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Temperature distribution in light-coloured flowers and inflorescences of early spring temperate species measured by Infrared camera
ARTICLE IN PRESS Flora 205 (2010) 282–289
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Temperature distribution in light-coloured flowers and inflorescences of early spring temperate species measured by Infrared camera Alzˇbˇeta Rejˇskova a,b,, Jakub Brom b,c, Jan Pokorny´ b,c, Jozef Korecˇko a,b a
136, Nove Hrady 373 33, Czech Republic University of South Bohemia, Institute of Physical Biology, Zamek ENKI o.p.s., not-for-profit organisation, Dukelska 145, Tˇrebonˇ 379 01, Czech Republic c ˇ University of South Bohemia, Faculty of Agriculture, Laboratory of Applied Ecology, Studentska 787/13, Cesk e Budˇejovice 370 05, Czech Republic b
a r t i c l e in f o
a b s t r a c t
Article history: Received 18 February 2009 Accepted 3 May 2009
Temperature is a limiting factor for plant reproduction under harsh conditions. Using an infrared camera, we studied temperature distribution in three early flowering light-coloured species of markedly different morphology. The influence of three environmental factors (temperature of the ambient air, temperature of the ground and irradiance) on the temperature of the flowers and inflorescences was evaluated. White petals and yellow centres of sun tracking Anemone nemorosa (Ranunculaceae) were shown to be on average 1.6 and 3.4 1C warmer than the ambient air, respectively. The surface temperature of the sun lit yellow discs of Bellis perennis (Asteraceae) was on average 7.4 1C warmer than the ambient air. Direct solar light was found to be responsible for large temperature differences between the discs and the marginal ray flowers. Bell-shaped white flowers of Galanthus nivalis (Amaryllidaceae) bent to the ground were on average 2.7 1C cooler than the surrounding air. The temperature relations of the different reproductive organs to the studied environmental factors are discussed. Temperature behaviour of the studied lowland species is compared with the results previously gained for alpine and arctic species by other authors. Ecological importance of our conclusions is considered. & 2009 Elsevier GmbH. All rights reserved.
Keywords: Flower Inflorescence Temperature distribution Ambient air Infrared camera
Introduction It is essential for plants to maintain the temperature of their reproductive organs at metabolic optima that promote growth and development (Galen, 2006; Patino and Grace, 2002). Morphology and colour have been suggested to play an important role in regulation of temperature in flowers growing in cold climates (Kevan, 1975, 1989; Knutson, 1981). In general, dark surfaces absorb radiation with higher intensity and warm up more quickly than light-coloured ones. However, the temperature within flowers and inflorescences is not simply a question of colour (Molgaard, 1989). Radiation incident on the flower is usually not reflected straight from the surface but in a complex manner from the inner epidermal layers being influenced by both the pigments and the shape and structure of epidermal cells (Kay et al., 1981). Several authors reported increased intrafloral temperatures in some alpine, arctic as well as montane spring ephemeral species related to special structural and optical features of the reproductive organs (Galen, 2006; Kudo, 1995; Luzar and Gottsberger,
Corresponding author at: ENKI o.p.s., Dukelska 145, Tˇrebon ˇ 379 01, Czech Republic. Tel.: +420 775147742; fax: +420 384724346. E-mail address: [email protected]. (A. Rejˇskova )
0367-2530/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2009.05.001
2001; Molgaard, 1989; Stanton and Galen, 1989; Totland, 1996; Tsukaya et al., 2002). In general, there are two possible ways of improving the energy budget of flowers and inflorescences under cold conditions. The first is to obtain more energy from the sun or from the environment. For some heliotropic species with light petals and parabolic shape a combined effect of reflective features of petals and the overall architecture of the flowers was demonstrated and the flowers were considered to function as parabolic or spherical solar collectors (Galen, 2006; Kevan, 1975; Kjellberg et al., 1982; Knutson, 1981; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). Some flowers and inflorescences bent to the ground seem to be capable of collecting energy coming from the ground or reflected from snow (Kevan, 1989; Sklena rˇ, 1999). The second possibility is to improve the heat storage capacity of the reproductive organs. Pubescence is an effective insulator, maintaining enhanced flower temperatures (Miller, 1986). This has been documented for highly pubescent catkins of the arctic willow Salix arctica (Kevan, 1990), for pubescent flowers of Puya species in Andean pa ramo (Miller, 1986) and suggested for a whole group of ‘‘downy plants’’ characterized by dense trichomes on bracts of inflorescences that help to keep the interior of buds warm (Tsukaya and Tsuge, 2001). Some plants combine both of these principles and form an intrafloral ‘‘micro-greenhouse’’. Having studied three colour variants of Crocus sp. McKee and
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Richards (1998) concluded that the proportion and spectral range of both absorbed and transmitted light is important for temperature distribution in flowers. The transmitted energy is trapped by reflective inner tepal surfaces and stored in the centres. For species from cold alpine and arctic regions even a slight warming up may enhance reproductive powers (Kevan, 1975; Kjellberg, et al. 1982; Stanton and Galen, 1989). Warmer flowers are visited more often by pollinating insects (Dyer et al., 2006; Ehleringer and Forseth, 1980; Herrera, 1995; Hocking and Sharplin, 1965; Kudo, 1995; Luzar and Gottsberger, 2001). In situations when the ambient temperature is often lower than the optimum temperature of many physiological processes, higher temperatures promote germination and growth of the pollen tube (Galen and Stanton, 2003; McKee and Richards, 1998) and later also the growth of seeds (Ehleringer and Forseth, 1980; Stanton and Galen, 1989). On the other hand excessive temperature may result in floral overheating (Galen, 2006). We decided to study temperature distribution in some vernal lowland species often exposed to very low but sometimes also to rather high temperatures, on assumption that their structural and physiological thermo-regulative adaptations may well differ from similar alpine and arctic species. In previous research prevailing temperature data of flowers have been collected with the help of contact thermometers, either thermocouples or thermistors (Kevan, 1975; Kjellberg et al., 1982; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). In our study an infrared camera was used. The aim of our study was to investigate temperature features of flowers and inflorescences of three common vernal species of temperate zone. The effect of colour was limited by selecting species with white or light coloured (white and yellow) reproductive organs only. We chose one inflorescence and two flowers with markedly different shapes to see whether the warming-up strategies differ in reproductive organs of dissimilar morphology. We studied (1) the capacity of heliotropic Anemone nemorosa L. with parabolic shaped flowers to warm up by concentrating solar rays, (2) temperature distribution in disc inflorescences of Bellis perennis L. and (3) ability of bent Galanthus nivalis L. flowers to warm up from the ground and function as a micro-greenhouse.
