Costly events in the life history cycle of organisms such as reproduction, migration and pelage/plumage replacement are typically separated in time to maximize their outcome. Such temporal separation is thought to be necessitated by energetical trade-offs, and mediated through physiological processes. However, certain species, such as tropical birds, are able to overlap two costly life history stages: reproduction and feather replacement. It has remained unclear how both events progress when they co-occur over extended periods of time. Here we determined the consequences and potential costs of such overlap by comparing molt and behavioral patterns in both sexes of captive zebra finches (Taeniopygia guttata castanotis) that were solely molting or were overlapping breeding and molt. Individuals overlapping the early stages of breeding with molt showed a roughly 40% decrease in the growth rate of individual feathers compared with birds that were molting but not breeding. Further, individuals that overlapped breeding and molt tended to molt fewer feathers simultaneously and exhibited longer intervals between shedding consecutive feathers on the tail or the same wing as well as delays in shedding corresponding flight feathers on opposite sides. Overlapping individuals also altered their time budgets: they devoted more than twice the time to feeding while halving the time spent for feather care in comparison to molt-only individuals. These data provide experimental support for the previously untested hypothesis that when molt and reproduction overlap in time, feather replacement will occur at a slower and less intense rate. There were no sex differences in any of the variables assessed, except for a tendency in females to decline body condition more strongly over time during the overlap than males. Our data indicate the existence of major consequences of overlapping breeding and molt, manifested in changes in both molt dynamics and time budgets of both sexes. It is likely that under harsher conditions in natural environments such consequences will be more severe and may result in fitness consequences.

Many longer-lived organisms undergo several life history stages on an annual basis, such as reproduction, renewal of the integument (pelage or plumage), migration, hibernation and quiescent phases (Wingfield, 2008). The timing of these events, as well as their sequence in the annual cycle, is assumed to be shaped by selective forces (likely environmental conditions), ensuring that each life history stage occurs at an optimal time of the year (McNamara and Houston, 1996; Visser et al., 2004; Barta et al., 2008). A sequential expression of life history stages is considered to be adaptive in avoiding competition between processes for limited resources, which could compromise the outcome of each process (Jacobs and Wingfield, 2000; Wingfield, 2008; Barta et al., 2008). However, a co-occurrence of major life history events does happen in certain species, resulting in what has been termed ‘super-stage’ (sensuWingfield and Jacobs, 1999). In most species, such co-occurrence is observed only for short periods of time (days), such as when the last phase of a given stage overlaps with the initiation of the following one. For example, some mammalian species overlap a portion of their final reproductive phase with migration, like Pacific walruses (Odobenus rosmarus divergens) (Garlich-Miller et al., 2011), plains zebras (Equus quagga) (Kahuranga and Silkiluwasha, 1997) or Mongolian gazelles (Procapra gutturosa) (Olson et al., 2010). In birds, the collared flycatcher (Ficedula hypoleuca) is a well-known example for frequently overlapping the end of the reproductive period with the beginning of feather molt (Hemborg, 1999; Hemborg et al., 2001). However, so far only few individuals from a handful of species have been shown to exhibit a full overlap of two major life history processes, such as the extended overlap of reproduction and molt found in some tropical bird species (Payne, 1969; Foster, 1974; Zann, 1985; Tallman and Tallman, 1997; Piratelli et al., 2000; Echeverry-Galvis and Córdoba-Córdoba, 2008). Thus, it has remained unclear how two major life history processes might interact when they co-occur over a longer period of time. Determining the existence and extent of consequences of such an overlap would be important for furthering our understanding of both the evolution and the proximate regulation of annual life history cycles.

In avian species, the temporal separation of reproduction and molt is thought to result primarily from energetic constraints, as both molt and breeding require a large energy investment. Reproduction is estimated to increase daily basal metabolic rate by approximately 25–50% [egg production (King, 1973; Ricklefs, 1974; Monaghan and Nager, 1997); incubation (De Heij et al., 2008)] and molt by 10–45% (Murphy and King, 1992; Lindström et al., 1993; Klaassen, 1995; but see Buttemer, 2003; Hoye and Buttemer, 2011). Therefore, undergoing each process separately would enhance the outcome of each: for reproduction it would increase offspring survival and quality whereas for molt it would maximize feather quality and minimize deficits in flight performance (Jenni and Winkler, 1994; De la Hera et al., 2010). Indeed, in species where molt co-occurs with the end of the reproductive period, feather structure is compromised (Hemborg, 1999; Dawson et al., 2000), adult movements are restricted and survival decreases (Stearns, 1992; Hemborg and Lundberg, 1998). Similar consequences of overlapping two life cycle stages are also present in some non-vertebrate species (Zera and Harshman, 2001).

