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2 Station Biologique de la Tour du Valat, le Sambuc, F-13200 Arles, France; and 3 Centre d'Ecologie Fonctionnelle et Evolutive, CNRS, 1919 route de Mende, F-34293 Montpellier cedex 5, France
Received for publication September 10, 1998. Accepted for publication July 8, 1999.
ABSTRACT
The clonal macrophyte Scirpus maritimus (Cyperaceae) propagates locally by rhizomes and reproduces sexually by achenes. The purpose of this paper was to examine whether in size-limited habitats in patchy and discrete marshes in two Mediterranean wetlands in southern France natural populations may suffer from a reduced maternal fecundity due to a deficit in outcross pollen. We first verified that S. maritimus suffers from a reduced fecundity when self-pollinated. At a site in the Camargue, mean fecundity (mean number of achenes per centimetre of spikelet) measured in 1995 and 1996 in seven and nine populations, respectively (surface area from 50 to 4500 m) increased significantly with population surface area in 1995 but not in 1996. In the second wetland at Roquehaute, which is composed of small ponds, fecundity was very low in all 12 local populations studied in 1996 (1.1 achenes per spikelet, SD = 1.2) and was not correlated with the population surface area (from 10 to 400 m). We performed a pollen supplementation experiment in five local populations at Roquehaute to determine whether this low fecundity may be due to a pollen limitation. A significant increase in fecundity after among-pond pollinations compared to within-pond pollinations indicated that local populations suffer from a deficit in outcross pollen, since each pond appears to contain one or a few number of clones (or incompatibility types). In S. maritimus, clonal spread may have a cost in terms of reduced fecundity in small habitats because each habitat is colonized by very few clones.
Key Words: clonal growth • colonization • Cyperaceae • habitat size • Mediterranean wetlands • Scirpus • self-incompatibility
The capacity for clonal growth by vegetative organs such as rhizomes, stolons, or bulbs is widespread in plants (Harper, 1977
; Klime
et al., 1997
). The advantages of clonal growth may be numerous. For example, clonal spread may facilitate resource uptake in patchy environmental conditions (Hutchings and Wijesinghe, 1997
) and potentially permit long-term survival by way of theoretically unlimited iteration (Orive, 1995
). Most clonal plants nevertheless continue to reproduce via sexual means, and clonal species with unobserved events of sexual recruitment are very rare (Ellstrand and Roose, 1987
; Eriksson, 1993
). The most accepted hypothesis for the maintenance of sexual reproduction in clonal species is that sexual reproduction allows for the creation and maintenance of the genetic diversity necessary for adaptation to changes in environmental conditions (see Stearns, 1987
, for a review). Sexual reproduction also has ecological advantages in plants related to their sessile nature. Sexually produced seeds permit an escape in time (dormancy) and in space (long-distance dispersion) from unfavorable environmental conditions and allow plants to colonize new habitats.
Clonal reproduction may nonetheless have several consequences for the function and maintenance of sexual reproduction. First, physiological trade-offs in resource allocation may exist between vegetative and sexual reproduction (e.g., Sutherland and Vickery, 1988
; Lovett-Doust, 1989
). Second, clonal growth may interfere with patterns of pollination and thus with the mating system (Handel, 1985
). Important here is the idea that the vegetative multiplication of flowering shoots can increase the probability of geitonogamy, i.e., pollination between two flowers on the same individual (Handel, 1985
; Back, Kron, and Stewart, 1996
). In self-compatible species, elevated rates of geitonogamy may incur a cost in two ways. First, it increases the risk of inbreeding depression (de Jong, Waser, and Klinkhamer, 1993
), and second, it may cause a wastage of pollen that could otherwise be used for outcrossing (Harder and Barrett, 1995
). In self-incompatible species, geitonogamy has a cost in terms of pollen wastage (i.e., pollen remaining on an individual) and risk of seed set reduction because of stigma saturation, style clogging, and/or abortion of self-pollinated ovules (de Jong et al., 1992
). Clonal reproduction may thus affect sexual reproduction via an influence on the capacity to produce viable seeds. An extreme case of such effects may occur when a single clone vegetatively colonizes a large surface area and forms a "population" composed of a single genotype. In aquatic plant communities, which are largely dominated by clonal plants (Grace, 1993
; Klime et al., 1997
), several studies have demonstrated that a single or few clones can vegetatively colonize large surface areas (Thompson, 1991
; Barrett, Eckert, and Husband, 1993
; Eckert and Barrett, 1993
; Lokker et al., 1994
).
