Functional Ecology ( IF 4.6 ) Pub Date : 2022-07-26 , DOI: 10.1111/1365-2435.14151 Kristin Denryter 1 , Mary M. Conner 2, 3 , Thomas R. Stephenson 4 , David W. German 4 , Kevin L. Monteith 5
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1 INTRODUCTION
Seasonal environments pose unique challenges to life and exert tremendous selective pressures by forcing life-history trade-offs related to differential investment in growth, reproduction and survival (Varpe et al., 2009). To balance trade-offs associated with life in seasonal environments, animals rely on adaptations (Tyler et al., 2020; Varpe, 2017) including accumulation of energy stores. Tactics for accumulating energy stores differ among species (e.g. food caching, hyperphagia, and fat accumulation), but the bioenergetic functions are similar: energy stores provide a buffer against seasonally limited energy supplies (Parker et al., 2009). Accumulation of energy stores, however, is not a ubiquitous life-history strategy and even within a single population, seasonal body fat stores can vary substantially (Cook et al., 2013; Stephenson et al., 2020). Thus, the function of body fat in the life-histories of many species may be diverse and variable relative to other aspects of life history (e.g. capital versus income breeders; Drent & Daan, 2002) and environment.
The extent to which animals can accumulate energy stores is underpinned by elements of the endogenous and exogenous nutritional environment of the animal. Endogenously, the amount of fat an animal accretes is influenced by nutritional state (i.e. level of body fat stores) and nutritional requirements (e.g. lactation, growth). Generally, skinnier animals accrete more fat over summer than fatter animals (Cook et al., 2013; Monteith et al., 2013; Smiley et al., 2022) and lactating females with elevated requirements for milk production often are less able to meet nutritional requirements, including those for fat accretion, than non-lactating animals (Cook et al., 2013; Denryter et al., 2020; Stephenson et al., 2020). The exogenous nutritional environment also exerts important constraints on fat accretion regardless of the endogenous environment of the animal. For example, quantity, quality and other aspects (e.g. plant architecture and effects on bite mass) of available food supplies determine maximum rates of energy intake (Cook et al., 2016; Denryter et al., 2020), which can be further constrained by population density, competitive interactions and predation risk (Ceacero et al., 2012; Festa-Bianchet & Jorgenson, 1998; McNamara & Houston, 1990). In environments where body fat is required seasonally for reproduction or survival, limits to acquiring energy may be catastrophic for individuals or populations, with the potential to result in substantial costs to fitness (e.g. delayed age of primiparity, reduced fertility; Cameron et al., 1993; Crête & Huot, 1993; Gerhart et al., 1996; Reimers, 1983). Thus, for populations to persist, the environment must either support levels of energy acquisition needed to satisfy nutritional requirements or animals must modify their exposure to that environment to alleviate the energy deficit.
Migration is a behavioural adaptation to seasonal environments that functions, in part, to allow animals to modify their nutritional environment. Migration allows animals to access seasonal pulses of nutrients and increase rates of energy acquisition or reduce energy expenditures by escaping deep snow (Aikens et al., 2017; Fryxell & Sinclair, 1988; Monteith et al., 2011). Migrants often face elevated risk of predation (Hebblewhite & Merrill, 2011; T. Stephenson, unpublished data), thus in partially migratory populations (i.e. wherein not all individuals migrate; Chapman et al., 2011) the decision of whether to migrate may be a function of an individual's risk tolerance for starvation versus predation. Animals with large body fat stores are well buffered against seasonal energy limitations and can choose to be risk-averse to predation. Animals with low to moderate stores of body fat face a challenging dilemma: if winter is mild, they may have enough fat to buffer against the nadir in energy intake in winter, but if winter is severe fat stores may be an insufficient buffer against undernutrition. Intermediate migratory tactics, such as vacillating migration or commuting between ranges (Cagnacci et al., 2011; Denryter, Stephenson, et al., 2021; van de Kerk et al., 2021), may alleviate this dilemma and provide a greater breadth of options to maximize survival relative to the buffer provided by fat reserves. Indeed, fat stores should be accreted and used somewhat anticipatorily to looming conditions dictated by an animal's environment (Bårdsen et al., 2011), but the requisite level of fat needed to survive may differ depending on how animals behaviorally ameliorate their environment.
