Behavioral Ecology Vol. 11 No. 2: 178-188
© 2000 International Society for Behavioral Ecology
Effects of ambient temperature on avian incubation behavior
a Montana Cooperative Wildlife Research Unit, Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA b U.S.G.S. Biological Resources Division, Montana Cooperative Wildlife Research Unit, University of Montana, Missoula, MT 59812, USA
Address correspondence to C. J. Conway, Department of Environmental and Forest Biology, State University of New York, Syracuse, NY 13210, USA. E-mail: conway{at}owt.com .
Received 3 May 1999; accepted 29 July 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Ambient temperature is commonly thought to influence avian incubation behavior. However, results of empirical studies examining correlations between ambient temperature and bout duration are equivocal. We propose that these equivocal results can be partly explained by developing a conceptual understanding of how we should expect temperature to influence incubation. We demonstrate why linear correlation analyses across a wide range of temperatures can be inappropriate based on development of an incubation model for small birds that incorporates how ambient temperature influences both embryonic development and adult metabolism. We found support for predictions of the model using incubation data from orange-crowned warblers (Vermivora celata) in Arizona. Both off- and on-bout duration were positively correlated with ambient temperature between 9° and 26°C, but unrelated to ambient temperature <9° and 26-40°C. Bout durations declined as ambient temperature approached or exceeded 40°C. Incubating orange-crowned warblers appeared to avoid bouts off the nest <7 min and bouts on the nest <20 min. Time of day, duration of the previous bout, and variation among nests all explained variation in both on- and off-bout duration. Although we found support for the general shape of the incubation model, temperature still explained only a small portion of the overall variation in on- and off-bout duration. Results of previous studies were generally consistent with the model for off-bout duration; most studies in colder environments reported positive correlations with temperature, and the one negative correlation reported was from a hot environment. However, the relationships between on-bout duration and temperature reported in previous studies were less consistent with our model and our data. Although some discrepancies could be explained by considering our model, some studies reported negative correlations in cold environments. The effect of ambient temperature on duration of on-bouts probably differs among species based on the amount of fat reserves females typically carry during incubation and the extent of male incubation feeding. Additional studies of the effects of temperature on avian incubation will help improve the general model and ultimately aid our understanding of energetic and ecological constraints on avian incubation.
Key words: ambient temperature, foraging, incubation behavior, incubation model, incubation rhythm, nest attentiveness, on-bout duration, off-bout duration.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Ambient temperature is commonly thought to influence avian incubation behavior (Baerands, 1959
;
Drent, 1970;
Haftron, 1988;
Lombardo et al., 1995;
Weathers and Sullivan, 1989;
Weeden, 1966;
White and Kinney, 1974;
Zerba and Morton, 1983).
Incubating parents must balance the thermal needs of the developing embryos
with their own energetic needs by leaving the nest to forage. Effective
resolution of this trade-off between embryos and parent is particularly
important in species with unassisted, single-sex incubation
(Williams, 1991). Empirical
studies have reported negative, positive, and no correlation between ambient
temperature and on- and off-bout durations (Appendix). Where significant
correlations exist, temperature typically explains only a small proportion of
the variation in bout length. The equivocal or minor relationship between
temperature and incubation behavior among empirical studies is contrary to
experimental studies in which decreased nest or egg temperature increases nest
attentiveness and decreases off-bout duration
(Biebach, 1979;
Davis et al., 1984;
Drent et al., 1970;
Haftron, 1984;
Vleck, 1981a;
von Haartmann, 1956;
White and Kinney, 1974). The
inconsistent relationships between ambient temperature and incubation behavior
in field studies are an enigma given the obvious importance of temperature to
embryo development (Webb,
1987) and the female's response to experimentally altered
temperature. In an attempt to resolve this enigma, we propose a conceptual model that relates on- and off-bout duration to ambient temperature in small-bodied birds with single-sex incubation (species in which incubating females periodically leave the nest to forage in order to balance their energy budgets over the course of each day). The model is appropriate for species that are time limited during incubation; the amount of food consumed during typical off-bouts is below limits imposed by rates of digestion and assimilation. Our model incorporates the influence of ambient temperature on both embryonic development and adult metabolism. We show that searching for linear correlations between bout duration and ambient temperature across wide ranges of temperature is misguided. Our model provides a conceptual framework of how ambient temperature should influence incubation behavior, attempts to explain the equivocal results of previous studies, and provides guidance for future studies. To explain the development of this model, we (1) consider how temperature should affect bout duration through its effects on embryonic development, (2) consider how temperature should affect bout duration through its effects on adult metabolism, and (3) present our conceptual model by simultaneously considering trade-offs between embryo thermal needs and adult energetic needs.