It is often difficult to define population limits for aquatic plants due to the extensive surface area they can occupy (Barrett, Eckert, and Husband, 1993
). However, in Mediterranean wetlands seasonally wet marshes that dry out during summer are not continuously distributed across the landscape and often form mosaics of patchy and discrete suitable habitats for aquatic plants. In these size-limited habitats, the capacity for clonal growth may have important effects on the population size of aquatic plants, as their small surface area may mean that such sites can be occupied by a single clone or a very small number of clones. The consequences for sexual reproduction may be serious in such situations, especially in self-incompatible species because of the risks of a deficiency in compatible pollen (i.e., pollen limitation). Hence, such seasonally wet discrete marshes provide an interesting situation to examine the effects of population size and composition on the fecundity of local populations of clonal plants.
The general purpose of the present study was to quantify whether maternal fecundity (defined as the mean number of achenes produced per spikelet) of the clonal macrophyte Scirpus maritimus in Mediterranean temporary marshes is reduced in small discrete habitats compared to large habitats and whether this variation may be due to small, size-limited habitats being colonized by one or a small number of clones. To do so we carried out three lines of work. First, we verified with a controlled pollination experiment that this species suffers from a reduced fecundity when self-pollinated. This experiment was performed in a natural population in the Tour du Valat reserve. Second, we quantified whether or not there is any relation between population surface area and fecundity in a range of populations at two sites: (a) the natural reserve of the Tour du Valat in the Camargue (Rhône delta) (in this site, marshes colonized by S. maritimus show a large range in surface area, from less than 100 m2 to several hectares) and (b) the wildlife reserve of Roquehaute (southern France). The later is composed of a mosaic of extremely small temporary ponds or "local populations." Third, we tested the hypothesis that maternal fecundity is limited in small habitats because of outcross pollen limitation due to small habitats being occupied by a small number of clones (or incompatibility types). In order to test this hypothesis we carried out a pollen supplementation experiment in which pollen donors were situated at varying distances in the same and different ponds as recipient plants in a range of small ponds in the Roquehaute site.
MATERIALS AND METHODS
Study species
Scirpus maritimus (Cyperaceae) is a common macrophyte in shallow brackish marshes with a widespread distribution in the temperate zone (Lieffers and Shay, 1982b
; Kantrud, 1996
). This emergent rhizomatous species forms dense monospecific stands in which clones cannot be distinguished by variation in morphology. Aboveground shoots, which can reach 1.4 m in height, are annual. In contrast, tubers formed at the base of shoots and rhizomes connecting tubers that can be longer than 20 cm persist for several years (Zákravsk
and Hroudovà, 1994
). In a single growing season, several tens of shoots can be produced by successive rhizome formations from a single sprouted tuber (Lieffers and Shay, 1982a
; Charpentier, Mesléard, and Thompson, 1998
). In spring, flowering shoots produce an apical inflorescence composed of several spikelets containing hermaphroditic flowers. The number of spikelets per inflorescence varies from less than ten to several tens (Krahulec, Frantik, and Hroudovà, 1997
). Flowers of S. maritimus are wind-pollinated and protogynous (Norlindh, 1972
). Achenes become mature during summer. They can float for several weeks on the water surface and are thus primarily dispersed by the water and also by waterfowl (Kantrud, 1996
). Achene germination takes place under conditions of shallow water and low salinity (Clevering, 1995
; Kantrud, 1996
). Furthermore, seedling mortality observed in mature populations (Lieffers and Shay, 1982a
) suggests that seedling recruitment is successful in open areas only because of competition with adults in established stands.
