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Wind effects on dispersal patterns of the invasive alien Cortaderia selloana in Mediterranean wetlands
Acta Oecologica 27 (2005) 129–133 www.elsevier.com/locate/actoec
Original article
Wind effects on dispersal patterns of the invasive alien Cortaderia selloana in Mediterranean wetlands S. Saura-Mas, F. Lloret * Departament de Biologia Animal, Biologia Vegetal i Ecologia, Center for Ecological Research and Forestry Applications and Unitat d’Ecologia, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain Received 31 March 2004 Available online 21 January 2005
Abstract Dispersal and establishment of recruits are key steps in the seed invasion process of alien plants. We analysed the effects of wind on the dispersal pattern of Cortaderia selloana, an invasive alien tussock grass in the wetlands of the Mediterranean basin. C. selloana dispersal curves (with QDx values, it is seed density at a given distance from the focal plant) for the four orientations north, east, south, and west, fitted well with exponential negative functions. Strong northern winds had a significant effect on the seed dispersal of C. selloana, so we found a greater number of seeds in the southward focal plants. This wind-orientation effect was found at relatively short distances (from 1 to 20 m), whereas no significant differences were found in orientations at 30 or more meters from the focal plants probably due to the seeds’ decreasing ability to remain in the air. The spatial distribution of recruits showed a similar pattern to that of the seed dispersal, with more recruits in a south orientation. This study demonstrates that wind is a notable factor determining invasive patterns of an anemochorous invasive species such as C. selloana at a local scale. This effect scales up from the dispersal phase to the seedling recruitment stages. © 2005 Elsevier SAS. All rights reserved. Keywords: Seed shadow; Cortaderia selloana; Pampas grass; Wind; Seed dispersal; Mediterranean wetlands; Spatial pattern; Plant recruitment
1. Introduction Human activity around the world has been the most important agent in the recent introduction of a large number of species that have later become biological invasions. Invasions by alien species are one of the global-change factors threatening the conservation of native species and integrity of ecosystems worldwide (Vitousek, 1994; Mack et al. 2000; Levine et al. 2003), with significant economic repercussions (Pimentel et al., 2000; Mc Neely, 2001). This process has impact at different levels, such as genetic contamination (i.e., hybridization), changing population dynamics or modifying community and ecosystem processes (Stuart, 1998; Parker et al., 1999). If we focus on the species traits that correspond with invasiveness, we see that species capable of dispersing widely after introduction processes have a greater tendency to become * Corresponding author. Fax: +34 93 5814151. E-mail address: [email protected] (F. Lloret). 1146-609X/$ - see front matter © 2005 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2004.12.001
invasive (Alpert et al., 2000; Kolar and Lodge, 2001; Lloret et al., 2004). With respect to these attributes of spatial distribution in invasive species, the colonization process depends on the vegetative propagation mode and the seed dispersal patterns (D’Antonio, 1990; Lonsdale, 1993; Higgins et al., 1996; Rejmánek, 2000). Species with structures that favour wind and animal dispersal have better regional and local invasion success (Lloret et al., 2004). At smaller spatial scales, more research is required on the determining factors of dispersal and colonization patterns from an invasion focus, as several models of population expansion have been developed, based on biogeographical information and empirical correlations to environmental variables (Londsdale, 1993; Higgins et al., 1996; Cain et al., 2000; Delisle et al., 2003). Seed shadows provide an estimate of the number of seeds reaching the soil in relation to focal plants and, consequently, they potentially determine the earlier stages of colonization. Although seed shadows have been estimated for a number of species (Carey and Watkinson, 1993; Willson, 1993; Clark et al., 1998), their description for invasive species has generally
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been neglected. Wind, in particular, may be a key driver of dispersal patterns for anemochorous species in areas with well-defined dominant winds. Under these conditions, the wind is expected to determine the seed shadow and to influence seedling establishment patterns on a number of spatial scales, from the microsite to the locality. On the other hand, seed dispersal and seedling spatial distribution may not necessarily be correlated, since various ecological factors may limit seed germination compared to seedling survival and establishment (Houle, 1992; Schupp and Fuentes, 1995). In particular, the range of suitable microsites for invasive species would be expected to be very broad, with a low temporal variability in reproductive success and spatial relationship between seed dispersal and seedling survival. Here, we explore wind effects on the seed dispersal and the establishment of recruits from the invasive species Cortaderia selloana in Catalonia. This species, a long-lived perennial grass native to South America, is a common anemochorous alien invasive plant in several types of ecosystems, such as Mediterranean plant communities (Lambrinos, 2002), and it is becoming a major concern in protected wetlands of the Iberian Peninsula. More specifically, we address the following questions: (1) does dominant wind determine seed shadows at the different orientations (north, south, east, and west)? (2) Does the dominant wind determine differences in long-distance dispersal? And, (3) are the spatial patterns of recruit distribution related to the dominant wind?
