Variation in temperature increases the cost of living in birds
1 School of Biological and Environmental Sciences, University of Stirling,
Stirling FK9 4LA, Scotland
2 Division of Integrative Biology, Roslin Institute (Edinburgh), Midlothian
EH25 9PS, Scotland
* Author for correspondence (e-mail: cjp2{at}stir.ac.uk)
Accepted 25 March 2004
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Summary |
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Key words: Japanese quail, Coturnix japonica, temperature variability, energy expenditure, egg production
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Introduction |
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This paper investigates the impacts of temperature variability on energy
expenditure, and the consequences for reproduction, using Japanese quail
Coturnix japonica as the model species. Costs of living, which are
clearly important for breeding due to their impact on reproductive decisions,
can be affected by changes in thermoregulation and foraging costs
(Bryant, 1997;
Feist and White, 1989
;
Kendeigh et al., 1977
).
Temperature can be important in determining the amount of time and energy that
can be allocated to the different stages of reproduction. For birds, this has
been demonstrated for egg production
(Stevenson and Bryant, 2000
;
Ward, 1996
), incubation
(Bryan and Bryant, 1999
) and
brood-rearing (Spencer and Bryant,
2002
). Food supply is also important for breeding birds, as the
levels of available nutrients are important in determining resource allocation
to egg production (Houston,
1997
).
Manipulation of roosting temperatures of breeding wild birds has
demonstrated the effects of mean temperature on egg quality
(Nager and van Noordwijk,
1992), timing of laying
(Meijer et al., 1999
), the
ability to maintain a daily laying schedule
(Yom-Tov and Wright, 1993
),
and incubation behaviour (Bryan and Bryant,
1999
). This implies that temperature can alter thermoregulatory
costs, leading to a reallocation of energy resources available for
reproduction. In this way, mean temperature could directly influence fitness
via the quality of eggs (Both et
al., 1999
; Christians,
2002
; Perrins,
1996
; Williams,
1994
) and the pattern of laying
(Nilsson and Svensson,
1993
).
Temperature variability is less commonly investigated than the effects of
mean temperature. However, an experiment involving captive Japanese quail
found that rapid sinusoidal temperature fluctuations resulted in an increase
in metabolism (Prinzinger,
1982). Another experiment involving captive turkeys (Meleagris
gallopavo) showed that, when they were transferred from a low to a high
temperature, metabolic rate decreased slowly during an acclimatisation period
of several days (MacLeod et al.,
1980b
).
These experiments suggest that temperature variability, as well as mean
temperature, may be important in determining daily living costs. This may then
have consequent effects on egg-laying ability
(Perrins, 1970;
Stevenson and Bryant, 2000
)
and fitness more generally. This paper uses two experiments to investigate
independently the effects on egg production and energy expenditure of: (i)
daily variation in temperature and (ii) a sudden change in temperature.
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Materials and methods |
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Four weeks prior to the experiments, each bird was randomly allocated to
one of four large chambers (1 mx1 mx1.2 m high). During this time,
the chambers were kept at a constant temperature of approx. 20°C, with a
lighting cycle of 14 h:10 h light:dark. The birds were provided with standard
quail layer feed (Savory and Gentle,
1976) and water ad libitum.
Experiment 1 Daily variation in temperature
A 2x3 factorial design was used for the experimental treatments. This
involved two levels of food quality and three levels of temperature variation.
The two levels of food quality were `high' (`HQ'; 100% standard food) and
`low' (`LQ'; 50% standard food, 50% cellulose). These were alternated each
week, with the aim of minimising changes in intestinal architecture
(Starck, 1999). The three
levels of temperature variation were `constant' (`C'; set at 18.3°C),
`low' (`L'; set at 25°C during the day and 15°C at night) and `high'
(`H'; set at 31.7°C during the day and 11.7°C at night). These
treatments aimed to provide the same mean daily temperature. The temperature
changes took place at 09:00 h and 17:00 h each day. The shorter warm-cycle
than light-cycle gave conditions with cooler dawns and dusks, compared to the
rest of the day.
Each treatment, run for a 7 day period, was randomly allocated to each chamber. This was then repeated. The experiment therefore lasted for 12 weeks. The 7 day period included an acclimatisation period of 3 days prior to measuring egg mass or gas exchange for that treatment. At the end of each 7 day period, all the birds were weighed to 0.1 g using an electronic balance (Sartorius UK, Epsom, Surrey, UK). Eggs were weighed on the day of laying to 0.01 g using an electronic balance. In each of the eight chambers, temperature was measured every 10 min using data loggers (Gemini Data Loggers Ltd., W. Sussex, England).