Temperature and embryonic development
Thermal tolerance of domestic chicken embryos is frequently used as a model
of temperature influences on embryonic development in wild birds
(Drent, 1970;
Haftron, 1984;
White and Kinney, 1974).
Chicken embryo development is suspended below 26°C [physiological zero
temperature (PZT); Lundy,
1969], and many authors have assumed that PZT is 26°C in all
birds (Drent, 1975;
Haftorn, 1984;
Webb, 1987;
White and Kinney, 1974).
Between 26°C (PZT) and 36°C (lower limit of optimal development;
LLOD), development is slowed but not impaired, but prolonged exposure can
cause developmental abnormalities (Lundy,
1969; Webb, 1987).
Optimal development occurs between 36°C and 40.5°C in chickens
(Lundy, 1969), and optimal
temperatures are often assumed to be the same across species
(Huggins, 1941;
Webb, 1987;
White and Kinney, 1974). Above
40.5°C (upper lethal temperature; ULT), malformations develop, and death
occurs with prolonged exposure (Lundy,
1969). Hence, embryonic development varies nonlinearly with
temperature (Figure 1a).
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Incubating females are commonly thought to limit off-bout duration such
that egg temperatures seldom fall below PZT
(Haftron, 1984;
Løfaldli, 1985;
Vleck, 1981b,
Weathers and Sullivan, 1989).
If this assumption is correct, off-bout duration should decline as ambient
temperature drops below 26°C because unattended eggs should cool at a
faster rate as temperature declines. Hence, we would expect a positive
correlation between off-bout duration and ambient temperature below 26°C
(Figure 1b). Because single-sex
incubators are often limited in time available for foraging
(Mertens, 1977), females
should take more off-bouts as bout duration declines, leading to shorter
on-bouts. Consequently, on-bout duration should also be positively correlated
with ambient temperature below 26°C
(Figure 1b). Similarly, as
temperature rises above 40.5°C, birds should be forced to take shorter
off-bouts to prevent eggs from overheating to lethal temperatures during their
absence (Figure 1b). At ambient
temperatures 26°-40.5°C, eggs will not cool below physiological zero
or overheat above upper lethal temperatures during off-bouts. Hence, we expect
bout length to be less correlated with ambient temperature in this range
(Figure 1b). Indeed, brief
periodic cooling to temperatures not lower than PZT during off-bouts may
actually increase hatching success (Batt
and Cornwell, 1972; Kendeigh
and Baldwin, 1932; Landauer,
1967; Oppenheim and Levin,
1975; Westerskov,
1956). Thus, variation in ambient temperature can influence
incubation behavior through its effect on embryonic development, but effects
on behavior may differ depending on the range of temperatures experienced
(Figure 1).
Temperature and adult metabolism
Variation in ambient temperature may also influence incubation behavior
through its effect on adult metabolism. Resting metabolic rate of homeotherms
is minimal across a range of temperatures (thermoneutral zone; TNZ) and
increases at temperatures below (lower critical temperatures; LCT) and above
(upper critical temperature; UCT) this zone
(Haftorn and Reinertsen, 1985;
Schmidt-Nielson 1994;
Figure 2a). Although the LCT
and UCT may differ among species (Hayworth
and Weathers, 1984), the general shape of the relationship between
temperature and metabolic rate (Figure
2a) is consistent among species. The width of the TNZ may be
narrower in incubating females (Figure
2a) compared to resting birds, but the relationship should
otherwise be similar. Indeed, the energy required during incubation increases
greatly in small birds when the ambient temperature falls below LCT (Biebach,
1981,
1984;
Haftorn and Reinertsen, 1985;
Vleck, 1981a). Increasing
metabolic needs of the incubating adult (below the LCT and above the UCT)
should force birds to take shorter on-bouts because they are metabolizing
available energy more quickly (especially in species that rely mostly on
exogenous resources for reproduction). Consequently, on-bout duration should
be positively correlated with ambient temperature at temperatures below the
LCT and negatively correlated with ambient temperature at temperatures above
the UCT (Figure 2b).