So far, most studies have documented the occurrence of molt–breeding overlap at the species or population level. Typically, data were collected during field surveys in which some individuals from one population showed evidence of molt (i.e. were missing or growing flight or body feathers) at the same time as others were in a reproductive state [as determined by the presence of brood patches, or enlarged cloacal protuberance, in a few cases by direct measurement of gonad size (Moreau, 1936; Snow, 1976; Marini and Durães, 2001; Newton and Rothery, 2005)]. By contrast, studies reporting the occurrence of molt–breeding overlap within a single individual are much fewer, and often come from tropical species in which individuals with large gonads were also in active molt (Payne, 1969; Foster, 1975; Wyndham, 1981; Wyndham et al., 1983). However, although we know that molt–breeding overlap can occur in individuals, we still lack longitudinal individual-based studies that would allow us to assess the consequences of the two processes co-occurring over long periods of time. Such longitudinal studies would provide a powerful way to evaluate potential trade-offs and fitness consequences caused by a full molt–breeding overlap in individuals.

Based on work in neotropical bird species, Foster (Foster, 1974) put forward the hypothesis that overlapping reproduction and molt could be an adaptive strategy for individuals living in habitats with sufficient and constant food supply to afford to breed year-round. To cope with the energetic demands of the co-occurrence of both events, individuals would decrease the intensity of both processes during the overlap. Here we aim at experimentally testing one prediction arising from this hypothesis: that overlapping individuals would decrease molt intensity as compared to individuals that only molt.

Zebra finches [Taeniopygia guttata castanotis (Gould 1837)] are an ideal species with which to conduct such a study, as they show an overlap of breeding and molt in the wild (Zann, 1996), and can easily be kept, bred and observed in captivity. We assessed whether zebra finches of both sexes, kept in captivity under benign environmental conditions (i.e. constant food supply, minimal foraging costs and few thermoregulatory demands) and maintained in an early reproductive stage (the egg-laying state, without incubation or brood care cost) would show alterations in molt dynamics and time budgets during the overlap as compared to molting only. We predicted that individuals overlapping breeding and molt would: (1) show slower feather growth rates and therefore take longer to molt each feather, (2) have lower molt intensity (assessed as the number of feathers being replaced simultaneously) and (3) alter the time allocated to some behaviors, in particular locomotor activity and feather maintenance as compared to molt-only individuals. We also predicted that (4) the effects of the overlap would be more pronounced in females because of greater energetic demands during egg production.

Study species

Taeniopygia guttata castanotis are found commonly in mainland Australia, inhabiting areas where surface water is accessible, grass seeds are easy to find, and bushes and shrubs for nesting and roosting are found (Davis, 1986). Zebra finches have been bred in captivity for at least 140 years, and both wild and captive individuals have been shown to overlap breeding and molt (Zann, 1985; Zann, 1996). In captivity, it has also been observed that zebra finches can exhibit a less rigid molting sequence (not following exactly the primary 1 through 9 feather sequence). The species has been estimated a molting period of approximately 260 days, with regrowth of individual feathers taking 21–26 days for completion (Zann, 1996).

Experimental protocol

A total of 40 young zebra finches of at least 90 days old and with no prior breeding experience were obtained from a breeding colony at the Max Planck Institute for Ornithology at Seewiesen, and kept for 12 weeks (from late April to early July 2010) at the Max Planck Institute for Ornithology at Radolfzell. Upon arrival at Radolfzell, we divided individuals into three groups in separate indoor rooms: (1) 20 individuals (10 males and 10 females) were paired and allowed to breed (male–female pairs); (2) 10 females were put into a cage with another female, resulting in five female–female pairs; and (3) 10 males were paired with another male, resulting in five male–male pairs. All pairs were kept in 80×80×50 cm cages. After creating the three groups, morphological measurements were taken (wing and tarsus length), and individuals were weighed using a Pesola spring scale (0.1 g). All rooms were maintained on an identical photoperiod (14 h:10 h light:dark) and at ambient temperature (20±1°C). Food (egg food, mixed seeds, ground egg shells, millet and apple pieces) and water were provided ad libitum. Male–female pairs were provided with nesting material and a pre-constructed nest in the cage. The experimental protocol was approved by the Regierungspraesidium Freiburg under permit number 35/9185.81/G-10/16.

