Variation In Phenological Responses Research Articles

Climate Adaptation in White Oak (Quercus alba, L.): A Forty-Year Study of Growth and Phenology

Climate change poses a significant threat to the resilience and sustainability of forest ecosystems. This study examines the performance of white oak (Quercus alba, L.) across a range of provenances in a common garden planting, focusing on the species’ response to climatic variables and the potential role of assisted migration in forest management. We evaluated the survival and growth rates of white oak provenances originating from various points along a latitudinal gradient over a period of 40 years. These provenances were planted in a common garden situated near the midpoint of this latitudinal gradient, where we also monitored their phenological traits, such as budburst and leaf senescence. The results revealed substantial variation in phenological responses and growth patterns among the provenances, with southern provenances demonstrating faster growth and later senescence relative to local sources, with limited impact on survival. In contrast, the northern provenances demonstrated slower growth, resulting in later-aged competition-induced mortality. The findings highlight the necessity of incorporating genetic diversity into white oak reforestation and conservation strategies, as the local provenance may no longer be the most suitable option for current and future conditions. We advocate for a nuanced approach to forest management that leverages genetic insights to optimize seed source selection for reforestation, fostering resilient forest landscapes in the face of ongoing climate shifts.

Sex-dependent phenological responses to climate vary across species' ranges.

Anthropogenic climate change has significantly altered the flowering times (i.e., phenology) of plants worldwide, affecting their reproduction, survival, and interactions. Recent studies utilizing herbarium specimens have uncovered significant intra- and inter-specific variation in flowering phenology and its response to changes in climate but have mostly been limited to animal-pollinated species. Thus, despite their economic and ecological importance, variation in phenological responses to climate remain largely unexplored among and within wind-pollinated dioecious species and across their sexes. Using both herbarium specimens and volunteer observations of cottonwood (Populus) species, we examined how phenological sensitivity to climate varies across species, their ranges, sexes, and phenophases. The timing of flowering varied significantly across and within species, as did their sensitivity to spring temperature. In particular, male flowering generally happened earlier in the season and was more sensitive to warming than female flowering. Further, the onset of flowering was more sensitive to changes in temperature than leaf out. Increased temporal gaps between male and female flowering time and between the first open flower date and leaf out date were predicted for the future under two climate change scenarios. These shifts will impact the efficacy of sexual reproduction and gene flow among species. Our study demonstrates significant inter- and intra-specific variation in phenology and its responses to environmental cues, across species' ranges, phenophases, and sex, in wind-pollinated species. These variations need to be considered to predict accurately the effects of climate change and assess their ecological and evolutionary consequences.

Shifts in competitive structures can drive variation in species' phenology.

For many species, a well documented response to anthropogenic climate change is a shift in various aspects of its life history, including its timing or phenology. Often, these phenological shifts are associated with changes in abiotic factors used as proxies for resource availability or other suitable conditions. Resource availability, however, can also be impacted by competition, but the impact of competition on phenology is less studied than abiotic drivers. We fit generalized additive models (GAMs) to a long-term experimental dataset on small mammals monitored in the southwestern United States and show that altered competitive landscapes can drive shifts in breeding timing and prevalence, and that, relative to a dominant competitor, other species exhibit less specific responses to environmental factors. These results suggest that plasticity of phenological responses, which is often described in the context of annual variation in abiotic factors, can occur in response to biotic context as well. Variation in phenological responses under different biotic conditions shown here further demonstrates that a more nuanced understanding of shifting biotic interactions is useful to better understand and predict biodiversity patterns in a changing world.

Seasonal variability in the effect of temperature on key phenological stages of four table grapes cultivars.