2. Materials and methods 2.1. Study species and study sites Pampas grass (C. selloana (Schult. & Schult. f.) Asch. & Graebn.) is a large perennial tussock grass which tolerates winter frost, intense sunlight, warm summer temperatures, and moderate drought (Bossard et al., 2000; Lambrinos, 2002). Tussocks can reach 2–4 m in height and 2–3 m in diameter. Their lateral roots can spread up to 4 m in diameter and 3.5 m in depth. Bossard et al. (2000) describe possible vegetative propagation when fragmented tillers receive adequate moisture. However, no evidence of this was observed in the studied population. This plant’s flowering stems can be 3 m in height and its inflorescences consist of attractive densely plumed heads at the end of a stiff stem. C. selloana is considered gynodioecious but functionally dioecious (Connor, 1971). This reproductive performance may limit seed production in isolated individuals. In late summer and early autumn it produces copious amounts of small, wind-dispersed seeds (as many as 106 seeds/individual) (Lambrinos, 2002). The populations seem to be expanding in several localities in the wetlands of north-eastern and central Catalonia (Mathieu, Domènech, personal communications). Most of these localities, such as our study sites, are surrounded by urban developments or cities where C. selloana is common
as an ornamental plant, since it has been commercially cultivated in Europe since 1874. Our study site is Aiguamolls de l’Empordà Natural Park (31T DG 0505 4675 UTM), a Mediterranean protected area, located in the NE of Catalonia, (North-East Iberian Peninsula). Vegetation is mainly dominated by Mediterranean wetlands, including marshes, grasslands, riparian woodlands, and agricultural fields (both in use and abandoned). In this area, C. selloana has a remarkable presence in coastal dunes and abandoned agricultural fields. The climate is Mediterranean, with cool winters, warm summers, and high humidity (annual mean humidity of 72%). The mean annual precipitation at the nearest weather station (Sant Pere Pescador-Alt Empordà) is 715.6 mm. The average annual temperature is 15.1 °C. The mean maximum and minimum temperatures are reached in July (26.6 °C) and January (2.8 °C), respectively. One of the most characteristic features of this protected area is the northern wind or “tramuntana”, which blows throughout the year, including autumn, when C. selloana dispersal occurs (Gósalbez et al., 1994). Concretely, the north-western winds blow 17.1% of hours, northern winds blow 21.4% of hours, and north-eastern winds blow 15.2% of hours (Fig. 1). 2.2. Seed production and seedfall We located nine female adult individuals of C. selloana in different parts of the Aiguamolls de l’Empordà Natural Park, all of them in farms and abandoned fields. Each individual was at least 100 m apart from the nearest neighbour of the same species, so that the effects of other plants on the respective seed shadows were minimal. These individuals were probably established from populations existing in gardens of neighbour urban areas.
Fig. 1. Wind direction distribution (percentage of hours) in Puig-Clapé (sited 15 km from the study site). This station is the closest source of wind distribution data. Hours of calm (wind force less than 2.5 on the Beaufort scale) are indicated in the central box. Source: ENHER, 1993.
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Each plant was surrounded by eight seed traps set at various distances from the focal plant (0.5, 1, 3, 5, 10, 20, 30, and 40 m) in four directions (north, south, east, and west), that is a total of 32 traps per focal plant. Seed traps were set on the floor and consisted of a flat tray with a sticky paper (0.285 × 0.19 m) on the bottom and a wire mesh (0.02 m diameter) on top to repel predators and prevent the possible death of any small vertebrate that might enter the trap. The mesh was coarse enough to allow the passage of seeds (Greene and Calogeropoulos, 2001). Seed traps were set up from 27th September to 27th December 2002 (92 days), and they were surveyed three times during this period, until the seed rain stopped. Some values proved accidentally unavailable due to the temporary loss of a seed trap. We estimated the seed production of each plant by correlating the length of the inflorescences of the plant with the seed production. We used inflorescence length as a nondestructive descriptor of seed production. The parameters for this correlation were obtained by sampling one inflorescence from 30 plants from neighbouring populations. We randomly selected ca. 0.2 g piece of each inflorescence, and we counted the number of seeds of each piece. Then, we correlated the number of seeds to the biomass of inflorescence piece. We estimated the total number of seeds to the whole inflorescence according to the total inflorescence’s biomass. Finally, we correlated the number of seeds to the inflorescence’s length. 2.3. Spatial distribution of recruits We surveyed the presence of recruits around each of the focal plants used to estimate seed shadows by surveying four 40 × 1 m transects oriented towards north, east, south, and west. We also surveyed recruits around non-isolated plants from the populations in the locality of La Rubina, a coastal dune area within the Park, and the only population inside the studied area with established recruits. We chose as focal plants all the adult and flowering individuals that were separated by at least 6 m from the nearest adult (n = 11). A criterion of longer distances would have precluded the possibility of finding enough plants for the survey. We surveyed recruits within a circle with a radius of 3 m around the focal adult plants. We considered as recruits those individuals with a canopy diameter of less than 1 m that had not had any inflorescences during the flowering period. We did not survey beyond a distance of 3 m to minimize surveying recruits from other focal plants. Although these distance, do not avoid completely the overlapping of seed shadow from different plants, most seed rain was expected to occur at a closer distance from focal plants. We measured plant height, distance to the nearest adult and the orientation (azymuth) in relation to the focal plant. 2.4. Data analysis We analysed differences in seed shadow in relation to distance and orientation from parent plants by a Repeated Mea-