Every second to third day, each individual was captured from its cage and the length of growing feathers was assessed (primary, secondary and tail feathers). Each feather was examined for presence/absence, and the length of a growing feather was measured to the nearest 0.01 mm with calipers. Each feather molted during the study period was measured until growth completion (i.e. when two consecutive measurements did not differ by more than 1 mm) and the daily growth rate was calculated for each feather. Body mass was assessed after each molt examination. We determined and categorized whether individuals were in an active breeding state by both observation of breeding behavior (copulation, carrying of nest material or egg laying) and unilateral laparotomy (except for laying females) at intervals of 3 weeks. Laparotomies were performed under light isoflurane anesthesia, and the length and width of the left testis in males or the diameter of the largest follicle in females was measured with a modified digital caliper (Hau et al., 1998; Hau et al., 2000). Testis volume was calculated based on the ovoid sphere formula V=4/3πa2b, where V represents the volume, a is half the length and b is half the width of the testis. Testis volumes of males in this study fell into one of two distinctive size classes: 11.3–13.6 mm3 [which we categorized as non-breeding individuals because these testis sizes are below those reported for being able to produce viable sperm (Sossinka, 1980; Vleck and Priedkalns, 1985; Perfito et al., 2006)] and 47.1–57.8 mm3 (categorized as breeding males). All males with enlarged testes were housed in male–female pairs and displayed courtship behavior. Female follicle sizes also showed a bimodal distribution, with non-breeding females having follicles of less than 3.0 mm in diameter and breeding females having follicles between 4.5 and 6.2 mm. Whenever eggs were laid, they were removed on the same day to standardize the reproductive stage to an early, egg-laying phase and removing any incubation or parental costs (a maximum four eggs were laid and removed per pair per breeding attempt). Even though some individuals enlarged their gonads soon after being paired (as revealed by first laparotomy), egg laying occurred no earlier than 21 days later (after the second laparotomy).

Behavioral observations were conducted three times a week, both in the morning (07:00–11:00 h) and the afternoon (14:00–17:00 h) for all cages. During a 5-min observation period, the activities of both members of a cage were scored using a scan sampling protocol (Altmann, 1974) every 5 s, resulting in a total of 60 observations per individual. We recorded the following behavioral states: locomotor activity (which included active flight and hopping but not walking), perching (only scored when individuals rested on a perch or on the floor), feeding (either at the feeders or on food on the floor), nesting (either being in the nest or actively adding nest material), singing (only in males) and feather care/preening (regardless of the location where it occurred).

In the discussion that follows, individuals that showed signs of active molt but had gonad sizes in the non-breeding range will be termed ‘molt-only’, whereas individuals that were in active molt and had gonad sizes and/or showed behaviors that classified them as being in a breeding condition will be termed ‘overlappers’.

Statistical analyses

Even though all feathers were measured in this study, only feathers molted on both wings were included in our analysis. We compared the total length of newly grown feathers between molt-only and overlapping individuals using a one-way ANOVA with feather ID as a covariate for primaries 6, 7 or 8, secondaries and tail feathers 3, 4 or 5. We focused analysis on these feathers because they were molted by the majority of individuals. Furthermore, the external primaries are of great importance for flight performance and stroke power (Swaddle and Witter, 1997).

Molt-only individuals from the different pairings (male–female vs same-sex pairs) did not differ significantly in any of the tested parameters; therefore, for all further analyses they were lumped into a ‘molt-only’ group. When the raw data violated assumptions of normality or heterogeneity of variance, they were transformed accordingly (as specified in the Results) or analyzed using a non-parametric test. We used generalized linear mixed models (GLMMs) with a backward stepwise removal of non-significant factors to test for differences in molt patterns and behavior between overlapping and molt-only individuals. In all models, individual ID was included as a random factor to control for repeated measurements of individuals over time, as well as for individuals switching from a molt-only to an overlapping status (see Results; such switches in status also account for the varying sample sizes for the groups). Body condition was calculated using the residuals from a linear regression of body mass versus tarsus length and was included in all GLMMs. Body mass changes between and within individuals were assessed using one-way repeated-measures ANOVAs (when sphericity assumptions were violated, we used the Greenhouse–Geisser correction). Post hoc pair-wise comparisons were performed using a Tukey’s honestly significant difference (HSD) test when the overall model revealed significant effects. Because of low sample sizes, we used a Kruskal–Wallis test using an individual’s average value per feather group (primaries, secondaries or tail) to assess group differences in the interval between shedding consecutive feathers. For behavioral analyses, only feeding and feather care or preening were analyzed using GLMMs because the other variables were highly correlated with either of those two variables as determined from Pearson’s correlations (r>0.068). In these models, individual ID and time of day were included as random factors to account for the repeated measurements of an individual and the morning and afternoon observation times.

