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Ecology |
2Instituto de Ecología, Universidad Nacional Autónoma de México, Departamento de Ecología de la Biodiversidad, Laboratorio de Dinámica de Poblaciones y Evolución de Historias de Vida, Apartado Postal 70-275 Ciudad Universitaria, UNAM, C.P. 04510 México, D.F., México; 3Departamento El Hombre y Su Ambiente-CBS-Universidad Autónoma Metropolitana-Xochimilco. Calzada del Hueso 1100, Col. Villa Quietud, 04960, México, D.F., México
Received for publication March 11, 2005. Accepted for publication January 19, 2006.
ABSTRACT
New individuals in clonal populations arise through the recruitment of sexual or clonal offspring. The predominance of one type of regeneration over the other has been correlated with different selective environmental pressures. We compared the reproductive mode (sexual through seeds and vegetative through plantlets or detached cladodes) of Opuntia microdasys from three desert habitats of the Chihuahuan Desert: bajada (BH), hill-piedmont (HPH), and an interdune (IDH). Successful establishment and growth of plantlets were determined in two experiments: (1) the effect of light (three levels of photosynthetically active radiation [PAR]: full, low, and medium) and two levels of watering and (2) maternal effects and provenance of plantlets. Adult plant densities did not differ among habitats (639 individuals/ha), but the number of offspring and fruit production increased significantly at BH. Plantlets (94.3%) dominated the form of recruitment for all habitats, followed by cladodes (3.1%) and seedlings (2.6%). A higher proportion of plantlets established in the low and medium PAR treatments (76%) in comparison to full exposure (39%). Maternal factors affected survival and growth, but plantlet provenance did not. The high fruit abortion rate resulting from environmental and maternal effects provided suitable conditions for establishment of plantlets.
Key Words: clonal propagation • fruit abortion • Opuntia • prickly pear • pseudovivipary • plantlet • sexual recruitment
The maintenance of populations depends on some form of recruitment that replenishes the loss of individuals through time. The modular construction of plants has in some cases (i.e., clonal plants) provided a means of propagating individual modules (ramets) that can potentially become detached and live independently (Herben et al., 1994
). Clonal plants can replenish individuals through sexual reproduction and/or vegetative propagation (Cook, 1985
; Eriksson, 1989
; Arizaga and Ezcurra, 2002
). However, recruitment via sexual reproduction is infrequent in harsh conditions such as those found in arid environments (Eriksson, 1989
; Mandujano et al., 2001
). For example, the establishment of cacti seedlings is rare because of the extremes in temperature, humidity, and herbivory, but it is mediated by nurse plants that diminish these environmental pressures (Shreve, 1911
; Valiente-Banuet and Ezcurra, 1991
; Callaghan et al., 1992
; Mandujano et al., 1998
; Jiménez-Sierra and Jiménez-González, 2002
).
In clonal plant species, the production of vegetative propagules, which ends with the formation of ramets with the same genetic information of the parent plant, is an important ecological strategy for the rapid colonization of suitable habitats (Anthony, 1954
; Cook, 1985
; Auge and Brandl, 1997
; Reusch et al., 1998
). In some cases, vegetative propagation can be the most frequent form of recruitment (Frego and Staniforth, 1985
; Eriksson, 1989
; Mandujano et al., 1997
; Mandujano et al., 1998
; Hicks and Mauchamp, 1999
; Arizaga and Ezcurra, 2002
). New clonal offspring can be produced by three pathways. (1) Asexual formation of unfertilized seeds (agamospermy) is common in some Opuntia (Pimienta-Barrios and Del Castillo, 2002
) and has mostly a genetic consequence (Cook, 1985
), but these seeds can be ecologically equivalent to sexual seeds (Cook, 1985
). (2) The development of new plants from vegetative structures such as stems, bulbs, rhizomes, and stolons, that have higher establishment probabilities and can eventually give rise to independent but genetically identical individuals (Callaghan et al., 1992
; Arizaga and Ezcurra, 1995
; Mandujano et al., 1998
; Bobich, 2005
). (3) In a number of families (Crassulaceae, Oxalidaceae, Polygonaceae, Saxifragaceae, Agavaceae, Bromeliaceae, Cactaceae, Poaceae, Juncaceae, Liliaceae, and Gesneriaceae), reproductive structures (e.g., a pericarpel or the apex of an inflorescence) can give origin to new clonal individual plants (i.e., pseudovivipary) by means of clonal propagules such as bulbils or plantlets in place of sexual reproductive structures (Youngner, 1960
; Elmqvist and Cox, 1996
; Diggle et al., 2002
; Wang and Cronk, 2003
; Cota-Sánchez, 2004
; Wang et al., 2004
). This last type of vegetative propagation that incorporates sexual structures that fail to produce sexual seeds to produce plantlets has been described as insurance against sexual reproductive failure (Arizaga and Ezcurra, 1995
).
