Rebecca C. Terry

On raptors and rodents: testing the ecological fidelity and spatiotemporal resolution of cave death assemblages

Abstract Natural accumulations of skeletal remains represent a valuable source of ecological data for paleontologists and neontologists alike. Use of these records requires a quantitative assessment of the degree to which potential biasing factors affect how accurately ecological information from the living community is recorded in the sedimentary record. This has been a major focus in recent years for taphonomists working with marine records, yet terrestrial systems have remained virtually unstudied—particularly communities of small-bodied taxa. Our ability to assess the potential origins and effects of postmortem bias in terrestrial skeletal assemblages (both modern and fossil) has therefore been limited. Predation is a common mechanism by which small-mammal skeletal remains are concentrated; raptors regurgitate the remains of their small-mammal prey in pellets rich in skeletal material, which accumulate below long-term roosting sites, especially in protected areas such as caves and rock shelters. Here I compare small-mammal death assemblages concentrated via owl predation at Two Ledges Chamber, a long-term owl cave roost in northwestern Nevada, with data from modern trapping surveys to evaluate (1) their ecological fidelity to the modern small-mammal community, (2) the effects of temporal variation and time-averaging (over months to centuries) on live-dead agreement, and (3) how spatial averaging affects the landscape-scale picture of the small-mammal community as reconstructed from dead remains. Despite potential obstacles to the recovery of ecological information from skeletal deposits generated via predation, I find high live-dead agreement across all ecological metrics and all temporal comparisons. I also find that the effects of time-averaging (specifically increased species richness of the death assemblage) become significant only at the century scale. Finally, I combine a mixing model approach with a principal coordinates analysis to show that the owls at Two Ledges Chamber sample from all habitats present in the immediate vicinity of the cave, producing a high-fidelity snapshot of the community that is spatially integrated at the local landscape scale.

Holocene shifts in the assembly of plant and animal communities implicate human impacts.

Understanding how ecological communities are organized and how they change through time is critical to predicting the effects of climate change. Recent work documenting the co-occurrence structure of modern communities found that most significant species pairs co-occur less frequently than would be expected by chance. However, little is known about how co-occurrence structure changes through time. Here we evaluate changes in plant and animal community organization over geological time by quantifying the co-occurrence structure of 359,896 unique taxon pairs in 80 assemblages spanning the past 300 million years. Co-occurrences of most taxon pairs were statistically random, but a significant fraction were spatially aggregated or segregated. Aggregated pairs dominated from the Carboniferous period (307 million years ago) to the early Holocene epoch (11,700 years before present), when there was a pronounced shift to more segregated pairs, a trend that continues in modern assemblages. The shift began during the Holocene and coincided with increasing human population size and the spread of agriculture in North America. Before the shift, an average of 64% of significant pairs were aggregated; after the shift, the average dropped to 37%. The organization of modern and late Holocene plant and animal assemblages differs fundamentally from that of assemblages over the past 300 million years that predate the large-scale impacts of humans. Our results suggest that the rules governing the assembly of communities have recently been changed by human activity.Understanding how ecological communities are organized and how they change through time is critical to predicting the effects of climate change. Recent work documenting the co-occurrence structure of modern communities found that most significant species pairs co-occur less frequently than would be expected by chance. However, little is known about how co-occurrence structure changes through time. Here we evaluate changes in plant and animal community organization over geological time by quantifying the co-occurrence structure of 359,896 unique taxon pairs in 80 assemblages spanning the past 300 million years. Co-occurrences of most taxon pairs were statistically random, but a significant fraction were spatially aggregated or segregated. Aggregated pairs dominated from the Carboniferous period (307 million years ago) to the early Holocene epoch (11,700 years before present), when there was a pronounced shift to more segregated pairs, a trend that continues in modern assemblages. The shift began during the Holocene and coincided with increasing human population size and the spread of agriculture in North America. Before the shift, an average of 64% of significant pairs were aggregated; after the shift, the average dropped to 37%. The organization of modern and late Holocene plant and animal assemblages differs fundamentally from that of assemblages over the past 300 million years that predate the large-scale impacts of humans. Our results suggest that the rules governing the assembly of communities have recently been changed by human activity.