All analyses were performed using JMP 9.0.0 (SAS Institute Inc., Cary, NC, USA). Significance was accepted at an alpha level of 0.05. Data are presented as least-square means ± s.e.m.

Of the 10 male–female pairs, five showed enlarged gonads and active flight feather molt already within 1 week after the start of the experiment. Three other male–female pairs were in a molt-only state for 4 weeks, and later enlarged their gonads to overlap molt and reproduction. The remaining two male–female pairs never developed enlarged gonads or showed any reproductive behavior, but continued to molt throughout the study period. All 20 individuals kept in female–female and male–male pairs retained small gonads and underwent symmetrical wing molt. Overall, molt-only data could be obtained from 30 individuals (20 individuals kept in same-sex pairs, four individuals kept in two male–female pairs that only molted, and the six individuals kept in male–female pairs that shifted from molt-only to overlapping). It should be noted that some overlapping females had enlarged follicles during the entire duration of this experiment but did not lay eggs continuously. Breeding pairs usually laid two clutches of approximately four eggs each, with inter-clutch intervals of 23–38 days.

Body condition of all individuals significantly decreased over time (F6.06,194.1=7.78, P<0.0001). However, there was no difference in body condition between individuals according to their status (whether an individual was overlapping or molt-only; P>0.08). Furthermore, although the time by status interaction was not significant (F6.06,194.1=2.05, P=0.06), overlapping individuals showed a trend to decrease body condition more strongly over time than molt-only individuals (F12,21=3.1, P=0.06). There was also a non-significant trend for a sex difference, with females tending to have lower body condition (F12,21=3.32, P=0.06; molt-only: F12,21=0.32, P=0.39).

Molt

All individuals molted primaries and secondaries in a standard sequential molt [descendant sequence, i.e. from the body towards the wing tip (sensuJenni and Winkler, 1994)]. Tail feathers were also molted sequentially, even when several feathers molted simultaneously. In all cases, secondaries were not shed before primaries 4 or 5 were in molt. No individual progressed through an entire molt cycle from dropping primary 1 to growing primary 9; hence the entire molt duration could not be directly assessed.

Sex was not a significant explanatory factor in any of the models on molt dynamics. The final length of newly grown feathers did not differ between molt-only or overlapping individuals for any of the feather categories (F1,8=2.15, P>0.1). However, feather growth rate (millimeters of material added to a feather per day) differed according to an individual’s status and feather type (primaries, secondaries or tail; Table 1): molt-only individuals grew their primaries at approximately twice the rate of overlappers (Fig. 1A). Also, post hoc tests revealed that overall, secondary feathers were grown at a faster rate than primaries or tail feathers (Fig. 1A). Molt-only individuals took approximately 26.3 days to fully regrow a primary, 25.4 days to replace a secondary and 28 days to replace a tail feather, whereas overlappers took 44 days to replace a primary or a tail feather and 40 days to replace a secondary feather (after correcting for absolute feather length for each feather).

Table 1.

Simplest GLMM showing variables that significantly explain differences in feather growth rate (arcsin transformed), number of feathers growing simultaneously (arcsin transformed) and time interval between shedding the same feather on each wing (GLMM with Markov chain Monte Carlo with zero inflated Poisson distribution)

Simplest GLMM showing variables that significantly explain differences in feather growth rate (arcsin transformed), number of feathers growing simultaneously (arcsin transformed) and time interval between shedding the same feather on each wing (GLMM with Markov chain Monte Carlo with zero inflated Poisson distribution)
Simplest GLMM showing variables that significantly explain differences in feather growth rate (arcsin transformed), number of feathers growing simultaneously (arcsin transformed) and time interval between shedding the same feather on each wing (GLMM with Markov chain Monte Carlo with zero inflated Poisson distribution)

Individuals that shifted from a molt-only status to overlapping (three male–female pairs) showed a feather growth rate similar to that of other overlapping individuals. On average, primary feathers in these individuals grew by 2.57±0.11 mm day–1 during the molt-only period, slowing down to 1.27±0.08 mm day–1 during the overlap. Secondaries and tail feathers grew by 2.05±0.09 and 2.12±0.05 mm day–1, respectively, when these individuals only molted and then decreased to 1.54±0.13 and 1.27±0.13 mm day–1 after they had started to overlap. Lumping all feather categories (to increase sample size) revealed that feather growth rates decreased after individuals switched from molt-only to overlapping (paired Wilcoxon signed rank: S=–10.5, P=0.03).

