{"title":"Organismal trade-offs and the pace of planktonic life","authors":"Thomas Kiørboe","doi":"10.1111/brv.13108","DOIUrl":null,"url":null,"abstract":"<p>No one is perfect, and organisms that perform well in some habitat or with respect to some tasks, do so at the cost of performance in others: there are inescapable trade-offs. Organismal trade-offs govern the structure and function of ecosystems and attempts to demonstrate and quantify trade-offs have therefore been an important goal for ecologists. In addition, trade-offs are a key component in trait-based ecosystem models. Here, I synthesise evidence of trade-offs in plankton organisms, from bacteria to zooplankton, and show how a slow–fast gradient in life histories emerges. I focus on trade-offs related to the main components of an organism's Darwinian fitness, that is resource acquisition, survival, and propagation. All consumers need to balance the need to eat without being eaten, and diurnal vertical migration, where zooplankton hide at depth during the day to avoid visual predators but at the cost of missed feeding opportunities in the productive surface layer, is probably the best documented result of this trade-off. However, there are many other more subtle but equally important behaviours that similarly are the result of an optimisation of these trade-offs. Most plankton groups have also developed more explicit defence mechanisms, such as toxin production or evasive behaviours that are harnessed in the presence of their predators; the costs of these have often proved difficult to quantify or even demonstrate, partly because they only materialise under natural conditions. Finally, all multicellular organisms must allocate time and resources among growth, reproduction, and maintenance (e.g. protein turnover and DNA repair), and mate finding may compromise both survival and feeding. The combined effects of all these trade-offs is the emergence of a slow–fast gradient in the pace-of-life, likely the most fundamental principle for the organisation of organismal life histories. This crystallisation of trade-offs may offer a path to further simplification of trait-based models of marine ecosystems.</p>","PeriodicalId":133,"journal":{"name":"Biological Reviews","volume":"99 6","pages":"1992-2002"},"PeriodicalIF":11.0000,"publicationDate":"2024-06-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/brv.13108","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Biological Reviews","FirstCategoryId":"99","ListUrlMain":"https://onlinelibrary.wiley.com/doi/10.1111/brv.13108","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
No one is perfect, and organisms that perform well in some habitat or with respect to some tasks, do so at the cost of performance in others: there are inescapable trade-offs. Organismal trade-offs govern the structure and function of ecosystems and attempts to demonstrate and quantify trade-offs have therefore been an important goal for ecologists. In addition, trade-offs are a key component in trait-based ecosystem models. Here, I synthesise evidence of trade-offs in plankton organisms, from bacteria to zooplankton, and show how a slow–fast gradient in life histories emerges. I focus on trade-offs related to the main components of an organism's Darwinian fitness, that is resource acquisition, survival, and propagation. All consumers need to balance the need to eat without being eaten, and diurnal vertical migration, where zooplankton hide at depth during the day to avoid visual predators but at the cost of missed feeding opportunities in the productive surface layer, is probably the best documented result of this trade-off. However, there are many other more subtle but equally important behaviours that similarly are the result of an optimisation of these trade-offs. Most plankton groups have also developed more explicit defence mechanisms, such as toxin production or evasive behaviours that are harnessed in the presence of their predators; the costs of these have often proved difficult to quantify or even demonstrate, partly because they only materialise under natural conditions. Finally, all multicellular organisms must allocate time and resources among growth, reproduction, and maintenance (e.g. protein turnover and DNA repair), and mate finding may compromise both survival and feeding. The combined effects of all these trade-offs is the emergence of a slow–fast gradient in the pace-of-life, likely the most fundamental principle for the organisation of organismal life histories. This crystallisation of trade-offs may offer a path to further simplification of trait-based models of marine ecosystems.
没有人是完美无缺的,在某些栖息地或某些任务中表现出色的生物,在其他方面的表现也会受到影响:这就是不可避免的权衡。生物的权衡决定了生态系统的结构和功能,因此,试图证明和量化权衡一直是生态学家的重要目标。此外,权衡也是基于性状的生态系统模型的关键组成部分。在这里,我综合了浮游生物(从细菌到浮游动物)中权衡的证据,并展示了生命史中如何出现慢-快梯度。我将重点放在与生物体达尔文适应性的主要组成部分(即资源获取、生存和繁殖)相关的权衡上。所有消费者都需要在吃而不被吃之间取得平衡,浮游动物白天躲在深海以躲避视觉捕食者,但代价是错过了在富饶表层觅食的机会,这种昼夜垂直迁移可能是这种权衡的最佳记录结果。然而,还有许多其他更微妙但同样重要的行为,同样是这些权衡的优化结果。大多数浮游生物群体还发展出了更明确的防御机制,例如在捕食者出现时利用毒素生产或回避行为;事实证明,这些行为的代价往往难以量化,甚至难以证明,部分原因是它们只有在自然条件下才会出现。最后,所有多细胞生物都必须在生长、繁殖和维持(如蛋白质周转和 DNA 修复)之间分配时间和资源,而寻找配偶可能会影响生存和进食。所有这些权衡的综合效应就是出现了生活节奏的慢-快梯度,这可能是组织生物生活史的最基本原则。这种权衡的具体化可能为进一步简化基于性状的海洋生态系统模型提供了途径。
期刊介绍:
Biological Reviews is a scientific journal that covers a wide range of topics in the biological sciences. It publishes several review articles per issue, which are aimed at both non-specialist biologists and researchers in the field. The articles are scholarly and include extensive bibliographies. Authors are instructed to be aware of the diverse readership and write their articles accordingly.
The reviews in Biological Reviews serve as comprehensive introductions to specific fields, presenting the current state of the art and highlighting gaps in knowledge. Each article can be up to 20,000 words long and includes an abstract, a thorough introduction, and a statement of conclusions.
The journal focuses on publishing synthetic reviews, which are based on existing literature and address important biological questions. These reviews are interesting to a broad readership and are timely, often related to fast-moving fields or new discoveries. A key aspect of a synthetic review is that it goes beyond simply compiling information and instead analyzes the collected data to create a new theoretical or conceptual framework that can significantly impact the field.
Biological Reviews is abstracted and indexed in various databases, including Abstracts on Hygiene & Communicable Diseases, Academic Search, AgBiotech News & Information, AgBiotechNet, AGRICOLA Database, GeoRef, Global Health, SCOPUS, Weed Abstracts, and Reaction Citation Index, among others.