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Keywords:

  • Avian breeding seasons;
  • climate change;
  • photoperiodism;
  • temperature

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    Birds use increasing photoperiod during spring as the major cue to time gonadal maturation and breeding so that nestlings are growing during peak food (normally invertebrate) abundance. Climate warming will advance invertebrate abundance, so birds relying entirely on photoperiod will breed too late. Can temperature modulate responses to photoperiod?
  • 2
    Common Starlings, Sturnus vulgaris, were kept in two indoor aviaries, in which photoperiod tracked natural changes, but temperature was held at either 20 °C or 5 °C (year 1), or at 18 °C or 8 °C (year 2).
  • 3
    Despite the large differences in temperature (15 °C and 10 °C), this had no effect on the rate or timing of testicular maturation.
  • 4
    However, unexpectedly, testicular regression occurred significantly earlier at the higher temperatures. Post-nuptial moult also started significantly earlier in both males and females.
  • 5
    Therefore, the degree to which birds can advance the timing of egg-laying in response to increasing spring temperature may be constrained. At the same time, increasing spring temperature will advance the end of the breeding season (fewer breeding attempts). The reported advances in median egg-laying dates may, in part, be a consequence of this rather than an indication of successful adaptation. Adaptation to climate change may require evolutionary changes in the physiological responses to photoperiod.

Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Birds time their breeding attempts so that the period of maximal nestling growth rate coincides with peak food availability. Birds (as other animals) use the vernal increase in photoperiod as a reliable cue to anticipate the onset of the breeding season so that the cascade of physiological and behavioural changes that must precede hatching is timed appropriately (Dawson et al. 2001; Ball & Balthazart 2003). Although increasing photoperiods during spring lead to gonadal maturation, later, long photoperiods cause gonadal regression through a mechanism known as photorefractoriness, and this essentially dictates the latest time that eggs can be laid. The beginning of the postnuptial moult is closely related to the time of gonadal regression.

Climate change may lead to increased spring temperatures and this will advance the time of the peak abundance of invertebrates (Buse et al. 1999), on which many species of birds rely to feed their young. If birds rely entirely on photoperiod to time breeding, they will be unable to compensate by adjusting the time of breeding and a mismatch will develop between the time of invertebrate abundance and peak nestling growth (Visser et al. 1998, Visser, Both & Lambrechts 2004; Coppack & Pulido 2004).

However, there is abundant evidence in many species that the time of egg-laying varies with temperature and that it has advanced over recent years, e.g. for Pied Flycatchers Ficedula hypoleauca (Both et al. 2004). Laying dates for Great Tits Parus major in Wytham Wood, UK, correlate with spring temperature (Perrins & McCleery 1989) and have advanced over the last four decades (Cresswell & McCleery 2003). However, this is not true for all European Parus study sites (Visser et al. 2003). In a population of non-migratory Common Starlings Sturnus vulgaris in the UK, first laying dates did not correlate with spring temperature and have not advanced over recent years (Feare & Forrester 2003). However, in a migratory population in southern Germany, there was a correlation with temperature immediately before egg-laying (Meijer et al. 1999). Analysis of breeding records for 65 species of birds in the UK shows that median egg-laying dates tended to get earlier between 1971 and 1995 and that this was significant for 20 species, including starlings (Crick et al. 1997). Median laying dates correlate with spring temperature (Crick & Sparks 1999). However, an advance in median laying date does not necessarily mean that first eggs are laid earlier – it could also reflect a decrease in the proportion of birds laying second or later clutches.

It is unclear how temperature may influence egg-laying dates. Does temperature directly modulate gonadal responses to photoperiod? Or is there an indirect effect, e.g. through changes in food supply? Perhaps surprisingly, there have been no detailed studies addressing whether temperature directly affects physiological responses to naturally increasing photoperiod during spring. In an early experiment on Great Tits, Soumalainen (1938) showed no apparent effect of increased temperatures on testicular size during early spring. A few studies have assessed the effects of temperature on gonadal maturation following an acute move from a short to a long photoperiod (Silverin & Viebke 1994; Wingfield et al. 1996; Wingfield et al. 1997; Wingfield et al. 2003– results are summarized in the Discussion) but such protocols may miss subtle effects of temperature on the rate of maturation during early spring.

The initial aim of this study was simply to determine whether temperature modulated photoperiodically induced gonadal maturation. The finding that temperature had no effect on the timing or rate of maturation was not unexpected. However, the additional finding that the duration of gonadal maturity was curtailed at higher temperatures was unexpected, but may explain results of recent field studies.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Experiment 1

Juvenile starlings were trapped from the wild during September 2002 and kept in outdoor aviaries. In mid-December, 34 males were laparotomized under isofluorane anaesthesia and the dimensions of the left testis measured to the nearest 0·1 mm using a binocular microscope (Home Office Licence PPL 80/1521). Testicular volume was calculated as 4/3 πa2b where a is half the width and b is half the length.