The intervals between molting consecutive feathers were significantly longer for overlappers than for molt-only individuals for primaries and tail feathers (z=2.32, P=0.02 and z=3.61, P=0.0003, respectively). However, intervals between molting consecutive secondaries only tended to be longer in overlapping individuals (z=1.80, P=0.06). On average, individuals showing the overlap took 7.2±0.2 days between shedding consecutive primaries and 5.3±0.2 days to shed consecutive tail feathers, in comparison to 6.2±0.3 and 2.0±0.2 days, respectively, for molt-only individuals.

Molt intensity (the number of feathers growing simultaneously) differed weakly between individuals of different status (P=0.049; Table 1). Tail feathers were molted more intensely by molt-only individuals, which grew up to eight feathers simultaneously. By contrast, overlappers molted only two feathers at a time (Table 1; for results of post hoc tests see Fig. 1B). However, there was no difference in the number of primary or secondary feathers being molted simultaneously between molt-only and overlapping individuals. Molt-only individuals also molted more tail feathers simultaneously than primaries or secondaries, whereas overlapping individuals showed a similar molt intensity for all feather categories (Fig. 1B).

Variation in the interval between dropping the corresponding feather on each wing was significantly explained by both an individual’s status and feather type (Table 1, Fig. 1C): overlappers showed longer intervals than molt-only individuals, and consecutive primaries were dropped after longer intervals than secondaries. The time to replace the same feather on both sides of the tail (left/right) did not differ between molt-only individuals and overlappers.

Behavior

As with our molt data, sex had no effect on our behavioral data. Time spent feeding and time spent preening differed between molt-only and overlapping individuals, with overlappers feeding almost twice as often and preening roughly half as much as molt-only individuals (Table 2, Fig. 2). Feeding rate in molt-only individuals was negatively correlated with perching and preening behaviors (Pearson’s correlation coefficients: r=–0.66, P<0.0001 and r=–0.44, P=0.005, respectively), and preening was negatively correlated with locomotor activity (r=–0.61, P=0.0001). In overlapping individuals, feeding behavior was negatively correlated with both preening and locomotor activity (r=–0.82, P<0.0001 and r=–0.65, P=0.0002, respectively).

Fig. 1.

Feather growth and molt characteristics in zebra finches. (A) Feather growth rate (mm day–1) (*P<0.01, ***P<0.0001). (B) Number of feathers grown simultaneously (*P=0.03, **P=0.002). (C) Interval (days) between shedding symmetrical feathers in opposite wings (comparing left and right) and tail (***P<0.0001). Data in all panels are least-squares means ± s.e.m., with molt-only (open bars) and overlappers (gray bars) by feather group.

Fig. 1.

Feather growth and molt characteristics in zebra finches. (A) Feather growth rate (mm day–1) (*P<0.01, ***P<0.0001). (B) Number of feathers grown simultaneously (*P=0.03, **P=0.002). (C) Interval (days) between shedding symmetrical feathers in opposite wings (comparing left and right) and tail (***P<0.0001). Data in all panels are least-squares means ± s.e.m., with molt-only (open bars) and overlappers (gray bars) by feather group.

Table 2.

Simplest GLMM showing variables that significantly explain differences in feeding (log transformed) and preening (square root transformed) between individuals overlapping breeding and molt, and molt-only individuals

Simplest GLMM showing variables that significantly explain differences in feeding (log transformed) and preening (square root transformed) between individuals overlapping breeding and molt, and molt-only individuals
Simplest GLMM showing variables that significantly explain differences in feeding (log transformed) and preening (square root transformed) between individuals overlapping breeding and molt, and molt-only individuals

We compared the behavior of the three pairs that started in a molt-only status and then switched to overlapping during the final 3 weeks of the study using pair-wise t-tests. When overlapping, all individuals fed more (t10=22.02, P<0.0001) and preened less compared with molt-only individuals (t10=–11.69, P<0.0001), in concordance with the above results comparing among individuals of different status.

