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Captured free-living male mallard Anas platyrhynchos at Abberton in southern Britain showed peak mass gain immediately prior to simultaneous remex moult. Individuals of both sexes were heavier before shedding wing feathers than when flightless confirming literature accounts that show mallard accumulate fat stores in anticipation of moult to contribute to meeting energy needs during remex re-growth. Over the course of four seasons, males lost 13 17% of initial body mass on average during re-growth of flight feathers, females 13 23%. Based on energy expenditure of 1.3 times BMR, male mallard were estimated to be able to fulfil 42 60% and females 41 82% of their energy needs throughout moult from stores. Free-flying male mallard fed ad libitum in a predator-free environment did not differ in starting body mass or rate of mass loss during wing moult compared to free-living Abberton birds, suggesting depletion of fat stores, irrespective of available sources of exogenous energy. Based on this evidence, we reject that the hypotheses that mass loss in moulting mallard is due to 1) simple energy stress and 2) restrictions on feeding and consider that 3) attaining the ability to fly at an earlier stage on incompletely grown flight feathers is not the primary factor shaping this trait. Rather, we consider the accumulation and subsequent depletion of fat stores, together with reductions in energy expenditure, enable mallard to re-grow feathers as rapidly as possible by exploiting habitats that offer safety from predators, but do not necessarily enable them to balance energy budgets during the flightless period of remex feather re-growth.
Virtually all wildfowl undergo simultaneous remex moult, re-growing flight feathers in a way that renders birds temporarily flightless. Mallard Anas platyrhynchos are flightless for 22 7 d (Owen and King 1979, Panek and Majewski 1990), during which time the inability to fly reduces the potential to escape predation and to move between profitable foraging opportunities (Hohman et al. 1992). In addition to these constraints, increased energy demand has been demonstrated to meet the costs of feather growth (Payne 1972, Thompson and Boag 1976, Dolnik and Gavrilov 1979, Qian and Xu 1986, Portugal et al. 2007), estimated at 1.3 times basal metabolic rate in mallard (Prince 1979). Faced with reduced mobility, mallard could meet the enhanced energy needs of growing new flight feathers through the adoption of one or more of three potential strategies: 1) compensatory food consumption (Hartman 1985); 2) reduction of energy consuming activities (inability to fly already profoundly reduces energy expenditure, Guillemette et al. 2007, but see also Portugal et al. 2010); 3) exhibit phenotypic plasticity, reconstructing body parts to minimise energy consumption and utilising body stores of fat and protein (accumulated prior to moult) to offset temporary increased demand (Young and Boag 1982, Fox and Kahlert 2005, Fox et al. 2008).
Young and Boag (1982) showed that during the flightless period, there was a significant decrease in mallard flight muscle mass and increase in leg muscle mass consistent with the predictions arising from the hypothesis of phenotypic plasticity (Ankney 1979, 1984, Fox and Kahlert 2005). Despite major changes in muscle architecture, these tend not to contribute to major overall changes in body mass during flightless moult in most studied Anatidae (Ankney 1979, 1984, Thompson and Drobney 1996). However, many European dabbling ducks (Sjöberg 1988, Panek and Majewski 1990, King and Fox 2012) and diving ducks (Fox and King 2011) conspicuously lose mass during flightless moult (although others do not, Fox et al. 2008), most likely due to consumption of body fat stores. Just as in the case of Saltholm moulting greylag geese Anser anser (Fox and Kahlert 2005), Folk et al. (1966) reported mass loss in moulting mallard and Young and Boag (1982) documented a reduction in fat stores in mallard through moult, although they asserted there was no overall change in total carcass lipid, total protein or total body mass. However, Panek and Majewski (1990) showed 12% declines in body mass amongst males and females through moult. So do mallard consistently lose body mass during moult and if so what is the explanation?
There has been debate as to whether such mass loss in moulting ducks is: 1) an adaptive trait, whereby fat stores provide an endogenous source of energy to regrow feathers as rapidly as possible whilst reducing reliance on external energy sources, access to which involves predation risk (as suggested for some geese, Fox and Kahlert 2005); 2) a simple reflection of the elevated energetic costs of feather synthesis which birds meet by catabolism of body ‘reserves’ (the energetic stress of Hohman 1993) rather than body ‘stores’ acquired specifically to fuel the process (sensu van der Meer and Piersma 1994); 3) due to predation risk, that imposes cryptic feeding behaviour and exploitation of habitats where foraging is less effective, such foraging constraints necessitate exploitation of fat (which does not necessarily preclude pre-moult accumulation of fat stores, Panek and Majewski 1990) and 4) because lighter body mass enables Anatidae to regain the capability of flight earlier on incompletely re-grown flight feathers earlier than if heavier (Owen and Ogilvie 1979, Brown and Saunders 1998).
