Collaborative research: Quantifying the influence of nonconsumptive predator effects on prey population dynamics

捕食者可以通过两种方式影响猎物的数量：消耗它们（“消耗效应”或“CE”），或者使猎物改变行为以避免与捕食者接触。例如，猎物通常花更少的时间进食，而花更多的时间提防捕食者，这是以食物摄入量减少和生长缓慢为代价的。这种“非消耗效应”（NCEs）已经被描述为广泛的陆地和海洋猎物物种，从麋鹿到蛤蜊，但大多是短期（1个月）的实验。这些先前的结果表明，在某些情况下，行为变化（NCEs）对猎物种群的影响大于捕食者的消耗（CEs）。然而，那些短期的、受控的实验可能会人为地夸大nce的重要性。在较长时间内，猎物可能会适应或逐渐适应捕食风险，nce可能变得不那么重要。此外，环境变化（例如，不同研究地点之间猎物食物可得性的差异）对猎物种群的影响可能比NCEs更大。该项目将结合短期（数月）和长期（年）的实地实验和数学模型来评估nce对佛罗里达牡蛎礁的作用。本研究的猎物种类为东部牡蛎，是美国东南部重要的海洋资源，可用于捕捞和生境创造；牡蛎的主要捕食者是泥蟹。在这项研究中，牡蛎种群数学模型的结果将与现场的实验数据进行比较，以了解在模型中包含NCEs是否会导致更好的模型预测。更好地了解牡蛎中的NCEs将改善对这一重要海洋资源的管理。此外，该数学模型将用于开发更广泛的、可推广的结论，这些结论可以应用于其他重要的猎物物种。该项目将为牡蛎资源管理提供有用的数据，将支持有关NCEs生态重要性的公众教育，并将加强研究区域中代表性不足群体的科学参与。该项目将支持与佛罗里达州瓜纳托洛马托马坦萨斯国家河口研究保护区建立伙伴关系，包括数据共享，赞助牡蛎管理研讨会，并资助在保护区开发多媒体科学推广材料，这些材料将供周边社区大量不同的K-12学生使用。该项目将培养一名博士后研究员、两名研究生和两名本科生，研究成果将由这些学生和主要研究人员在科学会议上、期刊出版物上以及通过与佛罗里达州公共电视台的持续合作在在线内容上传播。捕食者可以通过引起猎物特征的基于恐惧的变化来改变猎物的种群动态（非消耗效应，NCE）。相对于捕食者的直接消费（消费效应，CEs）， NCEs对猎物种群的重要性仍然不确定，特别是因为短期的NCEs研究无法估计它们对多代猎物的影响。该项目通过将短期和长期的实地实验与种群模型相结合来研究nce对佛罗里达河口牡蛎种群动态的重要性，从而解决了这一知识差距。核心问题是，计算NCEs是否能提高预测牡蛎种群丰度长期趋势的能力。该系统中存在几种类型的nce：暴露在含有捕食者气味的水中会减少牡蛎幼虫的招募，并导致幼牡蛎增加外壳厚度，减少其体细胞生长。除了ce和nce外，胁迫、食物和繁殖体传递方面的环境梯度也存在于该系统中。这些环境因素对牡蛎定居后的生存、生长和补充都有很大的影响，因此捕食者ce和非捕食者ce的相对重要性也可能在这些空间梯度上有所不同。这个项目将由四个部分组成。(1)通过一系列短期的野外实验，测试nce随捕食者密度和环境变量的变化，以及其中一种nce（增加壳厚）是否真的降低了对捕食者的脆弱性。(2)种群模型，用实验结果参数化；模式模拟将量化nce的相对重要性如何随时间、空间和环境梯度而变化。(3)较长期（3.5年）的野外试验；该实验的结果将与模型预测进行比较，以测试NCEs是否能改善对牡蛎种群动态长期变化的预测。(4)该模型的一般形式将被开发出来，以广泛地研究nce对非平衡、瞬态种群动态的影响。通过结合模型和实地实验，该项目将弥合NCEs如何影响种群动态的理论理解与该理论的实证检验之间的差距，推动该领域朝着预测多种相互作用因素如何构成群落的目标迈进。

Predators can affect populations of their prey in two ways: by consuming them ("consumptive effects" or "CE"s), or by causing the prey to change behavior to avoid contact with the predator. For example, prey often spend less time feeding and more time watching out for predators, which comes with the cost of lower food intake and thus slower growth. Such "non-consumptive effects" (NCEs) have been described for a wide range of terrestrial and marine prey species, from elk to clams, but mostly in short-term ( 1 month) experiments. These prior results suggest that in some cases, the behavioral changes (NCEs) have a bigger effect on prey populations than consumption by predators (CEs). However, those short-term, controlled experiments may artificially inflate the perceived importance of NCEs. Over longer time periods, prey may adapt or become acclimated to predation risk, and NCEs may become less important. Additionally, environmental variability (e.g., differences in the availability of the prey's food between study sites) may have a bigger effect on prey populations than NCEs do. This project will use a combination of short- (months) and long-term (years) field experiments and mathematical models to evaluate the role of NCEs on Florida oyster reefs. The prey species in this study is the eastern oyster, an important marine resource in the southeast US for harvesting and habitat creation; the main oyster predator is a mud crab. In this study, results from mathematical models of oyster populations will be compared to experimental data from the field to see whether including NCEs in the model leads to better model predictions. Better understanding of NCEs in oysters should improve management of that important marine resource. Furthermore, the mathematical model will be used to develop broader, generalizable