Differences in tail feather growth rate in storm-petrels breeding in the Northern and Southern hemisphere: a ptilochronological approach

Moulting and breeding are costly stages in the avian annual cycle and may impose trade-offs in energy allocation between both stages or in their timing. Here, we compared feather growth rates (FGR) of rectrices in adults between two pairs of small pelagic Procellariiformes species differing in moult-breeding strategies: the European storm-petrel Hydrobates pelagicus and Leach’s storm-petrel Oceanodroma leucorhoa breeding in the Northern Hemisphere (Faroe Islands), showing moult-breeding overlap in tail feathers; and the Wilson’s storm-petrel Oceanites oceanicus and black-bellied storm-petrel Fregetta tropica, breeding in the Southern Hemisphere (South Shetlands), temporally separating moult and breeding. We used ptilochronology (i.e., feather growth bar width) to reconstruct FGR reflecting relative energy availability during moult. Based on previous research, we expected positive correlations between feather length (FL) and FGR. Additionally, we expected to find differences in FGR relative to FL between the moult-breeding strategies, where a relatively higher FGR to FL indicates a higher energy availability for moult. To investigate if energy availability during moult in the studied species is similar to species from other avian orders, we used FGR and FL found in literature (n = 164) and this study. We fitted a phylogenetic generalized least squares (PGLS) model to FGR with FL, group (i.e., Procellariiformes vs. non-Procellariiformes) and the interaction FL * group as predictors. As it has been suggested that Procellariiformes may form two growth bars per 24 h, we fitted the same model but with doubled FGR for Procellariiformes (PGLSadj). The group term was significant in the PGLS model, but was not in the PGLSadj model, confirming this suggestion. Individually predicted FGR by the PGLSadj model based on FL, showed that the Southern species have a significantly higher FGR relative to FL compared to the Northern species. Additionally, we found no correlation between FL and FGR in the Northern species, and a positive correlation between FL and FGR in the Southern species, suggesting differences in the trade-off between feather growth and size between species from both hemispheres. The observed differences between the Northern and Southern species may be caused by different moult-breeding strategies. The Southern species may have had more energy available for moult as they are free from breeding duties during moult, while the Northern species may have had less free energy due to a trade-off in energy allocation between breeding and moulting. Our study shows how different moult-breeding strategies may affect relative nutritional condition or energy allocation during moult of migratory pelagic seabirds.


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Moulting and breeding are energetically costly stages of the annual cycle of birds. The 47 costs of feather synthesis can be illustrated by the fact that metabolic rate during moult increases 48 by more than 100% compared to pre-moulting (Lindström, Visser & Daan, 1993). Feather 49 production costs are linked with body mass in a way that moult is relatively more demanding for 50 smaller birds (Lindström et al., 1993). Additionally, moult gaps in the remiges and/or rectrices 51 formed after losing old feathers reduce aerodynamic performance, mostly through affecting Manuscript to be reviewed 3 manoeuvrability (Hedenström & Sunada, 1999;Slagsvold & Dale, 1996) and less so through 53 increased flight costs (Hedenström & Sunada, 1999). 54 The costs of breeding (e.g. incubation and chick provisioning) are apparent in the 55 increased field metabolic rates (e.g. 11% from incubation to chick rearing in Australasian 56 gannets, Morus serrator) (Green et al., 2013) and increased stress levels (e.g. higher feather providing some flexibility in allocation of energy between moulting, breeding and migration. 73 The extent of this flexibility partially depends on environmental circumstances (e.g. day-length 74 linked to latitude or food availability) (Hemborg et al., 2001), and the trade-off between 75 moulting and breeding may even differ strongly between closely related species (e.g. in  Investigating the trade-off in energy allocation between moulting and breeding may be 86 challenging in pelagic seabirds as they are only available for researchers when they come to land 87 for breeding. As at least part of the moulting period is often completed away from the breeding 88 colony, studying their energy management during feather growth may prove difficult.

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Ptilochronology may offer a way to retrospectively determine the relative amount of energy 90 availability during moulting in seabirds, and so evaluate their energy allocation towards feather 91 production. The method is based on feather growth rate, which is determined by the mean feather Manuscript to be reviewed 4 growth bar width (Grubb, 1989(Grubb, , 2006

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A similar correlation has been found between feather growth rate and body size, with larger 106 species having higher absolute feather growth rates, but lower relative growth rates per unit of 107 body size (Rohwer, Ricklefs, Rohwer & Copple, 2009).

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The aim of our study was to compare relative energy availability during moult between 109 pelagic storm-petrel species with contrasting moult-breeding strategies, i.e. moult-breeding 110 overlap or non-breeding moult. In order to understand the inter-and intra-specific differences in 111 energy availability during moult we compared feather growth rates with feather length.

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Additionally, to infer the relative energy allocation for each of the species towards moulting, we 113 compared their observed feather growth rate with feather growth rate data for other species found 114 in literature. This study is the first to compare differences in expected feather growth rates 115 between similar species breeding in both hemispheres. Due to their small size and pelagic life-116 style the non-breeding period of storm-petrels can be hard to study but thanks to recent 117 developments in technology specific migration routes of some species are being discovered

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Our study adds to the understanding of storm-petrel migratory, moulting and breeding strategies 120 by giving some, admittedly indirect, insights into their energy management.