Two groups of 12 of these birds were moved to indoor aviaries (3·1 × 3·1 × 2·6 m3) in which they were allowed to fly freely. One room was kept at 5 °C and the other at 20 °C with 15 changes of air per hour. Lighting was provided by three coolwhite fluorescent tubes and one grolux tube (to provide UV; Greenwood et al. 2002) per room resulting in about 1500 lux at perch height. The time that the lights came on and went off each day was controlled by an outdoor photocell (used commercially to control street lighting). Room lights were switched on when external light intensity had increased to 210 lux and off when it had decreased to 70 lux. The resulting photoperiod was equal to the time between sunrise and sunset plus 80 min at the solstices and plus 60 min at the equinoxes. Approximately 1 m2 of a wall in each aviary was painted with phosphorescent paint, which provided sufficient illumination immediately after the lights went out for the birds to settle down.

The third group, 10 birds, was left in the outside aviary and so was exposed to natural changes in photoperiod and temperature. Changes in temperature and photoperiod experienced by the three groups are shown in Fig. 1(a). Testicular volume was assessed at regular intervals between December 2002 and October 2003. Birds began to moult in May and the progress of moult was recorded thereafter at weekly intervals and scored as a proportion of final primary feather mass (Dawson & Newton 2004).

image

Figure 1. Male starlings were kept in indoor aviaries at 20 °C (n = 12) or 5 °C (n = 11), in which photoperiod matched natural changes in photoperiod, or in an outdoor aviary (n = 10). (a) Change in photoperiod experienced by all birds (broad grey line) and mean daily temperature for birds in the outdoor aviary (natural) and the two groups indoors (20 °C, grey-dashed, or 5 °C, black-solid) during the course of the study. (b) Solid circles, testicular volume. There was no difference between the two groups at any point during the period of testicular growth between December and April (each point represents geometric mean ± SE) However, testicular regression occurred nearly 3 weeks earlier (P < 0·001) in birds held at 20 °C. Open circles, moult score. The median start date for moult was 27 days earlier at 20 °C (P < 0·001) but moult duration was less at 5 °C. (c) Comparable data from birds in the outdoor aviary during the same period.

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Experiment 2

This experiment was done to confirm the result of experiment 1. In early December 2003, the birds in the indoor aviaries from experiment 1 were again laparotomized. Birds from the warm room were transferred to the cold room and vice versa. The temperature difference between the rooms was reduced from 15 °C to 10 °C (warm room 18 °C, cold room 8 °C) to determine whether the magnitudes of the differences in response were proportional to the temperature difference. Birds were laparotomized and moult was scored as in experiment 1. Twelve female starlings, which had also been caught as juveniles in 2002 and kept thereafter in an outdoor aviary, were moved into the indoor rooms, 6 into the cold room and 6 into the warm room. Females were not laparotomized (unlike males, full gonadal maturation is curtailed in captivity) but moult was scored.

Experiment 3

In experiment 1, moult started later in the cold group, but then proceeded more rapidly. The increased rate of moult is likely to have been due to different photoperiodic conditions at the time of the (delayed) start to moult (Dawson 2004), rather than a direct effect of temperature. To test this, 10 male starlings, also caught as juveniles in 2002 and kept thereafter in an outdoor aviary, were moved into a warm indoor room (20 °C) at the beginning of June 2003, just as they started to moult. Four weeks later, with moult approximately 20% completed, five birds were moved to a cold room (5 °C) and the rest left at 20 °C. Moult was recorded until completion.

Statistical analysis

Experiments in different years were analysed separately. Statistical differences within groups were assessed using one-way anova with repeated measures following log transformation of testicular volume. Differences between specific time points were assessed with Tukey's Multiple Comparison tests. Differences between the warm and cold groups were assessed with two-way anova (treatment and time) with repeated measures. Bonferroni post tests were used to determine specific differences between treatments. Moult start dates were calculated by regressing individual moult scores for the first 4 weeks after the start of moult back to zero, and two-tailed t-tests used to assess differences in start dates and moult duration between the groups.

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Experiment 1

There was a significant difference in testicular volume between the two indoor groups held at 5 °C and 20 °C (F1,21 = 9·58, P < 0·0001). Mean testicular volume increased from approximately 2 mm3 in December to 500 mm3 in early April (Fig. 1b). The two groups were essentially identical during this period of maturation. The 20 °C group showed significant testicular regression between 3 April and 24 April (P < 0·001). The 5 °C group underwent regression 3 weeks later, between 24 April and 14 May (P < 0·001). Testicular volume was significantly less in the 5 °C group than the 20 °C group on 24 April (P < 0·001). Consequently, the duration of full testicular function (volume > 125 mm3 when active sperm are present; Schwab 1971) was 1·5 times greater in the 5 °C group (58 days vs 37 days; P < 0·001). The postnuptial moult, which is closely associated with gonadal regression, started 27 days later in the 5 °C group (9 June vs 13 May; P < 0·0001; Fig. 2a). It then proceeded more rapidly in the 5 °C group (duration 82 days vs 99 days; P < 0·0001).

image

Figure 2. Mean ± SD of the time of the start of moult (between 1 May and 30 June) in male birds in 2003 (a), and in males (b) and females (c) in 2004, kept at different temperatures.

