the Late Glacial, people increasingly relied on bison and wapiti. By efficiently extracting some of the highest-ranked resources in the landscape, people are likely to have contributed to the trophic displacement or regional extirpation of other large predators. The ecological patterns that we observe in subarctic eastern Beringia are consistent with a mixture of both top-down and bottom-up controls over biotic turnover.
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Ice-age megafauna in Arctic Alaska: Extinction, invasion, survival
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Radical restructuring of the terrestrial, large mammal fauna living in arctic Alaska occurred between 14,000 and 10,000 years ago at the end of the last ice age. Steppe bison, horse, and woolly mammoth became extinct, moose and humans invaded, while muskox and caribou persisted. The ice age megafauna was more diverse in species and possibly contained 6× more individual animals than live in the region today. Megafaunal biomass during the last ice age may have been 30× greater than present. Horse was the dominant species in terms of number of individuals. Lions, short-faced bears, wolves, and possibly grizzly bears comprised the predator/scavenger guild. The youngest mammoth so far discovered lived ca 13,800 years ago, while horses and bison persisted on the North Slope until at least 12,500 years ago during the Younger Dryas cold interval. The first people arrived on the North Slope ca 13,500 years ago. Bone-isotope measurements and foot-loading characteristics suggest megafaunal niches were segregated along a moisture gradient, with the surviving species (muskox and caribou) utilizing the warmer and moister portions of the vegetation mosaic. As the ice age ended, the moisture gradient shifted and eliminated habitats utilized by the dryland, grazing species (bison, horse, mammoth). The proximate cause for this change was regional paludification, the spread of organic soil horizons and peat. End-Pleistocene extinctions in arctic Alaska represent local, not global extinctions since the megafaunal species lost there persisted to later times elsewhere. Hunting seems unlikely as the cause of these extinctions, but it cannot be ruled out as the final blow to megafaunal populations that were already functionally extinct by the time humans arrived in the region.
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Foraging and feeding ecology of the gray wolf (Canis lupus): Lessons from Yellowstone National Park, Wyoming, USA
Conference Paper
Full-text available
  • Jul 2006
The foraging and feeding ecology of gray wolves is an essential component to understanding the role that top carnivores play in shaping the structure and function of terrestrial ecosystems. In Yellowstone National Park (YNP), predation studies on a highly visible, reintroduced population of wolves are increasing our understanding of this aspect of wolf ecology. Wolves in YNP feed primarily on elk, despite the presence of other ungulate species. Patterns of prey selection and kill rates in winter have varied seasonally each year from 1995 to 2004 and changed in recent years as the wolf population has become established. Wolves select elk based on their vulnerability as a result of age, sex, and season and therefore kill primarily calves, old cows, and bulls that have been weakened by winter, Summer scat analysis reveals an increased variety in diet compared with observed winter diets, including other ungulate species, rodents, and vegetation. Wolves in YNP hunt in packs and, upon a successful kill, share in the evisceration and consumption of highly nutritious organs first, followed by major muscle tissue, and eventually bone and hide. Wolves are adapted to a feast-or-famine foraging pattern, and YNP packs typically kill and consume an elk every 2-3 d. However, wolves in YNP have gone without fresh meat for several weeks by scavenging off old carcasses that consist mostly of bone and hide. As patterns of wolf density, prey density, weather, and vulnerability of prey change, in comparision with the conditions of the study period described here, we predict that there will also be significant changes in wolf predation patterns and feeding behavior.
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The role of ammonia volatilization in controlling the natural 15N abundance of a grazed grassland
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Although the variation in natural 15N abundance in plants and soils is well characterized, mechanisms controlling N isotopic composition of organic matter are still poorly understood. The primary goal of this study was to examine the role of NH3 volatilization from ungulate urine patches in determining 15N abundance in grassland plants and soil in Yellowstone National Park. We additionally used isotopic measurements to explore the pathways that plants in urine patches take up N. Plant, soil, and volatilized NH3d15N were measured on grassland plots for 10 days following the addition of simulated urine. Simulated urine increased 15N of roots and soil and reduced 15N of shoots. Soil enrichment was due to the volatilization of isotopically light NH3. Acid-trapped NH3d15N increased from -28‰ (day 1) to -0.3‰ (day 10), and was lighter than the original urea-N added (1.2‰). A mass balance analysis of urea-derived N assimilated by plants indicated that most of the N taken up by plants was in the form of ammonium through roots. However, isotope data also showed that shoots directly absorbed 15N – depleted NH3-N that was volatilized from simulated urine patches. These results indicate that NH3 volatilization from urine patches enriches grassland soil with 15N and shoots are a sink for volatilized NH3, which likely leads to accelerated cycling of excreted N back to herbivores.
