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种群：一是通过吃掉它们(“消耗性效应”或“CE”S)，二是通过使猎物改变行为以避免与捕食者接触。例如，猎物通常花费较少的时间进食，而花更多的时间观察捕食者，这伴随着较低的食物摄入量和较慢的生长速度。这种“非消耗性效应”(NCEs)已经在从麋鹿到文蛤等广泛的陆地和海洋猎物物种中得到了描述，但主要是在短期(1个月)的实验中。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(CEs)的消耗。然而，这些短期的受控实验可能会人为地夸大NCE的重要性。在较长的时间内，猎物可能会适应或适应捕食风险，而NCEs可能变得不那么重要。此外，环境变异性(例如，研究地点之间猎物食物可获得性的差异)对猎物种群的影响可能比NCEs更大。该项目将使用短期(月)和长期(年)现场实验和数学模型相结合的方法来评估NCE在佛罗里达牡蛎礁上的作用。这项研究的猎物物种是东部牡蛎，这是美国东南部重要的海洋资源，用于收获和创建栖息地；主要的牡蛎捕食者是泥蟹。在这项研究中，牡蛎种群的数学模型的结果将与现场的实验数据进行比较，以查看是否在模型中包含NCE会导致更好的模型预测。更好地了解牡蛎中的NCEs应有助于对这一重要海洋资源的管理。此外，该数学模型将被用来得出关于NCEs重要性的更广泛、可概括的结论，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，将支持关于非国家环境许可证生态重要性的公共教育，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坦萨斯国家河口研究保护区的伙伴关系，包括数据共享，赞助牡蛎管理研讨会，并资助保护区多媒体科学宣传材料的开发，供周围社区大量不同的K-12学生使用。该项目将培训一名博士后研究员、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、期刊出版物上传播，并通过与佛罗里达州一家公共电视台的持续合作以在线内容传播。捕食者可以通过导致基于恐惧的猎物特征的变化来改变猎物的种群动态(非消耗效应，NCE)。NCEs对猎物种群的重要性--相对于捕食者的直接消费(消耗效应，CES)--仍然不确定，特别是因为对NCEs的短期研究无法估计其对多个猎物世代的影响。该项目通过将短期和长期野外实验与种群模型相结合来解决这一知识差距，以调查NCE对佛罗里达州河口牡蛎种群动态的重要性。核心问题是，计入NCEs是否会提高预测牡蛎种群数量长期趋势的能力。在这个系统中存在几种类型的NCEs：暴露在含有捕食者气味的水中会减少牡蛎幼体的招募，并导致幼贝增加外壳厚度，从而减少它们的躯体生长。除了CEs和NCEs外，压力、食物和繁殖体传递的环境梯度也存在于这个系统中。这些环境因素会对牡蛎在定居后的存活、生长和补充产生强烈的影响，因此捕食者CE和NCEs的相对重要性可能也会沿着这些空间梯度而变化。该项目将由四个部分组成。(1)一系列短期野外实验，以测试NCE如何随捕食者密度和环境变量而变化，以及其中一种NCE(增加的外壳厚度)是否真的降低了对捕食者的脆弱性。(2)人口模型，使用实验结果进行参数化；模型模拟将量化NCE的相对重要性应如何随时间、空间和环境梯度而变化。(3)较长期(3.5年)的野外实验；这项实验的结果将与模型预测进行比较，以测试考虑NCEs是否改善了对牡蛎种群动态长期变化的预测。(4)模型的一般形式将被用来广泛地研究NCEs对非平衡、暂态种群动力学的影响。通过将模型和实地实验相结合，该项目将弥合对NCE如何影响种群动态的理论理解和该理论的实证测试之间的差距，推动该领域朝着预测多种相互作用的因素如何构建社区的目标迈进。

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.