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Blumstein, D. T.

Publications and source records attributed to Blumstein, D. T..

15 recordsLinked to original sources

Can urban fence lizards identify cats?

Urban habitats can serve as wildlife refuges, or as ecological traps. As global urbanization continues to increase, native prey species may experience reduced threat from natural predators that tend to avoid human-populated areas. However, such protection often comes at the expense of susceptibility to synanthropic predators, one of the most prevalent being domestic house cats (Felis catus). While cats are a known driving force of mortalities in urban wildlife, their sublethal effects remain understudied. To better understand the behavioral effects of synanthropic predators on native urban prey, we examined responses of western fence lizards (Sceloporus occidentalis) to Artificial Intelligence (AI)-generated visual stimuli of native predators (snakes) and synanthropic predators (house cats). Visual stimuli included: California striped racers (Masticophis lateralis), a native predator; domestic cats, a synanthropic mammalian predator (Felis catus); and desert cottontails (Sylvilagus audubonii), a native mammalian non-predator. We quantified lizard responses as the change in rates of looking and locomotion during and following the video presentation. Our results revealed that lizards discriminated cats from the control by looking more within the first 90 seconds following exposure. Lizards looked more across the entire 5-minute observation period following exposure to all stimulus types compared to control conditions, indicating that AI generated visual stimuli effectively elicit behavioral responses. Together, these findings indicate that urban lizards initially detect and respond to visual cues of cats, suggesting that cat-induced mortality is not a result of inability to detect such predators. Thus, cats influence urban prey not only through direct predation risk, but also changes in behavior associated with the presence of synanthropic predators.

ecology↗

Deviations from an individual's average sociality have fitness consequences

Social relationships are consequential and affect survival, longevity and reproductive success in many species. Prior studies have successfully identified the fitness consequences of variation in sociality relative to other individuals. However, we have yet to quantify the fitness consequences of social variation within an individual over time. By using a within-individual centering approach, we can identify the consequences of deviations from an individuals average sociality. This approach has not been applied to the study of animal sociality. We used 20 years of data from a population of yellow-bellied marmots (Marmota flaviventer) to understand the fitness consequences of an individuals average affiliative social network position over their lifetime, and of individuals annual deviations from their average social position. We found that an individuals deviation from its average sociality was very strongly associated with both winter and summer survival. Deviations from some average measures of sociality were also associated with the likelihood of reproducing, but not in a consistent direction. Lifetime average social network positions had limited associations with survival and reproduction. Interestingly, litter size results varied between males to females; neither lifetime averages of social network traits nor deviations from these averages were associated with litter size in females, but deviations in sociality were associated with larger numbers of weaned offspring in males. Future studies of the consequences of social relationships may benefit from the use of an individual-centering approach, and further work is required to understand the environmental and social drivers of this intra-individual adaptive plasticity. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=184 SRC="FIGDIR/small/728517v1_ufig1.gif" ALT="Figure 1"> View larger version (44K): org.highwire.dtl.DTLVardef@9203bborg.highwire.dtl.DTLVardef@33155dorg.highwire.dtl.DTLVardef@1bfac92org.highwire.dtl.DTLVardef@daab44_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LILifetime averages of social network traits are not associated with fitness C_LIO_LIAnnual deviations from lifetime average sociality improves survival and reproduction C_LIO_LIIntra-individual behavioral plasticity may be an understudied fitness driver C_LIO_LIWithin-individual centering is a useful approach for the study of animal behavior C_LI

animal behavior and cognition↗

Multilevel selection on individual and group social behaviour in the wild

The degree to which phenotypes are shaped by multilevel selection - the theoretical framework proposing natural selection occurs at more than one level of biological organisation - is a classic debate in biology. Though social behaviours are a common theoretical example for multilevel selection, it is unknown if and how multilevel selection acts on sociality in the wild. We studied the relative strength of multilevel selection on both individual behaviour and group social structure, quantified with social networks and 19 years of data from a wild, free-living mammal, the yellow-bellied marmot (Marmota flaviventer). Contextual analysis revealed multilevel selection in specific fitness and life history contexts, with selection for group social structure being just as strong, if not stronger, than individual social behaviour. We also found antagonistic multilevel selection within and between levels, potentially explaining why increased sociality is not as beneficial or heritable in this system comparatively to other social taxa. Thus, the evolutionary dynamics of hierarchal or nested biological traits should be assessed at multiple levels simultaneously to tell a more accurate and comprehensive story. Overall, we provide empirical evidence suggesting that multilevel selection acts on social relationships and structures in the wild, and provide direct evidence for a classic, unanswered question in biology.

