Early plant stages may be the most vulnerable within the life cycle of plants especially in arid ecosystems. Interference from exotic species may exacerbate this condition. We evaluated germination, seedling survival and growth in the endangered Caribbean cactus Harrisia portoricensis, as a function of sunlight exposure (i.e., growing under open and shaded areas), ]]>
H. portoricensis seedling are optimal in shaded areas beneath the canopy of established species, but experiments also demonstrated that the identity of the shade provider can have a significant influence on the ]]>
Harrisia portoricensis seedlings had higher probabilities of survival and grew better (i.e., larger diameters) when they were transplanted beneath the canopy of native shrubs, than beneath the exotic grass species, where temperature and solar radiation values were on average much higher than those obtained under the canopies of native shrubs. We also detected that exclusión from potential predators did not increase seedling survival. Our combined results for H. portoricensis suggested that the modification of ]]>
Las etapas iniciales de las plantas parecen ser las más vulnerables de su ciclo de vida, especialmente en ecosistemas áridos. Interferencias de especies ]]>
Harrisia portoricensis, en función de la exposición a la luz solar, diferentes proveedores de sombra, exclusión de potenciales depredadores y condiciones micro-ambientales variables. Los experimentos demostraron que las condiciones adecuadas para la germinación y el establecimiento de plántulas de H. portoricensis son ]]>
H. portoricensis tuvieron mayores probabilidades de supervivencia y crecieron mejor cuando fueron transplantadas bajo la sombra de los arbustos nativos que bajo la sombra del pasto exótico, donde la temperatura y la ]]>
Palabras clave: cactus columnares, Harrisia portoricensis, Megathrysus ]]>
, Isla de Mona, plantas nodriza, germinación de semillas, supervivencia de plántulas.
Germination, seedling establishment, and survival of young plants appear to be the most critical phase in the life cycle of cacti (Bowers 1997, Pimienta & Del Castillo 2002, Valiente et al. 2002, ]]>
et al. 2003, Valverde et al. 2004). In arid and semi-arid environments, the combined effects of temperature, light, and water availability regulate germination, establishment, and survival of plants. Unpredictable rainfall, very high temperatures, and high solar radiation in those environments may influence these processes negatively leading to rare and sporadic germination and survival of early plant stages (Franco & Nobel 1989, Nolasco et al. 1997, Fleming & Valiente 2002, ]]>
Cacti may be buffered from the harsh environmental conditions that characterize arid and semi-arid ]]>
et al. 2003, Larrea & Soriano 2006). Trees, shrubs, grasses, agaves and other cacti may play the role of nurse plants. Evidence demonstrates that these nurse plants may protect early plant stages from intense sunlight, reduce soil temperatures, increase soil moisture, provide a shady microhabitat in which evapotranspiration is ]]>
et al. 1991, Sosa & Fleming 2002, Valiente et al. 2002, Godínez et al. 2005). This phenomenon has been reported in about 36 cacti species representing different life-forms within the family (Steenbergh & Lowe 1977, Jordan & Nobel 1981, Valiente & Ezcurra 1991, Suzán et ]]>
1996, Sosa & Fleming 2002, Godínez et al. 2003).
Harrisia portoricensis Britton is a columnar cactus endemic to four Caribbean islands of the Puerto Rican bank. At present, this species is extinct on the island of Puerto Rico and is ]]>
Harrisia portoricensis is listed as a threatened species under US Federal Regulation (US Fish and Wildlife Service 1990). This threatened status has been primarily attributed to habitat loss and vegetation changes from feral goats and pigs (US Fish and Wildlife Service 1990). The population on Mona Island is the largest remnant population of H. portoricensis to date and is distributed primarily across two ]]>
et al. 2008). At these sites, Croton discolor and Reynosia uncinata are xerophytic shrubs that dominate the landscape and are often found spatially associated with H. portoricensis (Rojas-Sandoval 2010). One hypothesis is that both species may serve as nurse plants of H. portoricensis. The grass ]]>
Megathyrsus maximus, is a perennial African grass that was introduced on Mona Island to support prior cattle activities at this reserve (Cintrón & Rogers 1991) and seems to be spreading into prime H. portoricensis hábitat (Rojas-Sandoval 2010). Literature suggests that grass invasions may have important negative effects on native biodiversity because they can compete effectively with native species (Hughes
et al. 1991, D’Antonio & Vitousek 1992, Cabin et al. 2002, Levine et al. 2003, Seabloom et al. 2003). At present, no data exist on whether or not the presence of M. maximus has negative impacts on H. portoricensis populations. While M. maximus may compete for ]]>
M. maximus on germination and establishment in H. portoricensis is one way to understand the potential interactions between this endemic cactus and the exotic grass that is invading its current habitat.