Materials and methods Study site and time of measurement The plants were measured in their natural habitats in ˇ in South Bohemia meadows and gardens near the town of Tˇrebon, (latitude 491N, longitude 141180 E, altitude 433 m). The mean temperature (data from 1977 to 2003) is 2.3 1C in January and ´ 2005). All sites had a 16.8 1C in July (Kova rˇova and Pokorny, homogenous surface without soil asperity. The measurements were carried out in March and April 2008 in the morning hours after morning mist lifted and the flowers and inflorescences opened. Cloudless and fogless weather conditions made it possible to study the effect of direct radiation on temperature distribution. Plant material Three plant species of early spring flora, widespread in the temperate zone, with white flowers and inflorescences were chosen for temperature analysis. A. nemorosa L. (Ranunculaceae) grew at the edge of a deciduous forest with Acer platanoides L. as a prevailing woody species. The ground in the forest was covered
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with dry leaves from the last growing season. Individual plants grew in loose groups; their leaves did not overlap. The bowl shaped flowers with white petals and yellow centres were about 3–4 cm large in diameter (Fig. 1A). The IR images of B. perennis L. (Asteraceae) were scanned in a garden. The size of inflorescences with white ray flowers and yellow discs (Fig. 1B) was about 1.5–2 cm in diameter. The low plants grew in a short lawn. In some places the vegetation was too scarce to cover the black and moist soil, which warmed up quickly when insolated. Also old leaves and pieces of wood heated up more easily than the transpiring grass. Flowers of G. nivalis L. (Amaryllidaceae) were measured in gardens because of their rare occurrence in cultural landscape. Their white oblong flowers (Fig. 1C) of about 2–4 cm length are bent to the ground. The plants – due to their vegetative propagation (bulbs) – often form clusters. Meteorological data Temperature at 0 and 10 cm above the ground in the immediate vicinity (within 5 m) of measured flowers and inflorescences was monitored. The temperature of studied plant material was compared with environmental factors (the temperature of the ground – T0 – and the temperature of the air in the approximate height of the flowers – T10). PT 100 thermometers (accuracy of measurement 70.4 1C) and data loggers (Comet System SO141, Rozˇnov pod Radhoˇstˇem, Czech Rep.) with automatic data logging at 5 min intervals were used. The measurements were carried out in still air. Relative humidity was measured by Comet System hygrometer S3120 (72.5 % from 5% to 95% of relative humidity) at 10 cm above the ground. The irradiance (Rs) was measured both manually with pyranometer Li 200 (LiCOR Biosciences, Lincoln, USA) in an immediate proximity of the measured plant and automatically at 15-min intervals by a Kipp & Zonen (Delft, The Netherlands) pyranometer CM 11 at a ˇ situated approximately 1 km meteorological station in Tˇrebon from the measuring site. Missing values were supplied using linear regression between the two methods used. A meteorological station was set up for monitoring temperature conditions of the plant material growing in the sun. To measure temperature in G. nivalis growing in shade, supplementary measurements were carried out. The air temperature was measured manually with a thermocouple ThermoPoint 64 plus (TMP 64P) from Flir Systems, Frankfurt/M., Germany (72.0 1C or 70.75%, whichever is greater). The mean surface temperature of the ground under the shaded conditions was calculated from the IR images. IR-camera measurements Temperatures in flowers and inflorescences were measured by means of an infrared camera-Therma CAMTM PM695 equipped with a Focal Plane Array detector (FPA) with an uncooled microbolometer (Flir Systems, Germany). The size of the image was 320 240 pixels. The IR-camera measured and imaged infrared radiation emitted from an object within a spectral ranging from 7.5 to 13 mm and assigned the appropriate temperature to each point – pixel – of the scanned image. The temperature span of the camera ranged from 40 to +120 1C (thermal sensitivity r0.08 1C at 30 1C). With 76800 readings of temperature in one image, the IR-camera equipped with a closeup lens (LW 64/150) made it possible to obtain a detailed image of temperature distribution in flowers and inflorescences. The temperature and humidity of the ambient air at 10 cm above the ground was set in accordance with the situation at the
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Fig. 1. Visual and IR images of Anemone nemorosa (A, D), Bellis perennis (B, E), Galanthus nivalis (C, F). Temperatures are expressed on a white to black scale.
time of measurement. The objects under study were measured from approximately 0.3 m. Based on data available in literature (Gates, 1964; Idso et al., 1969; Jackson, 1982; Ogawa et al. 2002; Qin et al., 2005), we set the emissivity of vegetation at 0.97. The measurements were conducted after droplets of morning dew adhering to the flowers and inflorescences were evaporated. Water (dew or rain) caused equalization of surface temperatures. ThermaCAMTMReporter 2000 Professional software was used for image processing. The temperature dynamics under changing irradiance in the flowers and inflorescences of A. nemorosa and B. perennis were studied by sequence scanning. Plants were scanned in 20 s intervals first in full sunlight then for 300 s under low irradiance and then irradiated again by direct sunlight (Figs. 4 and 7). Statistics To compare and analyse temperature of centres/discs and petals/rayflowers in flowers and inflorescences, respectively, we used the Student’s pair t-test, correlation and simple linear regression analysis. The dependencies of temperatures on environmental factors (Rs, T10 and T0) were tested using quadratic regression models. Since variability of the dependent variables could not be explained by individual factors a multiple backward stepwise polynomial (quadratic) regression model was used to examine the combined effect of Rs, T10 and T0. The dependency between the environmental factors was tested using simple linear regression. All analyses were tested on the 5% significance level. Statistica 7.1 software system (StatSoft, Inc. 2005) was used for all analyses.
Results Flowers of A. nemorosa (Fig. 1A) closed for night and opened in the morning to the east just like some other early spring species
(Kudo, 1995; McKee and Richards, 1998; van Doorn and van Meeteren, 2003) when temperature of the air reached approximately 10 1C. Sunlit white flowers had a clear pattern of temperature distribution (Fig. 1D). The pair t-test showed that the temperatures of the yellow centres were significantly higher (on average 1.8 1C) than the temperatures of the white petals (t ¼ 18.36, df ¼ 123, po0.05). A linear regression model showed that the temperature of the petals was dependent on the temperature of the centres (R ¼ 0.96, R2 ¼ 0.92, df ¼ 122, po0.05). The centres and the petals were on average 3.4 and 1.6 1C warmer than the air temperature and 5.4 and 3.5 1C warmer than the temperature of the ground, respectively (Fig. 2). Polynomial regressions showed that the temperature of both the centres and the petals of A. nemorosa was significantly dependent on all tested environmental factors: temperature of the air – T10 (Fig. 3A), temperature of the ground – T0 (Fig. 3B) and irradiance – Rs (Fig. 3C). The temperature of both the centres and the petals rose quickly with T10 under lower temperatures of the environment. Above approximately 18 1C the temperature increase slowed down (Fig. 3A). The relationship was similar for T0, although it was not so marked (Fig. 3B). On the contrary, the temperature of the flowers increased slowly under low irradiance. The increase of flower temperature became more marked with higher intensity above about 650 W m2 and this trend did not change up to 850 W m2, i.e. the highest irradiance values in our measurements (Fig. 3C). As the relationships between the temperatures of the flowers and the environmental factors were not linear and it was not possible either to study them separately, a backward stepwise polynomial regression was used to test them. The model showed (Table 1) that for the centres’ temperature, irradiance was responsible for the largest part of data variability. T10 showed to be also influential although with smaller significance. T0 was excluded from the regression model. Petals were significantly influenced by all tested factors although it was again irradiance that was found to be responsible for the largest part of variability.
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Fig. 2. Mean temperatures and their statistical deviations of the centres and petals of Anemone nemorosa and corresponding temperatures of the ambient air (T10) and of the ground (T0).
In both cases the polynomial stepwise regression model showed that Rs explained 86% of data variability (Table 1). When artificially shielded from the sun the temperature of the centres of A. nemorosa decreased in about 100 s to the temperature of the petals and the pattern of temperature distribution as well as the difference between the maximum and the minimum temperature within the flowers withered away (Fig. 4). As in the case of anemones the temperature distribution in inflorescences of B. perennis (Fig. 1E) lit by sunlight was clearly patterned. The yellow discs of the inflorescences were on average 6.5 1C (t ¼ 18.77, df ¼ 55, po0.05) warmer than the marginal white ray flowers. Also in the case of B. perennis the temperatures of petals and discs were significantly dependent (linear regression: R2 ¼ 0.87, df ¼ 54; po0.05). The temperatures of the sun lit discs and ray flowers were on average 7.4 and 0.9 1C warmer than the air, respectively (Fig. 5). On the contrary, the temperature of the dark and wet ground was significantly warmer than the temperature of both the discs (4.5 1C) and the ray flowers (10.9 1C) (Fig. 5). Polynomial regressions showed that the temperatures of both the centres and the petals of B. perennis were significantly dependent on all tested environmental factors: T10, T0 and Rs (Fig. 6A–C). The relationship between both the centres and the petals and T10 was to a large extent linear with no marked change of the relation with rising T10 (Fig. 6A). The influence of T0 on the temperature of the inflorescences was rising with growing T0 (Fig. 6B). The temperature of the inflorescences increased also with rising irradiance (Fig. 6C), although only up to about 680 W m2. Then the curve reached a plateau and even decreased. Backward stepwise polynomial regression (Table 1) showed that the variability of temperature of both the discs and the ray flowers was due mostly to T10 and partly to Rs (with less significance for the ray flowers). T0 could be excluded from the model (Table 1). The model explained 55% and 58% of data variability for the discs and ray flowers, respectively. When artificially shielded, the whole inflorescences cooled down and temperature differences within the inflorescences tended to equal out. The discs cooled down more quickly than the ray flowers (Fig. 7). However, during 300 s of shielding the temperature within the inflorescences did not equal out. The centres, which were on average 6.5 1C warmer before shielding, remained on average about 1.5 1C warmer than the marginal flowers at the end of the measuring period. G. nivalis, a protected species, was chosen for testing temperature relations in white vernal flowers bent to the ground.