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sures ANOVA model with two within-subject factors (distance and orientation) and the number of collected seeds as the dependent variable (after log (x + 1) transformation). Seven levels of distance (0.5, 1, 3, 5, 10, 20, and 30 m) and four levels of orientation (north, east, south, and west) were considered. Vandalism caused some missing values. We excluded from the analysis three plants with missing values. Data from traps at a distance of 40 m were also excluded from this analysis due to missing field values. Missing field values made it impossible to perform a complete design. We therefore made a separate analysis of the effect of orientation on collected seeds at each distance (0.5, 1, 3, 5, 10, 20, 30, and 40 m) by Repeated Measures ANOVA with one within-subject factor (orientation). Plants with missing field values were excluded from the analysis of each distance (see Table 1 for the number of plants used in each case). Differences on collected seeds (after log (x + 1) transformation) between orientations (north, east, south, and west) were analysed by Fisher’s PLSD post-hoc tests (significance values are shown in Fig. 2). The dispersal curve (with QDx values) was calculated as the density of seeds deposited at a given distance from the focal plant and it was estimated for each orientation. QDx values (seeds m–2) (Greene and Calogeropoulos, 2001) were obtained by the mean of collected seeds and weighted according to the estimated seed production of each plant. In order to facilitate comparisons to other studies, QDx values were were standardized by considering that the number of seeds produced by a plant is equal to 100,000, (Greene and Calogeropoulos, 2001). QDx dispersal curves were fitted to negative exponential functions for all the orientations (Table 2). For the analysis of the spatial pattern of recruits, the orientation azymuth values were categorized in one of the four orientations: north (from 316° to 45°), east (from 46° to 135°), south (from 136° to 225°) and west (from 226° to 315°). The independence of occurrence with respect to orientation was analysed by a v2 test. Statview 4.5 (Abacus concepts) and Kaleida Graph 3.08 (Synergy Software) programmes were used for the computation of analyses. When necessary, data were transformed to meet the assumptions of parametric analysis. Table 1 Summary table of repeated ANOVA measurements (one within factor variable) for the differences in the number of seeds collected in different orientation (North, East, South, and West). For each distance, the number of plants (n) available for the analysis is also indicated Distance (m) 0 1 3 5 10 20 30 40
n 9 8 8 9 9 8 7 4
F 2.70 12.27 5.03 5.35 9.23 3.48 0.88 0.02
P-value 0.0681 0.0001 0.0088 0.0058 0.0003 0.0341 0.4700 0.9960
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No recruits were found around the nine focal plants used to establish seed–shadow curves. Recruit distribution around plants in the population of “La Rubina” was not independent of the orientation (v2 = 12.85, p < 0.05, df = 3). Most of the seedlings (53%) were distributed at the south orientation, while 18% were at the north and 14% at both the east and west orientations.
4. Discussion
Fig. 2. Dispersal curves obtained from mean QDx values for each orientation (North, East, South, and West). * Collected seeds were different in South orientation than in East & West orientations, but not from North (P < 0.05 Fisher’s PLSD post-hoc test, log (x + 1) transformation). ** Collected seeds were different in South orientation than the other three directions (P < 0.05 Fisher’s PLSD post-hoc test, log (x + 1) transformation). ns = no significant differences between orientations. Note that dispersal curves and significance descriptions refer to two different variables: QDx (seed density at given distance) and collected seeds in traps, respectively.
3. Results The estimated mean production of seeds for the nine focal plants was 416,399 seeds per plant (SD = 265,744.76), ranging from 54,567 to 840,905 seeds per plant. Dispersal curves were obtained using QDx values for each one of the four orientations. Seed shadow in the south direction was significantly different from the other orientations (F3,15 = 8.09, p = 0.002) (Fig. 2). The number of collected seeds at the distances of 1, 3, 10, and 20 m was significantly higher in the south direction than in the other ones (see Fig. 2 for details), while no significant differences between orientations were observed at 0.5, 30, or 40 m (Fig. 2, Tables 1 and 2). The distance from the focal plant significantly reduced the number of seeds reaching the soil (F6,30 = 13.02, p < 0.0001). This pattern was observed in all the orientations, as indicated by the non-significant interaction between orientation and distance (F18,90 = 1.22, p = 0.26). In all the orientations there was a leptokurtic curve, which was successfully fitted to a negative exponential function (Table 2). Table 2 Exponential negative curve fit (y = a × e(–bx)) for table values for the different orientations (North n = 68, East n=67, South n = 70, West n = 66). Significance values are shown by asterisks; *, P < 0.05; **, P < 0.01; ***, P < 0.001 a b r Significance
North 909.3 1.958 0.287 *
East 7154.5 3.391 0.343 **
South 350.8 0.196 0.503 **
West 6504.5 3.633 0.336 ***
Wind effects have been found to determine the spatial pattern of trees and grass species (Okubo and Levin, 1989; Carey and Watkinson, 1993; Nathan et al., 2001). Our study site is characterised by significant periods of northern winds throughout the year (Fig. 1) that clearly determine the seed dispersal patterns of C. selloana. This effect was detected at intermediate distances from the focal plant (1–20 m), while most of the seeds collected at 0.5 m probably fell down due to gravitation. There were no wind effects at distances of more than 20 m. Okubo and Levin (1989) have described models that illustrate how dispersal distances from a source depend on factors such as wind speed and other physical agents. Our results suggest that wind effects decline with distance due to the seeds’ decreasing ability to remain in the air. In addition, density is expected to decrease with distance because of the dilution effect due to the quadratic increase of surface with distance. Therefore, the number of sampling points at longer distances may have been too low to detect any differences between the orientations when the density of seeds reaching the soil is very low (Clark et al. 1999; Cain et al. 2000). In addition, at longer distances from a given focal plant, the interference with seed shadows from other plants may reduce the directional effect of wind on the distribution of the seed rain. Seed–shadow curves have frequently been fitted into a 2Dt model (Clark et al., 1999; Nathan and Muller-Landau, 2000; Greene and Calogeropoulos, 2001). The use of the 2Dt curve did not seem to be the best solution in our case, since there was no evidence of convexity at the source (Clark et al. 1999). In fact, we obtained a satisfactory fit to an exponential negative function for all the four orientations. Lambrinos (2002) demonstrated how a set of environmental factors such as precipitation, soil disturbance, mammalian herbivory, and resource availability influenced the invasive establishment of C. selloana in central California. Anyway, the absence of recruits around the focal plants used to estimate seed shadow may be the result of the low number of viable seeds in female isolated individuals, in which low levels of fecundation are expected. Bossard et al. (2000) observed that viable seed only occurs in C. selloana populations of California when both female plants and plants with perfect flowers are present. Notwithstanding the difficulties in making a simple analysis of the origin of recruits in dense populations, the spatial pattern of C. selloana recruits in the La Rubina population reflects the effect of dominant winds not only on seed dispersal but also on seedling establish-
