taceae and Agavaceae) (Turner, Alcorn, and Booth, 1966;. Jordan and Nobel ... Ifowever, the l~w propbrti9n of sexually produced re- cruitments may be the ...
American Journal of Botany 83(1): 63-70. 1996.
REPRODUCTIVE ECOLOGY AND INBREEDING DEPRESSION IN 0PUNTIA RASTRERA (CACTACEAE) IN THE CHIHUAHUAN DESERT: WHY ARE SEXUALLY DERIVED RECRUITMENTS SO RARE? 1 MARIA DEL CARMEN MANDUJAN0, 2 •3 .4 CARLOS MONTANA, 3 AND LUIS E. EGUIARTE2 2
Centro de Ecologfa, Universidad Nacional Aut6noma de Mexico, Apdo. Postal 70-275, D.E, C.P. 04510, Mexico; and 3Instituto de Ecologfa, Apdo. Postal 63, 91000 Xalapa, Veracruz, Mexico
We evaluated the influence of the reproductive ecology on low recruitment of sexually derived progeny observed in Opuntia rastrera Weber in the Southern Chihuahuan Desert, in two vegetation types. The flowers are diurnal, remaining open 9-10 hr. Pollen is released in the morning and at the same time the stigmas become receptive. Nectar is produced all day, but the production rate is higher at noon. The flowers are visited by insects, mainly solitary bees (Diadasia sp. and Lithurge sp.). Floral characteristics and the pollen/ovule ratio suggest that Opuntia rastrera is a facultative xenogamous species. Controlled pollinations indicate that it is not apomictic and pollinators are required to set fruit; it is also selfcompatible, but there is strong inbreeding depression for fruit set. However, we were unable to demonstrate differences in reproductive characters between the populations in both vegetation types. The average density of adults per hectare was one order of magnitude higher in the nopalera (Opuntia-dominated scrublands) than in the grassland. However, the average density of plants that originated from seeds was one order of magnitude lower in the nopalera. Opuntia rastrera produces abundant flowers, fruits, and seeds in both vegetation types in natural conditions. The low success in the recruitment of new genets cannot be ascribed to the reproductive ecology. Key words: Cactaceae; Chihuahuan Desert; grassland; inbreeding depression; nopalera; Opuntia rastrera; recruitment; reproductive ecology.
Recruitment of sexually derived seedlings is very infrequent in many arid-land succulent species (e.g., Cactaceae and Agavaceae) (Turner, Alcorn, and Booth, 1966; Jordan and Nobel, 1979; Nobel, 1980; McAuliffe, 1984a; Franco and Nobel, 1989; Valiente and Ezcurra, 1991; Cody, 1993). In some species, most recruitment is through vegetative processes (Grant and Grant, 1971, 1980). Two sets of causal mechanisms have been proposed to explain the low recruitment rates of sexually derived progeny. Firstly low recruitment of seedlings may be a consequence of a very low production of viable seeds, due to various genetic and ecological reasons (Aspinwall and Christian, 1992; Eguiarte et al., 1992; Nilsson, 1992; Guitian, 1993), such as, a lack of suitable pollinators (Bierzychudek, 1981; Eguiarte and Burquez, 1988; Harder and Barrett, 1992; Fenner and Feil, 1993; Kudo, 1993), or low resource availability, and characteristics of the reproductive system (Grant and Grant, 1971, 1980; Burquez, Sarukhan, and Pedroza, 1987; Egtiiarte and Burquez, 1987; James et al., 1993; Douglas and Cru-
den, 1994). Secondly, low seedling recruitment may be related to environmental bottlenecks that drastically reduce the establishment of seedlings (e.g., Franco and Nobel, 1989). At least two hypotheses have been proposed to explain these environmental bottlenecks, the nurse-plant effect and the extinction of the coadapted seed dispersers. The nurse-plant effect hypothesis proposes that seedlings of some species cannot develop under the extreme desert environment except under the special conditions found below the canopy of a nurse plant (Nobel, 1988; McAuliffe, 1984a) where maximum temperatures, radiation, and evaporative demands are lower than in the surrounding environment (Franco and Nobel, 1989) and extreme low temperatures and frosts are less frequent (Steenbergh and Lowe, 1969; Nobel, 1980). In addition, the chances of being damaged by herbivory are lower under the canopy of a nurse plant than in open space (Turner, Alcorn, and Olin, 1969; McAuliffe, 1984b; Cody, 1993). Defenders of the early disperser extinction hypothesis suggest that large herbivores consuming the fleshy fruits of some succulents were the primary coadapted seed dispersers, but that most of them became extinct during the Pleistocene. In recent times livestock (cattle, goats, and horses) have partially replaced these original dispersers to different degrees for the different plant species; nevertheless it has been suggested that the quality of the dispersal by livestock may be inadequate (Janzen and Martin, 1982; Janzen, 1986). Both hypotheses assume that viable seeds are produced in sufficient quantities, but are either not dispersed or are killed by environmental stress after ·successful dispersal and germination.
