Functional Ecology ( IF 4.6 ) Pub Date : 2022-09-23 , DOI: 10.1111/1365-2435.14187 Vera Brust 1 , Cas Eikenaar 1 , Florian Packmor 1, 2 , Heiko Schmaljohann 1, 3 , Ommo Hüppop 1 , Gábor Á. Czirják 4
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1 INTRODUCTION
Migration facilitates the utilization of seasonally available resources and the evasion of adverse environmental conditions (Chapman et al., 2014). By moving in accordance with seasonally and locally changing resource availability, migratory animals increase their survival probability and fitness (Hansson & Åkesson, 2014). At the same time, these journeys are costly in terms of time, energy and safety (e.g. Alerstam & Bäckman, 2018; Alerstam & Lindström, 1990; Loonstra et al., 2019; Sillett & Holmes, 2002; Wikelski et al., 2003).
Songbirds can carry only limited amounts of energy (i.e. mainly subcutaneous fat) and migrate by alternating periods of flight with stopover periods, which are used to rest, recover and replenish energetic resources (Schmaljohann et al., 2022; Schmaljohann & Eikenaar, 2017). Since the rate of energy expenditure during migratory flight is much higher than the rate of accumulation during stopover (Alerstam & Lindström, 1990), migrating birds usually spend a greater proportion of their time at stopover sites as compared to actual migratory flights towards their destinations (Schmaljohann et al., 2012; Wikelski et al., 2003).
While multiple aspects of the timing and supply of resources on migration have been studied widely (as e.g. reviewed in McKinnon & Love, 2018; Schmaljohann & Eikenaar, 2017), safety and survival aspects during this life phase are especially difficult to assess (Klaassen et al., 2014; Sillett & Holmes, 2002). Most available information derives from investigations of external factors such as adverse weather (Loonstra et al., 2019; Newton, 2007; Richardson, 1990; Shamoun-Baranes et al., 2017), predation (Cimprich et al., 2005; Houston, 1998) or risk of collision (e.g. de Lucas & Perrow, 2017; Hüppop et al., 2019; Loss et al., 2014). Physiological aspects, such as oxidative stress or an individual bird's health status, have been studied to some extent, but still are largely understudied as compared to the aspects mentioned above (Jenni & Schaub, 2003; Jenni-Eiermann et al., 2014).
An effective immune system is an essential part of a good physical condition, yet it is energetically costly to produce and maintain (e.g. Hasselquist & Nilsson, 2012; Martin et al., 2003). Hence, downregulation of the immune system or reliance on energetically cheap immune functions has been repeatedly found in migrating birds to keep these costs low (Buehler et al., 2010a, 2010b; Eikenaar & Hegemann, 2016; Owen & Moore, 2006). At the same time, exposure to (potentially novel) pathogens is probably higher during migration, due to the diversity of locations, habitats and other birds encountered along the way (Figuerola & Green, 2000; Klaassen et al., 2012). Migrating birds may thus be especially susceptible to pathogens (Eikenaar et al., 2018; Hegemann et al., 2015), suggesting increased benefits for investing in immune function during migration (Buehler et al., 2010a, 2010b; Møller & Erritzøe, 1998).
Here, we investigate whether a songbird's immune status interplays with its migratory behaviour. Considering the complexity of the immune system and differences in associated energetic and pathological costs (Lee, 2006), we measured immune markers specific to both innate [i.e. bacterial killing activity (BKA), lysozyme concentration, natural antibodies (HA) and complement titres (HL)] and acquired/adaptive [i.e. the total concentration of immunoglobulin Y (IgY)] immunity. All these have previously been used as biomarkers for the immune system in various bird species, both for inter- (e.g. Pap et al., 2015; Vincze et al., 2022) and intraspecific comparisons (e.g. Giraudeau et al., 2010; Prüter et al., 2020).