Fig. 3. Temperature of centres and petals of Anemone nemorosa related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B) and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
No pattern of temperature distribution within the flower was found; the whole flowers had approximately the same temperature. The flowers showed to be on average 2.7 1C cooler than the surrounding air and on average 1.7 1C cooler than the ground (Fig. 8, group 1). However, the comparison of the flower temperature with the temperature of the ground was dependent on the time of the day and the amount of irradiance. Whereas early in the morning and in shadow the ground was cooler than the flowers and plants, in the sun the wet and dark ground warmed up high above the temperature of the observed objects. This was clearly reflected also in the mean temperature results when we divided
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Table 1 Backward stepwise polynomial regression showed the relevance of three tested environmental parameters (temperature of the ambient air T10, temperature of the ground T0 and solar irradiance Rs) for temperatures of Anemone nemorosa (AN, centres and petals), Bellis perennis (BP, discs and ray flowers) and Galanthus nivalis (GN, whole flowers).
T10 T210 T0 T20 Rs R2s R R2 (R2adj.) df P
AN – centre
AN – petals
BP – discs
BP – ray flowers
GN – total
1.44 1.74 EX EX 5.41 6.46 0.93 0.86 (0.85) 4, 117
1.86 2.22 0.18 EX 5.51 6.51 0.93 0.86 (0.85) 5, 116
0.75 EX EX EX EX 0.20 0.74 0.55 (0.54) 2, 163
0.77 EX EX EX 0.12 EX 0.76 0.58 (0.57) 2, 163
3.08 2.90 1.32 2.77 1.46 2.24 0.97 0.93 (0.93) 6, 70
The table shows the standardized regression coefficients ‘‘beta’’ and significance level of prediction (in the brackets) and the summary regression statistics. EX – excluded from the model by the backward stepwise polynomial regression. Significant at po0.05. Significant at po0.01. Significant at po0.001.
Fig. 4. Sequence scanning of flowers of Anemone nemorosa with different irradiance. Flowers were shaded and left for 300 s under low irradiance. The graph shows mean values of seven sequence measurements.
Fig. 5. Mean temperatures and their statistical deviations of discs and marginal ray flowers of Bellis perennis and corresponding temperatures of the ambient air (T10) and the ground (T0).
the data into two groups according to the amount of incoming irradiance. In shadow (Fig. 8, group 2) the flowers were on average 2.2 1C cooler than T10 and 1.9 1C warmer than the ground whereas in the sun the flowers were on average 3.4 1C cooler than T10 and as much as 6.4 1C cooler than the ground (Fig. 8, group 3). Polynomial regressions showed that also the temperatures of flowers of G. nivalis were significantly dependent on all tested environmental factors: T10, T0 and Rs (Fig. 9A–C). Under low temperature conditions the temperature of the flowers was increasing linearly with rising T10 and T0. However, when the temperature of flowers reached about 10 1C, it stopped increasing and gradually began to decrease again with rising temperature of the environment (Fig. 9A and B). The temperature of flowers of G. nivalis increased with increasing irradiance (Fig. 9C). Backward stepwise polynomial regression did not exclude any of the studied factors as having influence upon the flower temperatures (Table 1). The largest part of data variability was explained by the relationship with T10. Irradiance was responsible for only a minor part of data variability. The model explained 93% of data variability.
However, their ecological conditions are not narrow and warming up must not always represent an advantage for them. White-petalled heliotropic flowers of A. nemorosa were observed to be warmer than the ambient air. The temperature of both the centres and the petals was enhanced by sun tracking on average by 3.4 and 1.6 1C respectively. This corresponds well with results previously obtained with direct methods of temperature measurement for light coloured representatives of the Ranunculaceae family from arctic and alpine regions. Luzar and Gottsberger (2001) found in three white-petalled alpine Ranunculaceae (Callianthemum coriandrifolium Reichenb., Ranunculus alpestris L. and Pulsatilla alpina (L.) Del.) maximal values of excess temperatures to be between 2.0 and 6.2 1C above ambient air. Also Ranunculus adoneus Gray. (Stanton and Galen, 1989), Ranunculus acris L. (Totland, 1996) and Ranunculus montanus Willd. (Luzar and Gottsberger, 2001), yellow-petalled representatives of heliotropic Ranunculaceae, were reported to be in the proximity of gynoecium on average 4.0, 3.5 and 3.8 1C warmer than the ambient air, respectively. Enhanced temperatures were reported also in Dryas integrifolia Vahl. (Kevan, 1975) and Dryas octopetala L. (Wada, 1998) which, though from an other family (Rosaceae), are of similar appearance. Kudo (1995) measured temperatures in another spring ephemeral of the temperate deciduous forests in Japan from the Ranunculaceae family. He asserted that the gynoecium of sun tracking yellow-petalled Adonis ramosa Franch.
Discussion Early spring species from the temperate zone are commonly, though often only temporarily, exposed to extreme cold temperatures.
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Fig. 7. Sequence scanning of inflorescences of Bellis perennis under different irradiance, mean values of 13 measurements.
Fig. 8. Mean temperatures and their statistical deviations of the flowers of Galanthus nivalis and corresponding temperatures of the surrounding air and the ground. Group 1 – all flowers, group 2 – flowers in shade, and group 3 – insolated flowers.
Fig. 6. Temperature of discs and ray marginal flowers of Bellis perennis related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B), and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
was on average 5.5 1C warmer than the ambient air, and similarly to the previously cited authors he assigned this process to the heat-gathering function of petals. Kay et al. (1981) reported A. nemorosa to have a rare highly reflective structure of the petal surface, an optical feature considered essential for flowers concentrating radiation in their centres (Kevan, 1975; Kjellberg et al., 1982; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). However, although we stated that the flower centres of A. nemorosa species were on average 1.8 1C warmer than the petals, our results do not give evidence that flowers of A. nemorosa behave like small dish
antennas and function as solar collectors (Knutson, 1981). The temperatures of the centres and the petals were statistically interdependent and reacted in a similar way to all tested variables: Rs, T10 and T0 (Fig. 3A–C). The centres were warmer than the petals, most likely because they are more compact and because radiation among the stamens and carpels is retained more effectively than by the smooth and thin petals. If the corollas would focus heat on the sporophylls and would influence the heat distribution by adjusting the position of petals, than the difference in temperature between the centres and the petals would most probably change with changing Rs and T10. Irradiance was the most important environmental factor responsible for the largest part of data variability of the temperature of the Anemone flower centres. The flower temperature increased quickly with increasing irradiance (Fig. 3C). After shading, the temperature of the centres cooled down and the temperature gradient within the flowers disappeared (Fig. 4). The intrafloral temperature of A. nemorosa increased quickly also with increasing air temperature but later slowed down (Fig. 3A). It is probable that high temperatures could cause thermal damage of the reproductive organs in this early blooming species. Galen (2006) suggested that transpirational cooling reduced excess heat generated by heliotropism in Ranunculus adoneus. It is likely that
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Fig. 9. Temperature of flowers of Galanthus nivalis related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B), and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