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The outdoor group showed an intermediate response (Fig. 1c). The duration of full testicular function was 53 days, slightly less than the 5 °C group (not significant) but longer than the 20 °C group (P < 0·001). Ambient temperature during the period of maturity was nearer 5 °C than 20 °C (Fig. 1a). Moult started at the same time as in the 5 °C group and had approximately the same duration (84 days).

Experiment 2

The protocol for this experiment was similar to experiment 1, except that the two groups of males exchanged treatments and the temperature difference was less. The results were essentially the same as those for experiment 1, confirming that differences in the timing of gonadal regression and moult were temperature-dependent. There was a significant difference in testicular volume between the two groups F1,19 = 35·75, P < 0·0001 (Fig. 3a). There was no significant difference in testicular size between the two groups at any time except on 7 May, owing to delayed regression in the cold group. The 18 °C warm group showed significant (P < 0·001) regression between 5 and 23 April, and again between 23 April and 7 May The 8 °C group showed significant (P < 0·001) regression 2–3 weeks later, between 23 April and 7 May, and again between 7 May and 10 June. Moult started 20 days later in the 8 °C group (8 June vs 19 May; P < 0·001; Fig. 2b) and then proceeded more rapidly (duration 86 days vs 94 days; P < 0·01). The differences between the two groups were slightly less than in experiment 1, presumably reflecting the smaller difference in temperature.

image

Figure 3. (a) Male starlings were kept in indoor aviaries at 18 °C (n = 11) or 8 °C (n = 10). There was no significant difference between the two groups at any point during the period of testicular growth between December and April (solid circles, each point represents geometric mean ± SE). However, testicular regression occurred two weeks earlier (P < 0·001) in birds held at 18 °C. The median start date for moult (open circles) was 20 days earlier at 18 °C (P < 0·001) but moult duration was less at 8 °C. (b) Moult in female birds kept at 8 °C (n = 6) and 18 °C (n = 6). The median start date for moult was 23 days earlier at 18 °C (P < 0·001) but moult duration was less at 8 °C.

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Gonadal maturity was not assessed in females, but the timing of the start of moult is closely related to the timing of gonadal regression. Moult in females was similar to that in males (Fig. 3b). Moult started 23 days later in the 8 °C group (15 June vs 23 May; P < 0·001; Fig. 2c) and then proceeded more rapidly (duration 88 days vs 99 days; P < 0·01).

Experiment 3

Male starlings transferred from 20 °C to 5 °C early during moult, continued to moult at exactly the same rate as birds kept at 20 °C (Fig. 4). Differences in moult rate in experiments 1 and 2 were therefore the consequence of differences in the date at which moult started rather than a direct effect of temperature.

image

Figure 4. In early June, just as moult started, male starlings were moved into an indoor aviary at 20 °C. Four weeks later (arrow), with moult approximately 20% completed, five birds were moved to a cold room (5 °C) and the rest left at 20 °C. Temperature had no effect on the rate of moult.

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Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Extreme differences in temperature (15 °C and 10 °C) had no effect on the rate or timing of testicular maturation in starlings. In a population of non-migratory starlings in the UK, first laying dates did not correlate with spring temperature (Feare & Forrester 2003), but in a migratory population in southern Germany, there was a correlation with temperature immediately before egg-laying (Meijer et al. 1999). In the latter study, egg-laying could be advanced by heating nestboxes. So the exact timing of egg-laying may be influenced by temperature immediately before laying. However, if there is no effect of temperature on the timing and rate of gonadal maturation prior to then, the degree to which egg-laying can be advanced by temperature will be constrained. This leads to a potential problem for this species. Starlings feed their nestlings almost exclusively on leatherjackets (Tipula sp. larvae) and the timing of the increase in leatherjacket biomass during spring is advanced with increasing soil temperature (Dunnet 1955). If starlings rely entirely on photoperiod, they will breed too late. However, it is possible that temperature may advance breeding indirectly, for example through an advance in food supply (Meijer & Langer 1995). Increased food may act as a supplementary proximate cue rather than temperature.