Sierra Nevada bighorn sheep (Ovis canadensis sierrae; hereafter, Sierra bighorn) are exemplary for the study of interactions between energy reserves and migration. Body fat of Sierra bighorn can vary >3-fold in autumn, ranging from 8 to 26% (Stephenson et al., 2020), and Sierra bighorn have diverse migratory portfolios comprising traditional migrants, residents and vacillating migrants (Denryter, Stephenson, et al., 2021). Among Sierra bighorn, traditional migrants winter at low elevations (typically 1,500–2,700 m) where they experience little to no snow, early green up and higher risk of predation by mountain lions (Puma concolor; Conner et al., 2018; Gammons et al., 2021; Johnson et al., 2013). Residents remain on high-elevation (2700–>3500 m) ranges year-round, including during winter, and can experience substantial amounts of snow (500–1,500 cm annually; California Department of Water Resources, 2019), late green up and historically have had low risk of predation (Greene et al., 2012; Spitz et al., 2020). Vacillating migrants make multiple round trips between high and low-elevation ranges during winter, thus experiencing the full range of environmental conditions available to traditional migrants and residents, with respect to forage, snow and predation risk (Denryter, Stephenson, et al., 2021; Greene et al., 2012; Spitz et al., 2020). Differences in environmental conditions across elevational gradients thus may underpin differences in the requisite amount of body fat required for overwinter survival.
We investigated potential synergies between physiology (i.e. body fat stores) and behaviour (i.e. migratory tactics) that may contribute to fitness in seasonal environments. Using data from Sierra bighorn, we tested a set of competing hypotheses (Table 1) that aimed to explain how body fat and migratory tactic interact to affect survival in highly seasonal and variable environments. We hypothesized that body fat buffers animals against the environment, but that the buffering capacity differs relative to the environment (as dictated by migratory tactic). Regardless of migratory tactic, we predicted that large fat stores would lead to high survival because they provide a large energetic buffer. We predicted that larger stores of body fat would be required to survive as a high-elevation resident, given the harsh environmental conditions, than would be required to persist as a traditional migrant that winters at low elevation where conditions are milder and food is more predictable. Finally, we expected that survival would be highest and fat stores least influential to survival for vacillating migrants because they possess the greatest potential to mitigate their exposure to risk factors associated with predation and starvation.
| Hypothesis number | Hypothesis | Model |
|---|---|---|
| H1 | Neither body fat nor migratory tactic influence survival | S ~ base modela
a
Base model (S(sex + age)) was determined from a set of competing models including variables for sex, age, a binary variable for whether snow accumulation was above-average that winter (bigsnowyear), capture year and metapopulation unit. |
| H2 | Body fat alone influences survival | S ~ base model + sex × body fat |
| H3 | Migratory tactic alone influences survival | S ~ base model + sex × migration |
| H4 | Body fat and migratory tactic influence survival | S ~ base model + sex × body fat + sex × migration + body fat × migration |
| H5 | Body fat moderates the influence of snow on survival | S ~ base model + sex × body fat + snow × body fat |
| H6 | Migratory tactic moderates the influence of snow on survival | S ~ base model + sex × migration + snow × migration |
- a Base model (S(sex + age)) was determined from a set of competing models including variables for sex, age, a binary variable for whether snow accumulation was above-average that winter (bigsnowyear), capture year and metapopulation unit.