Progressive warming of the grape growing regions has reduced the land capability for sustainable grapevine production and the geographical distribution of grapes. Bud burst, blooming, berry set, veraison, and harvest are the key phenological stages of grapevine, and are crucial for managing vineyard activities. The objective of this study was to evaluate the effect of seasonal temperature variability on the timing of key phenological stages of table grape cultivars in a new emerging viticulture region, i.e., the Pothwar region of Pakistan. Phenological stages of four table grape cultivars were recorded during two consecutive growing seasons at two locations. All phenological stages were attained earlier for the relatively warmer location, i.e., Chakwal. Similarly, the length of the growing season from bud burst to harvest was 15 to 21days longer for the 2020 growing season than for the 2019 growing season, which corresponds to the inter-annual temperature variability. Moreover, the grapevine cultivars showed a distinct response for each growth phase; cv. Perlette matured earlier while cv. NARC Black was the last to ripen. Despite the large variability in the length of the active growing period from bud burst to harvest, accumulated growing degree days (GDD) varied only in a narrow range, i.e., 1510-1557 for cv. Perlette, 1641-1683 for cv. King's Ruby, 1744-1770 for cv. Sugraone, and 1869-1906 for cv. NARC Black. This implies that seasonal temperature variability using GDD is a better indicator for the phenology of table grape cultivars compared to regular time. It is clear from the results from this study that the variation in phenological responses of table grape cultivars due to temperature differences necessitates genotype and site-specific vineyard management.

The ecological implications of intra- and inter-species variation in phenological sensitivity.

Plant-pollinator mutualisms rely upon the synchrony of interacting taxa. Climate change can disrupt this synchrony as phenological responses to climate vary within and across species. However, intra- and interspecific variation in phenological responses is seldom considered simultaneously, limiting our understanding of climate change impacts on interactions among taxa across their ranges. We investigated how variation in phenological sensitivity to climate can alter ecological interactions simultaneously within and among species using natural history collections and citizen science data. We focus on a unique system, comprising a wide-ranged spring ephemeral with varying color morphs (Claytonia virginica) and its specialist bee pollinator (Andrena erigeniae). We found strongly opposing trends in the phenological sensitivities of plants vs their pollinators. Flowering phenology was more sensitive to temperature in warmer regions, whereas bee phenology was more responsive in colder regions. Phenological sensitivity varied across flower color morphs. Temporal synchrony between flowering and pollinator activity was predicted to change heterogeneously across the species' ranges in the future. Our work demonstrates the complexity and fragility of ecological interactions in time and the necessity of incorporating variation in phenological responses across multiple axes to understand how such interactions will change in the future.

Integrating microclimatic variation in phenological responses to climate change: A 28‐year study in a hibernating mammal

AbstractPhenological shifts associated with directional changes in climate, resulting in earlier spring activities, have been documented in several animal species. However, the extent to which species respond to overall climate change versus local climate variation is rarely studied. In addition, climate data are usually averaged over large spatial scales, even though local heterogeneity in habitats may be high, and species might be more susceptible to changes in local rather than global climate conditions. In this study, we examined the effects of spatiotemporal climate variation and climate change on the phenology of a hibernating mountain rodent, the Columbian ground squirrel (Urocitellus columbianus). Over 28 years of research (1992–2019), we studied the relationship between the microclimatic conditions experienced by adult and juvenile ground squirrels from four neighboring meadows, and their dates of emergence from hibernation. We used a microclimate model to calculate microclimate variables (local snow depth, soil temperature, air temperature, wind speed, and humidity) at an hourly scale, a 5‐m spatial resolution, and at animal height on the study sites over 28 years. Emergence dates varied with age and sex, among years, as well as among and within meadows, with some areas averaging up to 10 days earlier emergence dates from hibernation than others. While emergence dates tended to be delayed throughout the study period, long‐term temporal changes and interannual variability in emergence dates differed among meadows and depended on individual age and sex. Dates of hibernation emergence were correlated with local climate variables considered either during hibernation or during the preceding summer. Ground squirrels emerged earlier in years or at locations when/where snow melted earlier (years: all individuals excluding 2‐year‐old males, locations: yearlings and older females), and when the previous summer was less windy (≥3‐year‐old individuals) and more humid (2‐year‐old males). Two‐year‐old male ground squirrels also emerged later in locations where snow depth during winter was higher. Using a microclimate model allowed realistic predictions of phenological responses to climate, highlighting its potential for research on animal responses to abiotic change.