Each week, two pairs of birds (at different times; the same birds were used
each week) from each of the four groups, were moved into smaller calorimeter
chambers (600 mmx600 mmx450 mm high) for 2 days at a time. Here
they were provided with the same food, temperature and lighting conditions as
found in the larger chamber from which they came. Gas exchange was measured on
the second day, using the system described by Lundy et al.
(1978) and MacLeod et al.
(1985
).
Experiment 2 Sudden temperature change
A 2x4 factorial design was used for the experimental treatments. This
involved two levels of food quality and four temperature-change treatments.
The same two levels of food quality were used: `high' (100% standard food) and
`low' (50% standard food, 50% cellulose). The four temperature-change
treatments were changes from `high to medium' (`HM'), `medium to high' (`MH'),
`medium to low' (`ML') and `low to medium' (`LM') temperatures, where `high'
was set at 28°C, `medium' at 20°C, and `low' at 12°C.
Two females were kept in each of the smaller calorimeter chambers. The birds were subjected to a temperature change every 7 days, and the effects on gas exchange were measured over the subsequent days. At the end of each week, all the birds were weighed to 0.1 g using an electronic balance. In each of the chambers, temperature was measured every 10 min using data loggers (Gemini Data Loggers Ltd., W. Sussex, England). After 8 weeks, each bird had been subjected to each of the treatments. The experiment was then repeated with another eight birds.
Indirect calorimetry
Indirect calorimetry was used to measure energy expenditure for both
experiments. Metabolic rate was calculated from the rates of oxygen
consumption and carbon dioxide production. This was done by comparing the air
from the calorimeter chamber with ambient air. Energy expenditure (kJ
h1) was calculated using the equation of Romijn and Lokhorst
(1961):
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Statistical analysis
All data were analysed using Genstat for Windows, 5th edition. The effects
on egg mass and energy expenditure were analysed using a linear mixed model
using restricted maximum likelihood (REML) to control for the use of different
chambers for each group, and the repeated measurements on individual birds
(Patterson and Thompson,
1971). Values quoted in the text and tables are means ±
S.E.M. Vertical bars in graphs represent
S.E.M. The effect sizes for factors,
presented in tables, are relative to the reference group.
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Results |
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Energy expenditure
Energy expenditure is shown for the six treatment groups in
Fig. 1A. Energy expenditure was
significantly affected by the food quality treatment, temperature variation,
mean temperature and time of day (Table
1). Energy expenditure was higher for the low-quality, compared to
the high-quality food treatment, and increased with higher temperature
variability; and increased with a decrease in mean temperature.
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Egg production
Birds fed on the high-quality food laid significantly larger eggs than
birds fed the low-quality food (Table
2). There was also a significant interaction between food
treatment and temperature treatment (Table
2). Under the low-quality food treatment, significantly larger
eggs were laid under the constant-temperature treatment compared to both the
low and high temperature-variation treatments
(Fig. 1B). Under the
high-quality food treatment there was no such difference in egg mass between
the treatments. Also, under the low-quality food treatment only, egg mass
increased with maximum temperature by 0.23±0.10 g °C
1.
|
Effects of sudden temperature change
Temperature
There was a significant difference in mean temperature between the three
temperature levels (H, 29.4±0.1°C; M, 19.8±0.1°C; L,
12.5±0.1°C; 2=10399.76; d.f.=2;
P<0.001). This gave a difference of mean temperature between
`medium' and `low' levels of 7.4±0.02°C, and 9.6±0.02°C
between `medium' and `high' levels.
Energy expenditure
Energy expenditure was highest on the day after the change in temperature
and decreased over the next 6 days (Fig.
2A), when controlling for temperature treatment, time of day, and
week (Table 3). Highest energy
expenditures occurred when temperature was changed from `medium' to `high' or
`low', compared to `high' or `low' to `medium'
(Fig. 2B).