evolutionary biology↗

Validating an Immunoassay to Measure Fecal Glucocorticoid Metabolites in Yellow-Bellied Marmots

The yellow-bellied marmot (Marmota flaviventer) study at the Rocky Mountain Biological Laboratory near Crested Butte, Colorado, USA is the worlds second longest study of free-living mammals. Quantifying physiological stress is essential for understanding their health, reproductive success, and survival in a variable environment. Historically, we used a validated radioimmunoassay (RIA) to measure fecal glucocorticoid metabolites (FGMs). Given the costs and risks of working with radioisotopes, we have shifted to a more sustainable method. Here we evaluate the suitability of two competitive enzyme-linked immunosorbent assays (ELISA) from Cayman Chemical Company (CCC) and Arbor Assays (AA) to measure corticosterone levels in FGMs. The findings revealed that the AA ELISA, unlike the CCC ELISA, consistently matched the RIA in terms of accuracy across high and low corticosterone concentrations, demonstrated superior assay parameters, showed the highest correlations with RIA results and effectively captured the annual variations in FGM concentrations, indicative of its reliability for use in longitudinal studies. We further analytically validated the usage of the AA ELISA for FGMs, confirming its efficacy without matrix effects, thus establishing its suitability for ongoing and future studies of FGMs in marmots. The transition to the AA ELISA from the RIA ensures continued data integrity while enhancing safety and environmental sustainability.

physiology↗

Urban birds become less fearful following COVID-19 reopenings

Following the COVID-19 pandemic, many people around the world stayed home, drastically altering human activity in cities. This exceptional moment provided researchers the opportunity to test how urban animals respond to human disturbance, in some cases testing fundamental questions on the mechanistic impact of urban behaviors on animal behavior. However, at the end of this "anthropause," human activity returned to cities. How might each of these strong shifts affect wildlife in the short and long term? We focused on fear response, a trait essential to tolerating urban life. We measured flight initiation distance--at both individual and population-levels--for an urban bird before, during, and after the anthropause to examine if birds experienced longer-term changes after a year of lowered human presence. Dark-eyed juncos did not change fear levels during the anthropause, but they became drastically less fearful afterwards. These surprising and counter-intuitive findings, made possible by following the behavior of individuals over time, has led to a novel understanding that fear response can be driven by plasticity, yet not habituation-like processes. The pandemic-caused changes in human activity have shown that there is great complexity in how humans modify a behavioral trait fundamental to urban tolerance in animals.

animal behavior and cognition↗

Influence of anthropogenic light on puma road crossing movement

Wildlife may be attracted or repelled by anthropogenic stimuli - by understanding these responses we gain powerful tools to modify their behavior. Anthropogenic lighting is ubiquitous but little is known about how it influences carnivores. We focused on pumas (Puma concolor) living around Los Angeles, California for which vehicular collision is an important source of mortality. We used GPS collars to track their movement around roads and combined this with ground-level and remotely sensed data of human generated nighttime light to see how that influenced activity around roads. There are multiple landscape level scales, and metrics of light relevant at each scale, that influence the perceptual landscape of wildlife and thus these different scales must be considered. We found that, at a broad spatial scale, pumas crossed roads more frequently in areas with low levels of anthropogenic light (controlling for distance to urbanization). However, while pumas crossed roads in darker parts of the landscape at a broad-landscape scale, we did not find a statistically significant relationship between puma eye-level light intensity and predicted road crossing locations. Regarding pumas and nighttime light, it appears that having dark swaths of land, at a broad spatial scale, is important. This is important for puma conservation and road design as little is currently known about wildlife movement response to nighttime light and the ideal placement for mitigation structures. Ultimately, anthropogenic light at night is a landscape aspect that needs to be better understood and integrated into conservation as the human footprint increases.