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Energetic costs of rewarming cooled eggs are high relative to maintaining
optimal egg temperature during incubation
(Biebach, 1986;
Vleck, 1981a). In cold
environments, eggs cool much quicker after a female leaves the nest to forage
than they rewarm when the female returns
(Drent, 1975). Moreover, the
rate of egg cooling declines throughout an off-bout as egg temperature
approaches ambient temperature. Consequently, a bird trying to optimize
available energy should minimize rewarming episodes by taking few long
off-bouts rather than many short ones
(Drent, 1975). At ambient
temperatures within their TNZ, incubating birds should maximize on- and
off-bout duration within limits imposed by their metabolic rate, foraging
success during off-bouts, and the onset of developmental abnormalities
(Figure 2b).
Combining embryo thermal needs and adult energetic needs
Simultaneously considering embryo thermal needs and adult metabolic needs
allows us to develop a conceptual model of the relationship between ambient
temperature and both off- and on-bout duration
(Figure 3). As ambient
temperature drops below PZT, off- and on-bout duration should decline because
an incubating female must take shorter but more frequent off-bouts to obtain
needed energy while preventing egg temperatures from cooling below PZT during
her absences. As temperature continues to drop below both PZT and LCT, length
of off- and on-bouts should decline even faster with temperature because the
adult's metabolic needs start to increase inversely with temperature.
Consequently, the slope of the positive relationship between ambient
temperature and off- and on-bout duration should become steeper at
temperatures below either the PZT or LCT (whichever is lower)
(Figure 3). Similarly, we also
expect the slope of the negative relationship to become steeper at
temperatures above either the ULT or UCT (whichever is higher)
(Figure 3).
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However, we expect lower bounds on off- and on-bout duration. For example,
continued reduction in off-bout duration with decreasing temperature will
become unprofitable when the average energy obtained in such a short off-bout
no longer exceeds the energy expended in foraging and rewarming eggs. Hence,
at very low temperatures, further reductions in off-bout duration become
unprofitable, and we might expect incubating females to maintain some minimal
off- and on-bout duration despite further declines in temperature
(Figure 3). Similarly, we
expect a threshold at some high temperature above which the female stops
taking off-bouts altogether and stays on the nest, enduring a negative energy
balance (Maclean, 1967;
Vleck, 1981b;
Walsberg and Voss-Roberts,
1983; Figure 3).
Further increases in temperature above this threshold (or prolonged time at
this temperature) may result in nest abandonment or adult emaciation.
In summary, our conceptual model does not predict a consistent linear relationship between ambient temperature and off- or on-bout duration across all temperatures (Figure 3). Tests of predictions and future refinement of this general model should enhance our understanding of how ambient temperature limits incubation strategies available to incubating females. We tested predictions of this conceptual model using data from orange-crowned warblers (Vermivora celata) on a study site in central Arizona. This is a good system to test model predictions because only female orange-crowned warblers incubate the eggs, females rely mostly on exogenous resources during incubation, male incubation feeding is rare, and incubating females experience a relatively wide range of ambient temperatures on our study site.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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We collected data on length of on- and off-bouts at 34 orange-crowned warbler nests from 1991 to 1994 and in 1997 at our study site on the Mogollon Rim (2,600 m), Coconino National Forest, central Arizona, USA. Orange-crowned warblers on our study site produce only one brood per year. Although females will renest if a clutch is depredated early, most of our nests were first attempts, and we did not sample nests late in the season (initiation dates of the 34 nests were 4 May-27 June). The number of on-bouts (and off-bouts) we recorded per nest varied from 5 to 215 (mean = 85 bouts/nest) depending on stage of incubation, whether the nest was depredated, and number of concurrently active nests being monitored. We recorded bout duration by inserting a Copper-Constantan thermocouple through the wall of the nest among the eggs. At nine of the nests, we also inserted and glued a second thermocouple in the middle of one of the eggs of the clutch to measure egg temperature. The other ends of the thermocouple wires were attached to a Campbell Scientific CR10 datalogger, which recorded temperature at 30-s intervals. Another thermocouple was placed approximately 10 cm from each nest to measure ambient temperature at the nest site. The initiation and termination of each on-bout and off-bout was determined by examining nest temperature data. Sharp changes in temperature indicated when birds left the nest to forage and when birds returned to the nest to begin a new incubation bout.