In this paper, we first analyse changes in total body mass of free-living mallard captured during the flightless period to test whether or not they lose body mass during moult. Secondly, we look for support for the different explanations of how mallard would meet the enhanced energy demands during wing moult and assess whether body mass loss is an adaptive trait or should be explained by the alternative hypotheses. We use wing length as a measure of moult stage to examine how mass changes as birds move towards the point at which they regain the powers of flight. We also compare these results with those from free-flying male mallards provided with a non-limiting supply of food which select to moult in an artificially maintained predator-free area, to test whether observed patterns are the result of food limitation in the wild during the moult period or if the patterns can be considered adaptive. Males moult before females, so if mallard show adaptive mass (i.e. fat store) gain to meet the demands of wing feather replacement, we expect 1) body mass to peak just before the onset of moult and 2) that male mass would peak prior to their flightless period correspondingly earlier than females. The peak in body mass prior to wing moult would fail to support hypotheses 2) and 4) above, and if mallard fed ad libitum lost mass at the same rate as free flying birds, this would provide additional evidence for patterns of fat accumulation and depletion to meet the demands of moult, rather than simply result from energetic stress, i.e. consumption of reserves to meet energy demands contra stores (sensu van der Meer and Piersma 1994). Furthermore, because ad libitum fed males were present in a predator-free environment, we would expect there to be no feeding constraint on them and therefore if birds still lost mass under these circumstances this would fail to support hypothesis 3).
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Male mallard caught during the moult in 1978 at Abberton showed peak mass levels immediately prior to the most intensive period of wing moult for each sex. Females showed a similar pattern, although failing to reach statistical significance, but literature sources confirm that females attain peak body mass later than males in relation to moult (Cramp and Simmon 1977, Pehrsson 1987). During the peak period of moult, individuals of both sexes were significantly heavier pre-moult than those which had already shed old feathers and were re-growing new ones. Several studies have shown elevated body mass in both sexes amongst mallard immediately preceding remex moult (Folk et al. 1966, Young and Boag 1982 and Pehrsson 1987, the latter amongst captive birds). We therefore contend that Abberton mallard accumulated mass (in all probability fat stores) in advance of wing moult, a feature of the annual mass dynamics of mallard, gadwall Anas strepera, teal A. crecca and pintail A. acuta according to Oring (1969) and Cramp and Simmons (1977). All of these species then subsequently lose mass during flight feather moult (Cramp and Simmons 1977, Sjöberg 1988, King and Fox 2012). The fact that peak mass was attained immediately prior to the most intense period of moult earlier in males (21 June) than in females (17 August, given the delay and prolonged moult in females compared to males) provides some additional support for theory that this mass gain is specifically associated with meeting the future demands of wing moult, confirmed by Folk et al. (1966). This suggests that mallard acquire post-breeding fat stores to meet the energetic challenges of wing moult just as they do at other stages in the annual cycle. For instance, it is demonstrated that migratory mallard accumulate anticipatory fat stores for migration, to meet energy deficits during periods of harsh winter (when DEE exceeds energy supply from food) and potentially for pre-basic moult (Owen and Cook 1977, Heitmeyer 1988).
Furthermore, the comparisons of mass loss during different years at Abberton and amongst free-flying birds with access to ad libitum food at Slimbridge show that the degree of mass accumulation at the start of moult and rate of depletion through moult did not differ between years or treatments based on measurements from many different individuals (except in 1978, when both sexes apparently started moult with low body mass compared to other years, although differences were not statistically significant). Of course, we should be prudent about comparing between different seasons when the timing of the moult differed significantly between years and sexes, since this suggests that seasonal factors such as timing of breeding and food supply could affect phenology and restrict comparisons between years and sites. For this reason, we should also be careful when comparing data from males at Abberton and Slimbridge in different years. Nevertheless, the similarity in the rate of mass loss in birds from different seasons and sites was remarkable and suggests a common underlying mechanism. We also cannot fully rule out the possibility that the degree of fat accumulation under some circumstances is environmentally determined, with mallard acquiring less body mass in anticipation of moult in some seasons, perhaps because of food limitation, that could affect ultimate body mass on completion of moult.