animal behavior and cognition↗

Firmicutes and Bacteroidetes explain mass gain variation in an obligate hibernator

O_LIBody condition is an important life history challenge that directly impacts individual fitness and is particularly important for hibernating animals, whose maintenance of adequate body fat and mass is essential for survival. C_LIO_LIIt is well documented that symbiotic microorganisms play a vital role in animal physiology and behaviour. Recent work demonstrates that gut microbes are associated with fat accumulation and obesity; Firmicutes is consistently associated with obesity while Bacteroidetes is associated with leanness both in humans and other animals. C_LIO_LIThe focus of most microbiome studies has been on human health or involved lab reared animals used as a model system. However, these microbes likely are important for individual fitness in wild populations and provide potential mechanistic insights into the adaptability and survival of wildlife. C_LIO_LIHere we test whether symbiotic microorganisms within the phyla of Firmicutes and Bacteroidetes are associated with summer mass gain in an exceptionally well-studied wild population of yellow-bellied marmots (Marmota flaviventer) by quantifying microbial abundance over five years of fecal samples (2015 - 2019) collected during their summer active season. C_LIO_LIResults show that marmots with higher mass gain rates have a greater abundance of Firmicutes. In contrast, higher abundance of Bacteroidetes was associated with lower mass gain rates, but only for marmots living in harsher environments. Similar patterns were found at the family level where Ruminococcaceae, a member of Firmicutes, was associated with higher mass gain rates, and Muribaculaceae, a member of Bacteroidetes, was associated with lower mass gain rates, and similarly in harsher environments. C_LIO_LIAlthough correlative, these results highlight the importance of symbiotic gut microbiota to mass gain in the wild, a trait associated with survival and fitness in many taxonomic groups. C_LI

microbiology↗

Epigenetic predictors of maximum lifespan and other life history traits in mammals

Maximum lifespan of a species is the oldest that individuals can survive, reflecting the genetic limit of longevity in an ideal environment. Here we report methylation-based models that accurately predict maximum lifespan (r=0.89), gestational time (r=0.96), and age at sexual maturity (r=0.87), using cytosine methylation patterns collected from over 12,000 samples derived from 192 mammalian species. Our epigenetic maximum lifespan predictor corroborated the extended lifespan in growth hormone receptor knockout mice and rapamycin treated mice. Across dog breeds, epigenetic maximum lifespan correlates positively with breed lifespan but negatively with breed size. Lifespan-related cytosines are located in transcriptional regulatory regions, such as bivalent chromatin promoters and polycomb-repressed regions, which were hypomethylated in long-lived species. The epigenetic estimators of maximum lifespan and other life history traits will be useful for characterizing understudied species and for identifying interventions that extend lifespan.

evolutionary biology↗

Hibernation slows epigenetic aging in yellow-bellied marmots

Species that hibernate live longer than would be expected based solely on their body size. Hibernation is characterized by long periods of metabolic suppression (torpor) interspersed by short periods of increased metabolism (arousal). The torpor-arousal cycles occur multiple times during hibernation, and it has been suggested that processes controlling the transition between torpor and arousal states cause aging suppression. Metabolic rate is also a known correlate of longevity, we thus proposed the hibernation-aging hypothesis whereby aging is suspended during hibernation. We tested this hypothesis in a well-studied population of yellow-bellied marmots (Marmota flaviventer), which spend 7-8 months per year hibernating. We used two approaches to estimate epigenetic age: the epigenetic clock and the epigenetic pacemaker. Variation in epigenetic age of 149 samples collected throughout the life of 73 females were modeled using generalized additive mixed models (GAMM), where season (cyclic cubic spline) and chronological age (cubic spline) were fixed effects. As expected, the GAMM using epigenetic ages calculated from the epigenetic pacemaker was better able to detect nonlinear patterns in epigenetic age change over time. We observed a logarithmic curve of epigenetic age with time, where the epigenetic age increased at a higher rate until females reached sexual maturity (2-years old). With respect to circannual patterns, the epigenetic age increased during the summer and essentially stalled during the winter. Our enrichment analysis of age-related CpG sites revealed pathways related to development and cell differentiation, while the season-related CpGs enriched pathways related to central carbon metabolism, immune system, and circadian clock. Taken together, our results are consistent with the hibernation-aging hypothesis and may explain the enhanced longevity in hibernators.