In particular, pseudovivipary has been reported for very few species in the Cactaceae such as Opuntia rufida,O. phaeacantha,O. monacantha,O. salmiana,Cylindropuntia imbricata,C. fulgida,C. kleiniae,C. leptocaulis, C. tunicata,C. prolifera (Buxbaum, 1950
; Anthony, 1954
), O. echios (Hicks and Mauchamp, 1999
), and in some members of the Agavaceae (Agave marmorata,A. fourchroydes, and A. macroacantha;Arizaga and Ezcurra, 1995
, 2002
; Gentry, 1998
). Clonal reproduction has ecological advantages: (1) fast population growth rates increase the potential survival and future reproduction (Mandujano et al., 2001
); (2) established plants have an opportunity to inhabit current favorable sites; (3) space can be foraged, and plants can have further access to resources (Harper, 1981
); and (4) ramets, in general, have a higher probability of survival than seedlings in harsh environments (Mandujano et al., 1998; Hicks and Mauchamp, 1999
; Arizaga and Ezcurra, 2002
). In the short term, environments that maintain clonal propagation provide greater benefits, but the presence of ramets with the same genetic information that remain relatively close to the parent plant may drastically affect the mating system through an increase in inbreeding (Handel, 1985
; Trame et al., 1995
; Charpentier, 2002
), which can eventually lead to the evolution of different reproductive strategies (Lovett-Doust, 1989
).
In the southern Chihuahuan Desert, Opuntia microdasys vegetatively propagates by the establishment of one or several detached cladodes or by the fall of unripe fruits that produce plantlets. Propagation through cladodes appears to be less frequent than propagation through plantlets, the most frequent form of recruitment (M. Mandujano, unpublished data). Unlike the rest of the angiosperms, the fruits in the Cactaceae are composed of stem tissue (pericarpel) with embedded sexual structures, surrounded by viable areoles, which are true lateral meristems of caulinar origin (Buxbaum, 1950
; Bravo-Hollis, 1978
; Mauseth, 1984
).
The purpose of this study was to determine the relative importance of vegetative propagation through plantlets or detached cladodes of the bunny-ears prickly pear, Opuntia microdasys, in three different populations (habitats) in the Mapimi Biosphere Reserve (MBR) in the southern part of the Chihuahuan Desert in Mexico and to determine the relation of vegetative propagation to some of the factors (light, water, and provenance) that have been reported as being important for the recruitment of individuals in other species of Cactaceae (Shreve, 1911
; Gibson and Nobel, 1986
; Valiente-Banuet and Ezcurra, 1991
; Altesor et al., 1992
; Mandujano et al., 1998
, 2002
; Jiménez-Sierra and Jiménez-González, 2002).
MATERIALS AND METHODS
Study plant
Opuntia microdasys (Lehmann) Pfeiffer is a short plant approximately 60–80 cm tall, erect to sprawling shrubs and circular to elliptic-obovate, bright green pads without spines, with many reddish brown or usually yellow or whitish glochids. The flowers have bright yellow inner perianth segments and are ca. 2.5–3 cm long. The outer perianth segments are sometimes reddishly tinged. The fruits are red, fleshy, and globose to obovate ca. 2–2.5 cm long. They are usually found in sandy to loamy calcareous soils of desert hills and uplands at 1700–2100 m a.s.l. The species is distributed in the states of Coahuila, Zacatecas, Nuevo León, Tamaulipas, San Luis Potosí, and Hidalgo and apparently hybridizes with O. rufida near Saltillo, Coahuila, and Concepción del Oro, Zacatecas, Mexico (Bravo-Hollis, 1978
). The flowering period is from April to mid-May (Cornet, 1985
), and fruits ripen from June to August.