transpiration influences the temperature of the flowers of A. nemorosa as well, and its role becomes more important with growing air temperature. Solar tracking flowers lack the ability to orient themselves away from the Sun’s rays to maintain their optimal temperature under high temperature (Galen, 2006). It is likely that hot and dry spring seasons could negatively influence the regional distribution of A. nemorosa. B. perennis is a common lawn species from the Asteraceae family that blooms under a whole range of ambient temperatures including low temperatures of early spring. Kevan (1989) observed that disc flowers warm in proportion to the cosine of
the angle of incident irradiance and that flowers of Taraxacum arctogenum Dahlst., Arnica alpina (L.) Olin and Erigeron compositus Pursh. under sunny conditions attained maximum temperatures between 2 and 6 1C above ambient. Luzar and Gottsberger (2001) proved Leucanthemopsis alpina to be 4.5 1C warmer than the ambient air. Orueta (2002) measured enhanced temperature of Mediterranean early spring marigold Calendula arvensis to be on average 2 1C above the surrounding air. In our measurements, the surface temperature of the sun lit yellow discs of B. perennis was on average 7.4 1C warmer than the air (Fig. 5). Marginal ray flowers were considerably cooler which resulted in large temperature differences within inflorescences (on average 6.5 1C). As temperature of the ground rose it seemed to influence more the temperature of the inflorescences growing very close to the surface (Fig. 6B). However, when the three environmental factors Rs, T10 and T0 were considered together by a polynomial stepwise regression, T0 was excluded from the model. The temperature of the discs rose with increasing Rs, but surprisingly above an irradiance intensity of 680 W m2 it began to decrease again. This was probably caused by the fact that the temperature of the discs was related mainly to the ambient temperature, but the distribution of T10 and Rs during the measurement was not well correlated and the highest temperatures were not related to the highest irradiances. It is likely that the discs accumulate a certain surplus of heat from the irradiance which represents approximately the same amount within the whole range of tested irradiances (500– 800 W m2). Here again the capacity of the discs to retain heat was probably due to a combination of their peculiar structure and weight. When irradiance dropped to very low values during shading it did not provide the energy surplus anymore and the discs slowly cooled down. The inflorescences of B. perennis do not seem to be capable of actively influencing temperature within their inflorescences with changing T10, T0 and Rs. It is likely that this species of an ecologically broad range of occurrences behaves opportunistically obtaining energy surplus under all conditions and is not specially adapted to low temperatures. G. nivalis is one of the earliest blooming flowers in the temperate zone. It often grows and blooms between still lasting patches of snow. Its bell-shaped white flowers are opened to the ¨ ground. Budel (1959) (cited in McKee and Richards, 1998) showed that hanging flowers of Leucojum vernum were by up to 11 1C warmer than the ambient air. Kevan (1989) suggested that ‘‘hanging bells’’ of arctic Ericaceae act as traps for rising warm air from the ground and documented this by measuring overtemperatures of 3–4 1C in white flowers of Cassiope tetragona (L.) D. Don. Sklena rˇ (1999) measured enhanced temperatures by several degrees in pubescent nodding inflorescences of Culcitium canescens Humb. Bonpl. in cold weather of an Andean Superpa ramo during daytime. The temperature excess correlated with radiation reflected from the ground or snow. To our great surprise, flower temperatures of G. nivalis, contrary to the results published in literature and our other results, were always cooler than the ambient air (Fig. 8). Moreover, the floral temperature increased with increasing T10 and T0. However, when it reached approximately 10 1C the trend reversed and the temperature began to decrease again (Fig. 9A and B). Although the floral temperature constantly increased with rising irradiance (Fig. 9C), Rs explained only a minor part of data variability. The temperature of the flowers was homogenous without any observable warming. Although the amount of data was limited and the results were based on two methods for measuring T10 and T0, it is obvious that flowers of G. nivalis do not warm up. Nor do they act as traps for reflected light (Kevan, 1989) or as a micro-greenhouse transmitting light into the centres of the flowers where it would be retained and absorbed (McKee and Richards, 1998). The ecological meaning of the observed behaviour
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is not clear. It seems, however, that G. nivalis is a species adapted to cold temperatures that avoids warm temperatures. The whole plant exhibits similar temperature behaviour as the flowers themselves. This may be the result of cooling or high reflectance of both silvery leaves and shiny white flowers. The presented conclusions are to a large extent based on detailed knowledge of temperature distribution and dynamics in flowers and inflorescences. The infrared camera detects the exact radiative temperature of the surface with great resolution and without interfering with either the measured objects or their micro-environment. This helped us to eliminate inaccuracy in temperature measurements of fragile structures such as petals and of widely opened flowers or inflorescences that might be substantially influenced by the device itself or the temperature of their surroundings respectively when measured by direct methods. Our results suggest that it is not possible to describe the thermal strategy in vernal temperate zone flowers simply as ‘‘the higher the temperature, the better’’. The three light-coloured flowers and inflorescences of temperate zone species differed markedly in their temperature behaviour. Flowers of A. nemorosa and inflorescences of B. perennis were warmer than the ambient air. Solar rays stimulated quick and clearly patterned distribution of temperature in them. Flowers of G. nivalis directed to the ground had uniform temperatures and were colder than the ambient air. Drawing on the results we are of the opinion that ephemeral species adapted to cold and wet conditions of early temperate spring, such as A. nemorosa and G. nivalis, may not profit from too high temperatures and may be even harmed when exposed to high temperatures combined with drought. Recently, phenological studies in Central Europe showed tendencies towards earlier flowering of G. nivalis (Roetzer et al., 2000). The shift of phenophases into early spring may well be understood as an escape from too warm temperatures later in spring.
Acknowledgements We would like to thank Professor Walter Larcher for his kind and helpful comments on the text, Dr. Jan Kvˇet for letting us use his garden for the measurements and Dr. Mark Corner and Jana Rejˇskova for having read the text and corrected the English. This work has been supported by the Ministry of Education of the Czech Republic (MSM 6007665806 and NPVII 2B06023). References ¨ Budel, A., 1959. The microclimate of flowers blooming near the ground. Z. Bienenforsch. 4, 131–140. Dyer, A.G., Whitney, H.M., Arnold, S.E.J., Glover, J., Chittka, L., 2006. Bees associate warmth with floral colour. Nature 442, 525. Ehleringer, J., Forseth, I., 1980. Solar tracking by plants. Science 210, 1094–1098. Galen, C., 2006. Solar furnaces or swamp coolers: costs and benefits of water use by solar-tracking flowers of the alpine buttercup Rannunculus adoneus. Oecologia 148, 195–201. Galen, C., Stanton, M.L., 2003. Sunny side up: flower heliotropism as a source of parental environmental effects on pollen quality and performance in the snow buttercup, Ranunculus adoneus (Ranunculaceae). Am. J. Bot. 90, 724–729.
