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Ecology |
Département de biologie, Université Laval, Sainte-Foy, Québec, Canada G1K 7P4
Received for publication March 17, 2004. Accepted for publication November 18, 2004.
ABSTRACT
In monocarpic plants, reproduction is closely associated with senescence, which is itself often correlated to specific environmental signals. Floerkea proserpinacoides (Limnanthaceae) is a spring ephemeral annual of the deciduous forests of eastern North America. The phenology of its growth and reproduction is considered to be a specific adaptation to the short period during which there is a high availability of resources (mostly light). Indeed, flowering starts 2–3 wk following seedling emergence soon after snowmelt and continues until tree canopy closure. However, fruit maturation is postponed for several weeks and is followed by the plant's death. The objective of this study is to determine if senescence in F. proserpinacoides is primarily cued by fruit maturation or deteriorating light conditions associated with tree canopy closure. Plants for which reproductive investment was manipulated by removing their carpels were grown either in full light or in the shade. Carpel-removal plants reached a higher biomass than control plants (46.0– 57.5% higher), especially in full light. However, longevity was greater in carpel-removal plants, particularly in the shade (25.3–37.8% greater). These results thus suggest that fruit maturation, not deteriorating light conditions associated with canopy closure, is the primary cue of plant senescence in F. proserpinacoides.
Key Words: allocation conflicts • annual plants • fruit maturation • light conditions • longevity • spring ephemeral plant
A reproductive strategy is a suite of co-evolved traits conferring upon the organism an adaptive advantage under specific environmental conditions (Stearns, 1976
). It represents the way by which an organism apportions its resources to reproduction, considering the other functions it has to maintain (basic metabolism, growth, and defense; Snell and Burch, 1975
). Generally speaking, a reproductive strategy is linked to several components, such as: the duration, timing, and frequency of reproductive cycles; the quality and quantity of reproductive structures produced; and the relative distribution of resources between the production of gametes (pollen and ovules) and the maturation of embryos (Lovett Doust, 1989
). However, the manner by which an organism allocates resources to a given function not only limits the quantity, but also the phenology of allocation to the other functions affecting fitness; these constraints result in compromises or trade-offs that the organism must make (Cody, 1966
; Williams, 1966
; Watkinson and White, 1985
; Roff, 1992
; Obeso, 2002
).
The compromise or trade-off between current growth and reproduction, future reproduction, and survival differs according to whether the plant is monocarpic or polycarpic. In polycarpic plants, not all meristems differentiate into reproductive tissues: this type of plant goes through several cycles of reproduction (Noodén, 1988
). Consequently, reduced investment in reproduction at a given time because of greater investment in survival may be compensated for at future reproductive episodes. In monocarpic plants, however, all meristems "die" by differentiation through reproduction, resulting in the genet's death (Watkinson and White, 1985
). Consequently, there is no margin of flexibility for reproductive failure. The reproduction–survival compromise also differs according to whether the plant is an annual with deferred reproduction (these plants are characterized by a vegetative growth period in the first part of their cycle, followed by a reproductive episode preceding senescence [Cohen, 1971
]) or an annual with continuous reproduction (these plants start to reproduce early in their life cycle and continue to do so until senescence [King and Roughgarden, 1982
; Fox, 1992a
, b
]). In these latter species, growth and reproduction potentially compete for the same resources at the same time; consequently, they have little allocation margin.
Floerkea proserpinacoides Willd. is a spring ephemeral annual of the deciduous forests of eastern North America. In this species, flowering starts approximately 2–3 wk after seedling emergence and continues for approximately 6–7 wk, until the plant's complete senescence. Flowers are produced at the leaf axis, one at each node, and the production of new flowers is necessarily associated with the production of new leaves. Fruit maturation coincides with the onset of plant senescence, as the tree canopy closes. In the present study, we attempt to determine the impact of fruit maturation and decreasing light availability on F. proserpinacoides performance and longevity. Because natural senescence coincides with fruit maturation while light conditions are deteriorating as a result of canopy closure, we want to test whether it is fruit maturation or decreasing light availability that represents the major cue of plant senescence.
Study species
Floerkea proserpinacoides belongs to the family Limnanthaceae. It is considered rare in several parts of its range. In Québec, where the species reaches the northern limit of its distribution, F. proserpinacoides is mainly limited to humid and rich forests, on islands of the Saint Laurence River (McKenna and Houle, 2000b
). The phenology of its growth and reproduction is considered as being a specific adaptation to the short period during which there is a high availability of resources, mostly light (Leopold and Jones, 1947
; Cohen, 1971
; King and Roughgarden, 1982
; Fox, 1992a
, b
). The annual production of seeds is particularly significant for the persistence of F. proserpinacoides populations, given the fact that the seeds cannot remain dormant for a long time and that they have a limited capacity of dissemination (Houle et al., 1998
, 2001
).