Study site
The study was conducted in the Mapimi Biosphere Reserve (MBR) located in the southern Chihuahuan Desert (26°29'–26°52' N, 103°32'–103°58' W, 1100 m a.s.l., 264 mm mean annual rainfall [80.2% between June and October], 20.8°C mean temperature; Cornet, 1988
). The observations were made in populations of O. microdasys in three sites that differ in their biotic and abiotic characteristics: bajada, hill-piedmont, and interdune habitats (Fig. 1).
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) as the most common species. Individuals of O. microdasys, Jatropha dioica, and Agave asperrima can also be found as the dominant succulent life forms (Montaña, 1988
). Hill-piedmont is a habitat (HPH) of igneous rock, with an average slope of >10% and a shallow stony soil having scarce vegetation (Fig. 1A1; Montaña, 1988
). The dominant species in this habitat are F. splendens, L. tridentata, and Yucca rigida, with other secondary succulents such as Opuntia microdasys, O. rastrera, A. asperrima, and A. lechugilla, as well as hemicryptophyts (e.g., Selaginella lepidophylla; Montaña, 1988
). Extensive sandy plains, found between sandy dunes, constitute the interdune flats habitat (IDH) where the average slope is <1% (Fig. 1B). The dunes form a dense network of hills, that are connected by flat interdune plains. Flood plains are absent, because the sandy substrate facilitates fast infiltration and lateral water movement is mainly underground. The typical vegetation of dunes is dominated by Dalea scoparia and Yucca elata in the high sections of dunes and by different combinations of Acacia greggii, A. constricta, L. tridentata, and Lycium berlandieri in the lower parts of the dunes. Areas between the dunes constitute plains that present a moderately deep ground, with a secondary accumulated layer of lime (Montaña, 1988
). These plains are largely covered by vegetation of shrubbery communities dominated by Prosopis glandulosa and Flourensia cernua, sometimes having a dense layer of grass dominated by Hilaria mutica. In some cases, O. rastrera and O. microdasys can be found as the dominant species in the interdune habitats, along with Zinnia acerosa (Montaña, 1988
).
Description and frequency of clonal propagation
Several transects (15 in BH, 14 in HPH, and 16 in IDH) were made during May in each site to obtain a sample of at least 100 adult plants. From each plant, we measured height at the tip of the highest cladode, diameter in two orthogonal directions, and total number of cladodes (including lignified cladodes). We also counted the number of plantlets, floral buds, and aborted fruits found underneath each adult individual as well as fruits that were still connected to the adult to obtain a rate of abortion by plant and by habitat. In addition, the number of juveniles associated to the parent plant (directly under the canopy of the adult), which were produced by plantlets (i.e., rooted aborted fruits) or detached cladodes were registered. Of all the detached plantlets found on the ground we evaluated whether they were the product of immature floral buds that did not complete anthesis or aborted fruits (i.e., flowers that completed anthesis and were aborted post-pollination). We also assessed the development of a root system, which allowed us to establish the rate of recruitment of plantlets. The size of each plantlet was measured longitudinally (tip to point of abscission from cladode, in centimeters), and we counted the number of cladodes and measured the distance from each plantlet to the base of the parent plant (in centimeters). Finally, the frequency of fallen fruits with or without the development of seeds was estimated from a sample of 90 randomly collected fruits at each site and dissected to confirm the absence of seeds. Statistical analyses include chi-square test, residual analyses, and ANOVAs (SAS Institute, 1995
). Photosynthetically active radiation (PAR, in micromoles per second per square meter) was measured from eight cardinal points around four focal plants in open space (100 cm from parent plant) and under the shade of focal plants (50 cm, 16 measurements per plant). Light measurements were made in May 1999 at a randomly selected site (HPH) and were taken every three hours (from 0800 to 2000) using a steady state porometer quantum sensor (Model LI 1600; LI-COR, Lincoln, Nebraska, USA).