Test of self-incompatibility
In order to determine whether S. maritimus is self-incompatible, a bagging experiment with three treatments, i.e., self-pollination, adjacent-stem pollination, and among-clone pollination, was carried out in a pure stand of S. maritimus (named "Relongue Nord") situated in the Tour du Valat Wildlife Reserve, Rhône delta (43°30' N, 04°30' E). Forty-five inflorescences were bagged in May 1995 before inflorescences had opened. When styles became exserted from the flowers, bags were removed in order to hand-pollinate inflorescences and then immediately replaced and shaken. Pollen was collected by taping anthers onto the rim of a microcentrifuge tube. Pollen was then applied to stigmas by brushing the pollen in the tube onto stigmas with a fine paintbrush. Each bagged inflorescence was randomly assigned to one of the following treatments: (1) self-pollination (N = 25) in which no external pollen was added and bags were simply shaken to permit self-pollination, and (2) adjacent-shoot pollination (N = 10) in which each inflorescence received pollen collected from an inflorescence situated as close as possible in order to maximize the probability that the two shoots belong to the same clone. For eight shoots pollen was collected <50 cm away. Because of local damage by herbivores, two shoots were pollinated with pollen collected >2 m away (see 
Fig. 2). (3) In among-clone pollination (N = 10) each inflorescence received pollen from an inflorescence situated in a different marsh ("La baïsse salée"), which is 3 km from the "Relongue Nord" site. Unfortunately, four bags were destroyed in June. Forty-one bagged inflorescences were collected in July: 23 self-pollinated, nine adjacent-shoot pollinated, and nine among-clone pollinated. The number of achenes per spikelet was counted for each inflorescence. One-way ANOVA was used to compare the mean number of achenes per spikelet produced in bagged inflorescences after self-pollination, adjacent stem pollination, and among-clone pollination.
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The Tour du Valat reserve is composed of a large number of shallow brackish marshes whose surface area ranges from <100 m2 to several hectares. In August 1995 and 1996, the surface area of local populations of S. maritimus was measured and inflorescences were collected in order to estimate maternal fecundity. In 1995, 30 inflorescences per population were randomly collected in seven populations. In 1996, nine populations were sampled (six of them had been sampled in 1995) with ten inflorescences collected per population.
At Roquehaute, population surface area and mean number of achenes per spikelet (measured in ten inflorescences per pond) were determined in 12 ponds in August 1996. This site is composed of 205 ponds distributed over 158 ha, with each pond surrounded by a dense shrub vegetation. Only about a dozen of the ponds contained S. maritimus in the year of study (1996).
Because differences in the length of spikelets between populations had been noticed during field work (mean length ranged from 1 to 2.2 cm and from 1.8 to 2.2 cm at the Tour du Valat and the Roquehaute sites, respectively), the length of spikelets was measured and the fecundity was expressed as the number of achenes per centimetre of spikelet length. The relationship between population surface area and fecundity at each site and each year was determined using linear regression adjusted with the least square method.
Test for pollen limitation
In June 1996, a pollen supplementation experiment was carried out in five ponds at the Roquehaute site. Ponds were chosen within the constraints of having enough available flowering stems for pollination (i.e., at least 20 flowering stems at the time of pollination). Pollen supplementation consisted in collecting pollen from a single donor inflorescence and putting it on the styles of the recipient. Four types of pollen supplementation were performed in each pond with three or four replications (see Table 1). (1) "Within-pond near" donors were situated <3 m in the same pond as the recipient. (2) "Within-pond far" donors were situated 7–20 m away in the same pond, depending on the surface area of the local population (see Table 1). (3) "Among-pond near" donors were sampled from a different pond situated <50 m away. For pond 63 there was no population situated <50 m away and the nearest population was 120 m away. Hence, treatment 3 for this pond had a donor pond farther away in absolute distance, but it was a near pond in relative terms. (4) "Among-pond far" donors were sampled in ponds >100 m away from the recipient's pond.