conclusions about the importance of NCEs that could be applied to other important prey species. This project will provide data useful for oyster resource management, will support public education regarding the ecological importance of NCEs, and will enhance the scientific engagement of underrepresented groups in the study region. The project will support a partnership with the Guana Tolomato Matanzas National Estuarine Research Reserve in Florida, including data sharing, sponsoring an oyster management symposium, and funding the development of multimedia scientific outreach materials at the reserve that will be used by a large and diverse population of K-12 students in the surrounding community. The project will train a postdoctoral researcher, two graduate students, two undergraduate students, and research results will be disseminated by those students and the principal investigators at scientific conferences, in journal publications, and in online content through an ongoing partnership with a Florida public television station. Predators can alter prey population dynamics by causing fear-based shifts in prey traits (nonconsumptive effect, NCE). The importance of NCEs for prey populations - relative to direct consumption by predators (consumptive effects, CEs) - remains uncertain, particularly because short-term studies of NCEs cannot estimate their effect over multiple prey generations. This project addresses that knowledge gap by combining short- and long-term field experiments with population models to investigate the importance of NCEs on oyster population dynamics in a Florida estuary. The central question is whether accounting for NCEs improves the ability to predict long-term trends in oyster population abundance. Several types of NCEs are present in this system: exposure to water containing predator odors reduces oyster larval recruitment and causes juvenile oysters to increase shell thickness, reducing their somatic growth. In addition to CEs and NCEs , environmental gradients in stress, food, and propagule delivery are also present in this system. Those environmental factors can have strong effects on post-settlement survivorship, growth, and recruitment of oysters, so the relative importance of predator CEs and NCEs may vary along those spatial gradients as well. This project will consist of four components. (1) A series of short-term field experiments to test how NCEs vary with predator density and environmental variables, and whether one of the NCEs (increased shell thickness) actually reduces vulnerability to predators. (2) A population model, parameterized using experimental results; model simulations will quantify how the relative importance of NCEs should vary over time, space, and environmental gradients. (3) A longer-term (3.5 year) field experiment; the results from this experiment will be compared to model predictions to test whether accounting for NCEs improves predictions of long-term variation in oyster population dynamics. (4) A general form of the model will be developed to broadly investigate the effect of NCEs on non-equilibrium, transient population dynamics. By combining models and field experiments, this project will bridge the gap between the theoretical understanding of how NCEs affect population dynamics and empirical tests of that theory, advancing the field towards the goal of predicting how multiple interacting factors structure communities.