Owl Pellet Taphonomy: A Preliminary Study of the Post-Regurgitation Taphonomic History of Pellets in a Temperate Forest

Abstract Owls are important contributors to the Tertiary small-vertebrate fossil record. They concentrate small-vertebrate remains by producing pellets rich in skeletal material that provide a sample of the small-vertebrate fauna of an area. A common assumption is that different predators inflict unique fragmentation and skeletal element representation signatures, thus providing a method for identifying a field assemblage as pellet derived, and possibly identifying the predator. In addition to the digestive process of pellet formation, the taphonomic history of a pellet includes the post-regurgitation processes of weathering, disintegration, transport, and burial, all of which can introduce biases into an assemblage and confound paleoecological interpretation. Analysis of a modern accumulation of small-vertebrate remains from Great Horned Owl (Bubo virginianus) pellets in a temperate forest environment on San Juan Island, Washington, reveals that fragmentation and skeletal-element representation change with residence time on the forest floor as pellets disintegrate and skeletal elements become dispersed. Matted hair initially protects the skeletal elements. As the pellet breaks down, the bones become dispersed, fragmentation of the bones increases (from 99% intact bones in intact pellets to 75% intact bones in fully dispersed pellets), and small, fragile skeletal elements are lost, resulting in a residual concentration of larger, more robust skeletal elements. The spatial distribution of skeletal elements below the roosting site follows a right-skewed, bimodal pattern. Skeletal elements are preserved in the soil to a depth of three centimeters. Post-regurgitation processes have the potential to distort the original faunal and skeletal composition of pellet-derived assemblages, thus masking any original predator-specific signatures. Actualistic taphonomic studies are necessary in order to understand how well pellet-derived assemblages capture information on local ecological and environmental conditions. This is a critical question that must be addressed to enable correction for such biases before pellet-derived assemblages are used for assessment of small-vertebrate community change and paleoenvironmental reconstruction.

Small mammal responses to environmental change: integrating past and present dynamics

Abstract Forecasting the response of species and communities to environmental change is a priority for multiple disciplines in the natural sciences. In looking toward the future, much can be learned from examining faunal response under past episodes of environmental change. Typically, retrospective approaches are limited to one spatial and temporal scale. Here, we illustrate how integrating across spatiotemporal scales can provide powerful insights into faunal response, and can inform conservation and management. To do this we compare paleontological and neontological studies on the small mammal fauna of the Great Basin. Small mammal species and their assemblages have long been recognized as indicators of ecological change and ecosystem health. We use fossil data from two long-term owl roosts to reconstruct patterns of richness and the apportioning of abundance among functional groups across multiple episodes of warming during the Holocene (last 10,000 years). We then use these findings as a climate-only baseline against which to compare changes in richness and abundance in 2 independent mountain ranges over the past century. While the past century has been marked by climate warming, the modern day Great Basin landscape also has been subject to intense human land-use practices and the introduction of nonnative plant species. Our contrast highlights that for Great Basin small mammals, modern-day land-use practices are modifying climate-based expectations.

Biodiversity and Topographic Complexity: Modern and Geohistorical Perspectives

Topographically complex regions on land and in the oceans feature hotspots of biodiversity that reflect geological influences on ecological and evolutionary processes. Over geologic time, topographic diversity gradients wax and wane over millions of years, tracking tectonic or climatic history. Topographic diversity gradients from the present day and the past can result from the generation of species by vicariance or from the accumulation of species from dispersal into a region with strong environmental gradients. Biological and geological approaches must be integrated to test alternative models of diversification along topographic gradients. Reciprocal illumination among phylogenetic, phylogeographic, ecological, paleontological, tectonic, and climatic perspectives is an emerging frontier of biogeographic research.