Finally, diel patterns in time budgets differed according to status: overlappers preened more in the morning than in the afternoon (F1,14=314.2, P<0.0001) whereas molt-only individuals showed no diel variations in preening (F1,14=0.93, P=0.3). Furthermore, overlappers spent more time feeding in the afternoon than in the morning (F1,14=4.59, P=0.04), a diel pattern not detected in molt-only individuals (F1,30=1.26, P=0.28).

Even in captivity, under benign environmental conditions and ad libitum food supply, zebra finches that overlapped the early stages of reproduction with flight feather molt grew replacement feathers at a slower rate, molted fewer tail feathers at the same time, and showed longer intervals between shedding consecutive and symmetrical feathers when compared with individuals that only molted. Individuals overlapping reproduction and molt also fed more frequently and preened less than individuals just molting. Body condition of overlapping and molt-only individuals did not differ significantly, but showed a trend to decrease more strongly over time in overlapping individuals. First, these results show that individual zebra finches can plastically alter molt dynamics. Second, our data indicate that zebra finches of both sexes slow down some aspect of their molt when molt and breeding co-occur, thus supporting some parts of Foster’s (Foster, 1974) hypothesis.

We had expected to find sex-specific differences in molt patterns and behavior, especially in overlapping individuals, because females undergoing follicular development and egg-laying females are expected to carry a greater energetic burden than breeding males (King, 1973; Ricklefs, 1974). Indeed, Snow (Snow, 1976) found that female cotingas (e.g. Ampelion, Pipreola and Tityra spp.) during the early egg-laying period overlapped less frequently than males, and females overall took longer to complete their flight feather molt. Females in our experiment might have been able to compensate for some of the costs of the overlap. Feeding rates did not differ between sexes, indicating that females did not compensate by increasing food intake during the overlap. However, overlapping females tended to have lower body condition than males, suggesting that they were not able to fully defray the costs of the overlap. It is possible that under harsher environmental conditions in the wild, sex differences in molt patterns during the overlap would become more obvious. However, it is also possible that the overall energetic costs for early stages of reproduction in female birds are not as high as previously assumed, but that other sub-stages such as incubation and parental care account for most of the costs of female reproduction (Monaghan and Nager, 1997; Reid et al., 2002).

Fig. 2.

Frequency of preening and feeding (number of counts per 5 min) for molt-only individuals (open bars) and overlappers (gray bars) of zebra finches. Data are least-squares means ± s.e.m. (***P<0.0001).

Fig. 2.

Frequency of preening and feeding (number of counts per 5 min) for molt-only individuals (open bars) and overlappers (gray bars) of zebra finches. Data are least-squares means ± s.e.m. (***P<0.0001).

Even though body condition did not explain variation in molt dynamics or behavior, it decreased over the course of the study. Because we took repeated measurements from the same individuals, variation in body condition represents variation in body mass, which has been suggested to be one of the best indices for general condition (Labocha and Hayes, 2011). Several authors have demonstrated a loss of body mass during molt (Lindström et al., 1993; Swaddle and Witter, 1997; Portugal et al., 2007) (but see Zenatello et al., 2002) and have interpreted it to reflect energetical costs. Indeed, some zebra finch individuals that were initially part of the study but were not included in the final analyses because they neither molted nor bred showed no significant change in body condition over time (repeated-measures ANOVA, F1,2=1.78, P=0.2).

In north temperate zone birds, the growth rate of primary feathers ranges between 2.4 and 5 mm day–1 (Murphy and King, 1986; Jenni and Winkler, 1994; Newton and Dawson, 2011). For a south temperate species, a much slower growth rate of 2.3–2.9 mm day–1 has recently been reported (Hoye and Buttemer, 2011). Zebra finches predominantly occupy south temperate habitats, and our current data reveal even slower growth rates, with molt-only individuals growing feathers by 2.13 mm day–1 and overlappers adding as little as 1.30 mm to a feather each day. Hence, even though zebra finches already show a rather slow molt rate, the overlap between molt and breeding requires a further reduction in molt dynamics, as overlappers show a slower rate of material deposited in each feather, grow fewer feathers at the same time and in a less symmetric manner than molt-only individuals. This finding supports the hypothesis that individuals cope with the energetic demands of undergoing both molt and reproduction simultaneously by slowing down the rate of molt (Payne, 1969; Foster, 1974). However, although several aspects of molt in zebra finches are slowed down quite substantially during the overlap, the evidence from our data for a decrease in the intensity of molt (number of simultaneously molted feathers) is rather weak (P=0.049).

