Elsevier

Aquatic Botany

Volume 138, February 2017, Pages 37-44
Aquatic Botany

Respiration, thermogenesis, and thermoregulation of Victoria cruziana flowers

https://doi.org/10.1016/j.aquabot.2016.11.014Get rights and content

Highlights

  • V. cruziana flowers increase their metabolic rate on only the first night of blooming.

  • Floral heat production is not regulated in response to ambient temperature.

  • A second increase in metabolic rate could be induced by rewarming a cold flower.

  • Patterns of heat production differ between V. cruziana and V. amazonica.

Abstract

The flowers of Victoria cruziana bloom over two consecutive nights, during which time they dramatically increase their metabolic rate (MR) to raise their internal temperature by 7–10 °C above air temperature. To investigate the metabolic cost of thermogenesis in V. cruziana and determine the role of ambient temperature and developmental phase on floral temperature, flowers growing in an outdoor pond were measured in situ by placing them within a temperature-controlled, flow-through respirometry chamber. The flower’s metabolic rate and temperature were recorded simultaneously over the 40 h of their two-night flowering cycle. During this time, flowers were exposed to either a normal (cool nights, warm days) or an inverted (cool days, warm nights) thermal regime. V. cruziana flowers exposed to normal daily temperature variation showed a large increase in MR on the first evening that declined steadily over the subsequent days. Exposure to experimentally-manipulated cooler daytime temperatures did not stimulate flowers to increase their MR, indicating a lack of thermoregulatory capacity. However, rewarming a cooled flower on the second evening caused a large increase in MR, but not in temperature. This increase appeared to arise due to the delayed consumption of energy reserves that would otherwise have been used over the course of the preceding day, coupled with a more open, and less insulated, floral chamber. The pattern of thermogenesis shown by V. cruziana is unlike that of its closest relative, V. amazonica, which shows large increases in MR and temperature over both nights of flowering.

Introduction

The ability of an organism to produce heat is most often associated with warm-blooded animals. But some angiosperms also possess this capacity, dramatically increasing the metabolic rate (MR) of their flowers to elevate their temperature well above that of the surrounding air. While floral thermogenesis is comparatively unusual among the angiosperms, this ability is particularly well developed in some members of the Araceae (aroid lilies), Nymphaeaceae (water lilies), and Nelumbonaceae (sacred lotus) (Seymour and Schultze-Motel, 1997). These flowers generate heat within their tissues by using an alternative oxidase (AOX) pathway in the mitochondria (Elthon and McIntosh, 1987). Thus, heat production results from aerobic metabolism and the MR of the flower, measured indirectly either as oxygen uptake or carbon dioxide release, closely tracks thermogenic activity (Seymour et al., 2015). Although generating sufficient heat to increase the temperature of a flower is energetically costly, from an evolutionary perspective this strategy benefits the flower by providing their insect pollinators with a ‘heat reward’ in the form of a thermally suitable microclimate (Seymour et al., 2003), enhancing the release and distribution of volatile perfumes to signal to pollinators (Meeuse and Raskin, 1988), or by facilitating early flowering in sub-zero conditions (Knutson, 1974).

The pattern of heat production varies between the flowers of different thermogenic species. Heat production often increases and decreases during particular times of the day or night, coinciding with specific phases of floral development, such as the shedding of pollen (Seymour, 1999). As well as thermogenesis changing with the developmental stage of the flower, some species also possess the ability to up-regulate their heat production in response to decreases in ambient temperature, a central requirement for thermoregulation. A pronounced ability to thermoregulate has been found in the arum lily Philodendron selloum, the eastern skunk cabbage Symplocarpus foetidus, the voodoo lily Dracunculus vulgaris, and the sacred lotus Nelumbo nucifera (Seymour et al., 2010a). All of these flowers possess a biochemical feedback mechanism that produces a substantial increase in MR and heat production when the temperature of the flower undergoes a small decrease (Umekawa et al., 2016). Thus, thermoregulatory flowers show an inverse relationship between ambient temperature and MR, enabling them to maintain a relatively stable internal temperature across a range of ambient temperatures. While a strong thermoregulatory response has been found in the sacred lotus and in several aroid species, the temperature regulation abilities of members of the Nymphaeaceae have yet to be established.