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Discussion |
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The increase in energy expenditure during more variable temperatures, or
after a sudden change in temperature, could be caused by the feedback system
controlling metabolism `overshooting' while adjusting to new temperatures
(Prinzinger, 1982). This is
thought to be more important than the energy expenditure required by the
increase in activity in the neurological centres of the measuring and feedback
control systems, which is believed to be negligible
(Prinzinger, 1982
). Other
possible reasons include the inefficiency of changing from fat
synthesis/deposition during cold temperatures, and fat-catabolism at higher
temperatures, and more variable conditions resulting in increased physical
activity or feeding during warmer temperatures to compensate for increased
energy expenditure during cold temperatures.
The increase in energy expenditure following a sudden change of approx.
8°C suggests that acclimatisation to such a change can take several days.
This was also found for growing turkeys when temperature was changed from low
to high, but not vice versa
(MacLeod et al., 1980b).
Nevertheless, the period of acclimatisation may be shorter for wild animals
that are more familiar with variable temperatures, compared to the quail and
turkeys used in these experiments. Energy expenditure also tended to be higher
when the temperature was changed from `medium' to either `high' or `low',
compared to a change from `high' or `low' to `medium'. This suggests that it
is easier to adjust to average rather than more extreme temperatures.
Energy expenditure also showed circadian rhythmicity, being higher during
the day than at night (Lundy et al.,
1978; MacLeod et al.,
1980a
). This has been shown to be due mainly to increased activity
(MacLeod et al., 1982
),
controlled by the lighting cycle (MacLeod
et al., 1980a
). Basal metabolic rates are also higher during the
day than the night (Aschoff and Pohl,
1970
).
Food supply
Energy expenditure was also affected by food quality, with birds fed
low-quality food having higher energy expenditures than birds on high-quality
food. This is likely to be due to the greater time required for feeding under
the low quality food treatment, and the increased processing in the gut
required for a high-cellulose diet.
Food quality also had a major influence on egg mass. A positive effect of
food on egg mass has previously been found from: experiments with captive
birds (Yamane et al., 1979);
observations of wild birds over years of differing food availability
(Bryant, 1978
;
Hiom et al., 1991
;
Järvinen and Vaisanen,
1984
); and supplementary feeding experiments of wild birds
(Hill, 1988
;
Hiom et al., 1991
;
Högstedt, 1981
;
Källander and Karlsson,
1993
; Ramsay and Houston,
1997
). Food is therefore likely to directly affect the amount of
resources available for egg production.
Temperature variability and egg mass
Under the low-quality food treatment, significantly larger eggs were laid
when temperature was constant compared to when it was varied during the day.
The increased thermoregulatory costs imposed by higher temperature variability
may have therefore reduced resources available for egg production. Since an
increase in energy expenditure is required for egg production
(Stevenson and Bryant, 2000;
Ward and MacLeod, 1992
),
smaller eggs may therefore be produced under more variable conditions. Under
the high-quality food treatment, egg mass was not influenced by temperature
variability, suggesting that under good food conditions any negative effects
of temperature variation can be fully compensated. Since food conditions can
vary between years and areas (Bolton et
al., 1992
; Dijkstra et al.,
1982
), and within a breeding season
(Birkhead and Nettleship, 1982
;
Gibb, 1950
), our results
suggest that temperature variation is likely to be more important in some
situations compared to others. Alternatively, since foraging costs are higher
for wild birds than captive birds provided with food ad libitum,
birds in the wild may invariably experience relatively `poor' conditions, so
temperature variation may be more likely to affect energy expenditure. This
effect of temperature variability on reproduction is unlikely to be limited to
just birds. Similar effects could also be expected for other animals.
Conclusions
We have demonstrated an effect on energy expenditure of temperature
variability, in terms of daily variation and the effect of a sudden
temperature change. This had subsequent effects on the resources allocated to
egg production. Since daily temperature ranges have increased in some areas
due to climate change (Easterling et al.,
1997; IPCC, 2001
),
temperature variation is likely to become more important in determining daily
living costs in these areas. Where day-to-day variation in temperature is
decreasing, by contrast, daily living costs may also be reduced. Although
recent increases in mean temperatures
(IPCC, 2001
), and a reduction
in energy expenditure with temperature would be expected to reduce daily
living costs (Kendeigh et al.,
1977
; Walsberg,
1983
), our results suggest that increasing temperature variability
might counteract this affect. The effect of the exact pattern of temperature
change is thus likely to be important in predicting biotic responses to future
climate change.
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Acknowledgments |
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Footnotes |
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