Although an increase in temperature did not advance testicular maturation in starlings, this is not true for all species. Also, the rate of ovarian development in females may be more temperature dependent. Wingfield et al. (1992) have argued that non-photoperiodic supplementary factors, such as temperature, are more likely to affect the rate of gonadal maturation in species with longer and more flexible breeding seasons. A series of studies in which different subspecies of White-Crowned Sparrow (Zonotrichia leucophrys sp.) were transferred from a short to a long photoperiod at different temperatures has leant support for this. In Z. l. gambelii, which has a short predictable breeding season at high latitudes, temperature had no effect on the rate of testicular or ovarian maturation (Wingfield et al. 1996). In Z. l. pugetensis, which breeds at mid-latitudes, temperature did not affect testicular growth but did affect ovarian development, and in Z. l. oriantha, which breeds at lower latitudes but high altitudes and has a flexible breeding season, temperature affected gonadal maturation in both sexes (Wingfield et al. 2003). In Willow Tits (Parus montanus) high temperature accelerated testicular maturation, but in Great Tits (P. major) there was little effect (Silverin & Viebke 1994). However, in all of these studies, the experimental paradigm was an acute transfer from a short to a long photoperiod, rather than a natural increase in photoperiod. When Song Sparrows (Melospiza melodia) were exposed to naturally increasing photoperiods, higher temperature slightly enhanced testicular growth in birds from a mountain population, but had no effect in birds from a coastal population (Perfito et al. 2005).

Starlings have a short and predictable breeding season. Even if ovarian development is more temperature dependent than testicular development, fertile eggs could not be laid before full testicular maturation. The time of full testicular maturation in this study corresponded to first egg dates in free-living birds, and was not advanced by higher temperature.

Although temperature had no effect on the timing of testicular maturation in starlings, it did have a dramatic and significant effect on the timing of regression and on the timing of the start of postnuptial moult. The consequence of this is that increasing temperatures will decrease the duration of the breeding season. The number of pairs of starlings laying second clutches in the colony studied by Feare & Forrester (2003) has indeed decreased, but so too has the number of first clutches, reflecting a decrease in the population of this species. Analysis of data for starlings in the Nest Record Scheme of the British Trust for Ornithology shows that median egg-laying date has significantly advanced over the last three decades and that this does correlate with spring temperatures (H.Q.P. Crick, personal communication). Temperature during January, February and March had little effect, which is in accord with this study. April temperature was much more influential. However, first eggs are laid in early April so the scope for April temperature to influence first egg date is limited. The scope for April temperatures to affect median laying date through subsequent effects on the timing of the end of the breeding season is possibly greater.

No advance in the start of the breeding season, but a decrease in its duration, is what has been reported in some recent studies. During the last four decades, the beginning of the Turtle Dove Streptopelia turtur breeding season has not changed, but the end has advanced by 12 days, with fewer breeding attempts per pair (Browne & Aebischer 2003). There is evidence that first egg date has advanced in a population of Great Tits in the UK over the last four decades (Cresswell & McCleery 2003), but the timing of first clutches has advanced in only 5 of 13 European Great Tit study sites and in only 3 of 11 Blue Tit P. caeruleus sites (Visser et al. 2003). However, there has been a decrease in the proportion of pairs that start a second clutch (Visser et al. 2003). The number of breeding attempts per year may be an important factor in the recent decline in some bird species in the UK (Siriwardena et al. 2000).

The mechanism which leads to earlier regression at a higher temperature is unknown, but it may involve prolactin. High temperatures enhance prolactin secretion (Maney et al. 1999; Gahali, El Halawani & Rozenboim 2001) and high prolactin concentrations cause gonadal regression (Dawson & Sharp 1998). Prolactin also has a role in the control of moult (Dawson & Sharp 1998). Birds at lower temperatures started to moult later than those at higher temperatures in experiments 1 and 2, but then moulted more rapidly. The increased rate of moult was not a direct effect of temperature (experiment 3). Rather, it is an effect of photoperiod, and is dictated by the timing of the start of moult (Dawson et al. 2000; Dawson 2004). Consequently, birds in the outdoor aviary (experiment 1), which started to moult at the same time as the 5 °C group, then moulted at the same rate as the 5 °C group.

This study demonstrated that increased temperature does not advance the timing of gonadal maturation in starlings but does advance the timing of gonadal regression. This implies that there may be two detrimental consequences of increasing spring temperatures – an insufficient advance in breeding seasons to match the advance in invertebrate food supplies and breeding seasons that end sooner. The recorded advances in median egg-laying dates for many species (Crick et al. 1997; Crick & Sparks 1999) may result in part from an advance in the end of breeding seasons rather than reflecting successful adaptation. This may therefore understate the consequences of climate change for bird populations. The implication is that successful adaptation to climate change will require evolutionary changes in the physiological responses to photoperiod.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The author thanks Tony and Hazel Turk for animal husbandry and collecting some of the moult score data. The study was funded by the Climate Change Programme of the NERC Centre for Ecology and Hydrology.

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  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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