The spectacular flowers of the giant Victoria water lilies, V. amazonica and V. cruziana, have long been known to be thermogenic. Both species produce large, night-blooming protogynous flowers that display a two-night flowering sequence (for floral anatomy see Supplementary data Figs. S1 and S2). However, our understanding of the thermogenic and metabolic changes displayed by the flowers of Victoria comes almost entirely from studies on V. amazonica (Prance and Arias, 1975, Seymour and Matthews, 2006) and is as follows: on the first evening, mature flower buds show a steady increase in temperature and MR in advance of sunset. At sundown the air temperature begins to fall and the sepals and petals open, coinciding with a peak in both CO2 production rate (M˙CO2, a proxy of MR) and floral chamber temperature. The floral chamber achieves a mean maximum temperature of 34.7 °C when ambient air temperature falls below 25 °C (Seymour and Matthews, 2006). Following this initial thermogenic increase, the MR of the flower decreases throughout the night and following morning. Towards the second evening the flower undergoes another increase in MR, causing the temperature in the floral chamber to again rise above ambient, generally achieving a lower temperature than on the first evening. Despite the highest floral chamber temperatures occurring on the first evening, the maximum MR could occur on either the first or second night of flowering (Seymour and Matthews, 2006). An attempt was made during this 2006 study to also investigate the thermoregulatory capacity of V. amazonica, by manually applying ice water over a respirometry hood to cool the flower within. Although floral MR was observed to increase in the single flower exposed to artificially lowered midday temperatures (∼23 °C), a lack of access to ice in the field prevented this experiment from being repeated. From this initial work the presence or absence of a thermoregulatory capacity in this species remains an open question.

In contrast to the attention given to V. amazonica, only one study has attempted to measure the thermogenic behaviour of V. cruziana flowers growing in their native habitat (Valla and Cirino, 1972). Unfortunately, this work was not conducted in situ, but on flowers that were collected from wild plants as mature buds and transported to a laboratory where they were measured overnight. This study showed that floral chamber temperature increased to 32–33 °C, or 7.1–7.5 °C above air temperature between 20:00 h and 21:00 h. Two further studies on the thermogenesis and MR of V. cruziana flowers have also been undertaken on plants cultivated in glasshouses maintained under more stable air and water temperatures (mean temperatures of 25 °C and 30 °C, respectively) (Lamprecht et al., 2002a, Lamprecht et al., 2002b). Tracking floral temperatures over two days again revealed a peak in floral temperature on the first evening at 19:30 h, but on the following day there also appeared to be a second temperature peak that could occur in either the morning or afternoon (Lamprecht et al., 2002a, Lamprecht et al., 2002b). This pattern is in contrast to the regular nocturnal temperature increases observed in V. amazonica on both evenings of flowering (Seymour and Matthews, 2006).

Thus, while changes in MR and temperature have been measured over the complete two-night flowering sequence in V. amazonica, it has only been partially characterised in V. cruziana. Furthermore, it remains to be seen whether any Victoria flowers possess the ability to thermoregulate, and whether the differences in heating patterns observed between V. amazonica growing in the wild and V. cruziana growing under glasshouse conditions are also seen in plants growing under naturally fluctuating temperatures. To address this gap in our knowledge, the MR and temperature of V. cruziana flowers growing in an outdoor pond at Stellenbosch University Botanical Garden (33.9° S in South Africa), were measured over their two-night flowering cycle, and their responses to artificially induced changes in air temperature were recorded. This experimental approach provided the opportunity to determine whether Victoria flowers are theromoregulatory: capable of increasing their respiration rate and heat production in response to low ambient temperatures.

Section snippets

Cultivation of V. cruziana

This study was undertaken on five V. cruziana plants growing in an open-air pond at the Stellenbosch University Botanical Garden, Stellenbosch, South Africa. These outdoor ponds were heated by circulating the water through solar heating panels. Water temperature varied depending on ambient temperature but was between 20 and 28 °C. The pond depth ranged between 70 and 90 cm. All measurements were made between Feb.–Apr. 2015.

The plants used were grown from seed originally sourced from the

Floral chamber temperature

Profiles of floral chamber temperature were recorded from flowers blooming in the open air over the course of their two-night flowering sequence, beginning at 15:00 h (n = 6). All flowers showed the same pattern of thermogenesis, with the temperature of the floral chamber already rising by 15:00 h, showing the highest average absolute temperature of 29 °C before sunset at ∼17:45 h, just as the sepals began to move apart, revealing the white petals beneath (Fig. 1). The temperature within the floral

Thermogenesis and metabolic rate

Victoria cruziana flowers displayed a consistent pattern of thermogenesis (Fig. 1), with the highest floral chamber temperature and thermogenic activity occurring on the first evening, coinciding with sunset. The temperature within the flower fell throughout the first night, as did ambient air temperature. Following sunrise, increasing air temperature and insolation began to re-warm the flower. By the second evening, however, floral temperatures remained only a couple of degrees above air

Acknowledgements

This work was supported by an Association of Universities and Colleges of Canada-Africa Research Exchange Grant to PGDM and JST. We thank the kind assistance and patience of the staff at Stellenbosch University Botanical Garden, particularly Bonakele Mpecheni. Thanks also to Susana Clusella-Trullas for loan of equipment, Minette Karsen for logistical assistance, and the two anonymous reviewers for their valuable comments and suggestions.

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