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Gates, D.M., 1964. Characteristics of soil and vegetated surfaces to reflected and emitted radiation. Proc. Int. Symp. Remote Sens. Environ. 3, 573–600. Herrera, C.M., 1995. Floral biology, microclimate, and pollination by ectothermic bees in an early-blooming herb. Ecology 76, 218–228. Hocking, B., Sharplin, D., 1965. Flower basking by arctic insects. Nature 206, 215. Idso, S.B., Jackson, R.D., Ehrler, W.L., Mitchell, S.T., 1969. A method for determination of infrared emittances of leaves. Ecology 50, 899–902. Jackson, R.D., 1982. Canopy temperature and crop water stress. In: Hillel, D.I. (Ed.), Advances in Irrigation, vol. 1. Academic Press, New York, pp. 43–85. Kay, Q.O.N., Daoud, H.S., Stirton, C.H., 1981. Pigment distribution, light reflection and cell structure in petals. Bot. J. Linn. Soc. 83, 57–84. Kevan, P.G., 1975. Sun tracking solar furnaces in high arctic flowers: significance for pollination and insects. Science 189, 723–726. Kevan, P.G., 1989. Thermoregulation in arctic insects and flowers: adaptation and co-adaptation in behaviour, anatomy, and physiology. In: Mercer, J.B. (Ed.), Thermal Physiology, Proceedings of the International Symposium of Thermal Physiology, Tromso, Norway, 16–21 July, 1989. Elsevier, Amsterdam, pp. 747– 753. Kevan, P.G., 1990. Sexual differences in temperatures of blossoms on a dioecious plant, Salix arctica: significance for life in the arctic. Arct. Alp. Res. 22, 283–289. Kjellberg, B., Karlsson, S., Kertensson, I., 1982. Effects of heliotropic movements of flowers of Dryas octopetala L. on gynoecium temperature and seed development. Oecologia 54, 10–13. Knutson, R.M., 1981. Flowers that make heat while the sun shines. Nat. Hist. 90, 75–80. ´ J., 2005. Evaluation of long-term data on air temperature, Kova rˇova , M., Pokorny, relative air humidity and precipitation data in Mokre Louky Wetland by ˇ Meteorol. Bull. 58, 51–60 (in Czech). Tˇrebon. Kudo, G., 1995. Ecological significance of flower heliotropism in the spring ephemeral Adonis ramosa (Ranunculaceae). Oikos 72, 14–20. Luzar, N., Gottsberger, G., 2001. Flower heliotropism and floral heating of five alpine plant species and the effect on flower visiting in Ranunculus montanus in the Austrian Alps. Arct. Antarct. Alp. Res. 33, 93–99. McKee, J., Richards, A.J., 1998. Effect of flower structure and flower colour on intrafloral warming and pollen germination and pollen-tube growth in winter flowering Crocus L. (Iridaceae). Bot. J. Linn. Soc. 128, 369–384. Miller, G.A., 1986. Pubescence, floral temperature and fecundity in species of Puya (Bromeliaceae) in the Ecuadorian Andes. Oecologia 70, 155–160. Molgaard, P., 1989. Temperature relations of yellow and white flowered Papaver radicatum in north Greenland. Arct. Alp. Res. 21, 83–90. Ogawa, K., Schmugge, T., Jacob, F., French, A., 2002. Estimation of broadband land surface emissivity from multi-spectral thermal infrared remote sensing. Agronomie 22, 695–696. Orueta, D., 2002. Thermal relationships between Calendula arvensis inflorescences and Usia aurata bombyliid flies. Ecology 83, 3073–3085. ˜ o, S., Grace, J., 2002. The cooling of convolvulaceous flowers in a tropical Patin environment. Plant Cell Environ. 25, 41–51. Roetzer, T., Wittenzeller, M., Haeckel, H., Nekovar, J., 2000. Phenology in central Europe – differences and trends of spring phenophases in urban and rural areas. Int. J. Biometeorol. 44, 66. Qin, Z., Berliner, P.R., Karnieli, A., 2005. Ground temperature measurement and emissivity determination to understand the thermal anomaly and its significance on the development of the arid environmental ecosystem in the sand dunes across the Israel–Egypt border. J. Arid Environ. 60, 27–52. Sklena rˇ, P., 1999. Nodding capitula in superpa ramo Asteraceae: an adaptation to unpredictable environment. Biotropica 31, 394–402. Stanton, M.L., Galen, C., 1989. Consequences of flower heliotropism for reproduction in an alpine buttercup (Ranunculus adoneus). Oecologia 78, 477–485. Totland, O., 1996. Flower heliotropism in an alpine population of Ranunculus acris (Ranunculaceae): effects on flower temperature, insect visitation, and seed production. Am. J. Bot. 83, 452–458. Tsukaya, H., Tsuge, T., 2001. Morphological adaptation of inflorescences in plants that develop at low temperatures in early spring: the convergent evolution of ‘‘downy plants’’. Plant Biol. 3, 536–543. Tsukaya, H., Fujikawa, K., Wu, S.-G., 2002. Thermal insulation and accumulation of heat in the downy inflorescences of Saussurea medusa (Asteraceae) at high elevation in Yunnan, China. J. Plant Res. 115, 263–268. Van Doorn, W.G., van Meeteren, U., 2003. Flower opening and closure: a review. J. Exp. Bot. 54, 1801–1812. Wada, N., 1998. Sun-tracking flowers movement and seed production of mountain avens, Dryas octopetala L., in the High Arctic, NY/Alesund, Svalbard. Proc. NIPR Symp. Polar Biol. 11, 128–136.
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Flora journal homepage: www.elsevier.de/flora
Temperature distribution in light-coloured flowers and inflorescences of early spring temperate species measured by Infrared camera Alzˇbˇeta Rejˇskova a,b,, Jakub Brom b,c, Jan Pokorny´ b,c, Jozef Korecˇko a,b a
136, Nove Hrady 373 33, Czech Republic University of South Bohemia, Institute of Physical Biology, Zamek ENKI o.p.s., not-for-profit organisation, Dukelska 145, Tˇrebonˇ 379 01, Czech Republic c ˇ University of South Bohemia, Faculty of Agriculture, Laboratory of Applied Ecology, Studentska 787/13, Cesk e Budˇejovice 370 05, Czech Republic b
a r t i c l e in f o
a b s t r a c t
Article history: Received 18 February 2009 Accepted 3 May 2009
Temperature is a limiting factor for plant reproduction under harsh conditions. Using an infrared camera, we studied temperature distribution in three early flowering light-coloured species of markedly different morphology. The influence of three environmental factors (temperature of the ambient air, temperature of the ground and irradiance) on the temperature of the flowers and inflorescences was evaluated. White petals and yellow centres of sun tracking Anemone nemorosa (Ranunculaceae) were shown to be on average 1.6 and 3.4 1C warmer than the ambient air, respectively. The surface temperature of the sun lit yellow discs of Bellis perennis (Asteraceae) was on average 7.4 1C warmer than the ambient air. Direct solar light was found to be responsible for large temperature differences between the discs and the marginal ray flowers. Bell-shaped white flowers of Galanthus nivalis (Amaryllidaceae) bent to the ground were on average 2.7 1C cooler than the surrounding air. The temperature relations of the different reproductive organs to the studied environmental factors are discussed. Temperature behaviour of the studied lowland species is compared with the results previously gained for alpine and arctic species by other authors. Ecological importance of our conclusions is considered. & 2009 Elsevier GmbH. All rights reserved.
Keywords: Flower Inflorescence Temperature distribution Ambient air Infrared camera
Introduction It is essential for plants to maintain the temperature of their reproductive organs at metabolic optima that promote growth and development (Galen, 2006; Patino and Grace, 2002). Morphology and colour have been suggested to play an important role in regulation of temperature in flowers growing in cold climates (Kevan, 1975, 1989; Knutson, 1981). In general, dark surfaces absorb radiation with higher intensity and warm up more quickly than light-coloured ones. However, the temperature within flowers and inflorescences is not simply a question of colour (Molgaard, 1989). Radiation incident on the flower is usually not reflected straight from the surface but in a complex manner from the inner epidermal layers being influenced by both the pigments and the shape and structure of epidermal cells (Kay et al., 1981). Several authors reported increased intrafloral temperatures in some alpine, arctic as well as montane spring ephemeral species related to special structural and optical features of the reproductive organs (Galen, 2006; Kudo, 1995; Luzar and Gottsberger,
Corresponding author at: ENKI o.p.s., Dukelska 145, Tˇrebon ˇ 379 01, Czech Republic. Tel.: +420 775147742; fax: +420 384724346. E-mail address: [email protected]. (A. Rejˇskova )
0367-2530/$ - see front matter & 2009 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2009.05.001
2001; Molgaard, 1989; Stanton and Galen, 1989; Totland, 1996; Tsukaya et al., 2002). In general, there are two possible ways of improving the energy budget of flowers and inflorescences under cold conditions. The first is to obtain more energy from the sun or from the environment. For some heliotropic species with light petals and parabolic shape a combined effect of reflective features of petals and the overall architecture of the flowers was demonstrated and the flowers were considered to function as parabolic or spherical solar collectors (Galen, 2006; Kevan, 1975; Kjellberg et al., 1982; Knutson, 1981; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). Some flowers and inflorescences bent to the ground seem to be capable of collecting energy coming from the ground or reflected from snow (Kevan, 1989; Sklena rˇ, 1999). The second possibility is to improve the heat storage capacity of the reproductive organs. Pubescence is an effective insulator, maintaining enhanced flower temperatures (Miller, 1986). This has been documented for highly pubescent catkins of the arctic willow Salix arctica (Kevan, 1990), for pubescent flowers of Puya species in Andean pa ramo (Miller, 1986) and suggested for a whole group of ‘‘downy plants’’ characterized by dense trichomes on bracts of inflorescences that help to keep the interior of buds warm (Tsukaya and Tsuge, 2001). Some plants combine both of these principles and form an intrafloral ‘‘micro-greenhouse’’. Having studied three colour variants of Crocus sp. McKee and
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Richards (1998) concluded that the proportion and spectral range of both absorbed and transmitted light is important for temperature distribution in flowers. The transmitted energy is trapped by reflective inner tepal surfaces and stored in the centres. For species from cold alpine and arctic regions even a slight warming up may enhance reproductive powers (Kevan, 1975; Kjellberg, et al. 1982; Stanton and Galen, 1989). Warmer flowers are visited more often by pollinating insects (Dyer et al., 2006; Ehleringer and Forseth, 1980; Herrera, 1995; Hocking and Sharplin, 1965; Kudo, 1995; Luzar and Gottsberger, 2001). In situations when the ambient temperature is often lower than the optimum temperature of many physiological processes, higher temperatures promote germination and growth of the pollen tube (Galen and Stanton, 2003; McKee and Richards, 1998) and later also the growth of seeds (Ehleringer and Forseth, 1980; Stanton and Galen, 1989). On the other hand excessive temperature may result in floral overheating (Galen, 2006). We decided to study temperature distribution in some vernal lowland species often exposed to very low but sometimes also to rather high temperatures, on assumption that their structural and physiological thermo-regulative adaptations may well differ from similar alpine and arctic species. In previous research prevailing temperature data of flowers have been collected with the help of contact thermometers, either thermocouples or thermistors (Kevan, 1975; Kjellberg et al., 1982; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). In our study an infrared camera was used. The aim of our study was to investigate temperature features of flowers and inflorescences of three common vernal species of temperate zone. The effect of colour was limited by selecting species with white or light coloured (white and yellow) reproductive organs only. We chose one inflorescence and two flowers with markedly different shapes to see whether the warming-up strategies differ in reproductive organs of dissimilar morphology. We studied (1) the capacity of heliotropic Anemone nemorosa L. with parabolic shaped flowers to warm up by concentrating solar rays, (2) temperature distribution in disc inflorescences of Bellis perennis L. and (3) ability of bent Galanthus nivalis L. flowers to warm up from the ground and function as a micro-greenhouse.
