1 INTRODUCTION

Parasites are the most commonly occurring type of consumers (Lafferty et al., 2006; Dobson et al., 2008), and as such have also been coined missing links in aquatic and terrestrial food-webs (Lafferty et al., 2008; Sommer et al., 2012). Even though parasites can represent substantial biomass in natural ecosystems and affect a wide range of ecosystem processes (Hatcher et al., 2012; Kuris et al., 2008; Sures et al., 2017), their dynamics and biomass are rarely quantified at community level. Moreover, environmental variation can modulate the outcome of host–parasite interactions (Wolinska & King, 2009) but we still lack insight in the contribution of specific environmental variables on host–parasite dynamics in natural communities. Assessing baseline data on occurrence and biomass as well as the environmental factors associated with parasite infections will improve our understanding of the role of parasites in natural ecosystems.

Chytrids parasitising phytoplankton represent an interesting study system to assess the role of parasites in natural ecosystems due to their widespread occurrence and dominance in aquatic fungal communities (Beng et al., 2021; Comeau et al., 2016; Ortiz-Álvarez et al., 2018). Epidemics of host-specific chytrids can control size and timing of phytoplankton blooms and thereby influence their seasonal succession (Van Donk & Ringelberg, 1983). Moreover, chytrids can increase the intraspecific diversity of their host populations by preferentially infecting common host geno- or chemotypes (Agha, Gross, Rohrlack, et al., 2018; Gsell, de Senerpont Domis, Verhoeven, et al., 2013; Sønstebø & Rohrlack, 2011). By producing zoospores, nutritious and edible infectious lifestages (Gleason et al., 2009), chytrids can upgrade the biochemical composition of their hosts (Gerphagnon et al., 2019), serve as trophic links from large-sized, inedible phytoplankton to zooplankton consumers (i.e., the mycoloop [Kagami et al., 2014]), and thereby support zooplankton growth during inedible phytoplankton blooms (Agha et al., 2016; Frenken et al., 2018). As parasites of phytoplankton, chytrids influence carbon quality and cycling in aquatic ecosystems (Grami et al., 2011; Rasconi et al., 2020; Senga et al., 2018). However, most studies on the ecology of parasitic chytrids have only covered snapshots in time or focused on individual host–parasite model systems. The lack of baseline data on chytrid occurrence, and their seasonal and long-term dynamics in complex communities, hinders our understanding of the role of chytrids in aquatic ecosystems (Frenken, Alacid, et al., 2017; Sime-Ngando, 2012).

Environmental conditions are known to influence parasite fitness (Wolinska & King, 2009) and the seasonal and long-term patterns of parasite occurrence (Canter & Lund, 1948; Van Donk & Ringelberg, 1983). For parasites both the host environment (e.g., host density) and the abiotic environment are relevant. In laboratory experiments and field observations chytrid transmission has been shown to increase with host density once a minimum host density threshold was surpassed (Holfeld, 1998; Ibelings et al., 2011). Environmental conditions such as temperature and nutrient concentrations fluctuate with the seasons, while global change adds directional change across years (IPCC, 2013). Physiological rates increase with temperature (Brown et al., 2004), leading to the expectation that warmer temperatures also result in faster parasite generation times and infection spread (Marcogliese, 2008). In diatom and cyanobacterium host–chytrid systems, chytrid prevalence of infection showed an optimum curve relationship with temperature, with very cold and very warm conditions inhibiting parasite infections (Agha, Gross, Gerphagnon, et al., 2018; Gsell, de Senerpont Domis, Van Donk, et al., 2013; Rohrlack et al., 2015). Nutrient enrichment and subsequent changes in the elemental composition of hosts can result in higher infection prevalence due to higher production and nutritional quality of hosts (Frenken et al., 2021; McKenzie & Townsend, 2007). However, changes in host community composition due to eutrophication can also result in decreases in parasitism as well-defended or toxin-producing species may become dominant (Budria, 2017). Chytrids have shown relatively low carbon to nutrient ratios, indicating their relatively high nutrient requirements (Frenken, Wierenga, et al., 2017; Kagami et al., 2007; Sánchez Barranco et al., 2020). Nutrient enrichment experiments and model simulations have also shown that the net effect of eutrophication depends on the relative changes in host and chytrid growth rates. Eutrophication can lead to a higher infection prevalence, but also to the paradox of enrichment when overshooting infection cycles drive the host population size below the minimum host density necessary for maintenance of infection (Gerla et al., 2013). Conversely, nutrient limitation may also lead to enhanced, albeit short-lived chytrid success as the parasite can outgrow the host population (Bruning, 1991; Frenken, Wierenga, et al., 2017).

Here, we analysed 12 years of weekly (partly fortnightly) data on multiple chytrid parasites and their pelagic phytoplankton hosts in a shallow, temperate, eutrophic lake to infer occurrence, biomass (i.e., infected host biomass), seasonal and long-term (seasonally-detrended) prevalence of infection dynamics in phytoplankton under natural conditions. As phytoplankton host density, nutrient concentrations, and water temperature show the typical seasonal variations of temperate eutrophic lakes, we additionally assessed the response of chytrid infection prevalence to potential long-term trends in phytoplankton host density, nutrient concentrations, and water temperature. We expected that: (1) chytrid infection prevalence would scale with phytoplankton biomass and therefore also follow the seasonal dynamics and long-term trends of phytoplankton; and (2) chytrid infection prevalence would increase with water temperature—up to an optimum—and nutrient concentrations following the seasonal dynamics as well as long-term trends in associated environmental factors.

