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Thermogenesis and Respiration of Inflorescences of the Dead Horse

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Thermogenesis and Respiration of Inflorescences of the Dead Horse Functional Blackwell Publishing Ltd. Ecology 2003 Thermogenesis and respiration of inflorescences of 17, 886–894 the dead horse arum Helicodiceros muscivorus, a pseudo- thermoregulatory aroid associated with fly pollination R. S. SEYMOUR*, M. GIBERNAU† and K. ITO‡ *Environmental Biology, University of Adelaide, Adelaide, SA 5005, Australia, †Laboratoire d’Evolution et Diversité Biologique, Université Paul Sabatier, 118 route de Narbonne, 31062 Toulouse cedex, France, and ‡Cryobiosystem Research Center, Faculty of Agriculture, Iwate University, Iwate 020-8550, Japan Summary 1. In central Corsica, Helicodiceros muscivorus (Schott ex. K. Koch) produces a protogynous inflorescence that resembles the anal area of a dead mammal and pro- duces a foetid scent during the few hours after sunrise. Flies enter the floral chamber, pollinate the female florets and become trapped until the next morning, when pollen is shed from the male florets and the flies are released. 2. The exposed appendix exhibits a strong, unimodal episode of thermogenesis associated with scent production, reaching a maximum of 30 °C at 15 °C ambient temperature. The male florets in the floral chamber are highly thermogenic throughout the second night and generally maintain stable floret temperatures of about 24 °C at ambient temperatures down to 13 °C. µ −1 −1 3. Maximum respiration rates of the appendix (0·45 mol CO2 s g ) and the male florets (0·82 µmol s−1 g−1) may be the highest recorded for plant tissue. 4. Thermogenesis of the appendix does not depend on ambient temperature, but that of the male florets increases with decreasing ambient temperature in most cases. How- ever, the pattern of heat production by the males appears related more to time than to ambient temperature, hence the term ‘pseudo-thermoregulation’. 5. The behaviour and thoracic temperatures of flies emerging from captivity suggests that male floral warming does not enhance their activity. Key-words:Araceae, flower, heat production, pollination, protogyny Functional Ecology (2003) 17, 886–894 (1883) recorded 371 flies from a single inflorescence Introduction [primarily Lucilia (Somomyia) and Calliphora species] The dead horse lily Helicodiceros muscivorus (Schott and only seven beetles; in another inflorescence he ex. K. Koch) is a member of the arum lily family collected 385 flies, 107 of which were Lucilia caesar. (Araceae). Its distribution is limited to Corsica, Sardinia These insects are enticed to enter a floral chamber and the Balearic Islands in the western Mediterranean where they deliver pollen to receptive female florets, Ocean (Mayo, Bogner & Boyce 1997; Fridlender mainly between sunrise and noon. They are trapped in 2000). In Corsica, 30 known populations are located the chamber and remain there overnight, presumably on limestone and granite rock crevices on islets or while the receptivity of the female florets wanes. Early along the coast, and on inland rocky cliffs up to 700 m the next morning the male florets begin to produce on the main island (Fridlender 2000). The protogy- pollen, which coats the insects before their escape and nous inflorescence resembles the anal area of a dead attraction to another inflorescence. Helicodiceros mus- mammal, complete with a hairy spathe and a ‘tail’ con- civorus has been thought to be carnivorous, because sisting of the hairy appendix of the spadix, and it emits dead insects are commonly found at the bottom of the a putrid scent that attracts necrophilic insects (Knuth floral chamber (Fridlender 2000). The smaller carrion 1909; Bown 2000; Stensmyr et al. 2002). It is appar- flies attracted by the strong putrid odour were thought ently pollinated mainly by flies (Knuth 1909). Arcangeli to be unable to escape from the floral chamber because they were held firmly by sticky hairs and digested by © 2003 British *Author to whom correspondence should be addressed. their secretion (Knuth 1909). However, there is no evid- Ecological Society E-mail: [email protected] ence that the plant gains any nutrients from the flies. 886 887 Many species in the arum lily family are ther- Dead horse arum mogenic (Meeuse & Raskin 1988), but the extent and thermogenesis pattern of thermogenesis in H. muscivorus have not been measured. The pattern in its close relative, the Small thermocouples were inserted into the appendix beetle-pollinated Dracunculus vulgaris, is triphasic, and male florets in lateral holes made by a 15-gauge with a single, intense thermogenesis in the appendix hypodermic needle. This required that a ≈ 5 × 10 mm during the day, bracketed by two episodes of warming window be cut in the wall of the floral chamber. (The of the male florets in the floral chamber at night window also released any trapped flies in a few cases (Seymour & Schultze-Motel 1999). Thermogenesis of where the inflorescence was instrumented after some the appendix of D. vulgaris is an unregulated burst flies had entered.) Respiration rates of the appendix associated with scent production, but the male