]]>
In this study we evaluated whether or not germination and seedlings survival of H. portoricensis was influenced by micro-environmental variation and by extension whether or not these processes were influenced by the type of species under which they were occurring (i.e., exotic grass: M. maximus or native shrubs: C. discolor and R. uncinata). We used this ]]>
H. portoricensis populations to the potential effects of an exotic grass species, how important is the presence of shade providers for germination and establishment, and how susceptible are seedlings and young individuals to changes in micro-environmental factors. We hypothesized that germination, survival and growth of seedlings would be higher in shaded areas than in open areas as it occurs in many columnar cacti species. We also hypothesized that micro-environmental conditions (i.e., temperature, PAR, humidity) would ]]>
H. portoricensis seedlings beneath the canopies of native shrubs than beneath the leaf cover of the exotic grass, and as a result seedling survival and growth would also be higher under native shrubs.
Materials and methods ]]>
Study species:Harrisia portoricensis Britton is a slender columnar cactus where juveniles are usually unbranched and adults may reach heights of more than 2m and present an extensive branching pattern (Liogier 1994). The density of H. portoricensis on Mona ]]>
2 and a population size estímate of 59 857 (SE=1058) with a demographic profile that included plants in the adult (59%), juvenile (34%) and seedling stages (7%), indicating that at least some recruitment is occurring at this locality (Rojas-Sandoval 2010). This species is a night flowering cactus and plants produce flowers multiple times within a year (Rojas-Sandoval 2010). Reproductive plants produced large hermaphroditic flowers (mean length: 21.16±0.98cm; mean width: 5.25±0.27cm) that open only for one night. Flowers are nectariferous (mean volumen 0.26±0.04mL/night) but visits by ]]>
H. portoricensis is mainly through seeds and spread by vegetative ]]>
Study site: The study was conducted at Mona Island Reserve, a semi-arid island located in the Caribbean Sea between Puerto Rico and Hispaniola (18°05’ N - 67°54’ W). The island itself is a raised platform of dolomite (magnesium-rich limestone rock) reaching up to 100m at its highest point (Frank
et al. 1998, Cintrón 1991), and covering an area of 5 517ha. Mona has an annual mean temperature of 25°C, and receives an average annual rainfall of 810mm (Ewel & Whitmore 1973). The rainy season last from August to November with peaks in May and October, and the dry season run from December to April (Murphy & Lugo 1995). During the time of the experiments (May 2007-May 2009), annual mean rainfall was 986mm with peaks occurring always in May and between September-October. Mona is characterized by an irregular distribution of plants, exposed ]]>
et al. 2008). The island’s vegetation is classified as a subtropical dry forest. On the island, H. portoriscensis is most common at two plant communities: the lowland dry cactus shrubland and the lowland dry limestone shrubland (Martinuzzi et al. 2008). The lowland dry cactus ]]>
Croton discolor (Euphorbiaceae) and Reynosia uncinata (Rhamnaceae) are dominants species of both plant communities and frequently can be found in association with H. portoricensis. Croton discolor is a short ]]>
R. uncinata is a taller (up to 4m) woody evergreen shrub that gradually replaces its leaves throughout the year. Approximately a 25% of both forests have been invaded by the African grass Megathyrsus maximus (Rojas-Sandoval 2010).
