Respiration of turions and winter apices in aquatic carnivorous plants

Basic respiration characteristics were measured in turions of six aquatic plant species differing greatly in their ecological and overwintering characteristics both before and after overwintering, i.e., in dormant and non-dormant state: non-carnivorous Hydrocharis morsus-ranae and Caldesia parnassifolia and carnivorous Aldrovanda vesiculosa, Utricularia australis, U. ochroleuca, and U. bremii, and in non-dormant winter apices of three Australian (sub)tropical populations of Aldrovanda and of two temperate North American Utricularia species, U. purpurea and U. radiata. Respiration rate of autumnal (dormant) turions at 20°C ranged from 0.36 to 1.3 μmol O₂ kg⁻¹ (FM) s⁻¹ and, except for U. bremii, increased by 11–114% after overwintering. However, this increase was statistically significant only in two species. Respiration Q₁₀ in dormant turions ranged within 1.8–2.6 and within 2.3–3.4 in spring (non-dormant) turions. Turions of aquatic plants behave as typical storage, overwintering organs with low respiration rates. No relationship was found between respiration rate of turions and overwintering strategy. In spite of their low respiration rates, turions can usually survive only from one season to another, due to their limited reserves of respiratory substrates for long periods. Contrary to true turions, respiration rates in non-dormant winter apices both in Australian Aldrovanda populations and temperate U. radiata and U. purpurea, in sprouting turions, and growing shoot apices of Aldrovanda were high and ranged from 2.1 to 3.1 μmol kg⁻¹ (FM) s⁻¹, which is comparable to that in aquatic plant leaves or shoots.     

Life cycle and growth ofPotamogeton crispus L. in a shallow pond,ojaga-ike

The life cycle and growth ofPotamogeton crispus L. were studied in a shallow pond, Ojaga-ike. With respect to the shoot elongation and seed and turion formations, the life cycle of this plant in the pond could be divided into following five stages: germination, inactive growth, active growth, reproductive and dormant stages. It was suggested that the plant showed these successive stages depending mainly upon water temperature. The turions germinated on the bottom in autumn when the water temperature fell below ca. 20 C. The plant showed hardly any growth during winter (December—early March) when the temperature was below 10 C. In the spring when the bottom water temperature rose to above 10 C (mid-March), the plant started to grow again and the shoot elongated rapidly at the rate of 4.2 cm day⁻¹ until the shoot apex reached the pond surface in late April. Both the increment of node number and the internodal elongation were associated with this rapid shoot growth. On 10 May (last sampling date), the mean values of shoot length, internodal length and the number of nodes estimated for 10 predominant plants were 238.2±5.6 cm, 7.1±0.8 cm and 34.9±4.0 cm, respectively. The turion formation and flowering occurred during the period from mid-April to mid-May when the surface water temperature ranged 19 and 22 C. The dry weight of a plant reached the maximum mean value of 1180 mg on 10 May. At its peak biomass, an individual plant produced 1–10 turions (5.5 on average) of which the mean individual turion dry weight was 53.2 mg. The turion dry weight accounted for ca. 42% of the total plant biomass m⁻² at that time.     

Environmental and hormonal control of turion formation in Myriophyllum verticillatum

The turions of Myriophyllum verticillatum, an aquatic vascularplant, develop in the fall and function in propagation and dispersalas well as in over-wintering. Experiments with controlled evnironmentsindicate that both temperature and photoperiod regulate turionformation. Turions can be induced at 15°C or lower, butnot at 20°C. At 15°C, turions form in both 8- and 12-hrdays, but not in 16-hr days. Plants collected in early springdo not form turions readily in response to short days unlesspreviously exposed to long days; thus, turion formation is along-day-short-day response. This combination of photoperiodand temperature requirements probably prevents turion developmentin early spring when the temperature and photoperiod are similarto those in the fall. Treatment of plants with ABA (10^–5M) enhances turion development under marginally inductive conditions(12-hr days at 15°C) but cannot induce it under long days.On the other hand, the cytokinin benzyladenine (10^–5 M)blocks turion formation. GA3 (10^–5 M) and AMO-1618 (10^–5M) exert only small qualitative effects on turion development,while IAA (10^–5 M) retards it. During turion development,the level of ABAlike activity and of one or two unidentifiedinhibitors increases. Cytokinin activity decreases at the startof turion formation, increases during development, then decreasesat abscission. Thus two lines of evidence suggest that a decreasein cytokinin activity and an increase in acidic inhibitor activityplay important roles in turion induction. ¹Present address: Biological Station, University of Michigan,Ann Arbor, Michigan 48109, U. S. A. (Received December 1, 1975; )     