中文翻译：

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寄主密度、温度和养分的长期趋势和季节变化对寄生于湖泊浮游植物的壶菌有不同的影响

1 简介

寄生虫是最常见的消费者类型（Lafferty 等人，  2006 年；Dobson 等人，  2008 年），因此也被认为是水生和陆地食物网中缺失的环节（Lafferty 等人，  2008 年；Sommer等人，  2012 年）。尽管寄生虫可以代表自然生态系统中的大量生物量并影响广泛的生态系统过程（Hatcher 等人，  2012 年；Kuris 等人，  2008 年；Sures 等人，  2017 年），但它们的动态和生物量很少在群落中量化等级。此外，环境变化可以调节宿主-寄生虫相互作用的结果（Wolinska & King,  2009）但我们仍然缺乏对特定环境变量对自然群落中宿主 - 寄生虫动态的贡献的洞察力。评估有关发生率和生物量以及与寄生虫感染相关的环境因素的基线数据将提高我们对寄生虫在自然生态系统中的作用的理解。

寄生于浮游植物的壶菌代表了一个有趣的研究系统，用于评估寄生虫在自然生态系统中的作用，因为它们在水生真菌群落中广泛存在和占主导地位（Beng 等人，  2021 年；Comeau 等人，  2016 年；Ortiz-Álvarez 等人，  2018 年）。宿主特异性壶菌的流行可以控制浮游植物水华的大小和时间，从而影响它们的季节演替（V​​an Donk & Ringelberg,  1983）。此外，壶菌可以通过优先感染常见宿主基因或化学型来增加其宿主种群的种内多样性（Agha、Gross、Rohrlack 等人，  2018 年；Gsell、de Senerpont Domis、Verhoeven 等人，  2013 年）; Sønstebø 和 Rohrlack，  2011 年）。通过产生游动孢子、营养丰富和可食用的传染性生命阶段（Gleason 等人，  2009 年），壶菌可以升级其宿主的生化成分（Gerphagnon 等人，  2019 年），充当从大型不可食用浮游植物到浮游动物消费者的营养纽带（即 mycoloop [Kagami 等人，  2014 年]），从而支持浮游动物在不可食用的浮游植物大量繁殖期间生长（Agha 等人，  2016 年；Frenken 等人，  2018 年）。作为浮游植物的寄生虫，壶菌会影响水生生态系统中的碳质量和循环（Grami 等人，  2011 年；Rasconi 等人，  2020年；Senga 等人，  2018 年））。然而，大多数关于寄生壶菌生态学的研究只及时涵盖快照或关注个体宿主 - 寄生虫模型系统。缺乏关于壶菌发生的基线数据，以及它们在复杂群落中的季节性和长期动态，阻碍了我们对壶菌在水生生态系统中的作用的理解（Frenken、Alacid 等人，  2017 年；Sime-Ngando，  2012 年）。

众所周知，环境条件会影响寄生虫的适应性 (Wolinska & King,  2009 ) 以及寄生虫发生的季节性和长期模式 (Canter & Lund,  1948 ; Van Donk & Ringelberg,  1983 )。对于寄生虫，宿主环境（例如宿主密度）和非生物环境都是相关的。在实验室实验和现场观察中，一旦超过最小宿主密度阈值，壶菌的传播就会随着宿主密度的增加而增加（Holfeld，  1998 年；Ibelings 等人，  2011 年）。温度和养分浓度等环境条件随季节波动，而全球变化增加了跨年的方向变化（IPCC，  2013）。生理速率随温度增加（Brown 等人，  2004 年），导致预期温度升高也会导致更快的寄生虫生成时间和感染传播（Marcogliese，  2008 年）。在硅藻和蓝藻宿主-壶菌系统中，壶菌的感染率显示出与温度的最佳曲线关系，在非常冷和非常热的条件下抑制寄生虫感染（Agha、Gross、Gerphagnon 等人，  2018 年；Gsell、de Senerpont Domis， Van Donk 等人，  2013 年；Rohrlack 等人，  2015 年）。由于宿主的产量和营养质量较高，营养丰富和宿主元素组成的后续变化可导致较高的感染率（Frenken 等人，  2021 年；McKenzie 和 Townsend，  2007 年）。然而，由于富营养化引起的宿主群落组成变化也可能导致寄生减少，因为防御良好或产生毒素的物种可能成为主导物种（Budria，  2017 年）。壶菌的碳养分比相对较低，表明它们对养分的需求相对较高（Frenken, Wierenga 等人，  2017 年；Kagami 等人，  2007 年；Sánchez Barranco 等人，  2020 年））。营养富集实验和模型模拟也表明，富营养化的净效应取决于宿主和壶菌生长速率的相对变化。富营养化会导致更高的感染流行率，但也会导致富集的悖论，因为过度感染周期会使宿主种群规模低于维持感染所需的最小宿主密度（Gerla 等人，  2013 年）。相反，营养限制也可能导致提高，尽管是短暂的壶菌成功，因为寄生虫可以长得超过宿主种群（Bruning，  1991；Frenken，Wierenga 等，  2017）。

在这里，我们分析了 12 年每周（部分每两周一次）关于浅水、温带、富营养化湖泊中多种壶菌寄生虫及其中上层浮游植物宿主的数据，以推断发生率、生物量（即受感染的宿主生物量）、季节性和长期（季节性-去趋势）在自然条件下浮游植物感染动态的流行。由于浮游植物宿主密度、养分浓度和水温显示出温带富营养化湖泊的典型季节性变化，我们还评估了壶菌感染流行对浮游植物宿主密度、养分浓度和水温的潜在长期趋势的反应。我们预计：（1）壶菌感染流行率会随着浮游植物生物量的增加而增加，因此也遵循浮游植物的季节性动态和长期趋势；