The limited knowledge we have on the relation between birds' immune status and migration makes it difficult to find clear predictions of what to expect with regard to each of the measured parameters. In general, the immune system constantly hinders pathogens from replicating and spreading in the body (Paludan et al., 2021). Producing its effectors and keeping its function up are energetically costly and accordingly immune parameters are usually lower during physically demanding life phases and along with lower levels of energy reserves (Cornelius et al., 2014; Eikenaar, Hegemann, et al., 2019; Owen & Moore, 2006). Within the energetically demanding migration season, individual birds' immune parameters have been measured during stopover and linked to stopover behaviour. At the Swedish Baltic Sea coast, dunnocks Prunella modularis, European robins Erithacus rubecula and song thrushes Turdus philomelos with lower HL scores were found to make longer stopovers (Hegemann, Alcalde Abril, Muheim, et al., 2018; Hegemann, Alcalde Abril, Sjöberg, et al., 2018). Immune challenged birds of the same three species also significantly prolonged their stops, indicating their need for additional time to recover prior to resuming migration (Hegemann, Alcalde Abril, Muheim, et al., 2018; Hegemann, Alcalde Abril, Sjöberg, et al., 2018). Higher concentrations of immune parameters might consequently either reflect a reaction to an acute and ongoing infection (Hegemann, Alcalde Abril, Muheim, et al., 2018; Hegemann, Alcalde Abril, Sjöberg, et al., 2018) or an increased investment in immune parameters (Buehler et al., 2010a, 2010b; Eikenaar et al., 2020; Hegemann, Alcalde Abril, Muheim, et al., 2018; Hegemann, Alcalde Abril, Sjöberg, et al., 2018). Based on these findings, we hypothesize that birds stopping over at the German North Sea coast should adjust their stopover duration in accordance with their individual immunological status.
Beyond stopover, migratory flights might also be linked to an individual bird's immunological status. Bewick's swans Cygnus columbianus bewickii infected with low pathogenic avian influenza were found to cover a reduced overall migration distance as compared to non-infected individuals (van Gils et al., 2007). Evidence that the immune status also influences flight behaviour comes from captive western sandpipers Calidris mauri, where individuals with a higher bacterial killing activity measured 1–3 weeks prior to a wind tunnel experiment willingly flew for longer (Nebel et al., 2013). Yet, to our knowledge, there is no study investigating the link between immune status and migratory flight behaviour in songbirds under free-flying conditions. This is not surprising, as studying migratory behaviour in small free-flying birds is notoriously difficult. Recent advancements in automated radio-telemetry, enabling its use on a larger spatial scale and with increasingly light-weight transmitters, offer new options to track even small species over larger distances (Taylor et al., 2017). Accordingly, it is now possible to study eco-immunological aspects of not only stopover but also flight behaviour (Hegemann, Alcalde Abril, Muheim, et al., 2018; Hegemann, Alcalde Abril, Sjöberg, et al., 2018). With regard to the available studies on non-passerine birds, we hypothesize that individuals in poorer immune status measured during stopover may rather avoid lengthy flights and risky routes (e.g. over large bodies of open water) but prefer taking a series of shorter flights along safer routes.
To assess our hypotheses, we investigated five species of short- to medium-distance migrating songbirds, that is, redwings Turdus iliacus, song thrushes Turdus philomelos, Eurasian blackbirds Turdus merula; blackbirds hereafter, dunnocks Prunella modularis and Eurasian blackcaps Sylvia atricapilla, blackcaps hereafter. The birds investigated here breed in northern Europe and mainly winter in western to south-western Europe (Bairlein et al., 2014). They were caught at several stopover sites along the German North Sea coast during their spring and fall migration, blood sampled, fitted with radio-transmitters and immediately released back into the wild. Their subsequent movements were recorded by a network of radio-receiver stations along the coastline as well as on islands and offshore structures in the German Bight (Brust et al., 2019; Karwinkel et al., 2022; Michalik et al., 2020). By combining immunological and telemetry data, we are able to assess whether there are correlations between a suite of immune parameters and individual stopover behaviour and flight decisions.