中文翻译：
最胖者的生存：体脂和迁移如何影响高度季节性环境中的生存
1 简介
季节性环境对生命构成了独特的挑战，并通过迫使与生长、繁殖和生存的不同投资相关的生命史权衡来施加巨大的选择压力（Varpe 等人， 2009 年）。为了平衡与季节性环境中的生命相关的权衡取舍，动物依赖于适应（Tyler 等人， 2020 年；Varpe， 2017 年），包括能量储存的积累。不同物种积累能量储存的策略不同（例如，食物缓存、食欲过盛和脂肪积累），但生物能量功能相似：能量储存为季节性有限的能量供应提供缓冲（Parker et al., 2009）。然而，能量储存的积累并不是一种普遍存在的生活史策略，即使在单一人群中，季节性体脂储存也可能有很大差异（Cook 等人， 2013 年；斯蒂芬森等人， 2020 年）。因此，身体脂肪在许多物种的生活史中的功能可能是多种多样的，并且相对于生活史的其他方面（例如资本与收入育种者；Drent & Daan, 2002）和环境而言是可变的。
动物积累能量储存的程度取决于动物的内源性和外源性营养环境。就内源性而言，动物生长的脂肪量受营养状态（即身体脂肪储存水平）和营养需求（例如泌乳、生长）的影响。一般来说，在夏季，较瘦的动物比较胖的动物增加更多的脂肪（Cook 等人， 2013 年；Monteith 等人， 2013 年；Smiley 等人， 2022 年），并且对产奶量的要求较高的哺乳期雌性通常不太能够满足营养需求。与非哺乳期动物相比，包括脂肪堆积的要求（Cook 等人， 2013 年；Denryter 等人， 2020 年；Stephenson 等人， 2020 年）。无论动物的内源性环境如何，外源性营养环境也对脂肪的增加施加了重要的限制。例如，可用食物供应的数量、质量和其他方面（例如植物结构和对咬质量的影响）决定了能量摄入的最大速率（Cook 等人， 2016 年；Denryter 等人， 2020 年），这可能会受到进一步限制种群密度、竞争相互作用和捕食风险（Ceacero 等人， 2012 年；Festa-Bianchet 和 Jorgenson， 1998 年；McNamara 和休斯顿， 1990 年）。在季节性需要体脂以进行繁殖或生存的环境中，获取能量的限制可能对个人或群体造成灾难性的影响，并有可能导致大量的健康成本（例如，推迟初产年龄、降低生育能力；Cameron 等人， 1993 年；Crete & Huot， 1993 年；Gerhart 等人， 1996 年；Reimers， 1983 年）。因此，为了使种群持续存在，环境必须要么支持满足营养需求所需的能量获取水平，要么动物必须改变它们对环境的暴露以减轻能量不足。
迁徙是对季节性环境的行为适应，其部分功能是允许动物改变其营养环境。迁徙使动物能够获得季节性的营养脉冲，并通过逃离深雪来提高能量获取率或减少能量消耗（Aikens 等人， 2017 年；Fryxell 和 Sinclair， 1988 年；Monteith 等人， 2011 年）。移民通常面临较高的捕食风险（Hebblewhite & Merrill, 2011 ; T. Stephenson, 未发表的数据），因此在部分迁徙种群中（即并非所有个体都迁移；Chapman et al., 2011) 是否迁移的决定可能取决于个人对饥饿与捕食的风险承受能力。身体脂肪储存量大的动物可以很好地抵御季节性能量限制，并且可以选择规避捕食的风险。身体脂肪储存量低到中等的动物面临着一个具有挑战性的困境：如果冬天温和，它们可能有足够的脂肪来缓冲冬季能量摄入的最低点，但如果冬天严重，脂肪储存可能不足以缓冲营养不良。中间迁移策略，例如摇摆不定的迁移或范围之间的通勤（Cagnacci 等人， 2011 年；Denryter, Stephenson 等人， 2021 年；van de Kerk 等人， 2021 年)，可以缓解这种困境并提供更广泛的选择，以相对于脂肪储备提供的缓冲最大化生存。事实上，脂肪储存应该增加，并在一定程度上预先使用动物环境所决定的迫在眉睫的条件（Bårdsen 等人， 2011 年），但生存所需的必要脂肪水平可能会有所不同，具体取决于动物如何在行为上改善其环境。