We lack an empirical measure of lower critical temperature (LCT) for
orange-crowned warblers, but LCT of a 10.5-g bird during the daytime can be
estimated as 27°C using an allometric equation
(Weathers and van Riper,
1982). Hence, for orange-crowned warblers, PZT and LCT are
similar. Consequently, we examined four predictions of our conceptual model:
(1) bout duration is positively correlated with temperature at ambient
temperatures <26°C, (2) bout duration no longer declines with decreases
in temperature below some lower threshold, (3) bout duration is not related to
temperature between 26°C and 40.5°C, and (4) bout duration declines
with temperature >40.5°C.
Because bout duration differed according to time of day
(Figure 4), we examined the
relationship between bout duration and temperature for each of three time
intervals (0500-0859, 0900-1659, and 1700-1959 h) based on similarities in the
relationship observed in Figure
4. We also included hour of the day in ANCOVA analyses so that we
could examine the relationship between temperature and bout duration
independent of time of day. We did not include stage of incubation in our
models because the incubation period of orange-crowned warblers is short
(12-13 days), and bout duration did not differ among days of the incubation
period (F < 1.7, p >.19; also see
Davis, 1960;
Ettinger and King, 1980;
Kendeigh, 1952;
Lawrence, 1953;
Lombardo et al., 1995;
Smith and Montgomerie, 1992;
Sturm, 1945;
Weeden, 1966). We used
hierarchical ANCOVAs to examine the consistency of the linear relationship
between on- or off-bout duration and ambient temperature. In each ANCOVA, on-
or off-bout duration was the dependent variable, nest was a random factor,
hour of the day was a fixed factor, and previous bout duration and ambient
temperature were covariates. Including nest as the first factor in our
hierarchical models allowed us to examine the relationship between temperature
and bout duration after differences among individual nests were removed. We
included previous bout duration in our models because the length of an on-bout
should be influenced by the length of the previous off-bout (and vice versa)
if birds are indeed attempting to balance their energy budgets over short time
periods (an assumption of our model).
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We divided the range of temperatures experienced on our study area into three temperature zones (<9°C, 9-26°C, and >26°C) and classified each observation into one of the three zones. We identified 9°C as a possible lower threshold based on initial analyses. We included the ambient temperature x temperature zone interaction as the final variable in each hierarchical ANCOVA analysis, allowing us to address the prediction that the slope of the relationship between temperature and bout duration differs with ambient temperature after the influence of all other factors was removed. We also present on- and off-bout duration as a function of temperature for one nest that exemplifies the range of variation in ambient temperature on our study site.
We also summarized results of previous studies that have examined the
relationship between ambient temperature and incubation behavior. Although
previous studies have used linear correlation analyses and do not present raw
data, we wanted to address whether our model could explain some of the
discrepancies. We focused on studies of small birds that must get off the nest
periodically to forage in order to maintain daily energy balance. We also
recorded the mean, minimum, and maximum daytime temperature during the period
of study, where available. Because male incubation feeding can influence how
females respond to changes in ambient temperature, we recorded the frequency
of mate feeding for each species from the papers on incubation behavior and
from Birds of North America accounts
(Poole and Gill, 1992-1999).
We found few quantitative estimates of actual rates of mate feeding but many
qualitative descriptions, so we categorized the relative frequency of mate
feeding for each species as seldom or never (0), infrequent (1), moderate (2),
and frequent (3).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Overall, off-bouts averaged 8.7 min (SE = 0.1, n = 3067), and on-bouts averaged 34.1 min (SE = 0.3, n = 2855), but both off- and on-bout duration varied among nests (the factor "nest" was significant in ANCOVAs; Table 1). Hour of the day explained additional variation in the morning and evening time periods, but less so during the middle of the day (0900-1659 h; Table 1). Previous bout duration also explained variation in both off- and on-bout duration, even after removing differences among nests and time of day (Table 1). Indeed, on- and off-bouts were positively correlated within individuals (mean r =.247; 30 of 33 individuals had positive r values and 17 were significant; p <.05). Ambient temperature still explained substantial variation in both off- and on-bout duration after removing the effects of all other factors (Table 1).