Studies by van de Wetering and Cooke (2000) and Portugal et al. (2007) showed relationships between speed of moult and body mass loss and between body size and mass loss during moult in other Anatidae species during wing moult. These studies suggest that the degree of body resources available to an individual for feather growth at the start of flightless wing moult could affect the rate of re-growth of remex feather and/or the reliance of that individual on exogenous sources of energy. Such individual and seasonal patterns were beyond the scope of the present study, but clearly future research should address the extent to which starting moult in better condition (i.e. greater body stores) allows an individual to increase feather growth rate and/or spend more time resting, potentially reducing predation risk (Portugal et al. 2011).
The regular rate of subsequent depletion of stores during wing moult confirmed the findings of Pehrsson (1987) who also showed mallard fed ad libitum rolled oats also showed declines in body mass, which suggests this may be a heritable trait, since the loss of mass was not accentuated in wild birds (despite their exposure to food limitation and predation risk) compared to those fed ad libitum. The fact that male mallard with ad libitum access to food in a totally predator-free situation lost mass at a similar rate to free-living birds fails to support the hypothesis that loss of body mass relates to constraint on foraging (Panek and Majewski 1990). Rather we believe that the mallard may show restraint on foraging during moult, and that they choose (or are able) to feed less, especially avoiding risky habitats where predation may be more likely, and so reduce energy expenditure as well as predation risk by supplementing exogenous sources of energy by depleting fat stores (Portugal et al. 2010, 2011).
There remains some discussion about the true costs of wing feather replacement. Metabolic rate apparently increases during wing moult in Anatidae species, but not during body moult (as shown by elevated energy consumption, Qian and Xu 1986, Portugal et al. 2007). This suggests that increases in metabolic rate are associated with simultaneous replacement of the largest feathers or that this is a mechanism to facilitate rapid feather growth to foreshorten the flightless period. Either way, the mallard studied here appear to exploit fat stores laid down prior to moult, rather than burning mass of a form not stored as lipid in advance of this period of extra demand. For these reasons, despite apparent increased energetic demands, we reject the hypothesis that mass loss in mallard during wing moult is simply the result of energetic stress, i.e. individuals simply mobilising energy from body reserves (rather than fat stores, sensu van der Meer and Piersma 1994), i.e. burning the ‘engine’ rather than the ‘fuel’. Because both sexes accumulate body mass at slightly different periods in advance of moult, we also reject the suggestion that the mass loss is an effective shortening of the flightless period, by allowing the birds to fly on incompletely grown flight feathers – why accumulate stores immediately before remix moult if the end objective were to minimise mass in the latter part of the flightless period? Hence, the ability to fly on shorter wings is a consequence of the mass loss (Brown and Saunders 1998) but is unlikely to contribute to the explanation for this trait.
There is no doubt that testing of the theories behind mass dynamics and feather growth during remex growth in Anatidae can only be achieved by simultaneous measurement of feather growth, fat store depletion, food consumption and energy expenditure. Moulting waterbirds do not respond well to handling and stress under controlled captive conditions and manipulative experiments render themselves open to criticism about application of results to ‘wild’ situations. Nevertheless, there are limits to how much more study of free-living Anatidae can contribute to our understanding of how physiological state interacts with timing and rate of wing moult and with the quality of feather tissue produced under stress. There is no doubt that much more could be achieved by experimental studies to better enlighten moulting tactics of waterbirds replacing flight feathers in open habitats in relation to their energy needs.
Many species of dabbling and diving ducks deplete stores of body mass during moult (reviewed by Hohman et al. 1992), including some in the Southern Hemisphere
(Douthwaite 1976, Halse and Skead 1983, Halse and obbs 1985, Ndlovu et al. 2010), so the pre-wing moult fat accumulation trait to assist meet the energetic needs of flight feather re-growth is likely widespread in the Anatidae, although certainly not ubiquitous (Hohman et al. 1992, Fox et al. 2008). For this reason, it would be instructive to better understand the circumstances under which such adaptive traits have evolved and how these enable different populations to manage energetic balance during this period of enhanced energy cost, lost mobility and elevated predation risk. We conclude that the accumulation of body mass in mallard represents the build up of fat stores which are depleted during the flightless period to enable rapid regrowth of feathers whilst exploitating habitats (typically open water) that offers safety from predation, but do not necessarily enable the ducks to balance their energy budgets during the vulnerable flightless period of wing feather re-growth. We encourage the examination of other species to determine how widespread such a trait may be.