Co‐action of temperature and phosphate in inducing turion formation in Spirodela polyrhiza (Great duckweed)*

Increased phosphate concentration, higher temperature and addition of glucose all increased the number of fronds and turions of the duckweed Spirodela polyrhiza formed under in vitro conditions. Increasing the number of turions by increasing the plant biomass does not mean that the developmental process (switch of the programme of the primordia from vegetative fronds toward resting turions) has been specifically influenced. The specific turion yield (STY; number of turions formed by one frond) and the time of onset of turion formation have been used as more specific measures of turion induction. At more than 30 µm initial phosphate the STY was increased by lower temperature (15 °C) and became independent of the phosphate concentration. Between 10 and 30 µm and at higher temperatures (25 °C) the STY was increased by lower phosphate levels. The stimulatory effect of lower temperature was more pronounced than that of lower phosphate concentrations. Decreased phosphate concentration highly accelerated the formation of the first turions. The influence of low temperature was small at lower phosphate concentration but became dominant at higher concentrations (especially in autotrophic cultures). Low phosphate levels (e.g. 10 µm ) and low temperatures (e.g. 15 °C) both represent specific turion‐inducing factors having significant interactive effects. In S. polyrhiza, these signals may replace the interactive effects of photoperiods and low temperature known from other hydrophytes in turion induction under natural conditions.     

Cell wall polysaccharidase activities and growth processes: a possible relationship

The turions of Potamogeton crispus L. develop in early summer and function in propagation and dispersal. Under natural conditions during longday periods, an average minimum air temperature of more than 12°C was found to be important for turion formation. Experiments with controlled environments indicate that both temperature and photoperiod regulate turion formation. Turions can be induced at 13°C or above but not at 8 or 10°C. At a temperature range of 13–24°C turions form in both 12- and 16-h days, but not in 8-h days. By increasing temperature from 24 to 30 or 35°C turions can be induced under 8-h days. Light intensity was found to be important in the formation of turions.     

Interrelations between respiration and dormancy in buds of three hardwood species with different chilling requirements for dormancy release

 Respiration in vegetative buds of mature Betula pendula, Alnus glutinosa and Prunus padus trees was measured monthly at 15°C from mid-October 1996 to natural outdoor budburst in April 1997. In B. pendula the effect of bud water content on respiration was also estimated (December–April) by artificial imbibition of buds for 24 h prior to measurement of respiration. For estimation of corresponding bud dormancy status, batches of twigs were forced at identical monthly intervals at 15°C in long days (24 h), and budburst recorded. In all species dormancy was deepest when the leaves were shed in October, and dormancy was first alleviated in P. padus followed by B. pendula and A. glutinosa. However, bud respiration capacity was not related to dormancy release as it decreased in all species from October to November and displayed no notable increase until February in P. padus, March in B. pendula and April in A. glutinosa, after completion of dormancy release. Rather, increase in respiration coincided with growth resumption prior to budburst. Artificial imbibition of B. pendula buds increased the water content by approximately 10% (FW) and induced a doubling of the respiration rate (December–February). Moreover, the seasonal variation in bud water content (October–April) explained 94% of the variation in respiration in B. pendula and P. padus, and 84% in A. glutinosa. These observations suggest an important role of water content for respiration. During a cold period from mid-December to mid-January with mean temperature of –9.7°C dormancy release was arrested in P. padus, and to some degree in A. glutinosa, whereas dormancy release progressed normally in B. pendula. This indicates species differences in lower critical temperatures for dormancy release. Received: 30 June 1997 / Acceped: 1 October 1997     