Effect of radiation in the vegetative propagation by aborted fruits
We estimated the establishment of O. microdasys plantlets in a greenhouse at MBR using a completely randomized 2 x 3 split-plot design. The greenhouse is protected along all four edges and top with metallic mesh to prevent the entrance of vertebrates, but is exposed to the same weather conditions as study sites in MBR. Two factors were tested: (1) light (the main treatment assigned to whole plots) with three levels: full sunlight (high solar radiation); medium solar radiation (representing 43% PAR extinction, measured with a LI-COR sensor Q15494, achieved by a covering of a single layer of nylon mesh) and low solar radiation (70% PAR extinction with two layers of mesh), and (2) two soil moisture regimes (with or without watering). The experimental unit for each treatment was a pot with four fruits, with 20 pots for each light level and humidity combination of treatments. Soil moisture was kept at field capacity (every 4 days, each pot was watered with either 0.4 L for low solar radiation treatments, 0.5 L for medium, and 1 L for high). Therefore, two pots in each replicate were exposed to the same light conditions, but received different amounts of water. Plantlets were grown from May until November 2000, when surviving individuals were then counted, harvested, oven dried at 60°C, and weighed.
Data were analyzed using nested ANOVAs for split plot designs and Tukey honestly significant difference (HSD) tests (Zar, 1996
). The response variables were the proportions of survivors (arcsine transformed; Zar, 1996
) and dry mass (in grams) of plantlets. All statistical analyses were made with the JMP statistical program (SAS, 1995).
Site and parental effects
We experimentally assessed the possible effects of the parent plants over their progeny and verified the possible relationship between the habitat and the size of the parent plant on the quality of plantlets in a greenhouse at the Instituto de Ecología, Universidad Nacional Autónoma de México (UNAM), Mexico, in a completely randomized 3 x 10 factorial design with three replicates. In each of the three habitats, 10 focal plants were chosen, and 12 fruits were taken from each plant (N = 360 fruits). The development of fruits in each habitat was compared within the same watering conditions to evaluate the parental effect on survival. Fruits from each habitat (N = 120) were measured (length and width, in centimeters) and weighed, and four fruits were placed in each of 8 x 8 x 8 cm jiffy pots. Pots were watered every 4 d to keep field capacity, and survival was followed for 6 mo. At the end of the experiment, all remaining plantlets were oven dried and weighed to constant mass. Data analysis were carried out using ANOVAs, having survival percentage and dry mass as response variables for each treatment and the initial mass (in grams) as a covariable (Zar, 1996
).
The magnitude of selection on fruit size was determined by means of regression analysis on the relationship between maternal clonal success (number of aborted fruits x probability of establishment) and the size of the propagule (aborted fruit). Absolute fitnesses were transformed to relative fitnesses by dividing each absolute value by the mean absolute fitness (mean = 1; Lande and Arnold, 1983
; Arnold and Wade, 1984a
, b
).
RESULTS
Description and importance of the modes of clonal propagation
The density of adult plants did not differ between habitats (BH = 666, HPH = 785, and IDH = 637 individuals/ha; mean = 693.3 individuals/ha; P = 0.73), but when vegetative (plantlets and cladodes) and sexual recruitment are included, the density of individuals increased 3.9 times in BH (2620 individuals/ha), 1.3 times in HPH (1042 individuals/ha), and 1.8 times in IDH (1175 individuals/ha; Table 1). The HPH and IDH habitats were less favorable for the recruitment of plantlets (F2,309 = 25.46, P < 0.001; Tables 1, 2), while the IDH was also unsuitable for seedlings and the BH habitats were unsuitable for seedlings and cladodes. All differences in the density of sexual and clonal recruitment were highly significant (
2 = 591, 4 df, P < 0.0001; Tables 1, 2). The percentage of aborted fruits (amount of fruits on the ground/total of fruits per habitat) was significantly higher in the BH (40%) and in the HPH (36%) than in the IDH (19%, F2,309 = 14.63, P < 0.01; Table 2). However, the percentage of plantlets with respect to aborted fruits was significantly higher in BH (22.6%, P < 0.001) than in the other two habitats (IDH = 10.9%, HPH = 4.4%). In general, the number of aborted fruits was positively correlated to the number of plantlets (R2 = 0.22; P < 0.01) under individual plants.