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ment. In spite of the large production of seeds, we observed that well-established seedlings were very rare in this area, in agreement with previous observations in populations from California (Lambrinos 2002). As a result, microsite suitability would also play an important role in C. selloana recruitment, probably due to the dense cover of herbaceous vegetation in many abandoned agricultural fields. We therefore expect that the strong wind effect on seed dispersal would become progressively diluted in the later stages of the recruitment process. 5. Conclusion In conclusion, we have observed that the spatial pattern of seed dispersal by the invasive C. selloana on a local scale is determined by physical drivers, such as wind orientation (when a clearly dominant wind exists). This influence is relevant in the seed dispersal process and remains so up to the establishment of new individuals. However, no evidence of this effect has been found at distances longer than a few meters from focal plants. Our study approaches the questions of how wind determines seed dispersal of the invasive C. selloana from 1 to 20 m and of how this effect is still present in recruits’ spatial patterns. Finally, this study provides information about the invasiveness and spatial dispersal of C. selloana, an invasive species which is considered to produce alterations, especially to Mediterranean wetlands ecosystems. Acknowledgements We would like to thank M. Vilà and R. Domènech for their suggestions during the course of the study. Ll. Benejam, A. Saperas and M. Mas helped in the fieldwork. We are grateful to the officers of the Aiguamolls de l’Empordà Natural Park and, particularly, S. Romero for their support and permission to use the facilities. This study was funded by the CICYT project REN2000-0361 and by a grant from the Ministry of Education to S. Saura-Mas. References Alpert, P., Bone, E., Holzapfel, C., 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Urban & Fisher Verlag. Perspect. Plant Ecol. Evol. Syst. 3, 52–66. Bossard, C.C., Randall, J.M., Hshousky, M.C., 2000. Invasive Plants of California’s Wildlands. University of California, Berkeley, LA. Cain, M.L., Milligan, B.G., Strand, A.E., 2000. Long-distance seed dispersal in plant populations. Am. J. Bot. 87, 1217–1227. Carey, P.D., Watkinson, A.R., 1993. The dispersal and fates of seeds of the winter annual grass Vulpia ciliata. J. Ecol. 81, 759–767. Clark, J.S., Macklin, E., Wood, L., 1998. Stages and spatial scales of recruitment limitation in southern appalachian forests. Ecol. Monogr. 68, 213–235. Clark, J.S., Silman, M., Kern, R., Macklin, E., HilleRisLambers, J., 1999. Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80, 1475–1494.
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Connor, H.E., 1971. A naturalized Cortaderia (Graminae) in California. Madrono 21, 39–40. D’Antonio, C.M., 1990. Seed production and dispersal in the non-native, invasive succulent Carpobrotus edulis (Aizoaceae) in coastal strand communities of central California. J. Appl. Ecol. 27, 693–702. Delisle, F., Lavoie, C., Jean, M., Lachance, D., 2003. Reconstructing the spread of invasive plants: taking into account biases associated with herbarium specimens. J. Biogeogr. 30, 1033–1042. ENHER, 1993. Atlas eòlic de Catalunya. Generalitat de Catalunya, Departament d’Indústria i Energia. Institut Català d’Energia, Barcelona. Gosálbez, J.N., Serra, J.R., Velasco, E.V., 1994. Els sistemes naturals dels Aiguamolls de l’Empordà. Treballs de la Institució Catalana d’Història Natural, filial de l’Institut d’Estudis Catalans. Num 13. Barcelona. Greene, D.F., Calogeropoulos, C., 2001. Measuring and modelling seed dispersal of terrestrial plants. In: Bullock, J.M., Kenward, R.E., Hails, R.S. (Ed.), Dispersal Ecology. The 42nd Symposium of the British Ecological Society held at the University of Reading. Blackwell Publishing, Cornwall, pp. 3–23. Higgins, S.I., Richardson, D.M., Cowling, R.M., 1996. Modeling invasive plant spread: the role of plant–environment interactions and model structure. Ecology 77, 2043–2054. Houle, G., 1992. Spatial relationship between seed and seedling abundance and mortality in a deciduous forest of north-eastern North America. J. Ecol. 80, 99–108. Kolar, C.S., Lodge, D.M., 2001. Progress in invasion biology: predicting invaders. Trends Ecol. Evol. 16, 199–204. Lambrinos, J.G., 2002. The variable invasive success of Cortaderia species in a complex landscape. Ecology 83, 518–529. Levine, J.M., Vilà, M., D’Antonio, C.M., Dukes, J.S., Grigulis, K., Lavorel, S., 2003. Mechanisms underlying the impact of exotic plant invasions. Philosophical Transactions of the Royal Society of London 270, 775–781. Lonsdale, W.M., 1993. Rates of spread of an invading species—Mimosa pigra in northern Australia. J. Ecol. 83, 513–521. Lloret, F., Médail, F., Brundu, G., Hulme, P.E., 2004. Local and regional abundance of exotic plant species on Mediterranean islands: are species traits important? Glob. Ecol. Biogeogr. 13, 37–45. Mack, R.N., Chair, Simberloff, D., Londsdale, W.M., Evans, H., Clout, M., Bazzaz, F., 2000. Biological invasions: causes, epidemiology, global consequences and control. Issues in Ecology 5. Published by Ecological Society of America. McNeely, J.A., 2001. The Greta Reshuffling. Human Dimensions of Invasive Alien Species. IUCN, Publications Services Unit, Cambridge. Nathan, R., Muller-Landau, H.C., 2000. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15, 278–285. Nathan, R., Safriel, U.N., Noy-Meir, I., 2001. Field validation and sensitivity analysis of a mechanistic model for tree seed dispersal by wind. Ecology 82, 374–388. Okubo, A., Levin, S.A., 1989. A theoretical framework for data analysis of wind dispersal of seeds and pollen. Ecology 70, 329–338. Parker, I.M., Simberloff, D., Lonsdale, W.M., Goodell, K., Wonham, M., Kareiva, P.M., et al., 1999. Impact: toward a framework for understanding the ecological effects of invaders. Biol. Invasions 1, 3–19. Pimentel, D., Lach, L., Zuniga, R., Morrison, D., 2000. Environmental and economic costs of nonindigenous species in the United States. Bioscience 50, 53–65. Rejmánek, M., 2000. Invasive plants: approaches and predictions. Austral Ecol. 25, 497–506. Schupp, E.W., Fuentes, M., 1995. Spatial patterns of seed dispersal and the unification of plant population ecology. Ecoscience 2, 267–275. Stuart, L.P., 1998. Extinction. In: Shuterland, W.J. (Ed.), Conservation Science and Action. Blackwell Science Ltd, Oxford, pp. 20–38. Vitousek, P.M., 1994. Beyond global warming: ecology and global change. Ecology 75, 1861–1876. Willson, M.F., 1993. Dispersal mode, seed shadows, and colonization patterns. Vegetatio 107 (108), 261–280.