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RESULTS
Test of self-incompatibility
Hand-pollination had a significant effect on fecundity (df = 2, F = 28.7, P < 0.001). Mean achene production on self-pollinated inflorescences was very low and was significantly lower than obtained after among-clone pollination (Fig. 1). Mean achene production after pollination with adjacent stems did not differ from the self-pollination treatment and was significantly lower than among-clone pollination (Fig. 1). The two inflorescences that were hand-pollinated with pollen collected >2 m apart produced more achenes per spikelet than inflorescences pollinated with pollen collected on very close shoots (Fig. 2).
Fecundity in relation to population size
In 1995, fecundity in local populations at the Tour du Valat reserve increased significantly with increasing population surface area (N = 7, r2 = 0.67, F = 10.2, P < 0.05) (Fig. 3A). In 1996, mean fecundity at the Tour du Valat was in general higher than in 1995 (particularly in small ponds) and there was no significant relationship between population surface area and fecundity (N = 9, r2 = 0.001, F = 0.002, P > 0.05) (Fig. 3A). Two populations had low fecundity despite their large surface area: the population named "Tamarguiron" (2500 m2), which had also a low fecundity in 1995, and the "Relongue Nord" population (4000 m2). The latter population suffered from damage by wild boars in spring. Consequently, shoot distribution was not homogeneous over the 4000 m2 and several gaps were noticed within the cover.
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Test for pollen limitation
Pollen supplementation had a significant effect on fecundity in all five local populations at Roquehaute (Fig. 4). In the five ponds, the near and far among-pond supplementations significantly increased fecundity, except for the near among-pond supplementation in pond 90 where only the far among-pond pollination increased fecundity (Fig. 4). In all ponds, the near within-pond pollen supplementation had no significant effect on fecundity. The far within-pond supplementation had no significant effect for three ponds (numbers 53, 81, 90), but increased fecundity in the two other ponds (numbers 83 and 82) (Fig. 4).
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Our data clearly show that S. maritimus suffers from a reduced fecundity when self-pollinated. Achene production on self-pollinated inflorescences and inflorescences hand-pollinated with pollen collected on an adjacent shoot was zero or close to zero. Accidental pollen introduction when bags were removed for hand-pollination may explain what little achene production did occur in the self-pollinated treatment. The consistently near-zero fecundity after self-pollination compared to outcross pollination suggests the existence of an incompatibility system in S. maritimus. This is a new result for the genus Scirpus and for the Cyperaceae in which little is known about breeding systems, other than the presence of monoecy and dioecy in several Carex species, and the presence of self-compatibility in Carex bigelowii (Jonsson, Jónsdóttir, and Cronberg, 1996
) and C. platyphylla (Handel, 1985
).
In populations of S. maritimus at the Tour du Valat reserve, maternal fecundity was low in populations occupying a small surface area in 1995. Similar low levels of fecundity were also observed at the Roquehaute site in 1995 (A. Charpentier, personal observation) and in 1996 (Fig. 3). Reduced fecundity in these populations may be attributed to resource limitation and/or pollen limitation due to low quantity and/or poor quality of pollen (Byers, 1995
). Mineral nutrients do not vary among populations of different size at the Tour du Valat site (A. Charpentier, unpublished data). Hence, low fecundity is unlikely to be due to variation in resource levels and more probably results from pollen limitation. Nevertheless, large variations in fecundity were observed between 1995 and 1996 at the Tour du Valat. Such annual variation is very commonly observed in perennial plants and may be due to differences in climatic conditions (e.g., rainfall, temperature, wind) that can affect fertilization as well as pollen flow within and between populations. The Tour du Valat reserve is situated in a large wetland area (Rhône delta) in which S. maritimus is a common species. In this open landscape, the possibilities for pollen flow from large to small marshes may be numerous. Consequently, a reduced fecundity in small populations may occur only some years, when ecological and/ or climatic conditions are less favorable.