Molt-only individuals in the current experiment took 22–28 days to fully grow a primary feather and their interval between shedding consecutive primary feathers averaged 6 days. Based on these data, the estimated duration of the primary molt (i.e. from the time at which primary 1 was dropped until the complete regrowth of primary 9) would be 70–76 days. However, overlapping individuals took almost twice as long to grow a primary feather (32–44 days), and the interval between shedding subsequent feathers was on average 1 day longer, resulting in an estimated molting period for primaries of 88–100 days (with multiple feathers growing simultaneously). An alteration in the interval between shedding feathers has also been found in European starlings (Sturnus vulgaris) under artificial photoperiods (Dawson, 2004), with the inter-feather interval being shorter in larger primaries under shorter photoperiods.

The estimated duration (70–100 days) for the primary molt of zebra finches based on our data is shorter than that reported by Zann (Zann, 1985), who estimated primary molt to take approximately 229–239 days. Zann’s data were derived from wild individuals that were caught at least three times during their molt. However, our data support Zann’s (Zann, 1985) finding that on the population level molt was slower in times of high nesting activity. A complete flight feather molt in wild zebra finches takes approximately five times longer than the average 50–90 days that small songbirds typically need to fully replace their flight feathers (Jenni and Winkler, 1994). This extended molt period in zebra finches was hypothesized to be due mostly to the time spent between the completion of one feather and dropping the next one, which is the norm in this species in the wild. It is likely that the longer intervals between shedding consecutive feathers in overlapping individuals could contribute to explaining the extended molting period of this species in the wild. Based on our data, an overlapping individual could take 398 days to complete a full flight feather molt when not growing primaries simultaneously (using a mean of 38 days to grow a single primary and 7 days between shedding consecutive feathers), as has been reported in the wild, and assuming a constant breeding state [which is unlikely (Zann 1985)]. Molt duration is size dependent (Rohwer et al., 2009; Edwards and Rohwer, 2005), and small songbirds of the size of zebra finches (between 10 and 20 g) should, according to allometric relationships, molt much faster than the molt rates estimated above. However, other small songbird species, such as the rough-winged swallow, Stelgidopteryx serripennis, also exhibit rather slow molt rates, presumably as an adaptation to allow foraging on the wing while molting.

In addition to having longer intervals between molting consecutive feathers, overlapping individuals also showed longer intervals between molting the same feather on each wing, resulting in a less symmetric molt than in molt-only individuals. Overlappers took on average 7.5 days for primaries and 6.2 days for secondaries to replace the symmetrical feather on each wing. By contrast, molt-only individuals took only approximately 2 days to molt symmetrical primary or secondary feathers (see Fig. 1C). The corresponding in feather replacement in overlappers could result in aerodynamic and flight performance impairments (Hedenström and Sunada, 1999; Videler, 2006). These data also raise the possibility that the highly asymmetric molt in free-living birds previously considered to be accidental may in fact represent normal molt under energy limitation or during molt/breeding overlap. It is also noteworthy that none of the birds in this study showed any sign of suspended or arrested molt (Stresemann and Stresemann, 1966), as has been seen in a few tropical bird species that begin breeding when environmental conditions become favorable (Snow, 1966; Miller, 1961; Dorward, 1962; Snow, 1976).

Plasticity in feather growth and molt rate could be mediated at a physiological level by several hormones, which might interact with each other. For example, circulating corticosterone concentrations typically are downregulated during molt in species with short molt durations, but can remain seasonally unaltered in species with an extended molt, such as zebra finches (Cornelius et al., 2011). Increased corticosterone concentrations have been shown to slow down feather growth (Romero et al., 2005), thus the lack of a decrease in corticosterone levels might potentially contribute to the slow feather growth rates seen in zebra finches during the overlap. Corticosterone could also indirectly affect molt rate by decreasing protein storage via glucogenogenesis (Brown et al., 1992). Other hormones that may influence molt rate are prolactin, which has been shown to suppress molt in several species (Dawson, 1997; Dawson and Sharp, 1998; Deviche et al., 2000; Dawson and Sharp, 2010), and thyroid hormones (Kuenzel, 2003; Péczely et al., 2011). Despite efforts to understand the physiological mechanisms that underlie molt in avian species, we are still far from having a clear picture of its regulation (Bridge, 2011).