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The size of fruits is dependent on the origin of the detached fruit; aborted floral buds were significantly smaller than aborted fruits (1.36 ± 0.02 cm, 1.93 ± 0.07 cm respectively; P < 0.001). Similarly, the average distance of the nonrooted fruits from the parent plant (63.55 ± 1.076 cm) was greater than between plantlets and parents (44.93 ± 2.64 cm, P < 0.001; Table 2), probably due to the protection provided by the parent plant against excessive solar radiation. We found that the most suitable habitat for the establishment of plantlets was the BH (P < 0.0001; Tables 1, 2). Plantlets did not differ between habitats in the number of cladodes produced (mean = 1.68 ± 0.08 cladodes), but rooted fruits were significantly larger (1.93 ± 0.038 cm; N = 315) than nonrooted fruits (1.81 ± 0.016 cm, P = 0.002; N = 2613), suggesting that the probability of rooting is related to the size of the propagules, their location relative to a potential nurse plant, as well as the resources that can be acquired once established.
Effect of radiation on the vegetative propagation by aborted fruits
Survival percentages were dependent on light conditions. Plantlets under shade conditions had higher survival rates (77.5% and 74.4% for 70% and 43% PAR extinction, respectively) than those exposed to direct sunlight (39.4% for 0% PAR extinction; F2,57 = 19.01, P < 0.001). The average number of cladodes on plantlets depends on exposure to light, because growth, measured in terms of cladode production, significantly increased as light decreased (0.55 ± 0.08 cladodes/fruit at 0% extinction PAR; 1.61 ± 0.09 cladodes/fruit at 43% extinction PAR; 1.81 ± 0.09 cladodes/fruit at 70% extinction PAR; F2,57 = 50.01, P < 0.001). As a consequence, accumulated biomass was also dependent on light conditions as well as on the initial fruit size. The cladodes from fruits in shade were significantly heavier than those exposed to direct sunlight (0.04 ± 0.01 g at 0% extinction PAR; 0.16 ± 0.01 g at 43% extinction PAR; 0.18 ± 0.01 g at 70% extinction PAR; F2,57 = 33.92; P < 0.001). Survival between watering regimes (F1,57 = 2.06, P = 0.156) and the interaction term (F2,57 = 0.03, P = 0.96) were not significant.
Site and parental effects in controlled conditions
Even though plantlets and unrooted fruits were statistically different in size, we explored the effect of habitat and parent on the size of progeny. Our results suggest no statistical differences in the fruit attributes as a result of the parental habitat (P > 0.5). However, percentage survival (F27,29 = 3.5, P < 0.001), dry mass (F27,29 = 6.91, P < 0.01), mean number of roots (F27,29 = 3.63, P < 0.01), mean number of cladodes (F27,29 = 2.27, P < 0.01), and mean number of areoles that produced roots (F27,29 = 3.53, P < 0.01) were strongly influenced by the parent (Table 3). The characteristics associated with the parent plant strongly influenced the probability of survival of fallen fruits in all three habitats.
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Understanding the mechanisms and environmental conditions that favor the establishment of different types of newborns is crucial in plant ecology. This is especially so, because 75% of angiosperms have the ability to reproduce sexually and clonally (Tiffney and Niklas, 1985
). We found that the ability of facultative species to switch from one strategy to another allows species to survive in a wide range of habitats (Eckert, 2002
); arid environments are one of the most important areas to explore. In arid environments the successful establishment of sexual offspring for Cactaceae as well as for other succulent species is restricted by biotic factors such as predation (e.g., granivory, herbivory, and the absence of nurse plants) and the inability of seedlings to withstand the harsh abiotic conditions (e.g., light, temperature, water availability; Nobel, 1988
; Mandujano et al., 1998
). Vegetative structures, on the other hand, permit the growth of selected genotypes in an environment adequate for their survival (Anthony, 1954
; Cook, 1985
), are more resistant because they are generally more developed (e.g., developed root system, larger leaf surface; Miao et al., 1998
), and can even differ in metabolic pathways (C3 in seedlings, crassulacean acid metabolism [CAM] in adults; Altesor et al., 1992
). These characteristics provide more resources, protective structures, changes in predator preference, and adequate metabolism (e.g., spines, secondary metabolites, CAM), which allow vegetative structures to circumvent the critical seedling stage (Holthe and Szarek, 1985
; Arizaga, 1998
; Mandujano et al., 1998
).