Flowering phenology of a widespread perennial herb shows contrasting responses to global warming between humid and non‐humid regions

Abstract Plant phenology was assessed as one of the most key Essential Biodiversity Variables on species functional traits, which underpins a variety of aspects of ecosystem function and is a vital determinant of species distribution. Flowering phenology is one of the most sensitive indicators of the effects of recent climatic change. Understanding of intraspecific variation in phenological responses to climate change can contribute to the accurate prediction of phenology and the assessment of potential impacts of climate change on organisms. However, this intraspecific variation in phenological sensitivity in natural systems is still unclear, especially at large spatial scales. Using the widespread perennial herb Spiranthes sinensis, we quantified intraspecific variation in phenological responses to warming among groups located along climatic gradients. Phenological data were derived from 1,681 collections of herbarium specimens and photographs across eastern Asia and southeastern Australia over the period 1902–2017 and spans eight humid and eight non‐humid regions. We found that peak flowering dates of Spiranthe sinensis (FLss) showed substantial intraspecific variation in temperature sensitivity, ranging from −5.16 ± 1.13 to 4.16 ± 0.90 days/°C. Across all 16 regions, FLss exhibited the strongest delayed response to warming in southeastern Australia. Temperature sensitivity of the FLss was significantly correlated with annual precipitation and aridity index of a region, suggesting a possible role of declined water availability in reducing temperature sensitivity. Notably, contrasting phenological responses to warming were found between collections with different humidity regimes: humid regions generally flowered earlier (M: −3.57 days/°C) and non‐humid regions exhibited slightly delayed flowering (M: 1.25 days/°C). These findings provide empirical evidence of substantial intraspecific variation in phenological sensitivity across large spatial scales, and highlights that soil water availability may play a key role in a warming planet, especially in non‐humid regions.

Chronicles of nature calendar, a long-term and large-scale multitaxon database on phenology

We present an extensive, large-scale, long-term and multitaxon database on phenological and climatic variation, involving 506,186 observation dates acquired in 471 localities in Russian Federation, Ukraine, Uzbekistan, Belarus and Kyrgyzstan. The data cover the period 1890–2018, with 96% of the data being from 1960 onwards. The database is rich in plants, birds and climatic events, but also includes insects, amphibians, reptiles and fungi. The database includes multiple events per species, such as the onset days of leaf unfolding and leaf fall for plants, and the days for first spring and last autumn occurrences for birds. The data were acquired using standardized methods by permanent staff of national parks and nature reserves (87% of the data) and members of a phenological observation network (13% of the data). The database is valuable for exploring how species respond in their phenology to climate change. Large-scale analyses of spatial variation in phenological response can help to better predict the consequences of species and community responses to climate change.

Adaptive individual variation in phenological responses to perceived predation levels

The adaptive evolution of timing of breeding (a component of phenology) in response to environmental change requires individual variation in phenotypic plasticity for selection to act upon. A major question is what processes generate this variation. Here we apply multi-year manipulations of perceived predation levels (PPL) in an avian predator-prey system, identifying phenotypic plasticity in phenology as a key component of alternative behavioral strategies with equal fitness payoffs. We show that under low-PPL, faster (versus slower) exploring birds breed late (versus early); the pattern is reversed under high-PPL, with breeding synchrony decreasing in conjunction. Timing of breeding affects reproductive success, yet behavioral types have equal fitness. The existence of alternative behavioral strategies thus explains variation in phenology and plasticity in reproductive behavior, which has implications for evolution in response to anthropogenic change.

Local environment, not local adaptation, drives leaf-out phenology in common gardens along an elevational gradient in Acadia National Park, Maine.

Climate-driven changes in phenology are substantially affecting ecological relationships and ecosystem processes. The role of variation among species has received particular attention; for example, variation among species' phenological responses to climate can disrupt trophic interactions and can influence plant performance. Variation within species in phenological responses to climate, however, has received much less attention, despite its potential role in ecological interactions and local adaptation to climate change. We constructed three common gardens across an elevation gradient on Cadillac Mountain in Acadia National Park, Maine, to test population-level responses in leaf-out phenology in a reciprocal transplant experiment. The experiment included three native species: low bush blueberry (Vaccinium angustifolium), sheep's laurel (Kalmia angustifolia), and three-toothed cinquefoil (Sibbaldiopsis tridentata). Evidence for local adaptation of phenological response to temperature varied among the species, but was weak for all three. Rather, variation in phenological response to temperature appeared to be driven by local microclimate at each garden site and year-to-year variation in temperature. Population-level adaptations in leaf-out phenology appear to be relatively unimportant for these species in Acadia National Park, perhaps a reflection of strong genetic mixing across elevations, or weak differences in selection on phenological response to spring temperatures at different elevations. These results concur with other observational data in Acadia and highlight the utility of experimental approaches to understand the importance of annual and local site variation in affecting phenology both among and within plant species.