Seeds of F. proserpinacoides germinate in November and December, after 5 mo of dormancy. The radicle progressively elongates throughout the winter, but seedlings emerge only at the beginning of the following spring. The first leaves come out by the end of March and flowering starts 2–3 wk after emergence and continues through the beginning of June (Houle, 2002
). Floerkea proserpinacoides produces small, autogamous flowers, one per node, except for the first two or three nodes at the base of the plant (Ornduff and Crovello, 1968
; Smith, 1983
). Each of these lower nodes can develop a branch bearing flowers (Smith, 1984
). The petals are small, white, and caducous; however, the sepals are larger, green, and persistent. Each flower has 1–3 carpels and can produce one, two, or more rarely, three nutlets (1.5–2.5 mm in diameter), each containing a seed. At low density (100 individuals/m2) a plant can produce up to 12 nutlets, which is relatively few for an annual plant. However, mean fecundity may be as low as three nutlets per plant in natural populations at the margin of the species' range (Houle et al., 2001
). The green sepals and the floral peduncle progressively enlarge after anthesis. Nutlets increase in size mostly towards the end of the life cycle and are disseminated in mid-June. Senescence thus occurs after approximately 60–70 d of growth (Struik, 1965
) (more precisely, once fruit maturation is completed) and coincides with an increase in environmental temperatures and a decrease in irradiance as a result of canopy closure (Struik, 1965
; Houle et al., 1998
; McKenna and Houle, 2000a
).
MATERIALS AND METHODS
Nutlets used for the following experiment were from a population at Île aux Grues, Québec, Canada (47°02' N, 70°35' W). In early July 2001, three 25 x 50 x 5 cm blocs of soil were collected within the F. proserpinacoides population at île aux Grues. The soil material was mixed, spread uniformly in three trays, and left at ambient temperature (20–25°C) for a 5-mo stratification period without watering (in the dark). Then, the trays were watered and placed for a 2-mo stratification period at low temperature (5°C, in the dark).
After these two stratification periods, the trays were placed in a greenhouse. Seedling emergence started after a few days. Ninety-six similar-size seedlings (two-leaf stage) were selected from the three trays for the experiment. They were transplanted into pots (10 x 10 x 9 cm) containing a commercial potting soil (Hamel, Ste-Foy, Québec, Canada) and watered daily. The experiment started ca. 3 wk after transplantation (maximum and minimum temperatures in the greenhouse were 25.7° and 16.1°C, respectively).
Two factors were studied in this greenhouse experiment: light regime (affecting carbon gain; McKenna and Houle, 2000a
) and plant reproductive status. For the light regime, 12 cages were installed, each covered with a shading screen so as to simulate reduced light availability as the tree canopy develops in the natural habitat (mean photosynthetic photon flux density, PPFD, in those cages was 104.5 µmol · m–2 · s–1); 12 other cages, each covered with a transparent plastic sheet (with small holes for air circulation) served as a full-light treatment (mean PPFD in those cages was 193.2 µmol · m–2 · s–1). The whole set of 24 cages made up 12 blocks, each one with a shade cage and a full-light cage. Four plants were placed in each cage. Within cages, treatments were as follows: carpel removal and control, with two replications each. For the carpel removal, carpels were removed at an interval of 1 wk (for a total of five removal episodes); control plants were left intact. From the third removal episode onward, we reduced light intensity under the shade cages by adding one or two layers of shading screen to simulate thickening of the forest canopy in the natural habitat (mean PPFD in those cages was then 54.4 µmol · m–2 · s–1). Nothing was added on the full-light cages. Also, at the third removal, temperature was increased in the greenhouse (maximum and minimum temperatures were 29.8° and 17.2°C, respectively) and watering frequency was modified: plants were watered every 2 d so as to simulate conditions similar to those of the natural environment as the plants mature. When plants senesced in the full-light cages (ca. 7 wk after transplantation), one control plant and one carpel-removal plant were selected at random in each cage. For each of these plants, we separated the various aerial parts (stems, flowers, leaves, and fruits) from the underground parts. We placed these tissues in a drying oven for 24 hr at 75°C to obtain the dry mass of each part. We left one control plant and one carpel-removal plant under the cages in the greenhouse (watering every 2 d) and noted the date of death of each plant.
Carpel removal allows us to test for the effects of fruit production on plant growth and longevity. The use of shade and full-light cages allows us to determine how deteriorating conditions in the natural habitat (i.e., canopy closure) influence plant growth, reproduction, and longevity. We used two-factor ANOVAs in a randomized complete block design to test for the effects of light regime and carpel removal on several variables: total biomass, number of flowers, number of carpels, number of mature fruits, longevity, and four biomass ratios (reproductive ratio: reproductive biomass/total biomass; stem ratio: stem mass/total biomass; leaf ratio: leaf mass/total biomass; root ratio: root mass/total biomass).