The causes of sinking and floating in turions of Myriophyllum verticillatum

The sinking and floating (density) of the special winter buds (turions) produced by many aquatic plants play important roles in their life cycles, yet there has been little experimental study of these phenomena. However, it has been postulated that starch determines the density of turions. In order to test this hypothesis, turions of Myriophyllum verticillatum L. were collected from October through April and analyzed for density, dry-to-fresh-weight ratio and starch content. Density did not correlate closely (R² = 0.37) with the dry-to-fresh-weight ratios. Density strongly correlated (R² = 0.99) with starch only in the January collections, but not at several other times, so starch content alone is not always the major determinant of turion density. Intracellular lacunae (potentially gas spaces) also occur within the axes of these turions, and the lacunal volumes increased ca. 20-fold as they resumed growth, at which time the turions started to float. Significantly, turions, which were near the density of water, could be sunk or floated by changing the ambient pressure (which would alter their internal gas volume). Thus, starch has a role in determining the density of M. verticillatum turions, but the amount of intercellular gas space may be more important, especially when they resume growth in the spring.     

Turion formation and behaviour inSpirodela polyrhiza at two levels of phosphate supply

The clone SJ ofSpirodela polyrhiza (L.) Schleiden forms turions under various nutritive conditions. As compared to 1500 μmol 1⁻¹ phosphate (P+), growth and frond yield of mixotropic cultures decreased, when 60 μol 1⁻¹ phosphate (P-) were available. By contrast, P-conditions increased the number, individual size, dry matter content, and total turion yield (mg turions per ml of the nutrient medium) of P-turions as compared to P+ ones. Germination behaviour of P-turions is characterized by fairly low zero levels in the controls, and by low heterogeneity in individual size as well as in the response patterns concerning the influence of light and/or phytoactive substances. P-turions from youngSpirodela cultures are extremely dormant. However, they undergo an after-ripening process if kept inside ageing cultures.     

TURION FORMATION AND GERMINATION IN SPIRODELA POLYRHIZA

Three clones of Spirodela polyrhiza L. (Schleid.) formed dormant bodies called turions. A clone from Puerto Rico did not form turions under all conditions tried. In those clones producing turions, formation was stimulated by the addition of sucrose (10–50 mM) to the nutrient solution. Increased levels of Ca(NO₃)₂ plus sucrose stimulated turion production. In the absence of NO₃^–, Ca⁺⁺ was more effective than K⁺ in stimulating turion formation. Turion buoyancy was not light dependent, nor was it promoted by sucrose. Normal turions required light for germination, whereas sucrose-induced turions germinated in the dark. Dark germination was not promoted by either Ca⁺⁺ or K⁺. Sucrose stimulation of turion formation and subsequent promotion of dark germination was attributed to metabolic rather than osmotic effects. One hundred mM sucrose concentrations inhibited turion buoyancy and germination. Turions formed one primary abscission layer which separated them from the stolon and the mother frond. Subepidermal idioblasts appeared to seal the stolon stump after separation.     

Turion formation in Spirodela polyrhiza: The environmental signals that induce the developmental process in nature

The formation of turions of Spirodela polyrhiza is induced by a large number of environmental signals, already investigated under laboratory conditions. To get more close‐to‐nature experimental conditions, chemical composition and temperature of the water were measured during the growing season in 2002 and 2003 in a pond near Jena (50°52′N, 11°42′E). Whereas the concentrations of nitrate and sulphate (both in the millimolar range) remained fairly constant that of phosphate decreased from approximately 13 µM at the beginning of the season to 2 µM at the time of onset of turion formation (17 August in 2002, 21 July 2003). This concentration was used in experiments under controlled conditions together with the other outdoor data (day temperature, lower night temperature and photoperiod) in subsequent experiments to investigate their role in the induction of turion formation. The concentration of the nutrient media were kept constant. The following conclusions were drawn. (1) Low phosphate concentration appears to be the decisive factor in inducing turion formation. Growing fronds take up phosphate, and turion formation is then induced towards the end of the season. (2) Lower temperatures during the day (18 vs 25°C) and especially during the night (18 vs 15°C) evidently enhance the effect of the turion‐inducing factor phosphate by increasing the yield. (3) At much higher anthropogenic phosphate concentrations low temperature takes over the function of inducing turion formation. (4) Whereas much lower concentrations act directly to induce the formation of turions regardless of the season.     