Spatio-temporal variation in phenological response of citrus to climate change in Iran: 1960–2010

Recent studies investigating floral and faunal phenological responses to climate change have highlighted the extent to which these relationships are species and location specific. This study investigates temporal responses of citrus peak flowering to climate change in the cities of Kerman, Shiraz and Gorgan, Iran. Phenological data comprise peak flowering dates of five citrus types: orange, tangerine, sweet lemon, sour lemon and sour orange, collected daily from government heritage gardens located within each of the cities over the period 1960–2010. For the same period, daily Tmax, Tmin and rainfall data were acquired from the Iranian Meteorological Organization. Time trend analyses were undertaken for both the phenological and meteorological data, followed by linear regression to determine the nature and extent of relationships between these variables. We find that the mean peak flowering dates, and their long-term trends over the 51-year period, are similar across the five citrus types within each city, but demonstrate significant differences between cities. Flowering date advances of 0.12–0.17d/yr are recorded for Kerman, and more rapid advances of 0.56–0.65d/yr for Shiraz. Notably, progressive delays in flowering dates occur in Gorgan (0.05–0.1d/yr). The peak flowering dates in the former two cities demonstrate strong relationships with mean annual Tmin, ranging from r=0.47–0.61 (p=0.0045; p<0.0001) for Kerman to r=0.53–0.67 (p=0.0386; p<0.0001) for Shiraz, and equate to peak flowering advances of 3.15–3.39d/°C and 4.34–5.47d/°C, respectively. By contrast, the strongest relationships between peak flowering dates and annual climate in Gorgan are with rainfall (r=0.02–0.3, p=0.8874; p=0.0528), indicating a weak phenophase response of 0.01d/mm. For Gorgan, the strongest relationships (r=0.43–075, p=0.0002 to p<0.0001) are between peak flowering date and mean Tmax for May, the month during which peak flowering occurs, with a delay in flowering of 1.26–1.86d/°C cooling. This suggests a relatively more influential climatic role directly preceding peak flowering, which may be associated with anomalous cooling in May. However, Kerman and Shiraz demonstrate more consistent strength in correlation between peak flowering and climate variables across the months of the year, with only slight peaks for the months flanking peak flowering. Our study highlights the importance of considering location-specific phenophase shifts within given regions, as dissimilar trends may occur within a country; this has important implications for future agricultural planning and fruit crop supply to local and international markets.

Back to the future for plant phenology research.

Back to the future for plant phenology research.

Warming-induced shift in European mushroom fruiting phenology.

In terrestrial ecosystems, fungi are the major agents of decomposition processes and nutrient cycling and of plant nutrient uptake. Hence, they have a vital impact on ecosystem processes and the terrestrial carbon cycle. Changes in productivity and phenology of fungal fruit bodies can give clues to changes in fungal activity, but understanding these changes in relation to a changing climate is a pending challenge among ecologists. Here we report on phenological changes in fungal fruiting in Europe over the past four decades. Analyses of 746,297 dated and geo-referenced mushroom records of 486 autumnal fruiting species from Austria, Norway, Switzerland, and the United Kingdom revealed a widening of the annual fruiting season in all countries during the period 1970-2007. The mean annual day of fruiting has become later in all countries. However, the interspecific variation in phenological responses was high. Most species moved toward a later ending of their annual fruiting period, a trend that was particularly strong in the United Kingdom, which may reflect regional variation in climate change and its effects. Fruiting of both saprotrophic and mycorrhizal fungi now continues later in the year, but mycorrhizal fungi generally have a more compressed season than saprotrophs. This difference is probably due to the fruiting of mycorrhizal fungi partly depending on cues from the host plant. Extension of the European fungal fruiting season parallels an extended vegetation season in Europe. Changes in fruiting phenology imply changes in mycelia activity, with implications for ecosystem function.

Game theory sheds new light on ecological responses to current climate change when phenology is historically mismatched

Phenological changes are well documented biological effects of current climate change but their adaptive value and demographic consequences are poorly known. Game theoretical models have shown that deviating from the fitness-maximising phenology can be evolutionary stable under frequency-dependent selection. We study eco-evolutionary responses to climate change when the historical phenology is mismatched in this way. For illustration we model adaptation of arrival dates in migratory birds that compete for territories at their breeding grounds. We simulate climate change by shifting the timing and the length of the favourable season for breeding. We show that initial trends in changes of population densities can be either reinforced or counteracted during the ensuing evolutionary adaptation. We find in total seven qualitatively different population trajectories during the transition to a new evolutionary equilibrium. This surprising diversity of eco-evolutionary responses provides adaptive explanations to the observed variation in phenological responses to recent climate change.