Original article
Wind effects on dispersal patterns of the invasive alien Cortaderia selloana in Mediterranean wetlands S. Saura-Mas, F. Lloret * Departament de Biologia Animal, Biologia Vegetal i Ecologia, Center for Ecological Research and Forestry Applications and Unitat d’Ecologia, Universitat Autònoma de Barcelona, 08193 Bellaterra, Barcelona, Spain Received 31 March 2004 Available online 21 January 2005
Abstract Dispersal and establishment of recruits are key steps in the seed invasion process of alien plants. We analysed the effects of wind on the dispersal pattern of Cortaderia selloana, an invasive alien tussock grass in the wetlands of the Mediterranean basin. C. selloana dispersal curves (with QDx values, it is seed density at a given distance from the focal plant) for the four orientations north, east, south, and west, fitted well with exponential negative functions. Strong northern winds had a significant effect on the seed dispersal of C. selloana, so we found a greater number of seeds in the southward focal plants. This wind-orientation effect was found at relatively short distances (from 1 to 20 m), whereas no significant differences were found in orientations at 30 or more meters from the focal plants probably due to the seeds’ decreasing ability to remain in the air. The spatial distribution of recruits showed a similar pattern to that of the seed dispersal, with more recruits in a south orientation. This study demonstrates that wind is a notable factor determining invasive patterns of an anemochorous invasive species such as C. selloana at a local scale. This effect scales up from the dispersal phase to the seedling recruitment stages. © 2005 Elsevier SAS. All rights reserved. Keywords: Seed shadow; Cortaderia selloana; Pampas grass; Wind; Seed dispersal; Mediterranean wetlands; Spatial pattern; Plant recruitment
1. Introduction Human activity around the world has been the most important agent in the recent introduction of a large number of species that have later become biological invasions. Invasions by alien species are one of the global-change factors threatening the conservation of native species and integrity of ecosystems worldwide (Vitousek, 1994; Mack et al. 2000; Levine et al. 2003), with significant economic repercussions (Pimentel et al., 2000; Mc Neely, 2001). This process has impact at different levels, such as genetic contamination (i.e., hybridization), changing population dynamics or modifying community and ecosystem processes (Stuart, 1998; Parker et al., 1999). If we focus on the species traits that correspond with invasiveness, we see that species capable of dispersing widely after introduction processes have a greater tendency to become * Corresponding author. Fax: +34 93 5814151. E-mail address: [email protected] (F. Lloret). 1146-609X/$ - see front matter © 2005 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2004.12.001
invasive (Alpert et al., 2000; Kolar and Lodge, 2001; Lloret et al., 2004). With respect to these attributes of spatial distribution in invasive species, the colonization process depends on the vegetative propagation mode and the seed dispersal patterns (D’Antonio, 1990; Lonsdale, 1993; Higgins et al., 1996; Rejmánek, 2000). Species with structures that favour wind and animal dispersal have better regional and local invasion success (Lloret et al., 2004). At smaller spatial scales, more research is required on the determining factors of dispersal and colonization patterns from an invasion focus, as several models of population expansion have been developed, based on biogeographical information and empirical correlations to environmental variables (Londsdale, 1993; Higgins et al., 1996; Cain et al., 2000; Delisle et al., 2003). Seed shadows provide an estimate of the number of seeds reaching the soil in relation to focal plants and, consequently, they potentially determine the earlier stages of colonization. Although seed shadows have been estimated for a number of species (Carey and Watkinson, 1993; Willson, 1993; Clark et al., 1998), their description for invasive species has generally
130
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been neglected. Wind, in particular, may be a key driver of dispersal patterns for anemochorous species in areas with well-defined dominant winds. Under these conditions, the wind is expected to determine the seed shadow and to influence seedling establishment patterns on a number of spatial scales, from the microsite to the locality. On the other hand, seed dispersal and seedling spatial distribution may not necessarily be correlated, since various ecological factors may limit seed germination compared to seedling survival and establishment (Houle, 1992; Schupp and Fuentes, 1995). In particular, the range of suitable microsites for invasive species would be expected to be very broad, with a low temporal variability in reproductive success and spatial relationship between seed dispersal and seedling survival. Here, we explore wind effects on the seed dispersal and the establishment of recruits from the invasive species Cortaderia selloana in Catalonia. This species, a long-lived perennial grass native to South America, is a common anemochorous alien invasive plant in several types of ecosystems, such as Mediterranean plant communities (Lambrinos, 2002), and it is becoming a major concern in protected wetlands of the Iberian Peninsula. More specifically, we address the following questions: (1) does dominant wind determine seed shadows at the different orientations (north, south, east, and west)? (2) Does the dominant wind determine differences in long-distance dispersal? And, (3) are the spatial patterns of recruit distribution related to the dominant wind?