Adaptation and acclimation of growth and photosynthesis of five Antarctic red algae to low temperatures

Temperature requirements for growth, photosynthesis and dark respiration were determined for five Antarctic red algal species. After acclimation, the stenothermal species Gigartina skottsbergii and Ballia callitricha grew at 0 or up to 5 °C, respectively; the eurythermal species Kallymenia antarctica, Gymnogongrus antarcticus and Phyllophora ahnfeltioides grew up to 10 °C. The temperature optima of photosynthesis were between 10 and 15 °C in the stenothermal species and between 15 and 25 °C in the eurythermal species, irrespective of the growth temperature. This shows that the temperature optima for photosynthesis are located well below the optima from species of other biogeographical regions, even from the Arctic. Respiratory rates rose with increasing temperatures. In contrast to photosynthesis, no temperature optimum was evident between 0 and 25 °C. Partial acclimation of photosynthetic capacity to growth temperature was found in two species. B. callitricha and Gymnogongrus antarcticus acclimate to 0 °C, and 5 and 0 °C, respectively. But acclimation did in no case lead to an overall shift in the temperature optimum of photosynthesis. B. callitricha and Gymnogongrus antarcticus showed acclimation of respiration to 5 °C, and P. ahnfeltioides to 5 and 10 °C, resulting in a temperature independence of respiration when measured at growth temperature. With respect to the acclimation potential of the species, no distinction can be made between the stenothermal versus the eurythermal group. (Net)photosynthetic capacity:respiration (P:R) ratios showed in all species highest values at 0 °C and decreased continuously to values lower than 1.0 at 25 °C. In turn, the low P:R ratios at higher temperatures are assumed to determine the upper temperature growth limit of the studied species. Estimated daily carbon balance reached values between 4.1 and 30.7 mg C g⁻¹ FW day⁻¹ at 0 °C, 16:8 h light/dark cycle, 12–40 μmol m⁻² s⁻¹. Received: 4 November 1999 / Accepted: 7 March 2000     

Dormancy and germination in axillary turions ofHydrilla verticillata

Effects of environmental conditions and growth regulators on release from dormoncy of axillary turions inHydrilla verticillata were investigated. Coll treatment at 2 C for 33 days produced the most complete release from dormancy. One week of 2 C treatment was sufficient for the germination; however, longer cold periods produced more rapid growth in shoot or root lengths as well as a shorter lag time for germination. Dormancy in turions could be broken by a photoperiod of 16 hr but not by on of 8 or 12 hr, nor by continuous lighting. When a cold treatment was applied turions grew out in response to all of the photoperiodic conditions. Red and far-red irradiation during the incubation after a cold treatment promoted gremination; blue and green light markedly inhibited the germination. At 10⁻⁴ and 10⁻⁵ M, gibberellic acid broke dormancy of non-cold treated turions, but was toxic at 10⁻⁴ M to the development after germination. Gibberellic acid promoted growth of cold treated turions even at 10⁻⁶ M. Indoleacetic acid at 10⁻⁴, 10⁻⁵ and 10⁻⁶ M induced outgrowth of both non-cold treated and cold treated turions. Apparently normal growth and development was observed in a high concentration of indoleacetic acid.     

Effects of constant and fluctuating temperature on time to budburst in Betula pubescens and its relation to bud respiration

 Effects of fluctuating and constant temperatures on budburst time, and respiration in winter buds were studied in Betula pubescens Ehrh. Dormant seedlings were chilled at 0°C for 4 months and then allowed to sprout in long days (LD, 24 h) at constant temperatures of 6, 9, 12, 15, 18 and 21°C, and at diurnally fluctuating temperatures (12/12 h, LD 24 h) with means of 9, 12, 15 and 18°C. No difference in thermal time requirements for budburst was found between plants receiving constant and fluctuating temperatures. The base temperature for thermal time accumulation was estimated to 1°C. Respiration in post-dormant (dormancy fully released) excised winter buds from an adult tree increased exponentially with temperature and was 20 times as high at 30°C than at 0°C. However, respiration in buds without scales was 30% higher at 0°C, and it was 2.7 times higher at 24°C than in intact buds. Thus, the tight bud scales probably constrain respiration and growth and are likely to delay budburst in spring. Arrhenius plots of the respiration data were biphasic with breaks at 13–15°C. However, this phase transition is unlikely to be associated with chilling sensitivity since the present species is hardy and adapted to a boreal climate. Received: 10 January 1997 / Accepted: 23 June 1997     