Even if the metabolic costs of producing a feather were relatively low (Ankney, 1984; Murphy and King, 1986; Buttemer et al., 2003; Hoye and Buttemer, 2011), the total amount of energy required during the molting period is expected to be increased because of a combination of protein requirements for feather synthesis and increased costs of flying (Murphy and King, 1992; Lindström et al., 1993; Murphy and Taruscio, 1995; Schieltz and Murphy, 1995; Murphy, 1996; Swaddle and Witter, 1997; Fox et al., 2008; Strochlic and Romero, 2008). Indeed, even though zebra finches in our study reduced feather growth rate quite dramatically and slightly reduced aspects of molt intensity during the overlap, they also increased their feeding rate by as much as 80% and lowered preening by approximately 70% compared with individuals that only molted. Individuals that first molted and later overlapped molt with breeding also showed similar changes in behavioral time budgets. These behavioral changes appear to represent mechanisms to cope with the increased costs of the co-occurrence of both events. In our study, the combination of a decrease in feather growth rate, a more asymmetric molt, longer intervals between molting subsequent feathers and behavioral changes may have allowed overlapping individuals to compensate for costs arising from the overlap, as neither body condition nor feather length was compromised. Data on reproductive success or survival rate of individuals from the wild will be required to determine the fitness consequences of the overlap.

We observed interesting diel differences in feeding and preening behavior between overlapping and molt-only individuals. Energy demands for individuals may increase in advance of the night, when protein catabolism for molt is higher (Newton, 1968; Gavrilov, 1997). This could explain the increased feeding rate in our experiment of overlapping individuals in the afternoon, and the changes in preening activity observed during food restriction in European starlings during molt (Bauer et al., 2011). However, more detailed information of protein turnover times for molt and egg laying is needed to more conclusively understand the timing and regulation of food intake.

In conclusion, the present study corroborates the hypothesis that individuals overlapping two energetically demanding life history stages, reproduction and molt, face increased energy demands. Overlapping individuals appear to cope with such costs by slowing down feather growth rate and the time between replacement of sequential feathers, as well as a modifying their time budget to increase food intake while decreasing the preening of feathers. The tendency of the overlappers to lose more body condition over time suggests that the costs of the overlap were not fully compensated, even under the benign conditions of captivity. It is possible, however, that aspects of feather quality could have been compromised in overlappers, such as feather mass or structure (Dawson et al., 2000; DesRochers et al., 2009; De la Hera et al., 2010; Strochlic and Romero, 2008; Maenniste and Horak, 2011). Further characterizations of feather structural properties in relation to molt/breeding overlap are needed to resolve this question. Our results are consistent with earlier reports that zebra finches are able to overlap molt and reproduction (Immelmann, 1963; Zann, 1985). Furthermore, our data document the consequences of the overlap on molt dynamics and highlight that individuals can plastically switch between molt-only and overlapping. This plasticity in molt dynamics could have evolved in response to various selection pressures, such as variable environmental conditions and physiological trade-offs. It is likely that certain environmental conditions [for example, a high overall food abundance with little seasonal variation (Foster, 1974)] promote the simultaneous expression of life history events that are not found in species that experience highly seasonal conditions. Field observations suggest that an overlap between early stages of breeding and molt is especially prevalent in tropical birds species, including high altitude populations (Echeverry-Galvis and Cordoba-Cordoba, 2008). This strategy could represent a stable and previously under-appreciated life history stage, i.e. a ‘super-stage’ (sensuWingfield, 2008). Further data on the costs and benefits of overlapping life cycle stages, as well as their physiological bases, are needed to understand the factors promoting the expression of such ‘super-stages’ in vertebrate species.

We thank the Max Planck Institute for Ornithology at Seewiesen, especially Lisa Trost, Barbara Woerle and Barbara Helm for help with obtaining zebra finches, Michael Quetting for assistance with measurements, and the animal care team at Radolfzell for bird husbandry. The Behavior, Ecology, Evolution and Physiology group at Radolfzell provided valuable comments, especially Timothy Greives and Nicole Perfito. Thanks to Catarina Miranda for assistance with the statistical analyses. We thank two anonymous reviewers for comments that greatly improved the manuscript.

FUNDING

Funding was provided by the Max Planck Gesellschaft to M.H.

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