evolutionary biology↗

The effects of maternal social connectivity and integration on offspring survival in a marmot

In social species, maternal social relationships, in addition to direct care, impact offspring survival but much of what we know about these effects comes from studies of obligately social and cooperatively breeding species. Yellow-bellied marmots (Marmota flaviventer) are a facultatively social species whose social groups vary in composition, size, and cohesiveness. This natural variation in sociality and cooperative breeding behavior makes yellow-bellied marmots an ideal species within which to study the effects of maternal affiliative and agonistic social behavior on offspring. We used social network analysis to investigate the relationship between maternal social connectivity and integration on offspring summer and yearly survival, with the hypothesis that offspring with more affiliative mothers are more likely to survive than the offspring of more agonistic mothers. However, we found the inverse to be true: pups born to mothers who received more affiliative interactions were less likely to survive while the offspring of mothers who were more highly integrated into agonistic networks had enhanced survival. Overall, maternal social network measures were positively and negatively correlated with offspring survival, indicating that pups are influenced by their mothers social world, often in contradictory ways. Relative predation risk and colony location also mediated the effects of social relationships on pup survival. This study contributes to a small but growing body of work that demonstrates that specific attributes of sociality have specific consequences and that by adopting an attribute-focused view of sociality we are better able to understand how environmental conditions mediate the costs and benefits of sociality. Lay SummaryMaternal social relationships can impact offspring survival but much of what we know about these effects comes from studies of obligately social species. In faculatively social yellow-bellied marmots we found that pups born to mothers who received more affiliative interactions were less likely to survive while the offspring of mothers who were more highly integrated into agonistic networks had enhanced survival. Overall, pups are influenced by their mothers social world, often in contradictory ways.

animal behavior and cognition↗

Universal DNA methylation age across mammalian tissues

Aging is often perceived as a degenerative process resulting from random accrual of cellular damage over time. Despite this, age can be accurately estimated by epigenetic clocks based on DNA methylation profiles from almost any tissue of the body. Since such pan-tissue epigenetic clocks have been successfully developed for several different species, we hypothesized that one can build pan-mammalian clocks that measure age in all mammalian species. To address this, we generated data using 11,754 methylation arrays, each profiling up to 36 thousand cytosines in highly-conserved stretches of DNA, from 59 tissue-types derived from 185 mammalian species. From these methylation profiles, we constructed three age predictors, each with a single mathematical formula, termed universal pan-mammalian clocks that are accurate in estimating the age (r>0.96) of any mammalian tissue. Deviations between epigenetic age and chronological age relate to mortality risk in humans, mutations that affect the somatotropic axis in mice, and caloric restriction. We characterized specific cytosines, whose methylation levels change with age across most mammalian species. These cytosines are greatly enriched in polycomb repressive complex 2-binding sites, are located in regions that gradually lose chromatin accessibility with age and are proximal to genes that play a role in mammalian development, cancer, human obesity, and human longevity. Collectively, these results support the notion that aging is indeed evolutionarily conserved and coupled to developmental processes across all mammalian species - a notion that was long-debated without the benefit of this new compelling evidence. SUMMARYThis study identifies and characterizes evolutionarily conserved cytosines implicated in the aging process across mammals and establishes pan mammalian epigenetic clocks.

developmental biology↗

Individual variation in tolerance of human activity by urban dark-eyed juncos (Junco hyemalis).

An important goal of urban ecology is determining what differentiates urban-tolerant populations of birds from their non-urban ancestors and urban-intolerant species. One key to urban success may be reacting appropriately to human activity, and the degree to which birds view humans as threats can be quantified by their escape behavior. Understanding individual-level plasticity, however, requires the tracking of known individuals. We compared flight-initiation distances (FID) and distances fled (DF) from approaches by a human across urban and non-urban populations of individually-marked Dark-eyed Juncos (Junco hyemalis) in southern California. The urban population is more tolerant to people as evidenced by attenuated FIDs and DFs relative to non-urban birds. Although individual urban birds either habituated or sensitized to repeated approaches, there was no significant pattern at the population level. Overall, the behavioral patterns exhibited by urban juncos are more supportive of in situ evolution than either being a biased sample from an ancestral non-urban population or intrinsic behavioral plasticity that produces a uniform adjustment to urban life.