2. Materials and methods 2.1. Study species and study sites Pampas grass (C. selloana (Schult. & Schult. f.) Asch. & Graebn.) is a large perennial tussock grass which tolerates winter frost, intense sunlight, warm summer temperatures, and moderate drought (Bossard et al., 2000; Lambrinos, 2002). Tussocks can reach 2–4 m in height and 2–3 m in diameter. Their lateral roots can spread up to 4 m in diameter and 3.5 m in depth. Bossard et al. (2000) describe possible vegetative propagation when fragmented tillers receive adequate moisture. However, no evidence of this was observed in the studied population. This plant’s flowering stems can be 3 m in height and its inflorescences consist of attractive densely plumed heads at the end of a stiff stem. C. selloana is considered gynodioecious but functionally dioecious (Connor, 1971). This reproductive performance may limit seed production in isolated individuals. In late summer and early autumn it produces copious amounts of small, wind-dispersed seeds (as many as 106 seeds/individual) (Lambrinos, 2002). The populations seem to be expanding in several localities in the wetlands of north-eastern and central Catalonia (Mathieu, Domènech, personal communications). Most of these localities, such as our study sites, are surrounded by urban developments or cities where C. selloana is common
as an ornamental plant, since it has been commercially cultivated in Europe since 1874. Our study site is Aiguamolls de l’Empordà Natural Park (31T DG 0505 4675 UTM), a Mediterranean protected area, located in the NE of Catalonia, (North-East Iberian Peninsula). Vegetation is mainly dominated by Mediterranean wetlands, including marshes, grasslands, riparian woodlands, and agricultural fields (both in use and abandoned). In this area, C. selloana has a remarkable presence in coastal dunes and abandoned agricultural fields. The climate is Mediterranean, with cool winters, warm summers, and high humidity (annual mean humidity of 72%). The mean annual precipitation at the nearest weather station (Sant Pere Pescador-Alt Empordà) is 715.6 mm. The average annual temperature is 15.1 °C. The mean maximum and minimum temperatures are reached in July (26.6 °C) and January (2.8 °C), respectively. One of the most characteristic features of this protected area is the northern wind or “tramuntana”, which blows throughout the year, including autumn, when C. selloana dispersal occurs (Gósalbez et al., 1994). Concretely, the north-western winds blow 17.1% of hours, northern winds blow 21.4% of hours, and north-eastern winds blow 15.2% of hours (Fig. 1). 2.2. Seed production and seedfall We located nine female adult individuals of C. selloana in different parts of the Aiguamolls de l’Empordà Natural Park, all of them in farms and abandoned fields. Each individual was at least 100 m apart from the nearest neighbour of the same species, so that the effects of other plants on the respective seed shadows were minimal. These individuals were probably established from populations existing in gardens of neighbour urban areas.
Fig. 1. Wind direction distribution (percentage of hours) in Puig-Clapé (sited 15 km from the study site). This station is the closest source of wind distribution data. Hours of calm (wind force less than 2.5 on the Beaufort scale) are indicated in the central box. Source: ENHER, 1993.