florets and floral chamber were measured separately with regulate their temperature on the second night by methods similar to those described earlier (Seymour changing respiratory rate inversely with ambient tem- & Schultze-Motel 1999). After thermocouples were perature changes. Thus the inflorescence of D. vulgaris inserted, a close-fitting PVC hood, connected to 5 mm regulates floral temperature physiologically, as do PVC tubing, was placed over the appendix and sealed other monocot arum lilies such as Philodendron sell- loosely with plastic cling-wrap near the entrance to the oum (Nagy et al. 1972; Seymour 1999) and Symplo- floral chamber. Another PVC tube was sealed into the carpus foetidus (Seymour & Blaylock 1999) and the dicot window of the floral chamber with plastic duct tape. Nelumbo nucifera (Seymour & Schultze-Motel 1998). Gas samples from the appendix hood and floral cham- The physics and physiology of the phenomenon are ber were pumped into a portable respirometry setup known, but the molecular basis for temperature con- capable of measuring rates of oxygen consumption trol is not (Seymour 2001). Temperature regulation and carbon dioxide production in up to four chan- seems to be primarily associated with pollination by nels simultaneously. The apparatus, and the methods beetles that may benefit from the warm environment in and assumptions, are described in an earlier paper the floral chamber during their incarceration over- (Seymour & Schultze-Motel 1998), but the components night (Seymour & Schultze-Motel 1997). Beetles are were upgraded. Briefly, sampling pumps (Gilian often endothermic, raising their body temperatures by Instruments Corp., Gilian Sensidyne, Clearwater, FL, endogenous heat production during activity, but carrion- USA, model Gil-air R) pumped gas from the plant, loving flies seldom are (Heinrich 1993). Temperature through mass flow meters (Sierra Instruments Inc., regulation in the floral chamber of H. muscivorus Monterey, CA, USA, model 822) and into a combina- might not be expected, therefore, because flies are the tion oxygen and CO2 analyser (David Bishop Instruments, main pollinators. Alternatively, temperature regula- Bacharach Europe, Warwick, UK, model COMBO tion by the male flowers suggests that it is associated 280). A gas flow selection manifold, incorporating with some other function, such as regulation of the 12 V solenoid valves (Lee Company, Westbrook, CT, rate of floral development, including receptivity of the USA, model LFAA1200210H) sampled gas at 6 min female florets and pollen shedding by the males. This intervals from five channels: four from the appendix is the first study to investigate the relationship between and floral chamber of one or two inflorescences, thermogenesis and pollination biology in an essen- and the fifth from atmospheric air via a humidifier tially fly-pollinated arum lily under natural field chamber. A data logger (Grant Instruments, Cambridge, conditions. UK, model 1200) recorded the outputs from the ana- lyser, flow meters, thermocouples and a barometer at 2 min intervals to assure a stable reading, uninfluenced Materials and methods by changes in channel. A 12 V, 43 A-h automotive battery, which was replaced with a recharged one daily, powered the apparatus. All inflorescences were A local population of H. muscivorus was located at protected from direct sunlight under cardboard shades. Caporalino, 10 km south of Ponte Leccia, central Cor- Ambient temperature was recorded in the shaded air, sica. The plants were located on a steep, rocky slope next to the inflorescence. After the flowering sequence, above the railway tracks, as described by Fridlender the inflorescences were cut and sealed in plastic bags (2000), and were studied during the latter part of the until the floral parts were measured with callipers and flowering season between 22 April and 6 May 2002. a balance. The sequence of flowering was observed daily, usu- The oxygen analyser was calibrated with pure nitrogen ally in the early morning, between about 06:00 and before the study and with humidified atmospheric air 11:00. Notes were taken on the appearance of each automatically at 30 min intervals throughout record- inflorescence. The presence of pollen was determined ing. The CO2 analyser also periodically compared the by cutting a small window in the floral chamber and sample gas with atmospheric air, and its output was © 2003 British Ecological Society, touching the male florets with a cotton-tipped stick scaled against the oxygen data to achieve an overall Functional Ecology, covered with a piece of cellophane tape with its sticky respiratory quotient of 1·0, assuming that carbohydrate 17, 886–894 side out. The tape was then examined for pollen. was the energy source (James & Beevers 1950; ap Rees, 888 Fuller & Wright 1976; ap Rees, Wright & Fuller 1977; pollen evident on the first day of flowering when flies R. S. Seymour Bulpin & ap Rees 1978; Seymour & Schultze-Motel were attracted and trapped. Pollen release occurred et al. 1998; Seymour & Blaylock 1999). The CO2 analyser late in the following night or early in the morning of was about 10 times more sensitive than the oxygen the second day.
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