animal behavior and cognition↗

Ambient noise from ocean surf drives frequency shifts in non-passerine bird song

Effective communication in birds is often hampered by background noise, with many recent studies focusing on the effect of anthropogenic noise on passerine bird song. Continuous low-frequency natural noise is predicted to drive changes in both frequency and temporal patterning of bird vocalizations, but the extent to which these effects may also affect birds that lack vocal learning is not yet fully understood. Here we use a gradient of exposure to natural low-frequency noise to assess whether it exerts selective pressure on vocalizations in a species whose songs are innate. We tested whether three species of Pogoniulus tinkerbirds adapt their song when exposed to a source of continuous low-frequency noise from ocean surf. We show that dominant frequency increases the closer birds are to the coast in all the three species, and in line with higher noise levels, indicating that ocean surf sound may apply a selective pressure on tinkerbird songs. As a consequence, tinkerbirds adapt their songs with an increase in frequency to avoid the masking effect due to overlapping frequencies with ambient noise, therefore improving long-range communication with intended receivers. Our study provides for the first time, compelling evidence that natural ambient noise affects vocalizations in birds whose songs are developed innately. We believe that our results can also be extrapolated in the context of anthropogenic noise pollution, hence providing a baseline for the study of the effects of low-frequency ambient noise on birds that lack vocal learning. Significance StatementBirdsong is constantly under selection as it mediates key interactions such as mate attraction, competition with same-sex individuals for reproduction and competition with heterospecifics for space-related resources. Any phenomenon that interferes with communication can therefore have a profound impact on individual fitness. Passerines are more likely to avoid the masking effect of background noise because of their higher vocal flexibility. Many non-passerine species lacking such flexibility might therefore be more vulnerable to the negative effects on their fitness of exposure to low-frequency background noise. Species incapable of adapting their signals to background noise are predicted to disappear from noisy areas. Despite this, we show that species that lack song learning may show an adaptive response to natural noise which may develop over evolutionary timescales.

evolutionary biology↗

Seasonal Effects of Environmental Change on Yellow-Bellied Marmot Population Dynamics

Natural populations are exposed to seasonal variation in environmental factors that simultaneously affect several demographic rates (survival, development, reproduction). The resulting covariation in these rates determines population dynamics, but accounting for its numerous biotic and abiotic drivers is a significant challenge. Here, we use a factor-analytic approach to capture partially unobserved drivers of seasonal population dynamics. We use 40 years of individual-based demography from yellow-bellied marmots (Marmota flaviventer) to fit and project population models that account for seasonal demographic covariation using a latent variable. We show that this latent variable, by producing positive covariation among winter demographic rates, depicts a measure of environmental quality. Simultaneous, negative responses of winter survival and reproductive-status change to declining environmental quality result in a higher risk of population quasi-extinction, regardless of summer demography where recruitment takes place. We demonstrate how complex environmental processes can be summarized to understand population persistence in seasonal environments.

ecology↗

Measuring individual identity information in animal signals: Overview and performance of available identity metrics

O_LIIdentity signals have been studied for over 50 years but there is no consensus as to how to quantify individuality. While there are a variety of different metrics to quantify individual identity, or individuality, these methods remain un-validated and the relationships between them unclear. C_LIO_LIWe contrasted three univariate and four multivariate metrics (and their different computational variants) and evaluated their performance on simulated and empirical datasets. C_LIO_LIOf the metrics examined, Beechers information statistic (HS) was the best one and could easily and reliably be converted into the commonly used discrimination score (and vice versa) after accounting for the number of individuals and calls per individual in a given dataset. Although Beechers information statistic is not entirely independent of sampling parameters, this problem can be removed by reducing the number of parameters or by increasing the number of individuals. C_LIO_LIBecause it is easily calculated, has superior performance, can be used to describe single variables or signal as a whole, and because it tells us the maximum number of individuals that can be discriminated given a set of measurements, we recommend that individuality should be quantified using Beechers information statistic. C_LI

ecology↗