Like other succulent plants and some species of the same subfamily (Cylindropuntia imbricata and C. bigelovii), O. microdasys presents clonal propagation through two mechanisms: pseudovivipary and cladodes (i.e., stems; Johnson, 1918
; Anthony, 1954
; Arizaga, 1998
; Gentry, 1998
; Mandujano et al., 1998
). Although the clonal establishment of new plants has been reported for other species by a number of authors (Anthony, 1954
; Mandujano et al., 1998
, 2001
; Arizaga and Ezcurra, 2002
; Bobich, 2005
), little has been done in terms of field research to evaluate the real demographic significance of the phenomenon. Clonality assures offspring establishment, a trait especially important to colonize the bare areas common in arid environments and other extreme habitats where the conditions for sexual reproduction are not always appropriate and organisms depend on stored resources for survival (Lee and Harmer, 1980
; Nobel, 1988
; Elmqvist and Cox, 1996
; Mandujano et al., 2001
; Pierce et al., 2003
). Given the low probability of sexual establishment (through seeds) for O. microdasys and for other clonal species (Wang et al., 2004
), pseudovivipary is a benefit that enhances the permanence of species in extreme habitats (Youngner, 1960
; Lee and Harmer, 1980
; Arizaga and Ezcurra, 1995
; Elmqvist and Cox, 1996
; Pierce et al.,2003
; Wang and Cronk, 2003
). In particular, pseudovivipary in O. microdasys is favored by three factors in all three studied habitats: (1) high fruit abortion that increases the number of fruits on the ground that may develop a root system and become established, (2) parental traits that increase the probability of surviving fruits, and (3) the parent plants generate adequate microenvironmental conditions for the establishment of plantlets.
The prevalence of fruit abortion in plants has been thought to be a consequence of excess flower production followed by abortion of fruits, which guarantees adequate resources to support viable seeds (Stephenson, 1981
; Lee, 1988
). Excess of flower production has been said to (1) increase male function (Sutherland and Delph, 1984
; Bertin, 1988
), (2) attract more pollinators (Podolsky, 1992
), (3) increase fruit set during occasional but unpredictable years of resource or pollinator abundance (Lloyd, 1980
), (4) provide reproductive assurance (whereby sufficient ovaries are available for maturation after losses from biotic and abiotic stresses; Ehrlén, 1991
), and (5) provide variation in fruit quality (that can be selectively acted upon to maximize fitness; Burd, 1998
). We can add that the excess of flowers in O. microdasys and possibly in other species that are able to produce plantlets is also a trait that can be favored by selection to produce clonal offspring. Even though O. microdasys produces a large number of flowers during its reproductive season at the beginning of May, many of these fruits are aborted (aborted fruits are the products of flowers that were pollinated). Fruit abortion in O. microdasys seems to result of two different processes: a high incidence of parasitism and the consequences of self-incompatibility (H. Piña, Instituto de Ecología A. C., UNAM, personal communication). Even though the causes behind abortion are still being investigated, the generation of plantlets is clearly the main contribution to vegetative propagation for this species in the MBR by at least one order of magnitude over sexual reproduction and other forms of clonal propagation, even for other species of Opuntia (Mandujano et al., 1998
, 2001
). The success of vegetative reproduction is constrained by the amount of resources available to develop a root system and is therefore a reflection of the amount of stored resources, which produce a higher probability of survival and establishment (Hicks and Mauchamp, 1999
) and are especially important when vegetative structures are subject to high soil and wind temperatures. Survival, size, and development of fallen fruits were strongly influenced by the parental plant, possibly suggesting a maternal effect (Donohue, 1998
) that increases the success of plantlet establishment. For O. microdasys, the size of the parent plant affects the size of fruits, increasing the probability of recruitment with higher resources provided to fruits (Mandujano et al., 1998
, 2001
; Hicks and Mauchamp, 1999
), a similar effect found in other species for germination percentage, seed mass, seedling survival, and plant growth, fruit characteristics, and seed/fruit dispersal (Kahn et al., 1994
). The environmental characteristics generated by the parent plants (Shreve, 1911
; Mandujano et al., 1998
) and habitat (Van Zandt, et al., 2003
) also favor vegetative propagation. For seedlings in Cactaceae, the presence of nurse plants increases and in some cases determines the establishment of individuals (Steenberg and Lowe, 1969