Materials and methods Study site and time of measurement The plants were measured in their natural habitats in ˇ in South Bohemia meadows and gardens near the town of Tˇrebon, (latitude 491N, longitude 141180 E, altitude 433 m). The mean temperature (data from 1977 to 2003) is 2.3 1C in January and ´ 2005). All sites had a 16.8 1C in July (Kova rˇova and Pokorny, homogenous surface without soil asperity. The measurements were carried out in March and April 2008 in the morning hours after morning mist lifted and the flowers and inflorescences opened. Cloudless and fogless weather conditions made it possible to study the effect of direct radiation on temperature distribution. Plant material Three plant species of early spring flora, widespread in the temperate zone, with white flowers and inflorescences were chosen for temperature analysis. A. nemorosa L. (Ranunculaceae) grew at the edge of a deciduous forest with Acer platanoides L. as a prevailing woody species. The ground in the forest was covered
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with dry leaves from the last growing season. Individual plants grew in loose groups; their leaves did not overlap. The bowl shaped flowers with white petals and yellow centres were about 3–4 cm large in diameter (Fig. 1A). The IR images of B. perennis L. (Asteraceae) were scanned in a garden. The size of inflorescences with white ray flowers and yellow discs (Fig. 1B) was about 1.5–2 cm in diameter. The low plants grew in a short lawn. In some places the vegetation was too scarce to cover the black and moist soil, which warmed up quickly when insolated. Also old leaves and pieces of wood heated up more easily than the transpiring grass. Flowers of G. nivalis L. (Amaryllidaceae) were measured in gardens because of their rare occurrence in cultural landscape. Their white oblong flowers (Fig. 1C) of about 2–4 cm length are bent to the ground. The plants – due to their vegetative propagation (bulbs) – often form clusters. Meteorological data Temperature at 0 and 10 cm above the ground in the immediate vicinity (within 5 m) of measured flowers and inflorescences was monitored. The temperature of studied plant material was compared with environmental factors (the temperature of the ground – T0 – and the temperature of the air in the approximate height of the flowers – T10). PT 100 thermometers (accuracy of measurement 70.4 1C) and data loggers (Comet System SO141, Rozˇnov pod Radhoˇstˇem, Czech Rep.) with automatic data logging at 5 min intervals were used. The measurements were carried out in still air. Relative humidity was measured by Comet System hygrometer S3120 (72.5 % from 5% to 95% of relative humidity) at 10 cm above the ground. The irradiance (Rs) was measured both manually with pyranometer Li 200 (LiCOR Biosciences, Lincoln, USA) in an immediate proximity of the measured plant and automatically at 15-min intervals by a Kipp & Zonen (Delft, The Netherlands) pyranometer CM 11 at a ˇ situated approximately 1 km meteorological station in Tˇrebon from the measuring site. Missing values were supplied using linear regression between the two methods used. A meteorological station was set up for monitoring temperature conditions of the plant material growing in the sun. To measure temperature in G. nivalis growing in shade, supplementary measurements were carried out. The air temperature was measured manually with a thermocouple ThermoPoint 64 plus (TMP 64P) from Flir Systems, Frankfurt/M., Germany (72.0 1C or 70.75%, whichever is greater). The mean surface temperature of the ground under the shaded conditions was calculated from the IR images. IR-camera measurements Temperatures in flowers and inflorescences were measured by means of an infrared camera-Therma CAMTM PM695 equipped with a Focal Plane Array detector (FPA) with an uncooled microbolometer (Flir Systems, Germany). The size of the image was 320 240 pixels. The IR-camera measured and imaged infrared radiation emitted from an object within a spectral ranging from 7.5 to 13 mm and assigned the appropriate temperature to each point – pixel – of the scanned image. The temperature span of the camera ranged from 40 to +120 1C (thermal sensitivity r0.08 1C at 30 1C). With 76800 readings of temperature in one image, the IR-camera equipped with a closeup lens (LW 64/150) made it possible to obtain a detailed image of temperature distribution in flowers and inflorescences. The temperature and humidity of the ambient air at 10 cm above the ground was set in accordance with the situation at the
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Fig. 1. Visual and IR images of Anemone nemorosa (A, D), Bellis perennis (B, E), Galanthus nivalis (C, F). Temperatures are expressed on a white to black scale.
time of measurement. The objects under study were measured from approximately 0.3 m. Based on data available in literature (Gates, 1964; Idso et al., 1969; Jackson, 1982; Ogawa et al. 2002; Qin et al., 2005), we set the emissivity of vegetation at 0.97. The measurements were conducted after droplets of morning dew adhering to the flowers and inflorescences were evaporated. Water (dew or rain) caused equalization of surface temperatures. ThermaCAMTMReporter 2000 Professional software was used for image processing. The temperature dynamics under changing irradiance in the flowers and inflorescences of A. nemorosa and B. perennis were studied by sequence scanning. Plants were scanned in 20 s intervals first in full sunlight then for 300 s under low irradiance and then irradiated again by direct sunlight (Figs. 4 and 7). Statistics To compare and analyse temperature of centres/discs and petals/rayflowers in flowers and inflorescences, respectively, we used the Student’s pair t-test, correlation and simple linear regression analysis. The dependencies of temperatures on environmental factors (Rs, T10 and T0) were tested using quadratic regression models. Since variability of the dependent variables could not be explained by individual factors a multiple backward stepwise polynomial (quadratic) regression model was used to examine the combined effect of Rs, T10 and T0. The dependency between the environmental factors was tested using simple linear regression. All analyses were tested on the 5% significance level. Statistica 7.1 software system (StatSoft, Inc. 2005) was used for all analyses.
Results Flowers of A. nemorosa (Fig. 1A) closed for night and opened in the morning to the east just like some other early spring species
(Kudo, 1995; McKee and Richards, 1998; van Doorn and van Meeteren, 2003) when temperature of the air reached approximately 10 1C. Sunlit white flowers had a clear pattern of temperature distribution (Fig. 1D). The pair t-test showed that the temperatures of the yellow centres were significantly higher (on average 1.8 1C) than the temperatures of the white petals (t ¼ 18.36, df ¼ 123, po0.05). A linear regression model showed that the temperature of the petals was dependent on the temperature of the centres (R ¼ 0.96, R2 ¼ 0.92, df ¼ 122, po0.05). The centres and the petals were on average 3.4 and 1.6 1C warmer than the air temperature and 5.4 and 3.5 1C warmer than the temperature of the ground, respectively (Fig. 2). Polynomial regressions showed that the temperature of both the centres and the petals of A. nemorosa was significantly dependent on all tested environmental factors: temperature of the air – T10 (Fig. 3A), temperature of the ground – T0 (Fig. 3B) and irradiance – Rs (Fig. 3C). The temperature of both the centres and the petals rose quickly with T10 under lower temperatures of the environment. Above approximately 18 1C the temperature increase slowed down (Fig. 3A). The relationship was similar for T0, although it was not so marked (Fig. 3B). On the contrary, the temperature of the flowers increased slowly under low irradiance. The increase of flower temperature became more marked with higher intensity above about 650 W m2 and this trend did not change up to 850 W m2, i.e. the highest irradiance values in our measurements (Fig. 3C). As the relationships between the temperatures of the flowers and the environmental factors were not linear and it was not possible either to study them separately, a backward stepwise polynomial regression was used to test them. The model showed (Table 1) that for the centres’ temperature, irradiance was responsible for the largest part of data variability. T10 showed to be also influential although with smaller significance. T0 was excluded from the regression model. Petals were significantly influenced by all tested factors although it was again irradiance that was found to be responsible for the largest part of variability.