The very low fecundity of S. maritimus measured in all small ponds at Roquehaute and the increase in fecundity after among-pond pollen addition illustrate two important features of sexual reproduction in this site. First, local populations suffer from pollen limitation. Second, adjacent ponds are colonized by different clones (or incompatibility types). Although ponds are adjacent, the dense shrub vegetation may prevent pollen flow among ponds and consequently local populations may be isolated from one another due to reduced pollen flow.
The lack of achene production in eight out of ten within-pond pollen additions indicates that the number of clones (or incompatibility types) is very low in each local population. This very low within-pond diversity in incompatibility types may result from either a reduced population size (i.e., one or a few number of clones that colonize each pond) and/or a loss of incompatibility alleles due to genetic drift (Byers, 1995
). Our pollen addition experiment thus demonstrates that one of few incompatibility types occur in small habitats where they occasion reduced fecundity due to a deficit in outcross pollen. Although several pieces of work have illustrated the correlation between population size and seed set in animal-pollinated species (Agren, 1996
), there has been little empirical demonstration that this relationship exists in wind-pollinated and/or clonal species (but see Nilsson and Wästljung [1987]
for a wind-pollinated species). Aspinwall and Christian (1992)
examined this relationship in the clonal self-incompatible species Filipendula rubra, which is pollinated by small bees. However, they found no correlation between the number of clones per population and seed production. In this context, our study provides a rarely documented example of a correlation between population size and fecundity in wind-pollinated clonal plant species.
Another interesting result is the lack of achene production when pollination involved donors <3 m from the recipient stem and the failure of three out of five additions with pollen collected >7 m away, but within the same pond. This result suggests that the clones (or incompatibility types) may have a clumped distribution and can spread over distances exceeding 10 m. In nonclonal plants, distance-dependent reproductive success has been argued to be an important component of the effect of plant population structure on reproductive success. Where populations are structured, distance between mates is generally considered as a correlate of genetic similarity. As a consequence, reproductive success can vary with outcrossing distance, reflecting both inbreeding and outbreeding depression, with an intermediate optimal breeding distance (see review by Waser, 1993
). In clonal plant populations, two mates several metres apart can be genetically identical as a result of the vegetative propagation of genotypes. Clone architecture (e.g., clumped vs. random distribution of ramets), by interfering with population structure, will thus modify the relationship between mate distance and reproductive success.
Clonal plants with mass flowering may incur the risk of geitonogamy. Self-incompatibility in S. maritimus may reduce the consequences of such self-pollination, but clearly may have a cost in terms of seed-set reduction where compatible pollen transfer among plants is reduced. In the terrestrial clonal plant Rubus saxatilis, in which populations are composed of discrete patches formed by one or a few clones, between-patch distance can limit fecundity (Eriksson and Bremer, 1993
). In aquatic species such as S. maritimus, powerful vegetative propagation through rhizome production not only allows individuals to colonize local habitats but also, because of the size of clones, may cause fecundity to be limited by a deficit in compatible pollen in small and isolated habitats. Since the possibility of colonizing new sites is restricted to sexual propagule dispersal via temporary (e.g., inundations) or permanent (e.g., canals) hydraulic connections between marshes and/or via transport by waterbirds (Kantrud, 1996
), reduced fecundity in local populations may have consequences for the colonization of new sites. Consequently, very low achene production in small marshes may affect not only the dynamics of local populations (i.e., risk of local extinction) but also dynamics of the metapopulation, i.e., group of local populations linked by migration during periods of extinction and recolonization (Olivieri, Michalakis, and Gouyon, 1995
; Husband and Barrett, 1996
; Piquot et al., 1998
). The Roquehaute site would provide an interesting situation where this potential effect of reduced fecundity on metapopulation dynamics could occur. At Roquehaute, only 15 of the 205 ponds are colonized by S. maritimus. This suggests that colonization of new ponds could indeed be limited by achene availability. Future work on the consequences of clonal growth for sexual reproduction should thus consider the effects of reduced fecundity on the dynamics of colonization among local populations.
FOOTNOTES
1 This work was conduced while AC was in receipt of a Ph.D. grant from the Fondation Sansouire and the Ministère de L'Enseignement Supérieur et de la Recherche (CIFRE 649/94). 
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