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Ungulate vs. Landscape Control of Soil C and N Processes in Grasslands of Yellowstone National Park
Article
  • Oct 1998
Within large grassland ecosystems, climatic and topographic gradients are considered the primary controls of soil processes. Ungulates also can influence soil dynamics; however the relative contribution of large herbivores to controlling grassland soil processes remains largely unknown. In this study, we compared the effects of native migratory ungulates and variable site ('landscape') conditions, caused by combined climatic and topographic variability, on grassland of the northern winter range of Yellowstone National Park by determining soil C and N dynamics inside and outside 33-37 yr exclosures at seven diverse sites. Sites included hilltop, slope, and slope bottom positions across a climatic gradient and represented among the driest and wettest grasslands on the northern winter range. We performed two experiments: (1) a 12-mo in situ net N mineralization study and (2) a long-term (62-wk) laboratory incubation to measure potential N mineralization and microbial respiration. Results from the in situ experiment indicated that average net N mineralization among grazed plots (3.8 g N · m-2 · yr-1) was double that of fenced, ungrazed plots (1.9 g N · m-2 · yr-1). Mean grazer enhancement of net N mineralization across sites (1.9 g N · m-2 · yr-1) approached the maximum difference in net N mineralization among fenced plots (2.2 g N · m-2 · yr-1), i.e., the greatest landscape effect observed. Furthermore, ungulates substantially increased between-site variation in mineralization; grazed grassland, 1 SD = 2.2 g N · m-2 · yr-1, fenced grassland, 1 SD = 0.85 g N · m-2 · yr-1. In the long-term incubation, potential microbial respiration and net N mineralization were positively related to total soil C and N content, respectively. There was greater variation in potential respiration and net N mineralization early in the incubation, when labile material was processed, compared to late in the incubation, when more recalcitrant substrate was processed, suggesting that between-site variation in labile organic matter was greater than that of recalcitrant material. Herbivores improved the organic matter quality of soil, increasing the labile fractions and reducing the recalcitrant fractions. Grazers reduced C respired/N mineralized ratios, an index of microbial N immobilization, by an average of 21%. However, the largest landscape influence on the immobilization index was 13-fold greater than the grazer effect. Given that the greatest landscape influence on in situ net mineralization (2.2 g N · m-2 · yr-1) was similar to the average grazer impact on that rate (1.9 g N · m-2 · yr-1), we hypothesize that the landscape effect on field N availability was primarily caused by variation in microbial immobilization, while the grazing effect was primarily due to stimulation of gross mineralization. These results indicate that the relative importance of ungulates in controlling soil N cycling may be more important than previously suspected for grasslands supporting large herds of migratory ungulates, and that the dominant mechanisms underlying the landscape and ungulate influences on soil mineral fluxes may differ.
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Niche relationships within a guild of ungulate species in Yellowstone National Park, Wyoming, following release from artificial controls
Article
Niche relationships and diet overlaps were compared among elk (Cervus elaphus), bison (Bison bison), bighorn sheep (Ovis canadensis), mule deer (Odocoileus hemionus), and pronghorn antelope (Antilocapra americana) between 1967–1970 and 1986–1988, a period when total ungulate numbers nearly tripled on Yellowstone's northern range. Ungulate species ratios on Yellowstone's northern winter range during the latter period were 100 elk : 10 mule deer : 3 bison : 2 pronghorns : 1 bighorns. Elk numbers were positively correlated to bison, mule deer, and pronghorn numbers (r2 = 0.76, 0.97, and 0.48, respectively, P < 0.01). Few other changes in habitat use or habitat overlap occurred, and diets for only 2 of the 10 species pairs, elk-bighorn (Spearman's rank order coefficient (RHO) = 0.55, P < 0.05) and mule deer – pronghorn (RHO = 0.64, P < 0.05), were significantly associated with each other. Bison consumed more grass and fewer sedges, mule deer more fringed sage (Artemisia frigida) and more rabbit-brush (Chrysothamnus spp.), and bighorn sheep more grasses and fewer sedges, while pronghorns ate less saltsage (Atriplex nuttalli) but more big sagebrush (Artemisia tridentata) during 1986–1988 than during 1967–1970. Bison expanded their range and bison and bighorn sheep used a wider variety of habitats. We found little evidence of change in competitive interactions between ungulate species. A few diet and habitat overlaps increased, the opposite of the prediction from the competitive exclusion principle amongst species, suggesting that intraspecific competition was more important. Several explanations are proposed for the lack of changes in niche relationships during a period of near tripling in density of the ungulate guild.
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Spatial, Species, and Temporal Variation in the 13C/12C Ratios of C3 Plants: Implications for Palaeodiet Studies
Article
  • Jun 1999
The δ13C value of a C3plant is influenced by the species’ response to its environment, which is subject to natural changes with space and time. This paper reviews the magnitude of the resulting variations in plant δ13C values—the differences between species, and the variations at different spatial and temporal scales—with particular emphasis on studies of tree wood. Because of these variations, any attempt to estimate the absolute δ13C values of a plant food resource at a particular place and time in the past, even when based on analysis of archaeological plant remains, will be subject to uncertainties. Uncertainties due to a single factor are commonly 1 per mil, and in many cases a combination of factors will lead to uncertainties of at least 2 per mil. Many of these factors are also relevant to archaeological studies based on differences between the δ13C values of different individuals or populations of animal/humans. Where such differences are only a few per mil it may be difficult to unambiguously ascribe them to palaeodietary, rather than to palaeoenvironmental, causes.
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