中文翻译：
起飞和飞行路线的决定是否与迁徙鸣禽的免疫参数相关？
1 简介
迁徙有利于季节性可用资源的利用和不利环境条件的规避（Chapman 等， 2014）。通过根据季节性和局部变化的资源可用性移动，迁徙动物增加了它们的生存概率和适应性 (Hansson & Åkesson, 2014 )。同时，这些旅程在时间、精力和安全方面代价高昂（例如 Alerstam 和 Bäckman， 2018 年；Alerstam 和 Lindström， 1990 年；Loonstra 等人， 2019 年；Sillett 和 Holmes， 2002 年；Wikelski 等人， 2003 年).
鸣禽只能携带有限的能量（即主要是皮下脂肪）并通过交替的飞行期和中途停留期迁徙，用于休息、恢复和补充能量资源（Schmaljohann 等人， 2022 年；Schmaljohann 和 Eikenaar， 2017 年） . 由于迁徙飞行期间的能量消耗率远高于中途停留期间的能量消耗率 (Alerstam & Lindström, 1990 )，与实际飞往目的地的迁徙飞行相比，候鸟通常在中途停留地点花费更多的时间（ Schmaljohann 等人， 2012 年；Wikelski 等人， 2003 年）。
虽然移民的时间安排和资源供应的多个方面已得到广泛研究（如 McKinnon 和 Love， 2018 年；Schmaljohann 和 Eikenaar， 2017 年的评论），但这个生命阶段的安全和生存方面特别难以评估（Klaassen 等人）等人， 2014 年；Sillett & Holmes， 2002 年）。大多数可用信息来自对外部因素的调查，例如恶劣天气（Loonstra 等人， 2019 年；Newton， 2007 年；Richardson， 1990 年；Shamoun-Baranes 等人， 2017 年）、捕食（Cimprich 等人， 2005 年；Houston， 1998) 或碰撞风险（例如 de Lucas & Perrow， 2017 年；Hüppop 等人， 2019 年；Loss 等人， 2014 年）。生理方面，例如氧化应激或个体鸟类的健康状况，已经在一定程度上进行了研究，但与上述方面相比，在很大程度上仍未得到充分研究（Jenni & Schaub， 2003 年；Jenni-Eiermann 等人， 2014 年）。
有效的免疫系统是良好身体状况的重要组成部分，但其产生和维持的能量成本很高（例如 Hasselquist & Nilsson， 2012 年；Martin 等人， 2003 年）。因此，在候鸟中反复发现免疫系统下调或依赖能量低廉的免疫功能以保持较低的成本（Buehler 等人， 2010a，2010b；Eikenaar 和 Hegemann， 2016 年；Owen 和 Moore， 2006 年）。同时，由于地点、栖息地和沿途遇到的其他鸟类的多样性，迁徙过程中接触（可能是新的）病原体的几率可能更高（Figuerola & Green， 2000 年；Klaassen 等人， 2012 年）。因此，迁徙的鸟类可能特别容易受到病原体的影响（Eikenaar 等人， 2018 年；Hegemann 等人， 2015 年），这表明在迁徙期间投资于免疫功能会增加收益（Buehler 等人， 2010a，2010b；Møller & Erritzøe， 1998 年） ).