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Fig. 2. Mean temperatures and their statistical deviations of the centres and petals of Anemone nemorosa and corresponding temperatures of the ambient air (T10) and of the ground (T0).
In both cases the polynomial stepwise regression model showed that Rs explained 86% of data variability (Table 1). When artificially shielded from the sun the temperature of the centres of A. nemorosa decreased in about 100 s to the temperature of the petals and the pattern of temperature distribution as well as the difference between the maximum and the minimum temperature within the flowers withered away (Fig. 4). As in the case of anemones the temperature distribution in inflorescences of B. perennis (Fig. 1E) lit by sunlight was clearly patterned. The yellow discs of the inflorescences were on average 6.5 1C (t ¼ 18.77, df ¼ 55, po0.05) warmer than the marginal white ray flowers. Also in the case of B. perennis the temperatures of petals and discs were significantly dependent (linear regression: R2 ¼ 0.87, df ¼ 54; po0.05). The temperatures of the sun lit discs and ray flowers were on average 7.4 and 0.9 1C warmer than the air, respectively (Fig. 5). On the contrary, the temperature of the dark and wet ground was significantly warmer than the temperature of both the discs (4.5 1C) and the ray flowers (10.9 1C) (Fig. 5). Polynomial regressions showed that the temperatures of both the centres and the petals of B. perennis were significantly dependent on all tested environmental factors: T10, T0 and Rs (Fig. 6A–C). The relationship between both the centres and the petals and T10 was to a large extent linear with no marked change of the relation with rising T10 (Fig. 6A). The influence of T0 on the temperature of the inflorescences was rising with growing T0 (Fig. 6B). The temperature of the inflorescences increased also with rising irradiance (Fig. 6C), although only up to about 680 W m2. Then the curve reached a plateau and even decreased. Backward stepwise polynomial regression (Table 1) showed that the variability of temperature of both the discs and the ray flowers was due mostly to T10 and partly to Rs (with less significance for the ray flowers). T0 could be excluded from the model (Table 1). The model explained 55% and 58% of data variability for the discs and ray flowers, respectively. When artificially shielded, the whole inflorescences cooled down and temperature differences within the inflorescences tended to equal out. The discs cooled down more quickly than the ray flowers (Fig. 7). However, during 300 s of shielding the temperature within the inflorescences did not equal out. The centres, which were on average 6.5 1C warmer before shielding, remained on average about 1.5 1C warmer than the marginal flowers at the end of the measuring period. G. nivalis, a protected species, was chosen for testing temperature relations in white vernal flowers bent to the ground.
Fig. 3. Temperature of centres and petals of Anemone nemorosa related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B) and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
No pattern of temperature distribution within the flower was found; the whole flowers had approximately the same temperature. The flowers showed to be on average 2.7 1C cooler than the surrounding air and on average 1.7 1C cooler than the ground (Fig. 8, group 1). However, the comparison of the flower temperature with the temperature of the ground was dependent on the time of the day and the amount of irradiance. Whereas early in the morning and in shadow the ground was cooler than the flowers and plants, in the sun the wet and dark ground warmed up high above the temperature of the observed objects. This was clearly reflected also in the mean temperature results when we divided
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Table 1 Backward stepwise polynomial regression showed the relevance of three tested environmental parameters (temperature of the ambient air T10, temperature of the ground T0 and solar irradiance Rs) for temperatures of Anemone nemorosa (AN, centres and petals), Bellis perennis (BP, discs and ray flowers) and Galanthus nivalis (GN, whole flowers).
T10 T210 T0 T20 Rs R2s R R2 (R2adj.) df P
AN – centre
AN – petals
BP – discs
BP – ray flowers
GN – total
1.44 1.74 EX EX 5.41 6.46 0.93 0.86 (0.85) 4, 117
1.86 2.22 0.18 EX 5.51 6.51 0.93 0.86 (0.85) 5, 116
0.75 EX EX EX EX 0.20 0.74 0.55 (0.54) 2, 163
0.77 EX EX EX 0.12 EX 0.76 0.58 (0.57) 2, 163
3.08 2.90 1.32 2.77 1.46 2.24 0.97 0.93 (0.93) 6, 70
The table shows the standardized regression coefficients ‘‘beta’’ and significance level of prediction (in the brackets) and the summary regression statistics. EX – excluded from the model by the backward stepwise polynomial regression. Significant at po0.05. Significant at po0.01. Significant at po0.001.
Fig. 4. Sequence scanning of flowers of Anemone nemorosa with different irradiance. Flowers were shaded and left for 300 s under low irradiance. The graph shows mean values of seven sequence measurements.
Fig. 5. Mean temperatures and their statistical deviations of discs and marginal ray flowers of Bellis perennis and corresponding temperatures of the ambient air (T10) and the ground (T0).
the data into two groups according to the amount of incoming irradiance. In shadow (Fig. 8, group 2) the flowers were on average 2.2 1C cooler than T10 and 1.9 1C warmer than the ground whereas in the sun the flowers were on average 3.4 1C cooler than T10 and as much as 6.4 1C cooler than the ground (Fig. 8, group 3). Polynomial regressions showed that also the temperatures of flowers of G. nivalis were significantly dependent on all tested environmental factors: T10, T0 and Rs (Fig. 9A–C). Under low temperature conditions the temperature of the flowers was increasing linearly with rising T10 and T0. However, when the temperature of flowers reached about 10 1C, it stopped increasing and gradually began to decrease again with rising temperature of the environment (Fig. 9A and B). The temperature of flowers of G. nivalis increased with increasing irradiance (Fig. 9C). Backward stepwise polynomial regression did not exclude any of the studied factors as having influence upon the flower temperatures (Table 1). The largest part of data variability was explained by the relationship with T10. Irradiance was responsible for only a minor part of data variability. The model explained 93% of data variability.
However, their ecological conditions are not narrow and warming up must not always represent an advantage for them. White-petalled heliotropic flowers of A. nemorosa were observed to be warmer than the ambient air. The temperature of both the centres and the petals was enhanced by sun tracking on average by 3.4 and 1.6 1C respectively. This corresponds well with results previously obtained with direct methods of temperature measurement for light coloured representatives of the Ranunculaceae family from arctic and alpine regions. Luzar and Gottsberger (2001) found in three white-petalled alpine Ranunculaceae (Callianthemum coriandrifolium Reichenb., Ranunculus alpestris L. and Pulsatilla alpina (L.) Del.) maximal values of excess temperatures to be between 2.0 and 6.2 1C above ambient air. Also Ranunculus adoneus Gray. (Stanton and Galen, 1989), Ranunculus acris L. (Totland, 1996) and Ranunculus montanus Willd. (Luzar and Gottsberger, 2001), yellow-petalled representatives of heliotropic Ranunculaceae, were reported to be in the proximity of gynoecium on average 4.0, 3.5 and 3.8 1C warmer than the ambient air, respectively. Enhanced temperatures were reported also in Dryas integrifolia Vahl. (Kevan, 1975) and Dryas octopetala L. (Wada, 1998) which, though from an other family (Rosaceae), are of similar appearance. Kudo (1995) measured temperatures in another spring ephemeral of the temperate deciduous forests in Japan from the Ranunculaceae family. He asserted that the gynoecium of sun tracking yellow-petalled Adonis ramosa Franch.
