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Timing Manipulations Reveal the Lack of a Causal Link Across Timing of Annual-Cycle Stages in a Long-Distance Migrant Barbara M

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Timing Manipulations Reveal the Lack of a Causal Link Across Timing of Annual-Cycle Stages in a Long-Distance Migrant Barbara M © 2019. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2019) 222, jeb201467. doi:10.1242/jeb.201467 RESEARCH ARTICLE Timing manipulations reveal the lack of a causal link across timing of annual-cycle stages in a long-distance migrant Barbara M. Tomotani1,2,*, Iván de la Hera1,3, Cynthia Y. M. J. G. Lange1, Bart van Lith1, Simone L. Meddle4, Christiaan Both5 and Marcel E. Visser1,5 ABSTRACT and Wingfield, 2000; Wingfield, 2008). Annual cycles vary in Organisms need to time their annual-cycle stages, like breeding and complexity in a species-specific way: from simple breeding/non- migration, to occur at the right time of the year. Climate change has breeding transitions to the inclusion of other energetically demanding shifted the timing of annual-cycle stages at different rates, thereby stages like migration or moult (Wingfield, 2008). As the total time tightening or lifting time constraints of these annual-cycle stages, a available for the allocation of these seasonal stages is 1 year, more rarely studied consequence of climate change. The degree to which complex annual cycles will necessarily involve a concomitant increase these constraints are affected by climate change depends on whether in time constraints. This is especially true if these different stages are consecutive stages are causally linked (scenario I) or whether the all energetically demanding and need to be temporally segregated timing of each stage is independent of other stages (scenario II). (Dietz et al., 2013). Complex annual cycles would thus result in low Under scenario I, a change in timing in one stage has knock-on timing flexibility as further shortening or overlapping stages would lead to effects on subsequent stages, whereas under scenario II, a shift in the fitness costs (Jacobs and Wingfield, 2000; Wingfield, 2008). timing of one stage affects the degree of overlap with previous and To achieve synchronization between annual-cycle stages subsequent stages. To test this, we combined field manipulations, and environmental cycles, organisms use predictive cues, with captivity measurements and geolocation data. We advanced and photoperiod and temperature as the most relevant ones (Dawson, delayed hatching dates in pied flycatchers (Ficedula hypoleuca) and 2015; Wingfield, 2008; Winkler et al., 2014). While photoperiod is measured how the timing of subsequent stages (male moult and important as a long-term predictive cue, because it remains migration) were affected. There was no causal effect of manipulated unchanged across the years (Gwinner, 1989), temperature hatching dates on the onset of moult and departure to Africa. Thus, provides short-term temporal information for fine-tuning timing advancing hatching dates reduced the male moult–breeding overlap within a particular year and allows organisms to match their timing with no effect on the moult–migration interval. Interestingly, the with the year-to-year variation in optimal timing (Dawson, 2005; wintering location of delayed males was more westwards, suggesting Schaper et al., 2012; Visser et al., 2004, 2009). The importance of that delaying the termination of breeding carries over to winter photoperiod and temperature as cues varies across annual-cycle location. Because we found no causal linkage of the timing of annual- stages. Hence, increasing temperatures due to climate change will cycle stages, climate change could shift these stages at different cause shifts in the timing of stages that are temperature sensitive, rates, with the risk that the time available for some becomes so short such as reproduction (Knudsen et al., 2011; Parmesan, 2006; Visser that this will have major fitness consequences. and Both, 2005), while other stages may not shift if mainly affected by photoperiod or circannual rhythms (Both and Visser, 2001; KEY WORDS: European pied flycatcher, Ficedula hypoleuca, Tomotani et al., 2018a; Visser et al., 2004). How this affects the Climate change, Migration, Moult, Reproduction whole annual cycle, however, depends on how stages are interrelated (Crozier et al., 2008; Hera et al., 2013). INTRODUCTION One possibility is the existence of a tight link between stages. In Organisms living in seasonal environments, such as temperate zones, this scenario (scenario I: linked), the timing of a given stage depends are generally exposed to predictable changes in environmental strongly on the timing of the previous one(s). Such temporal links conditions that determine the organization of their annual-cycle across stages could be caused, for example, by pleiotropic effects of stages. As some of these stages, such as breeding and migration, are hormones regulating the transitions between stages (Dawson, 2006; energetically costly, their occurrence needs to be timed correctly to Jacobs and Wingfield, 2000; Williams, 2012). This would mean that match favourable conditions (Enright, 1970; Gwinner, 1996; Jacobs even if one stage is sensitive to temperature and the other not, shifts in a given stage would cause similar shifts in the subsequent ones. For 1Department of Animal Ecology, Netherlands Institute of Ecology (NIOO-KNAW), instance, in an experiment with captive juvenile Eurasian blackcaps 6708 PB Wageningen, The Netherlands. 