Energetics and fuel use vary with migration strategy across populations of Common Blackbirds

Read the free Plain Language Summary for this article on Journal blog. Migration is often an endurance event that requires sufficient fuel. While human athletes fail to eat optimally before competitions may cost themselves a chance at medaling or qualifying future events, wild animals fuel properly undertaking migrations face reduced fitness from missed breeding opportunities starvation (e.g. Biebach, 1985; Brodersen et al., 2008). Just as humans vary in their exercise regimes, species enormously propensity and capacity migrate well migratory modes which range diel vertical migration pelagic zooplankton (Lampert, 1989) annual circumpolar terns (Egevang 2010). Because costs benefits of spatiotemporally across habitats species' ranges Alerstam & Lindström, 1990; 2014), individuals populations within also distances they (Adriaensen Dhont, Kaitala 1993; Linek 2021; Lundberg, 1988; Zúñiga 2017). These diverse types require different amounts forms energy Bairlein, Berthold, 1984; Biebach 1986). Regardless total distance, birds primarily use fat previous studies suggest provides approximately 90% used long-distance flights (Bairlein, 2002; Bairlein Gwinner, 1994; Guglielmo, 2018; Jenni Jenni-Eiermann, 1998; McWilliams 2004; Ramenofsky, 1990). Compared with proteins carbohydrates, lipids contain eight times per unit wet mass, making stored most efficient source migrating (Jenni 1998). Birds appear take advantage density prior during stopovers by accumulating large fat, nearly doubling body mass due gain 2003; 2018). Previous alter intake dietary composition, providing evidence have both metabolic behavioural control over amount composition accumulate 1991). Numerous documented hyperphagia period (reviewed 1994) increased food utilization efficiency, result assimilation 1987). Studies degree related distance feeding en route, such further need more complete Hedenstrom Alerstam, 1997). During flight, omega-3 omega-6 polyunsaturated fatty acids (n-3 n-6 PUFAs), particular linoleic acid (18:2n-6; LIN) alpha linolenic (18:3n-3; ALA), be particularly important readily oxidizable sources (Guglielmo, 2010, Price, For example, found birds, including those measured migration, are able mobilize greater proportion PUFA, multiple double bonds, compared monounsaturated (MUFAs) saturated (SFAs) shorter carbon chain higher rates longer lengths (Price 2009; Price 2011). Early specifically PUFA suggested shorebirds seek out high n-3 foods stopover (Maillet Weber, 2006), potentially improving flight performance (i.e. natural doping) through muscle oxidative 2007). Findings subsequent laboratory were fed specific diets provide mixed findings about relative roles versus exact mechanisms fats might enhance Dick 2019a, 2019b; 2020; Nagahuedi 2010; 2009). instance, recent study al. (2020) European starlings Sturnus vulgaris expend 11% less when containing LIN ALA MUFA oleic (18:1n-9), but consuming experienced damage. In contrast, Guglielmo recently altered phospholipid decreased yellow-rumped Warblers Setophaga coronata content vs. n-6) did not lead differences (2019a) damage (2019b). Consequently, additional integrative work needed understand how metabolize acids. Species unique opportunity understanding seasonal shifts lipid metabolism preparations. Here, we examined songbirds select after restlessness Zugunruhe) varies strategy single species. We studied Common Blackbirds Turdus merula because blackbirds model system widely strategies (Biebach, 1977; Schwabl, 1983), thereby permitting partial transplant experimental design. Populations eastern Poland northern Russia fully migratory; Germany partially Spain southern France resident (Linek 2021). This Russia, southwest identical same environmental conditions, day length temperature, allowed us identify population-level independently geographic variation resources availability nutritional composition) cues. Our aviary permitted ask sedentary lifestyles increase relax selection storage oxidation fats. Before autumn season, orally administered 13C-labelled stearic (18:0), (18:2n-6) (18:3n-3) tracers then via 13C enrichment CO2 breath