]]>
Seeds collection: Fifteen mature fruits of H. portoricensis were randomly collected from plants growing in the study site in August 2007. Each fruit was collected from a different plant and their seeds were extracted and washed with tap and distilled water to remove the pulp. Seeds were dried using absorbent paper, pooled and placed in paper bags for storage at room temperature until required. These seeds were used to perform seedlings survival and seedlings performance field experiments. In August 2008, we repeated ]]>
Seed germination experiment: To estimate the rate of seed germination under natural and laboratory conditions, and to identify conditions required for seed germination, we performed a germination experiment in September 2008 ]]>
Croton discolor, the most common shrub species in the study site, and (3) control treatment: seeds were germinated in the laboratory under controlled conditions of light (15h light: 9h dark), humidity (90% relative humidity) and temperature (minimum 24ºC: maximum 30ºC) (Sosa & Fleming 2002). For open and shade treatments, 100 seeds were sown in the field and placed directly on the ]]>
C. discolor and seedlings received no direct sunlight at any time during the day even with changes in sun direction (shade treatment). Ten replicates were performed per treatment for a total of 1 000 seeds per treatment. For the control treatment, 1 000 seeds were sown among ten 12×22cm plastic-trays (100 seeds per trays) filled with non-sterilized soil ]]>
Seedling survival experiment: To estímate the survival and growth of
H. portoricensis seedlings under natural conditions, we designed an experiment that evaluated two contrasting sunlight exposure conditions, and ruled out the potential effects of natural predators on the outcomes by performing the experiments under conditions of exclusion and non-exclusion of potential predators. Five hundred seeds from 15 different fruits were sown in November 2007 in plastic nursery traits with multiple cavities filled with soil collected from the study site. We sowed one seed per cavity under greenhouse conditions on Mona Island. In February 2008, one month after seedling emergence, we randomly selected and ]]>
Croton discolor. Open and shaded sites were distributed on Mona Island across an area of approximately 10ha that included the two vegetation types where H. portoricensis is most common: lowland dry cactus shrubland and lowland dry limestone shrubland. At each site, ]]>
Seedling performance experiment: To compare the performance of H. portoricensis, we used a field experiment where seedlings were placed beneath the canopies of three shade provider species: Croton discolor, ]]>
and Megathyrsus maximus. Ten focal plants were randomly selected in February 2008 for each shade provider species, and two one-month-old seedlings were transplanted directly on soil beneath the canopy of each plant. Following the same methodology that we described in the previous experiment, seedling survival and growth parameters (height and diameter) were recorded monthly from February 2008 until May 2009 (15 months). Differences in ]]>
Results
Seed germination experiment: The number of seeds germinated after 120 days differed among treatments (Kruskal-Wallis χ2=24.34, df=2, p<0.001, Fig. 1). The proportion of germinated seeds under laboratory conditions was 4.3 times higher than ]]>
Fig. 1). On average, seeds began to germínate 54 days after sowing for both the laboratory and the field shade treatments (Fig. 2). The end of the experiment obtained the highest germination percentage under laboratory conditions with 31.4% of germination. In the shade treatment the percentage of germinated seeds was much lower and scarcely reached values of 7.2%. Seed ]]>
Fig. 2).
Seedling survival experiment: The survival of transplanted seedlings was low and upon completion of the experiment only seven individuals were alive at shaded sites in the field (Table 1). Analyses of the survivorship curves indicated significant differences among experimental treatments (Log-Rank test: χ2=34.2, p<0.0001, Wilcoxon test: χ2=30.4, p<0.0001, Fig. 3). All seedlings transplanted to open sites died by the second month and only seedlings that were placed at shaded sites survived after one year in the field. Contrary to our expectations, seedling survival in shaded sites was not higher when seedlings were excluded from potential predators (G test=3.06, df=1, p=0.2, Fig. 3). Finally, for the two growth parameters analyzed, surviving seedlings growing under exclusion and non-exclusion conditions did not differ neither in height (t=-0.69, df=5, p=0.52) nor in diameter (t=0.73, df=5, p=0.49) by the end of the experiment (Table 1).