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Each plant was surrounded by eight seed traps set at various distances from the focal plant (0.5, 1, 3, 5, 10, 20, 30, and 40 m) in four directions (north, south, east, and west), that is a total of 32 traps per focal plant. Seed traps were set on the floor and consisted of a flat tray with a sticky paper (0.285 × 0.19 m) on the bottom and a wire mesh (0.02 m diameter) on top to repel predators and prevent the possible death of any small vertebrate that might enter the trap. The mesh was coarse enough to allow the passage of seeds (Greene and Calogeropoulos, 2001). Seed traps were set up from 27th September to 27th December 2002 (92 days), and they were surveyed three times during this period, until the seed rain stopped. Some values proved accidentally unavailable due to the temporary loss of a seed trap. We estimated the seed production of each plant by correlating the length of the inflorescences of the plant with the seed production. We used inflorescence length as a nondestructive descriptor of seed production. The parameters for this correlation were obtained by sampling one inflorescence from 30 plants from neighbouring populations. We randomly selected ca. 0.2 g piece of each inflorescence, and we counted the number of seeds of each piece. Then, we correlated the number of seeds to the biomass of inflorescence piece. We estimated the total number of seeds to the whole inflorescence according to the total inflorescence’s biomass. Finally, we correlated the number of seeds to the inflorescence’s length. 2.3. Spatial distribution of recruits We surveyed the presence of recruits around each of the focal plants used to estimate seed shadows by surveying four 40 × 1 m transects oriented towards north, east, south, and west. We also surveyed recruits around non-isolated plants from the populations in the locality of La Rubina, a coastal dune area within the Park, and the only population inside the studied area with established recruits. We chose as focal plants all the adult and flowering individuals that were separated by at least 6 m from the nearest adult (n = 11). A criterion of longer distances would have precluded the possibility of finding enough plants for the survey. We surveyed recruits within a circle with a radius of 3 m around the focal adult plants. We considered as recruits those individuals with a canopy diameter of less than 1 m that had not had any inflorescences during the flowering period. We did not survey beyond a distance of 3 m to minimize surveying recruits from other focal plants. Although these distance, do not avoid completely the overlapping of seed shadow from different plants, most seed rain was expected to occur at a closer distance from focal plants. We measured plant height, distance to the nearest adult and the orientation (azymuth) in relation to the focal plant. 2.4. Data analysis We analysed differences in seed shadow in relation to distance and orientation from parent plants by a Repeated Mea-
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sures ANOVA model with two within-subject factors (distance and orientation) and the number of collected seeds as the dependent variable (after log (x + 1) transformation). Seven levels of distance (0.5, 1, 3, 5, 10, 20, and 30 m) and four levels of orientation (north, east, south, and west) were considered. Vandalism caused some missing values. We excluded from the analysis three plants with missing values. Data from traps at a distance of 40 m were also excluded from this analysis due to missing field values. Missing field values made it impossible to perform a complete design. We therefore made a separate analysis of the effect of orientation on collected seeds at each distance (0.5, 1, 3, 5, 10, 20, 30, and 40 m) by Repeated Measures ANOVA with one within-subject factor (orientation). Plants with missing field values were excluded from the analysis of each distance (see Table 1 for the number of plants used in each case). Differences on collected seeds (after log (x + 1) transformation) between orientations (north, east, south, and west) were analysed by Fisher’s PLSD post-hoc tests (significance values are shown in Fig. 2). The dispersal curve (with QDx values) was calculated as the density of seeds deposited at a given distance from the focal plant and it was estimated for each orientation. QDx values (seeds m–2) (Greene and Calogeropoulos, 2001) were obtained by the mean of collected seeds and weighted according to the estimated seed production of each plant. In order to facilitate comparisons to other studies, QDx values were were standardized by considering that the number of seeds produced by a plant is equal to 100,000, (Greene and Calogeropoulos, 2001). QDx dispersal curves were fitted to negative exponential functions for all the orientations (Table 2). For the analysis of the spatial pattern of recruits, the orientation azymuth values were categorized in one of the four orientations: north (from 316° to 45°), east (from 46° to 135°), south (from 136° to 225°) and west (from 226° to 315°). The independence of occurrence with respect to orientation was analysed by a v2 test. Statview 4.5 (Abacus concepts) and Kaleida Graph 3.08 (Synergy Software) programmes were used for the computation of analyses. When necessary, data were transformed to meet the assumptions of parametric analysis. Table 1 Summary table of repeated ANOVA measurements (one within factor variable) for the differences in the number of seeds collected in different orientation (North, East, South, and West). For each distance, the number of plants (n) available for the analysis is also indicated Distance (m) 0 1 3 5 10 20 30 40
n 9 8 8 9 9 8 7 4
F 2.70 12.27 5.03 5.35 9.23 3.48 0.88 0.02
P-value 0.0681 0.0001 0.0088 0.0058 0.0003 0.0341 0.4700 0.9960
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No recruits were found around the nine focal plants used to establish seed–shadow curves. Recruit distribution around plants in the population of “La Rubina” was not independent of the orientation (v2 = 12.85, p < 0.05, df = 3). Most of the seedlings (53%) were distributed at the south orientation, while 18% were at the north and 14% at both the east and west orientations.
4. Discussion
Fig. 2. Dispersal curves obtained from mean QDx values for each orientation (North, East, South, and West). * Collected seeds were different in South orientation than in East & West orientations, but not from North (P < 0.05 Fisher’s PLSD post-hoc test, log (x + 1) transformation). ** Collected seeds were different in South orientation than the other three directions (P < 0.05 Fisher’s PLSD post-hoc test, log (x + 1) transformation). ns = no significant differences between orientations. Note that dispersal curves and significance descriptions refer to two different variables: QDx (seed density at given distance) and collected seeds in traps, respectively.