Discussion Early spring species from the temperate zone are commonly, though often only temporarily, exposed to extreme cold temperatures.
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Fig. 7. Sequence scanning of inflorescences of Bellis perennis under different irradiance, mean values of 13 measurements.
Fig. 8. Mean temperatures and their statistical deviations of the flowers of Galanthus nivalis and corresponding temperatures of the surrounding air and the ground. Group 1 – all flowers, group 2 – flowers in shade, and group 3 – insolated flowers.
Fig. 6. Temperature of discs and ray marginal flowers of Bellis perennis related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B), and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
was on average 5.5 1C warmer than the ambient air, and similarly to the previously cited authors he assigned this process to the heat-gathering function of petals. Kay et al. (1981) reported A. nemorosa to have a rare highly reflective structure of the petal surface, an optical feature considered essential for flowers concentrating radiation in their centres (Kevan, 1975; Kjellberg et al., 1982; Kudo, 1995; Luzar and Gottsberger, 2001; McKee and Richards, 1998; Stanton and Galen, 1989). However, although we stated that the flower centres of A. nemorosa species were on average 1.8 1C warmer than the petals, our results do not give evidence that flowers of A. nemorosa behave like small dish
antennas and function as solar collectors (Knutson, 1981). The temperatures of the centres and the petals were statistically interdependent and reacted in a similar way to all tested variables: Rs, T10 and T0 (Fig. 3A–C). The centres were warmer than the petals, most likely because they are more compact and because radiation among the stamens and carpels is retained more effectively than by the smooth and thin petals. If the corollas would focus heat on the sporophylls and would influence the heat distribution by adjusting the position of petals, than the difference in temperature between the centres and the petals would most probably change with changing Rs and T10. Irradiance was the most important environmental factor responsible for the largest part of data variability of the temperature of the Anemone flower centres. The flower temperature increased quickly with increasing irradiance (Fig. 3C). After shading, the temperature of the centres cooled down and the temperature gradient within the flowers disappeared (Fig. 4). The intrafloral temperature of A. nemorosa increased quickly also with increasing air temperature but later slowed down (Fig. 3A). It is probable that high temperatures could cause thermal damage of the reproductive organs in this early blooming species. Galen (2006) suggested that transpirational cooling reduced excess heat generated by heliotropism in Ranunculus adoneus. It is likely that
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Fig. 9. Temperature of flowers of Galanthus nivalis related to temperature of the surrounding air, T10 (A), temperature of the ground, T0 (B), and solar irradiance, Rs (C). Polynomial regressions proved all the factors to be significant at po0.001.
transpiration influences the temperature of the flowers of A. nemorosa as well, and its role becomes more important with growing air temperature. Solar tracking flowers lack the ability to orient themselves away from the Sun’s rays to maintain their optimal temperature under high temperature (Galen, 2006). It is likely that hot and dry spring seasons could negatively influence the regional distribution of A. nemorosa. B. perennis is a common lawn species from the Asteraceae family that blooms under a whole range of ambient temperatures including low temperatures of early spring. Kevan (1989) observed that disc flowers warm in proportion to the cosine of
the angle of incident irradiance and that flowers of Taraxacum arctogenum Dahlst., Arnica alpina (L.) Olin and Erigeron compositus Pursh. under sunny conditions attained maximum temperatures between 2 and 6 1C above ambient. Luzar and Gottsberger (2001) proved Leucanthemopsis alpina to be 4.5 1C warmer than the ambient air. Orueta (2002) measured enhanced temperature of Mediterranean early spring marigold Calendula arvensis to be on average 2 1C above the surrounding air. In our measurements, the surface temperature of the sun lit yellow discs of B. perennis was on average 7.4 1C warmer than the air (Fig. 5). Marginal ray flowers were considerably cooler which resulted in large temperature differences within inflorescences (on average 6.5 1C). As temperature of the ground rose it seemed to influence more the temperature of the inflorescences growing very close to the surface (Fig. 6B). However, when the three environmental factors Rs, T10 and T0 were considered together by a polynomial stepwise regression, T0 was excluded from the model. The temperature of the discs rose with increasing Rs, but surprisingly above an irradiance intensity of 680 W m2 it began to decrease again. This was probably caused by the fact that the temperature of the discs was related mainly to the ambient temperature, but the distribution of T10 and Rs during the measurement was not well correlated and the highest temperatures were not related to the highest irradiances. It is likely that the discs accumulate a certain surplus of heat from the irradiance which represents approximately the same amount within the whole range of tested irradiances (500– 800 W m2). Here again the capacity of the discs to retain heat was probably due to a combination of their peculiar structure and weight. When irradiance dropped to very low values during shading it did not provide the energy surplus anymore and the discs slowly cooled down. The inflorescences of B. perennis do not seem to be capable of actively influencing temperature within their inflorescences with changing T10, T0 and Rs. It is likely that this species of an ecologically broad range of occurrences behaves opportunistically obtaining energy surplus under all conditions and is not specially adapted to low temperatures. G. nivalis is one of the earliest blooming flowers in the temperate zone. It often grows and blooms between still lasting patches of snow. Its bell-shaped white flowers are opened to the ¨ ground. Budel (1959) (cited in McKee and Richards, 1998) showed that hanging flowers of Leucojum vernum were by up to 11 1C warmer than the ambient air. Kevan (1989) suggested that ‘‘hanging bells’’ of arctic Ericaceae act as traps for rising warm air from the ground and documented this by measuring overtemperatures of 3–4 1C in white flowers of Cassiope tetragona (L.) D. Don. Sklena rˇ (1999) measured enhanced temperatures by several degrees in pubescent nodding inflorescences of Culcitium canescens Humb. Bonpl. in cold weather of an Andean Superpa ramo during daytime. The temperature excess correlated with radiation reflected from the ground or snow. To our great surprise, flower temperatures of G. nivalis, contrary to the results published in literature and our other results, were always cooler than the ambient air (Fig. 8). Moreover, the floral temperature increased with increasing T10 and T0. However, when it reached approximately 10 1C the trend reversed and the temperature began to decrease again (Fig. 9A and B). Although the floral temperature constantly increased with rising irradiance (Fig. 9C), Rs explained only a minor part of data variability. The temperature of the flowers was homogenous without any observable warming. Although the amount of data was limited and the results were based on two methods for measuring T10 and T0, it is obvious that flowers of G. nivalis do not warm up. Nor do they act as traps for reflected light (Kevan, 1989) or as a micro-greenhouse transmitting light into the centres of the flowers where it would be retained and absorbed (McKee and Richards, 1998). The ecological meaning of the observed behaviour
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is not clear. It seems, however, that G. nivalis is a species adapted to cold temperatures that avoids warm temperatures. The whole plant exhibits similar temperature behaviour as the flowers themselves. This may be the result of cooling or high reflectance of both silvery leaves and shiny white flowers. The presented conclusions are to a large extent based on detailed knowledge of temperature distribution and dynamics in flowers and inflorescences. The infrared camera detects the exact radiative temperature of the surface with great resolution and without interfering with either the measured objects or their micro-environment. This helped us to eliminate inaccuracy in temperature measurements of fragile structures such as petals and of widely opened flowers or inflorescences that might be substantially influenced by the device itself or the temperature of their surroundings respectively when measured by direct methods. Our results suggest that it is not possible to describe the thermal strategy in vernal temperate zone flowers simply as ‘‘the higher the temperature, the better’’. The three light-coloured flowers and inflorescences of temperate zone species differed markedly in their temperature behaviour. Flowers of A. nemorosa and inflorescences of B. perennis were warmer than the ambient air. Solar rays stimulated quick and clearly patterned distribution of temperature in them. Flowers of G. nivalis directed to the ground had uniform temperatures and were colder than the ambient air. Drawing on the results we are of the opinion that ephemeral species adapted to cold and wet conditions of early temperate spring, such as A. nemorosa and G. nivalis, may not profit from too high temperatures and may be even harmed when exposed to high temperatures combined with drought. Recently, phenological studies in Central Europe showed tendencies towards earlier flowering of G. nivalis (Roetzer et al., 2000). The shift of phenophases into early spring may well be understood as an escape from too warm temperatures later in spring.
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