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Since larger feathers have been linked to a higher growth rate both within (de la Hera, growth bar width both within and between the four storm-petrel species. Since the studied 125 species adopt contrasting moult-breeding strategies, we expected to find differences in feather 126 growth rate relative to feather length between the two strategies, indicating differences in relative 127 energy allocation towards moult.    We collected the right outermost rectrix from adults of the four species of storm-petrels. 166 In 2018 32 adults were recaptured that were previously caught in 2017, with fully formed 167 rectrices. Additionally, one Wilson's storm-petrel was recaptured within 2018 with a fully 168 regrown rectrix, though the regrown feather has not been used for the statistical analyses. We did 169 not notice anything untoward in their tail feathers, or during the analyses (e.g. obvious outliers), Manuscript to be reviewed 6 which leads us to assume that our plucking of the feathers did not cause long-term harm to the 171 birds. See below for pseudo-replication management.

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All individuals of the Northern species and some individuals of the Southern species 173 were captured in mist-nets, which could lead to uncertainty in the breeding stage of the adults.   Grubb (1989). A new piece of paper was used for each feather. We 197 used mean growth bar width per feather as a proxy for feather growth rate (FGR).

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Since we sampled the Southern species during two field seasons, we investigated the 200 inter-annual differences in FGR and FL using a Welch t-test (t.test, package stats in R version Wilson's storm-petrels, we deemed the absolute differences in FGR between the years small 205 enough (high overlap of the 95% confidence ellipses, Fig. S1) to justify pooling the data. FL did 206 not differ significantly between the years for either species (Welch t-test; WSP: t216.29 = -0.549, p 207 = 0.584; BBSP: t29.706 = -0.519, p = 0.608), and therefore we also pooled these data.

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The Spearman's rho correlations showed significant, positive relationships between mean 304 growth bar width and feather length for the Southern storm-petrel species, but not for the 305 Northern species. Additionally, using the PGLS model, we found that the Southern species had a 306 higher feather growth rate than predicted while the Northern species had a lower feather growth 307 rate than predicted.

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The difference in residual length between the studied species, and between the 309 hemispheres may be associated with a difference in relative energy availability during moulting 310 between species of both hemispheres, possibly caused by their different moult-breeding strategy.

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The Southern species, both moulting during the non-breeding period (Beck & Brown, 1972), are 312 free from breeding duties during moult and may use all available energy for feather synthesis,      Indeed, after doubling the feather growth rate of the Procellariiformes, their correlation between 363 feather growth rate and feather length was very similar to that of the other orders (Fig. 2B), as 364 shown by the lack of a significant group effect in the PGLSadj model. This seems to confirm 365 Langston and Rohwer's (1996) suggestion that Procellariiformes form two growth bars per 24 h.

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The four studied storm-petrel species may also have two activity-rest cycles per 24 h, which is 367 consistent with the main prey activity of the studied storm-petrels during the breeding season, albatrosses (Hedd & Montevecchi, 2006;Siegel, 2012), and several seabirds, including storm-370 petrels, forage in more oceanic habitats during the non-breeding period where they seem to 371 increase their intake of myctophid fish (Watanuki & Thiebot, 2018). 372 We are aware of several possible limitations of the present study. Although growth bar 373 widths have originally been linked to relative nutritional condition (Grubb, 1989;Hill & 374 Montgomerie, 1994), it is not a direct measurement of food availability and the results should be 375 interpreted with caution in that regard (Murphy and King, 1991). In this study we used feather 376 growth rate as a way to retrospectively infer energy availability during moulting, as direct 377 examinations of diet and food availability during moulting were impossible due to the pelagic 378 nature and small body size of our study species. In order to put the feather growth rates observed 379 in our study species into perspective, we compared their growth rates with data found in were not. Additionally, nests of Wilson's storm-petrels were more accessible and concentrated 395 than black-bellied storm-petrel nests, which were spread out over larger areas and more often 396 located on inaccessible cliffs and ledges. Nevertheless, our study provides the first comparison of 397 relative energy availability during tail-feather moult of storm-petrels differing in moult-breeding 398 strategies and breeding in different hemispheres.

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Our results suggest that for many pelagic seabirds ptilochronology may be a useful, non-400 invasive, and often only feasible, tool to study their relative energy allocation to feather growth  12 showed distinct differences in relative energy availability between four species of storm-petrels. 410 The Southern species had a higher feather growth rate than predicted by a model based on data 411 from multiple species and orders, while the Northern species had a lower feather growth rate 412 than predicted. We suggest that all these differences can be attributed to the different moult-  Manuscript to be reviewed Manuscript to be reviewed Manuscript to be reviewed Manuscript to be reviewed Manuscript to be reviewed Manuscript to be reviewed Figure 1 Correlation between feather growth rate (FGR) and feather length (FL) for all four studied storm-petrel species.
European storm-petrels (ESP) are shown in purple; Leach's storm-petrels (LSP) in blue; Wilson's storm-petrels (WSP) in green; black-bellied storm-petrels (BBSP) in yellow. Species from the Northern Hemisphere are shown with dots, species from the Southern Hemisphere with triangles. See Table 1 & 2 for statistical analyses.    Table 3 for model description and Table 4 for model comparison.