samples (McCue, 2011; McCue Welch, 2016). method determine extent oxidizing compounds fuel, resulting being exhaled breath. selected these several them make up substantial proportions pre-migratory deposited thought Pierce 2005, 2014) suite 18-carbon compounds, included SFA, MUFA, explore effects unsaturation bond position 2008, To accumulation varied collected 13CO2 analyses twice: (1) onset Zugunruhe (September) (2) end (late October), determined based radio telemetry freely moving outdoor aviaries. individual resting restless. predicted oxidization differing desaturation number bonds would combination season strategy. Based 2008), expected all generally bonds. PUFAs fuels 2020) been shown levels residents (Jensen 2020). Therefore, ALA) either SFA between sampling periods. oxidize Zugunruhe, whereas differ season. Wild caught mist nets Malinki, (55.45821°N, 37.17912°E) 2013 2015, Radolfzell, (47.77355°N, 9.04902°E) 2015 2018, Bollène, (44.27589°N, 4.72177°E) 2014, 2018 (Table S1). Capture transfer French was approved under permit DDTM34-2019-06-10454 Direction départmentale des territoires de la mer (DDTM). German permits 35-9185.81/G-17/109 35-9185.81/G-20/95 Regierungpräsidium Freiburg. Russian following §44 §6 Federal Law Federation No. 52 24 April 1995, obtained (withdrawal) wildlife objects listed game BC-02-04/32-5935 (26 2013) Service Supervision Natural Resources (Rosprirodnadzor), 2 (4 November 4 (18 March 2015) Ministry Ecology Nature Management Moscow District. quarantined 40 days transferred Animal Disease Control Station Southern Administrative District (Sovetsky Veterinary Hospital). Export FC/UVN-01/57843 June 2013), FC/UVN-01/93276 (06.05.2014), FC/AP01/127093 (20 Phytosanitary Surveillance (Rosselkhoznadzor). quarantine, analysis faecal infectious agents (Ornithosis [DNA Chlamydophila psttaci], Influenza virus type A RNA, Salmonellosis, Helminths) carried City Laboratory Association (veterinary sanitary inspection reports 193482, 193510, 16428/5, 16428/1, 16428/4). Captured transported our facility (47.7646°N, 8.9961°E). Additional bred 2014 2017 S1) experiment 2020. After facilities, paired housed semi-natural aviaries (L × B H m: 3.5 2.5 2.5). They received mixture food: live mealworms Tenebrio molitor, earthworms Dendrobena spp.; frozen fly larvae Alphitobius diaperinus; pellets Orlux Uni Pate Premium, Insect Country's Best Floating Micro, Nutribird T16 (all Versele-Laga) Granivit (Chemivit); vitamins minerals (Korvimin, Vitakalk) water ad libidum. The (Zugunruhe) each using continuous automated receiving (ARU, Sparrow Systems Fisher) attached mounted H-antennas (ATS) facility. fitted 60 (n = 20 Russian; n German; individuals; 10 male/female pairs; Table transmitter (≤2.6 g; frequencies 165 mHz band, pulse width: ms, interval: 3600 ms; means leg loop harness. Two ARUs searched deployed transmitters every 240 s, recording values signal noise. ARU 28 search 32 transmitters. placed so no signals pre-programmed missed. enabled activity monitored near basis. quantified comparing change strength recordings dB threshold (see 2016 details calibration general procedures System). Raw data visually inspected artefacts malfunctioning processed provided binary estimate whether bird active min throughout study. Individual month early September (Partecke 2007; 2016) remained until early-December period. characterized timing complementary methods. First, calculated time spent 2-h period, hour sunset sunrise 2017) described above. looked changes average nocturnal implementing changepoint (Killick Eckley, 2014; Van Doren 2017), penalized identifies mean variance series data. Changes identified where there than one individual, periods elevated (Helm 2019; Using changepoints, peak consistent manner populations. Individuals without noted calculate percentage population expressed Zugunruhe. confidence intervals exhibiting non-parametric bootstrap. captured adult hand combined /13C-labelled pre−/early (‘before Zugunruhe’) late/post-migratory (‘after (Figure 1a,b: Date early: 9 2020 late: 22 October 36 tracer had daily meal animal caretakers forage typically pairs, pair avoid repeatedly disturbing minimize social stress partner