2Museum of New Zealand Te Papa (Sylvia atricapilla), migratory activity was only initiated after the Tongarewa, Wellington 6011, New Zealand. 3School of Biological, Earth and completion of moult; thus, the interval between the two stages was Environmental Sciences, University College Cork, Cork, Ireland T23XA50. 4The Roslin Institute and Royal (Dick) School of Veterinary Studies, University of fairly constant among individuals (Pulido and Coppack, 2004). Edinburgh, Easter Bush, Midlothian EH25 9RG, UK. 5Groningen Institute for Under this scenario, climate change would not increase or decrease Evolutionary Life Sciences, University of Groningen, 9747 AG Groningen, the overlap of stages. However, depending on the magnitude of the The Netherlands. shift, stages could be displaced in time and desynchronized from the *Author for correspondence ([email protected]) optimal environmental conditions for that stage. Alternatively, consecutive stages may not be linked (scenario II: B.M.T., 0000-0002-8855-4803; C.Y.M.J.G.L., 0000-0003-0327-6726; M.E.V., 0000-0002-1456-1939 independence). Thus, if the effect of cues varies between stages, climate change will lead to shifts in the timing of annual-cycle Received 20 February 2019; Accepted 8 August 2019 stages with different rates, causing an increase or decrease in the Journal of Experimental Biology 1 RESEARCH ARTICLE Journal of Experimental Biology (2019) 222, jeb201467. doi:10.1242/jeb.201467 degree of overlap between events. This could result in time (Hemborg, 1998, 1999; Hemborg and Merila, 1998; Tomotani constraints being tightened or lifted throughout the annual cycle et al., 2018b). We were mostly interested in how adult males were because a shift in one stage would lead to more time in one part of affected; because they supposedly invest less in their current the cycle, but subsequently may result in less time available for reproduction, males present a larger moult–breeding overlap than other stages. For example, between 1980 and 2000, European pied females. Moreover, males have a higher fidelity to the breeding area flycatchers (Ficedula hypoleuca) advanced egg-laying dates more (Both et al., 2016), making them more suitable for evaluating the strongly than their arrival dates at breeding grounds, associated with effects of our manipulations. Thus, after the chick-rearing phase, we climate change. This has led to a shorter interval between arrival and monitored the males’ post-breeding moult by temporally keeping breeding, constraining how much laying dates could continue to them in captivity, their moult control via analyses of the hormone advance with increased climate change (Both and Visser, 2001; prolactin and, after release, the timing of their autumn migration and Tomotani et al., 2018a). wintering site selection using light-level geolocators. Finally, it is also possible that both of the above-mentioned The timing of moult and departure could (scenario I) depend on a scenarios occur in different parts of the cycle (Salis et al., 2017; previous stage (linked). Such a previous stage could be: (Ia) Tomotani et al., 2016). For example, it has been suggested that pre- termination of breeding, the manipulated stage; thus, shifting the breeding stages are more time selected than post-breeding stages, and termination of breeding also shifts the onset of moult and migration; are, as a result, less plastic (Conklin et al., 2013; Karagicheva et al., or (Ib) spring arrival or onset of breeding, which are non-manipulated 2016). Under that perspective, it would be expected that pre-breeding stages. Alternatively, (scenario II) timing does not depend on a stages are more likely to fall under scenario II than post-breeding previous stage (independence). It could, for example, simply depend stages. Because these two scenarios have very different consequences on photoperiod or other cue(s), but not on the timing of breeding. in terms of costs of climate change, understanding annual-cycle Notice that in both scenarios Ib and II, the timing of moult and adaptation to environmental changes requires knowledge on how migration departure will not be related to the manipulation, but, while consecutive stages are temporally linked. between-year variation in the timing of moult and migration will
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