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As our conceptual model predicts, both on- and off-bout duration were positively correlated with ambient temperature between 9° and 26°C (Figures 5, 6). However, a positive relationship between ambient temperature and bout duration is not as apparent at temperatures <9°C and >26°C (Figures 5, 6). Indeed, off- and on-bout durations appear to decline (negative relationship) as ambient temperature exceeds UCT (Figures 5, 6). As Figures 5 and 6 suggest, the slope of the relationship between on-bout duration and ambient temperature differs among the three ranges of temperature (significant ambient temperature x temperature zone interaction; Table 1). The relationship between off-bout duration and ambient temperature (Figures 5, 6) also appears to support the general shape of our model (Figure 3), but the ambient temperature x temperature zone interaction term was not significant (Table 1). The general relationships between ambient temperature and off- and on-bout duration are similar when we examine our data for the one nest that best exemplifies the range of temperature variation (Figure 7). Hence, data from orange-crowned warblers generally support all four predictions of our conceptual model.
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The reported relationship between ambient temperature and both off- and
on-bout duration varied among previous studies
(Table 2, Appendix). The
majority of studies reported a positive correlation between temperature and
off-bout duration (Table 2),
but many suggested that the relationship was not linear across all
temperatures sampled. Most previous studies were in colder, temperate climates
(Appendix). The one study that reported a negative correlation between
temperature and off-bout duration was in a very hot environment
(Vleck, 1981b; Appendix).
These results would be expected based on predictions of our model.
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The reported relationship between temperature and on-bout duration was less
consistent among studies (Table
2, Appendix). However, studies in the two coldest environments
reported positive correlations (Norton,
1972; Zerba and Morton,
1983), and those in the two hottest environments reported negative
correlations (Crook, 1960;
Purdue, 1976). Still, some
studies in cold environments reported a negative correlation between
temperature and on-bout duration and Vleck
(1981b) reported a positive
correlation in a hot environment, opposite that predicted by our model.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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Previous empirical studies examining the effects of temperature on avian incubation behavior have used linear correlation/regression analyses (Appendix). Yet our conceptual model predicts a nonlinear relationship between bout duration and temperature in small birds. Our incubation model suggests that the use of linear analyses across wide temperature ranges for examining the influence of temperature on incubation behavior may have caused previous investigators to overlook nonlinear relationships.
Data from orange-crowned warblers supported predictions of our conceptual model. Both off- and on-bout duration were positively correlated with ambient temperature between 9° and 26°C, even after controlling for time of day, previous bout duration, and differences among nests (Table 1, Figures 5,6,7). However, bout durations were not correlated with temperature >26°C (LCT and PZT) and appeared to decline as temperature exceeded UCT (Figures 5,6,7)—both patterns predicted by our model. Moreover, off- and on-bout duration were positively correlated within individuals.
Another prediction of our conceptual model is a lower threshold in both on-
and off-bout duration. As our model predicts, orange-crowned warblers appeared
to refrain from taking off-bouts shorter than 7 min and on-bouts shorter than
20 min; bout durations were less correlated with temperature <9°C
(Figures
5,6,7).
Indeed, we detected a significant temperature-dependent change in the slope of
the relationship between ambient temperature and on-bout duration in ANCOVA
analyses (Table 1). The
relationship between off-bout duration and ambient temperature (Figures
5,6,7)
also appeared to support the general shape of our model, even though our
ANCOVAs failed to detect a significant ambient temperature x temperature
zone interaction (Table 1).
Skutch (1962) also observed
that the relationship between temperature and incubation behavior breaks down
in extremely cool weather.
Lower thresholds in bout duration may represent a minimally efficient incubation strategy. For example, on-bouts consistently shorter than 20 min on our study area may not adequately provide for the thermal needs of the developing embryos because some portion of that time will be required simply to rewarm eggs to optimal incubation temperature. These minimally efficient bout durations undoubtedly vary among species, populations, individuals, and even among days based on food abundance, foraging efficiency, individual quality, and thermal conductance of the bird, nest, and nest site.
On- and off-bouts were shortest and least correlated with temperature
during the first four morning hours (Figure
6). After fasting overnight, incubating females are emaciated and
appear to incubate their eggs in a way that maximizes foraging time regardless
of air temperature (also see Nolan,
1978; Weathers and Sullivan,
1989). Hence, females may be forced to make many short trips off
the nest to replenish energy reserves while still providing for the embryos'
thermal needs. As the previous nights' energy debt is replenished, bout
duration becomes more correlated with ambient temperature
(Figure 6). On- and off-bout
duration were correlated with hour of the day early in the morning and late in
the evening, but much less so during the middle of the day (0900-1659 h;
Table 1). During the 3 h before
darkness, on- and off-bouts once again become shorter
(Figure 6). Taking shorter
on-bouts increases the number of foraging bouts as the nighttime approaches
(Figure 6).