Seedling performance experiment: In the field, all three shade provider species had a fraction of surviving H. portoricensis seedlings ]]>
2=31.2, p<0.0001, Wilcoxon test: χ2=48.2, p<0.0001, Fig. 4). By the end of the experiment, a higher percentage of seedlings survived beneath the canopy of R. uncinata (40%) and C. discolor (30%) than beneath the shade of M. maximus ]]>
2,14=3.21, p=0.04, Fig. 5A) but not in seedling height (F2,14=1.87, p=0.17, Fig. 5B). At the end of the experiment, the ]]>
C. discolor and R. uncinata were twice the average diameter of seedlings growing under M. maximus (Fig. 5A).
Monthly mean temperatures were ]]>
3,61=3.32, p=0.02, Table 2), but contrary to our expectations did not differ among shade provider species (Table 2). During the experiment, mean temperatures varying from 29.09ºC in open sites to 27.62ºC under shade providers (Table 2). In contrast, monthly mean maximum temperatures were significantly ]]>
3,61=4.33, p=0.03, Table 2). We found that máximum temperatures in open areas and beneath M. maximus were significantly higher than beneath the canopies of the native shrubs. Maximum temperatures were beneath the canopy of M. maximus and in open areas were 1.4ºC and 3.8ºC respectively, and higher than under the canopies of native shrubs (
Table 2). We did not find differences in the percentages of relative humidity recorded beneath the shade providers and in open sites over the length of the experiment (F3,61=0.07, p=0.92, Table 2). As we expected, PAR values were significantly higher in open sites than underneath the shade providers, but they were also highest beneath M. maximus foliage than under the ]]>
C. discolor and R. uncinata in March and September (p<0.0001 in all cases, Table 2). On average PAR values were 2.8 times higher beneath the leaf cover of M. maximus than beneath the canopy of the native shrubs (Table 2).
Discusion
We predicted that germination, survival and growth of H. portoricensis seedlings on Mona Island would be higher in shaded areas than in open areas due to more benign microclimatic conditions. In general, our results for field and laboratory experiments support this hypothesis and demonstrate the ]]>
H. portoricensis. Studies have shown that shade created by perennial nurse plants can decrease solar radiation, temperatures, and water evaporation, and as a result enhance the germination, growth and establishment of young cacti beneath their canopies (Jordan & Nobel 1981, Valiente & Ezcurra 1991, Valiente et al. 1991, ]]>
et al. 1997, Leira & Parra 1999, Sosa & Fleming 2002). For many species of cacti, in addition to nurse plants, rocks and other surface irregularities such as holes and cracks may act as potential facilitators of germination and seedling establishment (Godínez et al., 2003, Mungía & Sosa 2007, Peters et al. 2008). However, for H. portoricensis ]]>
Our combined results for H. portoricensis also demonstrated that suitable conditions for germination and seedling establishment are tied to type of shade provided by the different species in our study. Although the number of ]]>
H. portoricensis seedlings on Mona Island have higher probabilities of survival and grew better (i.e., higher diameters) if they were transplanted beneath the canopies of two native shrubs species C. discolor and R. uncinata than beneath the exotic grass M. maximus. It ]]>
Seedling survival and seedling ]]>
C. discolor and R. uncinata which in contrast to M. maximus do not suffer from leaf loss during the dry season and thus provide a more consistent foliage cover and less solar radiation underneath their canopies throughout the year (Rojas-Sandoval 2010). Areas with high solar radiation can lead to high temperatures, high evapotranspiration and low soil moisture availability, and as a result lower the probability of survival and ]]>
et al. 1997, Suzán & Sosa 2006). Another alternative explanation, although not mutually exclusive, for the observed lower seedling survival and performance under M. maximus canopies relative to the native shrub species is that this grass is indeed a better competitor for water and/or nutrients than H. portoricensis seedlings (Williams & Baruch 2000, ]]>
et al. 1991, D’Antonio & Vitousek 1992, Cabin et al. 2002, Levine et al. 2003, Seabloom et al. 2003). A recent study reports that regeneration of the columnar ]]>
Pachycereus pectenaboriginum is inhibited at areas dominated by buffelgrass (Pennisetum ciliare) in the Sonoran Desert. For those areas, the authors suggest that interference with buffelgrass and the extraction of water from the upper soil surface by this grass may be responsible for the high levels of mortality in this cactus species (Morales-Romero & Molina-Freaner 2008).