RESULTS
Carpel removal significantly increased total plant biomass (by 57.5% for full-light plants and by 46.0% for shaded plants; P = 0.0014; Fig. 1). Light regime also had a significant effect on total biomass: shaded plants produced 26.0% (control) and 31.3% (carpel-removal) less biomass than full-light plants (P = 0.0100; Fig. 1). These percentages were calculated without taking into account biomass of the removed carpels, which was, however, negligible compared to total plant biomass (individual carpels at removal were <<< 0.0001 g).
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0.0001; data not shown). Not surprisingly, carpel removal caused an important decrease in the reproductive ratio of both full-light and shaded plants (79.0% and 76.7% decrease, respectively). This difference is mainly due to a much lower reproductive biomass in carpel-removal plants, which did not produce mature fruits. Light regime had no significant effect on any of the four biomass ratios analyzed.
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DISCUSSION
Carpel removal increased overall biomass and allowed the plants to invest in growth resources, which otherwise would have been used for fruit maturation (see Avila-Sakar et al., 2001
, for similar results on Cucurbita pepo, an annual vine; see also: Lloyd, 1979
; Hensel et al., 1994
; Delesalle and Mooreside, 1995
). In fact, both stem mass and leaf mass increased significantly in response to carpel removal (as did stem and leaf ratios). Although they start flowering 2–3 wk after emergence, naturally growing individuals of F. proserpinacoides do not mature their fruits until the leaves start senescing and the root system begins to disintegrate (Houle et al., 1998
). This suggests that reserves (carbon and nutrients) mostly accumulated in the leaves and stem (roots represent <5% of the total plant biomass) are translocated to the maturing fruits (see also Bloom et al., 1985
; Rose, 1991
; Bazzaz and Ackerly, 1992
; Larcher, 1995
). Temporal segregation of functions (i.e., growth and fruit maturation) may allow F. proserpinacoides to produce more fruits by optimizing resource uptake early in the life cycle and fruit maturation later on (Hautekèete et al., 2002
). Consequently, plants may be able to adjust their reproductive schedule to variable environmental conditions (Slade and Hutchings, 1987
; Aikio and Markkola, 2002
). Indeed, we showed that each fruit reduced longevity by ca. 0.3 d. Better conditions allowing plants to grow a few more days before the onset of fruit maturation may allow more fruits to be produced. In this sense, keeping a reserve of carpels (Stephenson, 1981
) may allow F. proserpinacoides to take advantage of its environment. Flowering, which does not represent a costly activity in this species (Houle, 2002
), takes place as the plants grow.
For spring ephemeral species (e.g., Erythronium americanum Ker-Gawl.), fruit maturation typically coincides with the deterioration of the environmental conditions as the canopy closes in the natural habitat (Lapointe, 2001
). At this time, light decreases in the understory, air temperature increases, and carbon loss from plants increases through respiration (mostly night respiration). The combination of these conditions may cause F. proserpinacoides to lose its positive carbon balance and, eventually, to die (McKenna and Houle, 2000a
). Fruit maturation and canopy closure thus remain two major processes liable to cue senescence in F. proserpinacoides.
In this study, we showed that carpel removal allowed plants to attain a greater longevity (an increase of 37.8% for full-light plants and of 25.3% for shade plants) and that shade conditions prolonged life in comparison with full-light conditions (6.8% and 17.4% greater for carpel-removal and control plants, respectively). To answer our initial question (is it fruit maturation or decreasing light availability that primarily cues plant senescence?), deteriorating light conditions do not seem immediately responsible for plant senescence; fruit maturation does (with its associated phytohormonal signals, particularly ethylene increase; Sohn and Policansky, 1977
; Noodén, 1988
; Young and Augspurger, 1991
; Larcher, 1995
; Hautekèete et al., 2001
). If deteriorating light conditions had caused senescence, then full-light plants would have had a greater longevity and carpel removal would have had no or little effect; clearly, this was not the case. Our results do not support a strict environmentally cued senescence in F. proserpinacoides (Houle, 2002
) and, potentially, in other spring ephemeral plants. Yet, fruit maturation likely is initiated by some environmental and/or endogenous signal(s) in those species.
FOOTNOTES
1 The authors thank P.-M. Charest and L. Lapointe for their insightful comments on a previous version of the manuscript and the Natural Sciences and Engineering Research Council of Canada for financial support. 
2 gilles.houle{at}bio.ulaval.ca
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