Long on-bouts are preceded by long off-bouts, and vice-versa (Table 1). Long off-bouts allow females to obtain more food and hence to stay on the nest longer during the next on-bout. Similarly, a relatively long on-bout depletes the female's energy reserves, forcing her to forage longer during the next off-bout (Table 1). These results support one key assumption of our model: incubating warblers appear to be making behavioral decisions that allow them to balance their energy budgets over short time frames. Most previous studies examining the effects of temperature on incubation behavior have failed to control for time of day and previous bout duration. Future studies should consider these important factors.
Length of on- and off-bouts differed among nests
(Table 1). Variation in
incubation behavior among nests limits the ability to detect the true
relationship between temperature and bout duration in studies that fail to
account for such variation (ours did). One individual averaged 37.0 min on and
10.5 min off, while another individual averaged 21.6 min on and 4.9 min off.
This difference in incubation behavior results in an 80% increase in nest
activity between these two individuals (2.5 versus 4.5 nest trips/h). Such
large intraspecific variation in incubation behavior may reflect variation in
territory or individual quality because frequent nest trips are energetically
inefficient (Drent, 1975) and
may increase the risk of nest predation
(Conway and Martin, in press;
Martin, 1996;
Prescott, 1964;
Skutch, 1949). Variation in
individual or territory quality and variation among species or populations in
risk of nest predation would be expected to influence the typical length of
on- and off-bouts, but not the general relationship with ambient temperature
predicted by our model.
Although we found support for our model of the effects of temperature on
incubation behavior, we were able to explain only 17-47% of the variation in
on- and off-bout duration (Table
1). Bout duration is obviously influenced by other factors (e.g.,
predation risk, male behavior) in addition to those considered here, and
future research should attempt to evaluate the relative importance of these
factors. Indeed, analyses across species suggest that risk of nest predation
influences incubation behavior (Conway and
Martin, in press).
Our model helps explain some, but not all, of the conflicting results from
previous studies (Appendix). In agreement with our model, most previous
studies have been conducted in colder temperate environments and have reported
a positive correlation between temperature and off-bout duration
(Table 2, Appendix). Moreover,
several studies with large sample sizes reported that the nature of the
relationship changed with ambient temperature
(Davis et al., 1963;
Haftorn, 1979;
Kendeigh, 1952;
Kluijver, 1950;
Norton, 1972;
Zerba and Morton, 1983). The
only reported negative correlation between off-bout duration and ambient
temperature was a study of Costa's hummingbirds in a hot climate
(Vleck 1981b); a thermal
environment in which our model predicts a negative correlation [although Vleck
(1981b) also reports a
positive correlation with on-bout duration, opposite that predicted by our
model]. The studies that failed to detect a correlation between off-bout
duration and ambient temperature may have used inadequate sample sizes, failed
to account for differences among nests, and/or worked in environments with
moderate (or more variable) temperatures. Because temperature is only one
factor influencing incubation behavior, one needs a large amount of data to
quantify the relationship between ambient temperature and bout duration
(Skutch, 1962). Failure to
report raw data and failure to control for time of day and variation among
nests limits our ability to interpret the lack of correlation reported in some
studies. However, the results from previous studies on the relationship
between off-bout duration and ambient temperature generally support our model,
and our model helps explain conflicting results.
The relationship between on-bout duration and temperature varied even more
among studies (Table 2). Our
model helps explain some of this variation; studies in the two coldest
environments reported positive correlations
(Norton, 1972;
Zerba and Morton, 1983),
whereas those in the two hottest environments reported negative correlations
(Crook, 1960;
Purdue, 1976; Appendix).