3. Results The estimated mean production of seeds for the nine focal plants was 416,399 seeds per plant (SD = 265,744.76), ranging from 54,567 to 840,905 seeds per plant. Dispersal curves were obtained using QDx values for each one of the four orientations. Seed shadow in the south direction was significantly different from the other orientations (F3,15 = 8.09, p = 0.002) (Fig. 2). The number of collected seeds at the distances of 1, 3, 10, and 20 m was significantly higher in the south direction than in the other ones (see Fig. 2 for details), while no significant differences between orientations were observed at 0.5, 30, or 40 m (Fig. 2, Tables 1 and 2). The distance from the focal plant significantly reduced the number of seeds reaching the soil (F6,30 = 13.02, p < 0.0001). This pattern was observed in all the orientations, as indicated by the non-significant interaction between orientation and distance (F18,90 = 1.22, p = 0.26). In all the orientations there was a leptokurtic curve, which was successfully fitted to a negative exponential function (Table 2). Table 2 Exponential negative curve fit (y = a × e(–bx)) for table values for the different orientations (North n = 68, East n=67, South n = 70, West n = 66). Significance values are shown by asterisks; *, P < 0.05; **, P < 0.01; ***, P < 0.001 a b r Significance
North 909.3 1.958 0.287 *
East 7154.5 3.391 0.343 **
South 350.8 0.196 0.503 **
West 6504.5 3.633 0.336 ***
Wind effects have been found to determine the spatial pattern of trees and grass species (Okubo and Levin, 1989; Carey and Watkinson, 1993; Nathan et al., 2001). Our study site is characterised by significant periods of northern winds throughout the year (Fig. 1) that clearly determine the seed dispersal patterns of C. selloana. This effect was detected at intermediate distances from the focal plant (1–20 m), while most of the seeds collected at 0.5 m probably fell down due to gravitation. There were no wind effects at distances of more than 20 m. Okubo and Levin (1989) have described models that illustrate how dispersal distances from a source depend on factors such as wind speed and other physical agents. Our results suggest that wind effects decline with distance due to the seeds’ decreasing ability to remain in the air. In addition, density is expected to decrease with distance because of the dilution effect due to the quadratic increase of surface with distance. Therefore, the number of sampling points at longer distances may have been too low to detect any differences between the orientations when the density of seeds reaching the soil is very low (Clark et al. 1999; Cain et al. 2000). In addition, at longer distances from a given focal plant, the interference with seed shadows from other plants may reduce the directional effect of wind on the distribution of the seed rain. Seed–shadow curves have frequently been fitted into a 2Dt model (Clark et al., 1999; Nathan and Muller-Landau, 2000; Greene and Calogeropoulos, 2001). The use of the 2Dt curve did not seem to be the best solution in our case, since there was no evidence of convexity at the source (Clark et al. 1999). In fact, we obtained a satisfactory fit to an exponential negative function for all the four orientations. Lambrinos (2002) demonstrated how a set of environmental factors such as precipitation, soil disturbance, mammalian herbivory, and resource availability influenced the invasive establishment of C. selloana in central California. Anyway, the absence of recruits around the focal plants used to estimate seed shadow may be the result of the low number of viable seeds in female isolated individuals, in which low levels of fecundation are expected. Bossard et al. (2000) observed that viable seed only occurs in C. selloana populations of California when both female plants and plants with perfect flowers are present. Notwithstanding the difficulties in making a simple analysis of the origin of recruits in dense populations, the spatial pattern of C. selloana recruits in the La Rubina population reflects the effect of dominant winds not only on seed dispersal but also on seedling establish-
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ment. In spite of the large production of seeds, we observed that well-established seedlings were very rare in this area, in agreement with previous observations in populations from California (Lambrinos 2002). As a result, microsite suitability would also play an important role in C. selloana recruitment, probably due to the dense cover of herbaceous vegetation in many abandoned agricultural fields. We therefore expect that the strong wind effect on seed dispersal would become progressively diluted in the later stages of the recruitment process. 5. Conclusion In conclusion, we have observed that the spatial pattern of seed dispersal by the invasive C. selloana on a local scale is determined by physical drivers, such as wind orientation (when a clearly dominant wind exists). This influence is relevant in the seed dispersal process and remains so up to the establishment of new individuals. However, no evidence of this effect has been found at distances longer than a few meters from focal plants. Our study approaches the questions of how wind determines seed dispersal of the invasive C. selloana from 1 to 20 m and of how this effect is still present in recruits’ spatial patterns. Finally, this study provides information about the invasiveness and spatial dispersal of C. selloana, an invasive species which is considered to produce alterations, especially to Mediterranean wetlands ecosystems. Acknowledgements We would like to thank M. Vilà and R. Domènech for their suggestions during the course of the study. Ll. Benejam, A. Saperas and M. Mas helped in the fieldwork. We are grateful to the officers of the Aiguamolls de l’Empordà Natural Park and, particularly, S. Romero for their support and permission to use the facilities. This study was funded by the CICYT project REN2000-0361 and by a grant from the Ministry of Education to S. Saura-Mas. References Alpert, P., Bone, E., Holzapfel, C., 2000. Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Urban & Fisher Verlag. Perspect. Plant Ecol. Evol. Syst. 3, 52–66. Bossard, C.C., Randall, J.M., Hshousky, M.C., 2000. Invasive Plants of California’s Wildlands. University of California, Berkeley, LA. Cain, M.L., Milligan, B.G., Strand, A.E., 2000. Long-distance seed dispersal in plant populations. Am. J. Bot. 87, 1217–1227. Carey, P.D., Watkinson, A.R., 1993. The dispersal and fates of seeds of the winter annual grass Vulpia ciliata. J. Ecol. 81, 759–767. Clark, J.S., Macklin, E., Wood, L., 1998. Stages and spatial scales of recruitment limitation in southern appalachian forests. Ecol. Monogr. 68, 213–235. Clark, J.S., Silman, M., Kern, R., Macklin, E., HilleRisLambers, J., 1999. Seed dispersal near and far: patterns across temperate and tropical forests. Ecology 80, 1475–1494.
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