Past agricultural land use affects multiple facets of ungulate antipredator behavior

Antipredator behavior affects prey fitness, prey demography, and the strength of ecological interactions. Although predator-prey interactions increasingly occur in habitats that experience multiple forms of human-generated disturbance, it is unclear how different forms of disturbance might affect antipredator behavior. Fire is a contemporary disturbance that has dramatic effects on terrestrial habitats. Such habitats may have also experienced past disturbances, like agricultural land use, that leave lasting legacies on habitat structure (e.g., overstory and understory composition). It is unclear how these past and present disturbances affect the use of different antipredator behaviors, like temporal avoidance and vigilance. We examined whether variation in disturbance regimes generates differences in ungulate antipredator behavior by using cameras to measure white-tailed deer vigilance and activity time across 24 longleaf pine woodlands that vary in past land use and contemporary fire regime. Regardless of land-use history, woodlands with high fire frequencies had 4 times less vegetation cover than low-fire woodlands, generating riskier habitats for deer; however, deer responded to fire with different antipredator strategies depending on land-use history. In nonagricultural woodlands, fire affected deer activity time such that activity was nocturnal in low-fire woodlands and crepuscular in high-fire woodlands. In post-agricultural woodlands, fire affected vigilance and not activity time such that deer were more vigilant in high-fire woodlands than in low-fire woodlands. These results suggest that ungulate antipredator behavior may vary spatially depending upon past land use and contemporary fire regime, and such disturbances may generate “landscapes of fear” that persist for decades after agricultural use. --
Methods
This study was conducted at the Savannah River Site (SRS; Aiken, SC). Sites that were farmland in 1951 were classified as “post-agricultural woodlands,” and sites that were forested were classified as “nonagricultural woodlands.” The number of fires since 1991 was determined from annual fire records, and sites were characterized as low (five or less burns) or high (more than five burns) fire frequency. Sites were not burned the year of the study. At each of our 24 sites, we deployed an unbaited, motion-activated camera trap between June 8 and July 9 in 2018 for a total trapping period of 33 days. For every photo capturing deer activity during an independent foraging bout, the observer recorded the date and time, the sex of the individual, whether or not it was in a group, group size, and if the individual was foraging (1) or being vigilant (0) as a binomial variable. If the individual’s head was up in a non-feeding posture, then the photo was classified as vigilant, and if the individual’s head was down in a feeding posture, then the photo was classified as foraging. We characterized independent foraging bouts as any sequence of deer photos of the same sex captured within 30 minutes at a site. Vertical vegetation cover was measured by a single observer using a density board that estimated percent visibility across 1 x 1 foot quadrats. The density board was placed 15-m from the observer standing at the camera-trap station. The observer took four measurements (one in each cardinal direction from the station) at each site.

反捕食行为（antipredator behavior）会影响猎物适合度（prey fitness）、猎物种群动态（prey demography）以及生态相互作用的强度。尽管捕食者-猎物相互作用日益发生在遭受多种人为干扰（human-generated disturbance）的生境中，但目前尚不清楚不同类型的干扰会如何影响反捕食行为。火灾是一类对陆地生境具有显著影响的当代干扰。此类生境可能还经历过诸如农业土地利用这类过去的干扰，这些干扰会对生境结构（如林冠层与林下植被组成）留下持久遗留效应。目前仍不明晰这些过去与当前的干扰会如何影响不同反捕食行为的表达，比如时间避让与警戒行为。

我们通过相机陷阱（camera trap）在24处不同土地利用历史与当代火制度（fire regime）的长叶松林地中，测定白尾鹿（white-tailed deer）的警戒行为与活动时长，以此探究干扰制度的差异是否会导致有蹄类（ungulate）反捕食行为产生分化。无论土地利用历史如何，高火频林地的植被盖度仅为低火频林地的1/4，这为鹿类营造了风险更高的生境；然而，鹿类依据土地利用历史采取了不同的反捕食策略。在非农业林地中，火况改变了鹿类的活动时长：低火频林地中的鹿类呈夜行性活动，而高火频林地中的鹿类则转为晨昏性活动。在农后林地中，火况仅影响警戒行为而非活动时长：高火频林地中的鹿类比低火频林地中的鹿类更为警觉。上述结果表明，有蹄类的反捕食行为可能会依据过往土地利用历史与当代火制度呈现空间异质性，且此类干扰可能会在农业活动结束后的数十年间持续塑造“恐惧景观（landscapes of fear）”。

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方法
本研究于萨凡纳河站点（Savannah River Site, SRS；南卡罗来纳州艾肯市）开展。1951年为农田的样地被归类为“农后林地”，原本为森林的样地则归类为“非农业林地”。基于年度火灾记录统计1991年以来的火灾次数，将样地划分为低火频组（火灾次数≤5次）与高火频组（火灾次数>5次）。本研究开展当年未对样地进行火烧处理。在24处样地的每一处，我们均于2018年6月8日至7月9日之间部署无诱饵运动触发式相机陷阱，总监测时长为33天。

对于每一张捕捉到鹿类独立觅食回合（independent foraging bout）的照片，记录人员将标注日期与时间、个体性别、是否结群、群大小，以及该个体处于觅食（赋值为1）还是警戒状态（赋值为0）的二分类变量（binomial variable）。若个体头部抬起且处于非觅食姿态（non-feeding posture），则该照片被归类为警戒状态；若个体头部低下且处于觅食姿态（feeding posture），则归类为觅食状态。我们将独立觅食回合定义为：在同一样地内、30分钟内拍摄到的同一性别的鹿类照片序列。

垂直植被盖度由一名观测人员使用密度板（density board）进行测定，该密度板可估算1×1英尺样方（quadrat）内的可见度百分比。密度板放置于距相机监测站15米处，观测人员在每个样地的四个主方位（cardinal direction）各进行一次测量。