Stefanie D. Moorthi , Michaela Busch , Ulrike Feudel , Urban Tillmann , Bernd Krock , Bob W. Kooi , Jana Brinkmann , Subhendu Chakraborty
{"title":"Allelochemicals determine competition and grazing control in Alexandrium catenella","authors":"Stefanie D. Moorthi , Michaela Busch , Ulrike Feudel , Urban Tillmann , Bernd Krock , Bob W. Kooi , Jana Brinkmann , Subhendu Chakraborty","doi":"10.1016/j.hal.2024.102704","DOIUrl":null,"url":null,"abstract":"<div><p>The production of allelochemicals by the toxigenic dinoflagellate <em>Alexandrium catenella</em> is one of the suggested mechanisms to facilitate its bloom formation and persistence by outcompeting other phototrophic protists and reducing grazing pressure. In Southern California, toxic events caused by <em>A. catenella</em> and paralytic shellfish toxins (PSTs) regularly impact coastal ecosystems; however, the trophic interactions and mechanisms promoting this species in a food web context are still not fully understood. In the present study, we combined a dynamical mathematical model with laboratory experiments to investigate potential toxic and allelochemical effects of an <em>A. catenella</em> strain isolated off the coast of Los Angeles, Southern California, on competitors and a common zooplankton consumer. Experiments were conducted using three toxigenic strains of <em>A. catenella</em>, comparing the new Californian isolate (Alex Cal) to two strains previously described from the North Sea, a lytic (Alex2) and non-lytic (Alex5) strain, testing for donor density-dependent effects on two phytoplankton species (<em>Rhodomonas salina, Tetraselmis</em> sp.) and on the rotifer <em>Brachionus plicatilis</em>. Bioassays revealed a steep decline in competitor and consumer populations with increasing Alex Cal concentrations, indicating an intermediate lytic activity compared to the North Sea strains (lytic Alex2 and non-lytic Alex5). The rotifer fed and grew well on the PST- toxic, but non-lytic Alex5 strain, while its survival significantly decreased with increasing concentrations of the two lytic strains Alex Cal and Alex 2, indicating that negative effects on the rotifer were mediated by allelochemicals rather than PST-toxins. Mixed culture experiments including both competitors and consumers demonstrated that the intensity of allelochemical effects not only depended on the <em>A. catenella</em> density but also on the target density. Negative effects on grazers were alleviated by co-occurring competitors with a lower sensitivity to allelochemicals, thus reducing harmful compounds and allowing grazing control on the dinoflagellate to come into effect again. Results from mixed culture experiments were supported by the mathematical approach used in this study which was calibrated with data from simple monoculture growth, pairwise competition and predator-prey experiments, demonstrating the applicability of this model approach to predict the outcome of more complex food web dynamics at the community level.</p></div>","PeriodicalId":12897,"journal":{"name":"Harmful Algae","volume":"138 ","pages":"Article 102704"},"PeriodicalIF":5.5000,"publicationDate":"2024-08-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.sciencedirect.com/science/article/pii/S1568988324001379/pdfft?md5=ae622d24fdffe1176b6f0d883cee3929&pid=1-s2.0-S1568988324001379-main.pdf","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Harmful Algae","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1568988324001379","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MARINE & FRESHWATER BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
The production of allelochemicals by the toxigenic dinoflagellate Alexandrium catenella is one of the suggested mechanisms to facilitate its bloom formation and persistence by outcompeting other phototrophic protists and reducing grazing pressure. In Southern California, toxic events caused by A. catenella and paralytic shellfish toxins (PSTs) regularly impact coastal ecosystems; however, the trophic interactions and mechanisms promoting this species in a food web context are still not fully understood. In the present study, we combined a dynamical mathematical model with laboratory experiments to investigate potential toxic and allelochemical effects of an A. catenella strain isolated off the coast of Los Angeles, Southern California, on competitors and a common zooplankton consumer. Experiments were conducted using three toxigenic strains of A. catenella, comparing the new Californian isolate (Alex Cal) to two strains previously described from the North Sea, a lytic (Alex2) and non-lytic (Alex5) strain, testing for donor density-dependent effects on two phytoplankton species (Rhodomonas salina, Tetraselmis sp.) and on the rotifer Brachionus plicatilis. Bioassays revealed a steep decline in competitor and consumer populations with increasing Alex Cal concentrations, indicating an intermediate lytic activity compared to the North Sea strains (lytic Alex2 and non-lytic Alex5). The rotifer fed and grew well on the PST- toxic, but non-lytic Alex5 strain, while its survival significantly decreased with increasing concentrations of the two lytic strains Alex Cal and Alex 2, indicating that negative effects on the rotifer were mediated by allelochemicals rather than PST-toxins. Mixed culture experiments including both competitors and consumers demonstrated that the intensity of allelochemical effects not only depended on the A. catenella density but also on the target density. Negative effects on grazers were alleviated by co-occurring competitors with a lower sensitivity to allelochemicals, thus reducing harmful compounds and allowing grazing control on the dinoflagellate to come into effect again. Results from mixed culture experiments were supported by the mathematical approach used in this study which was calibrated with data from simple monoculture growth, pairwise competition and predator-prey experiments, demonstrating the applicability of this model approach to predict the outcome of more complex food web dynamics at the community level.
毒性甲藻亚历山大藻(Alexandrium catenella)产生的等位化学物质是促进其藻华形成和持续的建议机制之一,其作用是淘汰其他光养原生动物并减少放牧压力。在南加州,由亚历山大藻(A. catenella)和麻痹性贝类毒素(PSTs)引起的毒性事件经常影响沿海生态系统;然而,在食物网中促进该物种的营养相互作用和机制仍未得到充分了解。在本研究中,我们将动态数学模型与实验室实验相结合,研究了南加州洛杉矶沿海分离出的一种 A. catenella 菌株对竞争者和一种常见浮游动物消费者的潜在毒性和等位化学效应。实验中使用了三种毒性猫尾蛙菌株,将加利福尼亚的新分离菌株(Alex Cal)与之前在北海描述的两种菌株(溶解性菌株(Alex2)和非溶解性菌株(Alex5))进行了比较,测试了供体密度对两种浮游植物(Rhodomonas salina、Tetraselmis sp.)和轮虫 Brachionus plicatilis 的影响。生物测定显示,随着 Alex Cal 浓度的增加,竞争者和消费者的数量急剧下降,这表明与北海菌株(溶解性 Alex2 和非溶解性 Alex5)相比,Alex Cal 的溶解活性处于中等水平。轮虫在具有 PST 毒性但无溶解性的 Alex5 菌株上摄食和生长良好,而随着两种溶解性菌株 Alex Cal 和 Alex 2 浓度的增加,其存活率显著下降,这表明对轮虫的负面影响是由等位化学物质而非 PST 毒素介导的。包括竞争者和消费者在内的混合培养实验表明,等位化学效应的强度不仅取决于A. catenella的密度,还取决于目标密度。对等位化学物质敏感性较低的竞争者的共存减轻了对食草动物的负面影响,从而减少了有害化合物,使对甲藻的食草控制再次生效。混合培养实验的结果得到了本研究使用的数学方法的支持,该方法通过简单的单培养生长、成对竞争和捕食者-被捕食者实验数据进行校准,证明了该模型方法适用于预测群落水平上更复杂的食物网动态结果。
期刊介绍:
This journal provides a forum to promote knowledge of harmful microalgae and macroalgae, including cyanobacteria, as well as monitoring, management and control of these organisms.