Spatiotemporal Variation in Avian Migration Phenology: Citizen Science Reveals Effects of Climate Change

A growing number of studies have documented shifts in avian migratory phenology in response to climate change, and yet there is a large amount of unexplained variation in the magnitude of those responses across species and geographic regions. We use a database of citizen science bird observations to explore spatiotemporal variation in mean arrival dates across an unprecedented geographic extent for 18 common species in North America over the past decade, relating arrival dates to mean minimum spring temperature. Across all species and geographic locations, species shifted arrival dates 0.8 days earlier for every °C of warming of spring temperature, but it was common for some species in some locations to shift as much as 3–6 days earlier per °C. Species that advanced arrival dates the earliest in response to warming were those that migrate more slowly, short distance migrants, and species with broader climatic niches. These three variables explained 63% of the interspecific variation in phenological response. We also identify a latitudinal gradient in the average strength of phenological response, with species shifting arrival earlier at southern latitudes than northern latitudes for the same degree of warming. This observation is consistent with the idea that species must be more phenologically sensitive in less seasonal environments to maintain the same degree of precision in phenological timing.

Genetic diversity increases regional variation in phenological dates in response to climate change

AbstractClimate change is inducing changes in the phenological timings of organisms. Genetic diversity could influence phenological responses to climate change, but empirical evidence is very limited. We estimated the regional variation across Japan in flowering and leaf budburst dates of plants based on a dataset of phenological timings from 1953 to 2005. The observed plants' genetic diversities varied according to human cultivation. The within‐species variations of phenological response to temperature as well as regional variations were less in the plant populations with lower genetic diversity. Thus, genetic diversity influences the variation in phenological responses of plant populations. Under increased temperatures, low variation in phenological responses may allow drastic changes in the phenology of plant populations with synchronized phenological timings. Our findings indicate that we should pay attention to maintaining genetic diversity of populations to alleviate changes in phenology due to future climate change.

Hepatotoxicity Associated with Etanercept in Psoriatic Arthritis

<h3>Abstract</h3> Climate change has induced pronounced shifts in the reproductive phenology of plants, with the timing of first flowering advancing in most species. Indeed, population persistence may be threatened by the inability to track climate change phenologically. Nevertheless, substantial variation exists in biological responses to climate change across taxa. Here, we explore the consequences of climate change for flowering phenology by integrating data from a long-term observational study and a manipulative experiment under contemporary conditions. Dissecting the environmental factors that influence phenological change will illuminate why interspecific variation exists in responses to climate change. We examine a 43-year record of first flowering for six species in subalpine meadows of Colorado in conjunction with a 3-year snow manipulation experiment on the perennial mustard <i>Boechera stricta</i> from the same site. We analyze shifts in the onset of flowering in relation to environmental drivers known to influence phenology: the timing of snowmelt, the accumulation of growing degree days, and photoperiod. At our study site, climate change is reducing snowpack and advancing the timing of spring snowmelt. We found that variation in phenological responses to climate change depended on the sequence in which species flowered, with early-flowering species flowering faster, at a lower heat sum, and under increasingly disparate photoperiods in comparison to species that flower later in the season. Furthermore, climate change is outpacing phenological change for all species. Early snow removal treatments confirm that the timing of snowmelt governs observed trends in flowering phenology of <i>B. stricta</i> and that climate change can reduce the probability of flowering, thereby depressing fitness. Shorter-term studies would not have captured the trends that we document in our observational and experimental datasets. Accurate predictions of the biological responses to climate change require a thorough understanding of the specific environmental factors driving shifts in phenology.