1 Manuscript received 3 March 1995; revision accepted 30 May 1995. The authors thank G. Perez-Chirinos, A. Mandujano, A. Herrera, E Herrera, and A. Rojas for their help during field work. L. Godfnez for identifying the bees, and A. Burquez, J. Nufiez-Farfan, V. Souza, J. Golubov, E. Ezcurra, V. Parra, A. Flores, and E Vargas for reading a previous version of the manuscript. The first author also thanks J. Golubov for his help in different aspects of the work. This study was supported by the Mexican Council for Science and Technology (CONACyT). 4 Author for correspondence: Centro de Ecologfa, Universidad Nacional Aut6noma de Mexico, Apdo. Postal 70-275, D.E, C.P. 04510, Mexico.
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AMERICAN JOURNAL OF BOTANY
Ifowever, the l~w propbrti9n of sexually produced recruitments may be the cot\sequence of the unpredictability and hatsh conditions of life in the desert. Possibly the majority of the sexually produced genotypes cannot survive, but in some years a few genotypes do establish and froth these, plants grow and propagate by asexual means (Williams, 1975; Stearns, 1987). More than 160 species of Opuntia are common and widely distributed in North American deserts (Britton and Rose, 1919-1923; Bravo-Hollis, 1978; Gibson and Nobel, 1986; Gonzalez-Espinosa and Quintana-Ascencio, 1986; Trujillo-Argueta and Gonzalez-Espinosa, 1991). Some species reportedly reproduce mainly or exclusively by vegetative propagation (e.g., Grant and Grant, 1971, 1980; Bravo-Hollis, 1978; Frega and Staniforth, 1986), but relatively little is known about their reproductive ecology. In addition, low germination rates in several other species of Cactaceae have been reported (e.g., Alcorn and Kurtz, 1959; Martfnez-Holgufn, 1983; Adams, Smith, and Osmond, 1987; Trujillo-Argueta and Gonzalez-Espinosa, 1991). In this paper we study the reproductive ecology of Opuntia rastrera Weber to elucidate its influence on the low seedling recruitment, particularly in plant communities (nopaleras, Opuntia-dominated scrublands), where paradoxically this species is dominant. MATERIALS AND METHODS Study area-Field work was carried out in the Mapimi Biosphere Reserve (MBR) in the Southern Chihuahuan Desert, Durango, Mexico (26°40'N, l03°40'W, 1100 m altitude, 264 mm rainfall, 80.2% between June and October, 20.8 C mean temperature; Montana, 1990). Yearly rainfall during the study period was 199.3 mm for 1992 and 239.4 mm for 1993 (MBR climatic station). The vegetation of the area has been described by Montana (1990). Studies were conducted in the two vegetation types, nopalera and grasslands, where 0. rastrera is present. Opuntia rastrera-Larrea tridentata nopalera occupies gentle sloping (2--4%) bajadas where soils are gravelly sandy loam to clay loam. Grasslands, where 0. rastrera is present, tend toward monospecific stands of the tussock grass Hilaria mutica growing on clay-loam to clay soils in periodically flooded playas of < 1% slopes. Very sparsely distributed individuals of Prosopis glandulosa var. torreyana and 0. rastrera are found among the grasses. Study plant-The prickly-pear, 0. rastrera, is a member of the family Cactaceae, subfamily Opuntioideae, within the subgenus Opuntia. It is a species with high morphological variability and its distribution encompasses the semiarid portion of central and northern Mexico within the Chihuahuan Desert, commonly growing on its plains (Britton and Rose, 1919-1923; Bravo-Hollis, 1978). The flowers are. perfect, with yellow or pink corollas, 4-6 em in diameter, and a green stigma. The fruit is green, turning to purple when ripe. The flowering season is in spring (Bravo-Hollis, 1978). At the study sites, blooming starts in March, reaches a peak by early April, and ends in June. Voucher specimens are deposited in the MEXU herbarium of the UNAM. Floral behavior-The floral cycle was determined in each vegetation type, using buds that opened on a single day (N = 14 buds of ten plants in nopalera on 18 April 1992, N = 15 buds of nine plants in grassland, on 19 April 1992). For these flowers, the following measures were made every hour until floral closure: diameter of the corolla at its widest point, pollen availability at the anthers (estimated visually from dehiscence), and stigma receptivity (determined by observing pollen adhesion).