]]>
Our results indicated that the percentages of seeds germinated and the probabilities of seedling survival for H. portoricensis under natural conditions were very low. For field experiments, seed germination was nil in open areas but even under the shade only 7.2% seeds germinated. Because temperature and soil moisture are often inversely related in the field (as temperature increases soil moisture decreases), one possibility is that in open areas direct solar radiation warms the soil and reduces soil moisture ]]>
etal. 2003). On Mona Island, soil temperatures can reach 70ºC in open areas (Rojas-Sandoval 2010), and these elevated temperatures may also directly inhibit germination or damage seeds placed in the field. Nevertheless, experiments that control air temperatures independent from surface moisture are needed to decide on the ]]>
H. portoricensis were noticeably different than what is reported for other cactus species. Literature on seed germination shows that for most cactus species, seeds germinate within a week (Rojas & Vázquez 2000). For H. portoricensis, seed germination, on average, occurred after 54 days. It is possible that germination may require ample hydration periods as a way to keep ]]>
H. portoricensis but has been shown for cacti in the subfamily Opuntiodeae, in which germination may take few ]]>
Surprisingly, we found that predator exclusions did not improve the probability of
H. portoricensis seedling survival but our study only evaluated this possibility at one point in time. Previous studies comparing predation on seedlings have indicated that predation intensity may vary depending on environmental conditions, intensity of the drought, latitude, and predator abundance (Valiente & Ezcurra 1991, Sosa & Fleming 2002). In addition, predation intensity on columnar cactus seedlings could also vary depending upon whether seedlings are located beneath shrubs species or in open areas (Sosa & Fleming 2002). Temporal studies that look at potential cactus-predator interactions at times where environmental ]]>
H. portoricensis at Mona Island.
Overall, our data suggested that for H. portoricensis, microenvironmental conditions
provided by native shrubs species from the understory may play a primary role in the germination, establishments, and growth of this cactus species. During the study period rainfall was above the average annual rainfall value reported for Mona Island, thus water limitation appears not to be a factor affecting the establishment and survivorship of H. portoricensis seedlings. The presence and expansión of M. maximus may diminish the availability of environmental conditions that are optimal (i.e., ]]>
et al. 2006) may be conditions that could facilitate further spread and invasion of
M. maximus. Further spread of this African grass may reduce the amount of optimal environments for germination and establishment of H. portoricensis and if so present and added vulnerability beyond those listed thus far to this native endemic and threaten cactus. From a management perspective,efforts to protect H. portoricensis would ]]>
Acknowledgments
The authors thank ]]>
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*Correspondencia a: Julissa Rojas-Sandoval: Department of Biology, University of Puerto Rico, Río Piedras Campus, P.O. Box 23360, San Juan, Puerto Rico 00931-3360 USA; julirs07@gmail.com Julissa Rojas-Sandoval & Elvia Meléndez-Ackerman: Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Río Piedras Campus, P.O. Box 23341, San Juan, Puerto Rico 00931-3341 USA. Institute for Tropical Ecosystems Studies, University of Puerto Rico, Río Piedras Campus, P.O. Box 21910, San Juan, Puerto Rico 00931-1910 USA; elmend@gmail.com
1. Department of Biology, University of Puerto Rico, Río Piedras Campus, P.O. Box 23360, San Juan, Puerto Rico 00931-3360 USA; julirs07@gmail.com 2. Center for Applied Tropical Ecology and Conservation, University of Puerto Rico, Río Piedras Campus, P.O. Box 23341, San Juan, Puerto Rico 00931-3341 USA. 3. Institute for Tropical Ecosystems Studies, University of Puerto Rico, Río Piedras Campus, P.O. Box 21910, San Juan, Puerto Rico 00931-1910 USA; elmend@gmail.com
Received 27-V-2011. Corrected 20-X-2011. Accepted 23-XI-2011.
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