在这里，我们调查鸣禽的免疫状态是否与其迁徙行为相互作用。考虑到免疫系统的复杂性以及相关能量和病理成本的差异 (Lee, 2006 )，我们测量了先天特异性免疫标记 [即细菌杀灭活性 (BKA)、溶菌酶浓度、天然抗体 (HA) 和补体滴度 ( HL)]和获得性/适应性[即免疫球蛋白Y(IgY)的总浓度]免疫。所有这些以前都被用作各种鸟类免疫系统的生物标志物，用于种间比较（例如 Pap 等人， 2015 年；Vincze 等人， 2022 年）和种内比较（例如 Giraudeau 等人， 2010 年；Prüter等人， 2020 年）。
我们对鸟类的免疫状态和迁徙之间的关系了解有限，因此很难找到关于每个测量参数的预期结果的明确预测。一般来说，免疫系统会不断阻止病原体在体内复制和传播（Paludan 等人， 2021 年）。产生其效应器并保持其功能的能量成本很高，因此在体力要求高的生命阶段免疫参数通常较低，能量储备水平较低（Cornelius 等人， 2014 年；Eikenaar、Hegemann 等人， 2019 年；Owen & 摩尔， 2006 年). 在精力充沛的迁徙季节，在中途停留期间测量了个体鸟类的免疫参数，并将其与中途停留行为联系起来。在瑞典波罗的海沿岸，研究发现 HL 分数较低的黑眼鹬Prunella modularis、欧洲知更鸟Erithacus rubecula和画眉Turdus philomelos停留时间更长（Hegemann、Alcalde Abril、Muheim 等， 2018 年；Hegemann、Alcalde Abril、Sjöberg等人， 2018 年）。同一三个物种的免疫挑战鸟类也显着延长了它们的停留时间，表明它们在恢复迁徙之前需要更多时间来恢复（Hegemann、Alcalde Abril、Muheim 等， 2018 年）; Hegemann、Alcalde Abril、Sjöberg 等人， 2018 年）。因此，较高浓度的免疫参数可能反映了对急性和持续感染的反应（Hegemann、Alcalde Abril、Muheim 等人， 2018 年；Hegemann、Alcalde Abril、Sjöberg 等人， 2018 年）或增加了对免疫的投资参数（Buehler 等人， 2010a、2010b；Eikenaar 等人， 2020 年；Hegemann、Alcalde Abril、Muheim 等人， 2018 年；Hegemann、Alcalde Abril、Sjöberg 等人， 2018 年). 基于这些发现，我们假设在德国北海沿岸停留的鸟类应该根据它们的个体免疫状态调整它们的停留时间。
除了中途停留，迁徙飞行也可能与个体鸟类的免疫状态有关。发现感染低致病性禽流感的Bewick 天鹅Cygnus columbianus bewickii与未感染的个体相比，总体迁徙距离缩短（van Gils 等人， 2007 年）。免疫状态也会影响飞行行为的证据来自圈养的西部鹬Calidris mauri，其中在风洞实验前 1-3 周测得具有较高细菌杀灭活性的个体愿意飞行更长时间（Nebel 等人， 2013 年）). 然而，据我们所知，尚无研究调查鸣禽在自由飞行条件下的免疫状态与迁徙飞行行为之间的联系。这并不奇怪，因为研究自由飞翔的小型鸟类的迁徙行为是出了名的困难。自动无线电遥测技术的最新进展使其能够在更大的空间范围内使用并配备越来越轻的发射器，提供了新的选择来追踪更远距离的小型物种（Taylor 等人， 2017 年）。因此，现在不仅可以研究中途停留的生态免疫学方面，还可以研究飞行行为（Hegemann、Alcalde Abril、Muheim 等人， 2018 年；Hegemann、Alcalde Abril、Sjöberg 等人， 2018 年）). 关于对非雀形目鸟类的现有研究，我们假设在中途停留期间测量的免疫状态较差的个体可能宁愿避免长途飞行和危险路线（例如，在大片开阔水域上空），但更喜欢沿着更安全的方向进行一系列较短的飞行路线。
为了评估我们的假设，我们调查了五种中短距离迁徙的鸣禽，即红翅Turdus iliacus、画眉Turdus philomelos、欧亚画眉Turdus merula；黑鸟以下，dunnocks Prunella modularis和 Eurasian blackcaps Sylvia atricapilla，blackcaps 以下。此处调查的鸟类在北欧繁殖，主要在西欧和西南欧过冬（Bairlein 等人， 2014 年）). 在春季和秋季迁徙期间，它们在德国北海沿岸的几个中途停留点被捕获，采集血液样本，安装无线电发射器，并立即放回野外。他们随后的活动被德国湾沿岸以及岛屿和近海结构上的无线电接收站网络记录下来（Brust 等人， 2019 年；Karwinkel 等人， 2022 年；Michalik 等人， 2020 年） . 通过结合免疫学和遥测数据，我们能够评估一套免疫参数与个体中途停留行为和飞行决策之间是否存在相关性。
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