Moreover, eight studies reported that the relationship between on-bout
duration and ambient temperature was nonlinear across the range of
temperatures sampled. In several studies, on-bout duration was not correlated
(or was even slightly negatively correlated) with temperature at very low
ambient temperatures but was positively correlated with temperature at more
moderate temperatures (Haftorn,
1978; Zerba and Morton,
1983); patterns that support our model. However, numerous studies
conducted in generally cold environments reported a negative correlation
between on-bout duration and temperature (Appendix). The fact that these
females take longer, rather than shorter, on-bouts when ambient temperature
declines raises the question as to why these females do not take longer bouts
at more moderate temperatures because long bouts are beneficial (Drent,
1972,
1975;
Morton and Pereyra, 1985;
Skutch, 1949;
Vleck, 1981b). Two
possibilities are that as temperature declines, the frequency of male
incubation feeding might increase (Skutch,
1957), or females may rely more on endogenous energy reserves.
Although our model does help explain some of the conflicting empirical
results of the effects of temperature on incubation behavior, the nature of
the relationship probably differs among populations that vary in their
reliance on endogenous reserves and/or the extent of male incubation feeding.
For example, some species might increase their use of endogenous fat reserves
(rather than alter bout durations) during extreme temperatures to compensate
for increased metabolic needs. Bout duration in populations that exhibit a
temperature-dependent change in the use of endogenous versus exogenous energy
sources during incubation would be expected to be less influenced by
temperature (e.g., reduced slopes and/or thresholds at more extreme
temperatures than those predicted by our model). Hence, we expect our model to
be most appropriate for populations that rely predominantly on exogenous
energy sources during incubation. Moreover, we expect the relationships
between bout duration and ambient temperature presented in our model to be
weaker in populations in which the frequency of male incubation feeding
increases at extreme temperatures. An increase in male incubation feeding
during extreme temperatures would help compensate for the increased metabolic
rate of the incubating female and allow her to continue taking long on-bouts
(Smith et al., 1989). Hence,
we might expect species that rely mostly on exogenous energy sources during
incubation and that do not exhibit mate feeding to fit our model best. Female
orange-crowned warblers on our study site have no visible fat reserves during
incubation, and males rarely feed incubating females (Conway and Martin,
personal observations). Comparative data on the extent of reliance on fat
reserves during incubation are not currently available for the species in the
Appendix, and the extent of mate feeding does not help explain the variation
in results among studies. However, temperature-dependent changes in
mate-feeding frequency (rather than extent of mate feeding) would affect the
relationship between bout duration and temperature most, and these data are
also not currently available. Inflection points and thresholds predicted by
our model may be at more extreme temperatures for species or populations in
which males increasingly feed incubating females as ambient temperature
declines.
Our conceptual model presents only a general framework of the relationship
between temperature and incubation behavior in small birds. Inflection points
are probably not abrupt, and relationships between incubation behavior and
ambient temperature will also vary among species exposed to the same range of
temperatures because LCT, UCT, and embryo thermal tolerance may vary across
species (Hayworth and Weathers,
1984; Williams and Ricklefs,
1984). The relationship between temperature and bout duration will
also vary among taxa according to the temporal scale over which incubating
birds balance their energy budgets. Such intra- and interspecific variation
limits our ability to evaluate predictions of our model from previously
published correlative studies; predictions could be best tested by
experimentally manipulating temperature at nests in future studies.
In summary, we found general support for a new conceptual model of temperature influences on avian incubation. As the model predicted, off- and on-bout duration were positively correlated with ambient temperature between 9° and 26°C. No correlations were observed at temperatures <9°C and >26°C (Figures 5, 6). Length of on-bouts declined as ambient temperatures approached the upper lethal temperature (Figures 5, 6). Hence, previous studies that have used linear correlation analyses across a wide range of temperatures may have overlooked, or simplified, important relationships. Our model provides testable predictions about the way temperature influences incubation strategies in small birds and should help increase our understanding of the energetic costs of incubation. Inflection points and slopes may vary across species and populations, but the general shape of our model should be consistent for species in which females rely primarily on exogenous energy sources for incubation and are rarely fed by their mates. A review of previous studies suggests that our model explains disparate results based on off-bout duration and some of the inconsistencies based on on-bout duration. This general model is a first step at improving our understanding of temperature effects on avian incubation by taking into account the combined effects of temperature on the thermal needs of the embryos and metabolic needs of the incubating adult; additional data on avian incubation across a wide range of taxa and thermal environments will undoubtedly allow model improvements.
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APPENDIX |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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ACKNOWLEDGEMENTS |
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W. W. Weathers, D. Kilgore, E. Greene, D. Patterson, and three anonymous reviewers provided comments that improved the manuscript.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONAPPENDIXREFERENCES |
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