removed. capture, immediately cloth bags adjacent indoor laboratory. laboratory, weighed nearest 0.1 g Ohaus Scout Pro STX balance. acclimating respirometry chamber 15 min, 20-mL syringe (Poulten und Graf GmbH, Fortuna Series, DE) collect background sample drawing excurrent gas into mL min−1 injecting helium-evacuated 12-mL-vacutainer vials (Labco Limited). taking sample, gavaged three bolus 50 mg (Cambridge Isotope Laboratories, Inc; USA) (SA, 18:0), (OA, 18:1n-9), (LA, 18:2n-6) alpha-linolenic (ALA, 18:3n-3) suspended 0.5 sunflower oil 1.5 mm gavage needle (McCue Each only labelled compound Zugunruhe’ ‘after Zugunruhe’). measurable remains 30 administration, returned respired Exetainers (over 3 h) procedure Thereafter, libitum. δ13C vial analysed HeliFANPlus nondispersive infrared spectrometer (Fischer, Analysen Instrumente GmbH; Germany) interfaced FANas autosampler previously Guzman, 2015; McCue, Passement, Plasman 2019). Internal calibrations conducted round 60) unknown built-in standards manufacturer. Additionally, gases known (hereafter: standards) run triplicate detect correct any minor baseline drift. consisted two cylinders custom-blended representing abundance −36‰) artificial 495‰) verified aliquots University Arkansas Stable Laboratory. reported terms units ‘per mil’ (‰ Vienna Pee Dee Belmnite (VPDB) ratio 12C 0.0112372). As part measurements dosing, October. again December routine husbandry. investigate measurement periods, normalized against individual. individuals, modelled relationship response variable Gaussian linear interaction populations, sex, wild-caught aviary-bred performed pairwise post-hoc comparisons estimating marginal least-square group (modality sex population) R. sex. group. if individual-, sex- energetics ‘before’ rate mixed-effects (LMM) fixed predictors identity random effect. tested percent ALA, LA, OA SA dose oxidized generalized LMMs Gamma error structure log link. (nmols) origin, date ID global above type, predictors. spanned weeks trend females earliest (28 September, 95% CI October) males latest (19 November). median 1a,b). However, differed (LM, F11,45 1.206, p 0.31, Adj. R2 0.04) significant. find accounting population, origin aviary-bred) 1.309, 0.25, 0.06), undergoing having greatest proportion, intermediate German, least (proportion observed bootstrap: 0.85, 0.62–0.95, 0.63, 0.40–0.81, 0.45, 0.25–0.66). Post-hoc estimated contrasts significant (Russian—French, odds 0.144, 0.03). Between late male female gained significantly weight Germans gaining combinations 1c; [g], RU 5.10, 2.72–7.48, 6.79, 4.41–9.18, DE −1.93–2.83, 1.08, −1.30–3.47). Both (Males RU—DE, t65 2.75, < 0.05, Females 3.38, 0.05). addition, put FR—DE, 2.35, There whole organism S2) sexes (LMM, Population: F1,65.56 0.53, Sex: F1,65.57 3.57, 0.063) mass-specific 1.68, 0.20, F1,65.55 1.67, 0.19). nor Across types, oleic, (cumulative %: 0.03% dose, 0.02%–0.05%; 0.59% 0.38%–0.92%; 0.53% 0.33%–0.83%; 0.40% 0.26%–0.63%). All Kenward–Roger stearic—oleic, z 9.066, 0.05; stearic—linoleic, 8.98, stearic—alpha-linolenic, 7.78, Similarly, second post 0.61% 0.39%–0.95%; 0.57% 0.37%–0.87%). 3.678, 3.47, (t −1.224, 0.221). non-significant decreasing 180 ALA. similar pattern maximal acids, wherein lower (maximal rate: 0.86 nmol, 0.53–1.4 nmol; 11.67 7.39–18.46 9.84 6.16–15.73 5.89 03.78–9.21 nmol). 7.94, 7.67, 5.73, 3.9 2.45–6.24 10.30 6.60–16.08 9.01, 5.78–14.02 hoc 3.27, 3.02, 2.62, −1.379, 0.17). first 180-min trial 1d; cumulative [%], 0.58% 0.39–0.88, FR 0.24% 0.16–0.36, 0.17% 0.12–0.26). (ALA % RU—FR, 2.859, 4.32, opposite pattern—Russian 0.43% 0.29–0.63, 0.83% 0.55–1.3, 0.65% 0.44–0.94). 2.43, 0.05) 1.49, 0.30). early—late, 10.231, 8.99, difference 1e,f). 1g; dose: 0.04%–0.24% 4.00, 0.02%–0.34% 6.34, 0.02%–0.12% 3.99, oxidized. (stearic nmol: 1.1–4.2 3.76, 0.5–5.4 6.61, 0.6–2.1 3.36, 0.05), none models, oxidation. study, showed preparations expression gain, metabolism, mode shared conditions. Remarkably, despite captivity 7 years hatching S1), went year-round demonstrated preferentially post-migratory even area consist non-migratory individuals. pre- highest experiencing (Zugunruhe). Together, environment. demonstrate among upon diversity especially (McWillia