内华达山脉大角羊 ( Ovis canadensis sierrae；以下简称 Sierra bighorn) 是研究能量储备和迁移之间相互作用的典范。Sierra bighorn 的体脂在秋季变化超过 3 倍，范围从 8% 到 26%（Stephenson 等人， 2020 年），而且 Sierra bighorn 的迁徙组合多种多样，包括传统移民、居民和摇摆不定的移民（Denryter、Stephenson 等人）等人， 2021 年）。在 Sierra bighorn 中，传统移民在低海拔地区（通常为 1,500-2,700 m）过冬，那里几乎没有雪、早期的绿化和更高的山狮捕食风险（Puma concolor；Conner 等人， 2018 年；Gammons 等人） ., 2021; 约翰逊等人， 2013 年）。居民全年都处于高海拔（2700–>3500 m）范围内，包括在冬季，并且可能会经历大量降雪（每年 500–1,500 cm；加利福尼亚水资源部， 2019 年）、晚绿化和历史捕食的风险较低（Greene 等人， 2012 年；Spitz 等人， 2020 年）。摇摆不定的移民在冬季在高海拔和低海拔范围之间进行多次往返，从而体验到传统移民和居民可以使用的各种环境条件，包括草料、雪和捕食风险（Denryter、Stephenson 等人， 2021 年） ；Greene 等人， 2012 年；Spitz 等人， 2020 年）。因此，海拔梯度环境条件的差异可能会导致越冬生存所需的身体脂肪量的差异。
我们调查了生理学（即身体脂肪储存）和行为（即迁徙策略）之间的潜在协同作用，这些协同作用可能有助于季节性环境中的健康。使用 Sierra bighorn 的数据，我们测试了一组相互竞争的假设（表 1），旨在解释体脂和迁徙策略如何相互作用以影响在高度季节性和多变的环境中的生存。我们假设体脂缓冲动物对环境的影响，但缓冲能力相对于环境不同（由迁徙策略决定）。无论迁移策略如何，我们预测大量脂肪储存会导致高存活率，因为它们提供了大的能量缓冲。我们预测，考虑到恶劣的环境条件，作为高海拔居民的生存需要更多的身体脂肪，作为一个传统的移民，在低海拔地区越冬，那里的条件更温和，食物更可预测。最后，我们预计对于摇摆不定的移民来说，生存率最高，脂肪储存对生存的影响最小，因为他们拥有最大的潜力来减轻与捕食和饥饿相关的风险因素的暴露。
| 假设数 | 假设 | 模型 |
|---|---|---|
| H1 | 体脂和迁徙策略都不会影响生存 | S~基础型号a
a
基础模型 (S(sex + age)) 是从一组竞争模型中确定的，包括性别变量、年龄变量、积雪是否高于冬季（大雪年）平均水平的二元变量、捕获年份和集合种群单位。 |
| H2 | 体脂单独影响生存 | S~基础款+性别×体脂 |
| H3 | 仅迁移策略就影响生存 | S~基模+性×迁移 |
| H4 | 体脂和迁徙策略影响生存 | S~基础模型+性别×体脂+性别×迁移+体脂×迁移 |
| H5 | 体脂调节雪对生存的影响 | S~基础款+性别×体脂+雪×体脂 |
| H6 | 迁徙策略缓和了雪对生存的影响 | S~基础款+性×迁徙+雪×迁徙 |
- a 基础模型 (S(sex + age)) 是从一组竞争模型中确定的，包括性别变量、年龄变量、积雪是否高于冬季（大雪年）平均水平的二元变量、捕获年份和集合种群单位。
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