: Nobel, 1988
; Valiente-Banuet and Ezcurra 1991
; Mandujano et al., 2002
). In other species of Opuntia, intermediate shade (approximately 40% of PAR extinction) doubled the survivorship of vegetative propagules (i.e., cladodes; Mandujano et al., 1998
). For O. microdasys, the drastic reduction in solar radiation and temperature generated by the parent plant creates a favorable microenvironment under which the probability of establishment increases. Even though we found no effect of the habitat on the survival and establishment of plantlets in the common garden, similar to what has been found in other clonal species (Eckert, 2002
; Clark-Tapia et al., 2005
), characteristics of the habitats affected the rates at which sexual recruitment and vegetative propagation occurr. The HPH habitat favors sexual recruitment, suggesting that the fruits that are produced by plants at HPH generate seeds that can establish successfully and that the mechanisms that lead to fruit abortion are less influential (e.g., more resources, diminished self-pollination) than in the other two habitats. On the contrary, both the BH and IDH habitats produce more fruits and abortion is higher, leading to an increased probability of establishment through pseudovivipary. Even though these two habitats have higher fruit set, which could potentially lead to higher seed availability for sexual recruitment, environmental conditions needed for successful seedling establishment are not found. The environmental causes of seedling establishment and vegetative propagation of O. microdasys in all habitats have not been explored; however, environmental effects have been shown to affect the type of recruitment (Callaghan et al., 1992
; Arizaga and Ezcurra, 1995
; Mandujano et al., 1998
; Bobich, 2005
).
The timing of fruit abortion seems to be crucial for establishment. Small fruits tend to have lower probabilities of establishment, and it seems as though the first strategy followed by O. microdasys is the abortion of floral buds that did not complete anthesis. The production and final abortion of floral buds do not contribute to sexual or vegetative propagation. The second strategy followed by O. microdasys is pseudovivipary that can be considered a means of reproductive insurance (Wang and Cronk, 2003
; Wang et al., 2004
).
For O. microdasys, abortion soon after the beginning of development has become a strategy to avoid wasting resources (formation of seeds, fruit growth, sugar or reserve substances), insurance against the loss to predation and quite possibly an effect of the mating system (self-incompatibility and/or inbreeding depression). Even though the cost of flower production in the Cactaceae has not been explored, resources that have been invested in their production can be channeled to pseudovivipary when conditions are not adequate for seed development (environmental stochasticity, which leads to variable resource availability over time as well as pollinator limitations). These "empty fruits" are providing vegetative recruitment for the genotype and can be considered an insurance against reproductive failure as has been suggested for other species (Arizaga and Ezcurra, 1995
). However, this form of recruitment may lead to other ecological limitations (Honnay and Bossuyt, 2005
). The establishment of plantlets in close proximity to the parent plant due to the lack of adequate dispersal mechanisms (limited to gravity and superficial water movements) and the fact that the species is self-incompatible may lead to a positive feedback in abortion by increasing geitonogamous pollination and therefore setting a spatial constraint to the mating system (Charpentier, 2002
). The high abortion of fruits that occurs postpollination could be an indication of the problems that O. microdasys is facing through sexual reproduction. In the short term, pseudovivipary is a mechanism that is ensuring the survival of established genotypes and promoting colonization. However, this type of recruitment can lead to decreasing sexual reproduction over longer time periods, with a positive feedback for pseudovivipary that can lead to other ecological problems in the long term, such as diminished fitness and loss of genetic variability.
FOOTNOTES
1 The authors thank A. Flores-Martínez, L. E. Eguiarte, A. Silva, and three anonymous reviewers for advice and comments on previous versions of the manuscript, A. Herrera for field assistance, and F. Herrera and the Instituto de Ecologia, A. C. for logistic support during our stay in the Mapimi Biosphere reserve. This study was partially financed by grants from Semarnat-CONACyT no. 0350, CONACyT no. 34980V and PAPIIT no. IN205500 to M.C.M. 
4 Author for correspondence (mcmandu{at}miranda.ecologia.unam.mx
)
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