Aberrant clones: Birth order generates life history diversity in Greater Duckweed,Spirodela polyrhiza

Environmental unpredictability is known to result in the evolution of bet‐hedging traits. Variable dormancy enhances survival through harsh conditions, and is widely cited as a diversification bet‐hedging trait. The floating aquatic plant, Spirodela polyrhiza (Greater Duckweed), provides an opportunity to study diversification because although partially reliable seasonal cues exist, its growing season is subject to an unpredictable and literally “hard” termination when the surface water freezes, and overwinter survival depends on a switch from production of normal daughter fronds to production of dense, sinking “turions” prior to freeze‐over. The problem for S. polyrhiza is that diversified dormancy behavior must be generated among clonally produced, genetically identical offspring. Variation in phenology has been observed in the field, but its sources are unknown. Here, we investigate sources of phenological variation in turion production, and test the hypothesis that diversification in turion phenology is generated within genetic lineages through effects of parental birth order. As expected, phenotypic plasticity to temperature is expressed along a thermal gradient; more interestingly, parental birth order was found to have a significant and strong effect on turion phenology: Turions are produced earlier by late birth‐order parents. These results hold regardless of whether turion phenology is measured as first turion birth order, time to first turion, or turion frequency. This study addresses a question of current interest on potential mechanisms generating diversification, and suggests that consistent phenotypic differences across birth orders generate life history variation.     

Photophysiology of turion germination inSpirodela polyrhiza (L.)Schleiden. The cause of germination inhibition by overcrowding

Red-light-induced (via phytochrome) germination decreased with increasing numbers of turions per germination flask (overcrowding). Three hypotheses concerning the mechanism of this germination inhibition were tested, related to abscisic acid, ethylene, and oxygen deficiency: (i) Although abscisic acid is a powerful inhibitor of turion germination it had to be excluded as a cause, because abscisic acid was not secreted from turions into the nutrient solution, (ii) Ethylene (ethrel) strongly inhibited growth of newly formed sprouts, but germination response itself was not inhibited, (iii) Germination inhibition did not appear if short light pulses were substituted by continuous irradiation. It reappeared in the presence of the photosynthesis inhibitor 3-(3, 4-dichlorophenyl)-l, 1-dimethylurea, but it was not observed in aerated nutrient solutions, or when Petri dishes instead of Erlenmeyer flasks were used. Decreased oxygen concentrations in the nutrient solution were produced by turion respiration. Consequently, anaerobiosis within the nutrient solution caused by turion respiration was the reason for germination inhibition by overcrowding.     

Cytochemical and ultrastructural aspects of aquatic carnivorous plant turions

Turions, which are modified shoot apices, are vegetative, dormant overwintering organs produced by perennial aquatic plants. In this study, the turion cytochemistry and ultrastructure of Aldrovanda vesiculosa, Utricularia vulgaris and U. stygia were compared with particular emphasis placed on storage substances. These three aquatic, rootless carnivorous plant species were studied at the end of their winter dormancy. At this stage, the turions of all species had starch as their main storage material. In contrast with A. vesiculosa, Utricularia turions were rich in protein storage vacuoles, and proteins were also accumulated as crystalline inclusions in the nuclei. All examined species accumulated lipid droplets in cells of epidermal glands.     

Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligo-mesotrophic lake (Lake Stechlin, Germany)

In winter of 2009/2010, Aphanizomenon flos-aquae bloomed in the ice and snow covered oligo-mesotrophic Lake Stechlin, Germany. The photosynthesis of the natural population was measured at eight temperatures in the range of 2–35°C, at nine different irradiance levels in the range of 0–1,320 μmol m⁻² s⁻¹ PAR at each applied temperature. The photoadaptation parameter (I _k) and the maximum photosynthetic rate (P _max) correlated positively with the temperature between 2 and 30°C, and there was a remarkable drop in both parameters at 35°C. The low I _k at low temperatures enabled the active photosynthesis of overwintering populations at low irradiance levels under ice and snow cover. The optimum of the photosynthesis was above 20°C at irradiances above 150 μmol m⁻² s⁻¹. At lower irradiance levels (7.5–30 μmol m⁻² s⁻¹), the photosynthesis was the most intensive in the temperature range of 2–5°C. The interaction between light and temperature allowed the proliferation of A. flos-aquae in Lake Stechlin resulting in winter water bloom in this oligo-mesotrophic lake. The applied 2°C is the lowest experimental temperature ever in the photosynthesis/growth studies of A. flos-aquae, and the results of the P–I and P–T measurements provide novel information about the tolerance and physiological plasticity of this species.     