Modeling the Effects of Predation, Prey Cycling, and Time Averaging on Relative Abundance in Raptor-Generated Small Mammal Death Assemblages

Abstract Raptors concentrate the remains of their small mammal prey in pellets rich in skeletal material. Stratified pellet deposits beneath long-term roost sites should, therefore, represent valuable archives of Holocene faunal change. Accurate paleoecological reconstruction from such deposits, however, requires a complete assessment of factors that may bias the ecological information that such records preserve. Three factors that could bias or obscure the community structure of a small mammal death assemblage relative to the living community include: (1) short-term transient dynamics of prey populations; (2) feeding activity of the raptors; and (3) extent of time averaging represented in individual stratigraphic horizons. Here I model (1) how much summed time is necessary for a raptor-derived small mammal death assemblage to capture a long-term (centennial to millennial) signal of relative abundance; and (2) the accuracy of the relative abundance information preserved in such death assemblages given short-term (decadal) cycling of small mammal prey populations. Results generated from an empirically parameterized model of prey dynamics assuming a multi-species type III functional response of raptors to fluctuations in density of two prey species suggest that the maximum extent of time averaging necessary to capture a stable relative abundance signal in a death assemblage is ∼140 years. This estimate is highly conservative, yet still remains fine enough to analyze phenomena operating at the centennial to millennial time scales critical for addressing long-term community response to habitat transitions through the Holocene. Results also suggest that the mismatch between relative abundance information in the living community and the death assemblage is generally low (<1%), except for a few specific parameter combinations that result in the population dynamics of the prey species being extremely similar to one another.

Where does the time go?: Mixing and the depth-dependent distribution of fossil ages

Knowing how time is distributed within a fossil record is fundamental to paleobiology. Many efforts to quantify temporal resolution have estimated rates of specimen decay from the frequency distribution of specimen ages in near-surface assemblages. The implicit assumption has been that the shape of these distributions is invariant with depth and thus decay-rate estimates reflect the temporal resolution of a fossil record’s deeper layers as well. Here we present a new model that predicts how age-frequency distribution shape will change with depth due to the interplay of burial, mixing, and decay. Unlike previous models, this model distinguishes the dimensions of time, specimen age, and depth, and predicts a right-to-left shift in age-frequency distribution skewness, and a decrease in kurtosis, with increasing stratigraphic depth. We find support for these predictions with the accelerator mass spectrometry 14C dating of 80 small mammal specimens spanning the Quaternary fossil record of Homestead Cave, Utah (United States). Our study indicates (1) that previous models overestimate rates of specimen decay, (2) that the acuity of ecological information captured in near-surface assemblages is higher than previously inferred, and (3) how time-averaging can alter the apparent dynamics of biodiversity over time. We thereby offer a new quantitative framework to account for time-averaging, to merge modern and paleontological archives, and to place ecological systems within the context of their past dynamics.

Energy flow and functional compensation in Great Basin small mammals under natural and anthropogenic environmental change

Significance Small mammals play a critical role in the maintenance of desert ecosystems. Using Quaternary fossils from the Great Basin, we show that energy flow through a small mammal community during today’s heightened climate warming differs from that experienced during natural rapid warming in the past. This discrepancy highlights a modern breakdown in energetic compensation among functional groups, and stresses the importance of novel anthropogenic impacts, such as the replacement of shrublands by invasive annual grasses introduced to North American deserts more than a century ago. Use of the fossil record to untangle the effects of climate and anthropogenic habitat change on ecosystem function today is thus critical for understanding how ecosystems will respond to future environmental change. Research on the ecological impacts of environmental change has primarily focused at the species level, leaving the responses of ecosystem-level properties like energy flow poorly understood. This is especially so over millennial timescales inaccessible to direct observation. Here we examine how energy flow within a Great Basin small mammal community responded to climate-driven environmental change during the past 12,800 y, and use this baseline to evaluate responses observed during the past century. Our analyses reveal marked stability in energy flow during rapid climatic warming at the terminal Pleistocene despite dramatic turnover in the distribution of mammalian body sizes and habitat-associated functional groups. Functional group turnover was strongly correlated with climate-driven changes in regional vegetation, with climate and vegetation change preceding energetic shifts in the small mammal community. In contrast, the past century has witnessed a substantial reduction in energy flow caused by an increase in energetic dominance of small-bodied species with an affinity for closed grass habitats. This suggests that modern changes in land cover caused by anthropogenic activities—particularly the spread of nonnative annual grasslands—has led to a breakdown in the compensatory dynamics of energy flow. Human activities are thus modifying the small mammal community in ways that differ from climate-driven expectations, resulting in an energetically novel ecosystem. Our study illustrates the need to integrate across ecological and temporal scales to provide robust insights for long-term conservation and management.