Impacts of experimental warming and fire on phenology of subalpine open-heath species

The present study examined experimentally the phenological responses of a range of plant species to rises in temperature. We used the climate-change field protocol of the International Tundra Experiment (ITEX), which measures plant responses to warming of 1 to 2°C inside small open-topped chambers. The field study was established on the Bogong High Plains, Australia, in subalpine open heathlands; the most common treeless plant community on the Bogong High Plains. The study included areas burnt by fire in 2003, and therefore considers the interactive effects of warming and fire, which have rarely been studied in high mountain environments. From November 2003 to March 2006, various phenological phases were monitored inside and outside chambers during the snow-free periods. Warming resulted in earlier occurrence of key phenological events in 7 of the 14 species studied. Burning altered phenology in 9 of 10 species studied, with both earlier and later phenological changes depending on the species. There were no common phenological responses to warming or burning among species of the same family, growth form or flowering type (i.e. early or late-flowering species), when all phenological events were examined. The proportion of plants that formed flower buds was influenced by fire in half of the species studied. The findings support previous findings of ITEX and other warming experiments; that is, species respond individualistically to experimental warming. The inter-year variation in phenological response, the idiosyncratic nature of the responses to experimental warming among species, and an inherent resilience to fire, may result in community resilience to short-term climate change. In the first 3 years of experimental warming, phenological responses do not appear to be driving community-level change. Our findings emphasise the value of examining multiple species in climate-change studies.

Adaptive responses of wild mungbean (Vigna radiata ssp. sublobata) to photo-thermal environment. I. Phenology

The phenology of 11 diverse accessions of wild mungbean was observed under natural and artificial photoperiod–temperature conditions, in order to examine whether genotypic differences might be attributed to adaptive responses to photo-thermal conditions. There was large variation in phenological response among accessions and across environments, much of which was due to differences in the duration of the pre-flowering phase. Accessions that flowered earlier tended to flower for longer, apart from 2 earlier flowering, inland Australian lines that were also earlier maturing. The patterns of response in time from sowing to flowering over environment were consistent with quantitative short-day photoperiodic adaptation, a conclusion supported by the effects of artificial day-length extension and by ‘goodness of fit’ of the observed responses to standard models relating rate of development to photoperiod and temperature. The fitted models indicated that rate of development towards flowering was hastened by warmer temperatures, and delayed by longer day lengths, with differential sensitivity between accessions to both factors. The models also suggested that photoperiod was more important for accessions collected closer to the equator, which were generally later flowering as a consequence. Conversely, temperature was relatively more important in lines from higher latitudes. Modelling also suggested that the period from first flowering to maturity was sensitive to photoperiod and temperature. Again, longer days appeared to prolong growth and delay maturity. However, cooler temperatures accelerated rather than slowed maturity, by suppressing further vegetative growth. The variation observed indicated that there is considerable scope for using the wild population to broaden the adaptation of cultivated mungbean. In particular, the unusual response of a late-flowering, photoperiod-insensitive accession warrants further study to establish whether the wild population contains a unique ‘long juvenile’ trait analogous to that being used for improving phenological adaptation in soybean.

The Storing Habit of the Columbian Ground Squirrel

Previous articleNext article FreeThe Storing Habit of the Columbian Ground SquirrelWilliam T. ShawWilliam T. Shaw Search for more articles by this author PDFPDF PLUS Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 60, Number 669Jul. - Aug., 1926 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/280108 Views: 4Total views on this site Citations: 4Citations are reported from Crossref PDF download Crossref reports the following articles citing this article:Anouch Tamian, Vincent A. Viblanc, F. Stephen Dobson, Peter Neuhaus, Tracey L. Hammer, Anna P. Nesterova, Shirley Raveh, Amy L. Skibiel, David Broussard, Theodore G. Manno, Nandini Rajamani, Claire Saraux Integrating microclimatic variation in phenological responses to climate change: A 28‐year study in a hibernating mammal, Ecosphere 13, no.55 (May 2022).https://doi.org/10.1002/ecs2.4059Anna Strauss, Ilse E. Hoffmann, Hanna Vielgrader, Eva Millesi Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation, Acta Theriologica 53, no.11 (Mar 2008): 47–56.https://doi.org/10.1007/BF03194278B. Livoreil, C. Baudoin Differences in food hoarding behaviour in two species of ground squirrels Spermophilus tridecemlineatus and S. spilosoma, Ethology Ecology & Evolution 8, no.22 (May 2010): 199–205.https://doi.org/10.1080/08927014.1996.9522929Gail R. Michener Sexual differences in over-winter torpor patterns of Richardson's ground squirrels in natural hibernacula, Oecologia 89, no.33 (Mar 1992): 397–406.https://doi.org/10.1007/BF00317418