Effects of sediment anoxia and light on turion germination and early growth of Potamogeton crispus

Potamogeton crispus is a cosmopolitan aquatic species and is widely used as a pioneer species for vegetation restoration of eutrophic lakes. However, many restoration projects applying P. crispus turions have not been successful. Earlier studies focused on effects of light and temperature on turion germination. The purpose of this study was to determine whether sediment anoxia and light interactively affected the turion germination and early growth of P. crispus. Anoxic conditions in the experiment were produced by adding sucrose to the sediment. The germination rate of the turions was 68–73% lower in the highly anoxic condition treatment than in the control. Medium light intensity (10% of natural light at the water surface) was more favorable for germination under slightly anoxic conditions than either low or high light intensity. The growth of newly-formed sprouts was also significantly inhibited by sediment anoxia. Photosynthesis and shoot biomass were reduced under sediment anoxia, whereas total chlorophyll content, root biomass, and soluble protein content were highest in the low anoxic condition treatment. Medium light improved net photosynthesis and biomass production of the sprouts. We conclude that turion germination and sprout growth can be significantly inhibited by sediment anoxia. Medium light intensity may alleviate this inhibition by anoxia, but light has little effect when sediment anoxia is severe. For the purposes of vegetation restoration, more attention should be paid to the role of sediment anoxia, and it is necessary to improve sediment and light conditions for turion germination and early growth of P. crispus in eutrophic lakes. These results will contribute to a more complete understanding of turion germination dynamics of P. crispus and will be useful for future restoration programs. Handling editor: S. M. Thomaz     

Stem respiration of Norway spruce trees under elevated CO2 concentration

Measurements of stem respiration were conducted for a period of four years (1999–2002) in 14-year old Norway spruce (Picea abies [L.] Karst) trees exposed to ambient (CA) and elevated CO₂ concentration (CE; ambient plus 350 μmol mol⁻¹). Stem respiration measurements of six trees per treatment were carried out 2–3 times per month during the growing season. Stem respiration in CE treatment was higher (up to 16 %) than in CA treatment. Temperature response of stem respiration (Q₁₀) for the whole experimental period ranged between 1.65–2.57 in CA treatment and 2.24–2.56 in CE treatment. The mean stem respiration rate normalized to 10 °C (R₁₀) in CA and CE treatments ranged between 1.67–1.95 and 2.19–2.72 μmol(CO₂) m⁻² s⁻¹, respectively. Seasonal variations in stem respiration were related to temperature and tree growth.     

Temperature dependence and ontogenetic changes of metabolic rate of an endemic earthworm <Emphasis Type="Italic">Dendrobaena mrazeki</Emphasis>

Ontogenetic changes and temperature dependency of respiration rate were studied in Dendrobaena mrazeki, an earthworm species inhabiting relatively warm and dry habitats in Central Europe. D. mrazeki showed respiration rate lower than in other earthworm species, < 70 μl O₂ g⁻¹ h⁻¹, within the temperature range of 5–35°C. The difference of respiration rate between juveniles and adults was insignificant at 20°C. The response of oxygen consumption to sudden temperature changes was compared with the temperature dependence of respiratory activity in animals pre-acclimated to temperature of measurement. No significant impact of acclimation on the temperature response of oxygen consumption was found. The body mass-adjusted respiration rate increased slowly with increasing temperature from 5 to 25°C (Q₁₀ from 1.2 to 1.7) independently on acclimation history of earthworms. Oxygen consumption decreased above 25°C up to upper lethal limit (about 35°C). Temperature dependence of metabolic rate is smaller than in other earthworm species. The relationships between low metabolic sensitivity to temperature, slow locomotion and reactivity to touching as observed in this species are discussed.