Collaborative Research: Using herbivore kairomones to assess short-term and legacy risk responses in the early life stages of long-lived woody plants

即使植物不能移动，它们对食草动物也绝非毫无防备。虽然探索植物如何保护自己的研究主要集中在植物对食草动物攻击的反应中发生的防御变化，但最近有研究表明，植物甚至在攻击开始之前就可以探测到食草动物的信号并做出反应（称为“kairomones”）。蜗牛和蛞蝓是食草动物，它们会攻击种子和幼苗，它们的粘液会引发幼苗的防御反应，帮助植物在随后受到蛞蝓或其他食草动物的攻击后存活下来。这种防御措施可能对糖枫树的幼苗尤其重要，糖枫树是美国东北部的一种标志性树木，对整个范围内正在下降的枫糖工业至关重要。一种入侵的蛞蝓，暗翼龙，对新发芽的糖枫幼苗构成了主要威胁；该项目研究了这种鼻涕虫的粘液如何影响糖枫从幼苗到树苗的抗草食防御。它还评估了早期接触粘液是否有助于保护糖枫免受后来到达的食草动物的侵害，这些食草动物包括舞毒蛾和白尾鹿。该项目还资助了罗德岛州的科学和数学研究性学习（SMILE）项目，这是一个以课堂为基础的组织，与4-12年级的孩子一起工作，以增加高中毕业后准备进入高等教育并从事STEM职业的教育劣势学生的数量。学生与项目科学家一起进行实地和课堂体验，采用探究式学习来揭示生态原理并探索当地生态系统。尽管有大量的研究探索了植物在食草动物攻击期间和之后的防御诱导，但对于植物是否以及如何利用攻击前的线索，如kairomones（食草动物释放的化学物质，与攻击无关，被植物检测到，因此对植物有益）来先发制人地诱导防御，人们知之甚少。草食性激素最近在多个系统中被证实；鼻涕虫/蜗牛黏液是一种易于获取和操作的生物激素，可用于研究植物风险感知和诱导反应的新问题。事实上，蛞蝓优先攻击幼苗，这是一个高度脆弱的生活史阶段，突出了攻击前粘液检测和反应的选择性优势。在长寿命木本植物系统中研究了以下问题：不同的风险因素如何影响不同年龄幼苗的生长和防御？易感性的个体发生变化如何决定反应模式？风险感知和个体发生在该领域的直接和遗留后果是什么？这些问题是用蛞蝓Arion subfuscus和糖槭saccharum进行的，在短期（~1个月）和长期（1年）的时间内探索风险提示质量和幼苗年龄之间的相互作用。这是第一个关于kairomones如何影响木本植物的防御、生长和随后的食草动物脆弱性的研究。草食线索、个体发生和季节内和季节间的差异易感性的操纵探讨了当前的植物防御是否反映了“过去草食风险的幽灵”；考虑到植物过去所接收到的信息，现在的防御往往是有意义的。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

Even though plants cannot move, they are far from defenseless against their herbivores. While research exploring how plants protect themselves has focused largely on changes in plant defense that occur in response to herbivore attack, it has recently been shown that plants can detect and respond to herbivore cues (referred to as ‘kairomones’) even before an attack begins. Mucus from snails and slugs, herbivores that attack seeds and seedlings, triggers defensive responses in seedlings that help the plants survive subsequent attack by slugs or other herbivores. Such defenses may be particularly important for seedling sugar maple trees, an iconic tree in the northeastern US critical to the maple sugar industry that is declining throughout its range. An invasive slug, the dusky Arion, poses a major threat to newly germinated sugar maple seedlings; this project addresses how mucus from this slug affects the anti-herbivore defenses of sugar maples ranging in age from seedlings to saplings. It also evaluates whether early-life exposure to mucus can help protect sugar maples against later-arriving herbivores ranging from gypsy moths to white-tailed deer. The project also funds work by the Rhode Island-based Science and Math Investigative Learning (SMILE) program, a classroom-based organization that works with kids grades 4-12 to increase the numbers of educationally disadvantaged students who graduate from high school prepared to enter higher education and pursue STEM careers. Students work with project scientists on field- and classroom-based experiences that employ inquiry-based learning to reveal ecological principles and explore local ecosystems.Despite substantial research exploring plant defense induction during and after herbivore attack, little is known about whether and how plants use pre-attack cues such as kairomones (herbivore-emitted chemicals not associated with attack that are detected by - and thus provide benefits to - a plant) to preemptively induce defense. Herbivore kairomones have recently been documented in multiple systems; slug/snail mucus, an easily obtained and manipulable kairomone, can be used to ask novel questions about plant risk perception and induced responses. The fact that slugs preferentially attack seedlings, a highly vulnerable life history stage, highlights the selective advantage of pre-attack mucus detection and response. The following questions are addressed in a long-lived woody plant system: How do different risk cues affect growth and defense of different-aged seedlings?; How do ontogenetic shifts in susceptibility determine patterns of responses?; What are the immediate and legacy consequences of risk perception and ontogeny in the field? These questions are asked using the slug Arion subfuscus and the sugar maple Acer saccharum in experiments exploring interactions between risk cue quality and seedling age over both short (~1 month) and long (1 yr.) time periods. This is the first study of how kairomones affect woody plant defense, growth, and subsequent herbivore vulnerability. The manipulation of herbivore cues, ontogeny, and differential susceptibility within and across seasons explores whether current plant defense reflects the ‘ghost of herbivory risk past’; present-day defense may often only make sense considering past information received by plants.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.