[Vol. 83
Nectar production-At both the nopalera and grassland sites, mature flower buds of 15 plants were bagged with soft mesh bags (N = 45 and N = 27, respectively) to avoid the removal of nectar by floral visitors. Flower nectar that accumulated in each flower .During 2-hr periods was removed and measured using graduated 1-1.Ll micro pipettes. Sampling was made from 0900 to 1730 hr on 21 April 1992 for the nopalera and on 22 April 1992 for the grassland. Results were analyzed by ANOVA with repeated measurements using the BMDP program (Dixon et al., 1988). Sugar concentration of sucrose equivalents for all the nectar samples was estimated using a temperature-compensated field refractometer (American Optical model A010432) (Kearns and Inouye, 1993). Floral visitors-Floral visitors were collected for identification and their activities were studied during the blooming period in 1992 and 1993. Frequency and general behavior of floral visitors was observed on two consecutive days in the nopalera during the blooming peak for individual flowers (N = 15 and N = 20, respectively). For each flower observed, activity (pollen or nectar removal, stigma and/or anther contact), flower visited, time of day, and species of insect visitors were recorded. The observations covered the entire floral cycle (0900-2000 hr) and were pooled according to visiting species in four time intervals (0900-1100, 1200-1400, 1500-1700, and 1800-2000 hr). The flowers observed were tagged and the fruit set recorded 2 mo later. Results were analyzed using a contingency table with adjusted residuals to determine the differences between visitation frequencies for the most abundant solitary bee species (Everitt, 1977). In addition, a mean/variance rate analysis was made to determine if the temporal pattern of visits in the site differed from a random pattern (Greig-Smith, 1983). Mating system (pollen and ovule ratios)-The outcrossing index (OIC) and the pollen/ovule ratios were determined following Cruden (1976) and Cruden and Miller (1981). The OIC is based on the sum of three floral characteristics of the flower and floral behavior: diameter of the flower (corolla), spatial separation between anther and stigma, and temporal separation of anther dehiscence and stigma receptivity (Cruden, 1976). Twenty flowers were chosen at random and for each one corolla diameter, the number, length, and position of stamens (average of ten), style length, ovule number, and average number of pollen grains from two anthers multiplied by total stamen number were recorded , (Cruden, 1976). Controlled pollinations-In the nopalera, from 54 randomly selected plants, 180 flowers that opened on 16 April 1992, were bagged and from them 36 flowers were used for each of five treatments. Pollinations were performed at the time of highest stigma receptivity (1000-1200 hr). The treatments were: (1) automatic self-pollination: bagged flowers were not manipulated but floral visitors were excluded; (2) self-pollination: pollen from a flower was applied on its own stigma; (3) crosspollination: pollen from ten neighboring plants was applied to previously emasculated flowers; (4) apomixis: to prevent any pollen deposition the stigma of each flower was covered with a tape cylinder with a plastic top; (5) control: flowers were bagged at the end of the day. In 1993, we bagged all the flowers from 30 individuals from the nopalera and 11 from the grassland. On each plant we used six flowers and the aforementioned treatments were performed, and a hand-pollinated control (with the stigma covered) for the apomixis treatment was added. From 1992 treatments fruit set was obtained, and ensuing fruits were collected, dried, weighed, and the seed number per fruit was determined. Seeds from each treatment were germinated in petri dishes on 1% bacterial agar and placed in an environmental chamber at 28 C, the optimum germination temperature for Opuntia spp. (Potter, Petersen, and Veckert, 1986; Timmons, 1942 in Nobel, 1988). Seeds were monitored for 3 mo and seedlings were transplanted to tree nurseries containing soil from the original sites. Seedlings were grown in a greenhouse and monitored for 1 yr. From 1993 treatments, fruit set was as-
January 1996]
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MANDUJANO ET AL.-REPRODUCTION OF 0PUNTIA RASTRERA
sessed; further observations could not be performed because of the high fruit removal by frugivores. The data analyses were done using GLIM statistical package (Crawley, 1993). A log-linear model was adjusted, using a binomial probability distribution for percentages and Poisson for counts, and multiple comparison t tests were calculated (Zar, 1984; Crawley, 1993). Confidence intervals at 95% were calculated for the percentages (Rohlf and Sokal, 1981). For 1993, to assess the differences in germination (at 3 mo) and seedling survival (at 1 yr) between environments, we collected fruits produced under natural conditions (nonmanipulated flowers) from ten randomly selected plants from each vegetation type. The germination and survival percentages (arcsine transformed) were analyzed using a nested ANOVA, with site as a fixed factor and plants as a random factor (Zar, 1984).
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Inbreeding depress(on-The relative fitness of inbred progeny obtained in 1992 from the controlled pollination treatm~ts was calculated as the ratio of the performance of selfed progeny to the performance of progeny produced by outcrossing (Levin, 1984; Charlesworth and Charlesworth, 1987). The relative fitness was estimated for the fruit set, seed set, germination at 3 mo, and seedling survival at 1 yr. Census-The density of 0. rastrera individuals per hectare was determined for the two plant communities. Adult plants and juveniles originated from seeds were counted in four 20 X 20 m permanent plots in nopalera and five 20 X 50 m permanent plots in grassland. Juveniles originated from seeds (i.e., the recruits that stem from sexual reproduction) are easily recognized, because of the persistent hairs at the base of the plant for several years. The number of adult plants and pl~nts originated from seeds in both vegetation types were compared using chi-square (Everitt, 1977). In the permanent plots we counted the total number of adult plants, flowers, and fruits produced in both years. From them we estimated the total production of seeds by multiplying the average of seeds per fruit (208 obtained in natural pollination treatments) by the total fruit set in each type of vegetation.
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