A trait-based framework for discerning drivers of species co-occurrence across heterogeneous landscapes

Null model analysis of species co-occurrence patterns has long been used to gain insight into community assembly but is often limited to identifying non-random patterns without providing clarity about underlying ecological mechanisms. This challenge is especially apparent when sampling units are spread across a heterogeneous landscape or along an environmental gradient because multiple mechanisms can produce similar co-occurrence patterns. We developed a trait-based approach for discriminating between environmental filtering and biotic interactions as the probable driver of cooccurrence patterns across environmentally heterogeneous sites. We demonstrate our framework by analyzing the co-occurrence of small mammals over elevation in three independent mountain ranges in the Great Basin of the western United States. Our sampling design accounts for landscape scale environmental variability and within-site habitat heterogeneity. We identified 52 non-random species pairs, of which 36 were aggregated and 16 were segregated. For each pair, we determined which mechanism was the likely ecological explanation using a hypothesis-testing framework based on functional trait similarity. Expectations of biotic interactions were based on similarity of diet and body size whereas habitat affinity and geographic range were used for environmental filtering. Only four pairs were consistent with expectations under biotic interactions, including pairs for which competitive exclusion has previously been documented. In addition to analyzing individual pairs, we used binomial tests of observed versus expected totals of intraand inter-guild pairs to determine assemblage-wide deviations from random community structure. Signatures of environmental filtering were consistent across mountain ranges and scales. Despite differences in species composition and significant pairs among data sets, our approach revealed consistent mechanistic conclusions, emphasizing the value of trait-based methods to co-occurrence and community assembly.

How specialized is a diet specialist? Niche flexibility and local persistence through time of the Chisel-toothed kangaroo rat

ummary Rapid environmental changes are putting many species at risk, particularly niche specialists. In response, species can shift their ranges, or remain in place by taking advantage of new resources. The potential for specialists to undergo in situ niche shifts is not well understood yet can buffer species from the effects of long-term environmental change over centuries and millennia. In the Great Basin of western North America, the Chisel-toothed kangaroo rat, Dipodomys microps, is a folivore thought to be an obligate specialist on the desert shrub Atriplex confertifolia. Because of its association with A. confertifolia, D. microps is presumed to have tracked the shrub as it moved south during the last glacial maximum. However, recent phylogeographic evidence indicates that D. microps did not shift or contract its range into a southern refugium. Here we evaluate the role that niche flexibility may have played in allowing this presumed dietary specialist to cope with a changing environment and resource base. We do so using carbon and nitrogen isotopes measured in D. microps bone collagen from modern and fossil specimens spanning the last 8,000 years at Two Ledges Chamber (TLC) in northwestern Nevada. δ13C values indicates that, contrary to expectation, the population of D. microps at TLC consumes a variety of plants other than A. confertifolia, an isotopically distinct C4 shrub, and has done so for millennia. Mixing models suggest that the proportion of C4 in the diet was highest (˜35%) in the middle Holocene, and has declined towards the recent, especially over the last 30 years. δ15N values are consistently elevated through time suggesting that D. microps at TLC are potentially also consuming a high proportion of insects. Our results indicate that this population of dietary specialists has greater niche flexibility than previously assumed. This implies that, at the species level, even presumed niche specialists may be capable of undergoing niche shifts over centennial to millennial time scales in response to changing environmental conditions, and highlights the unique role that historical and paleontological data can play in establishing resource-use baselines of the past. This article is protected by copyright. All rights reserved.