2010 SOUTHEASTERN NATURALIST 9(2):259–274 The Effect of Shrubs on the Establishment of an Endangered Perennial (Asclepias curtissii) Endemic to Florida Scrub Patrick Mondo1, Kristen D. Marshall Mattson2, and Cynthia C. Bennington1,* Abstract - Asclepias curtissii (Curtiss’ Milkweed) is an endangered perennial herbaceous plant endemic to Florida scrub habitat. Although many scrub perennials are gap specialists, Curtiss’ Milkweed is often found growing in close association with woody vegetation. We asked whether seed germination and seedling establishment are enhanced by the microsite conditions created beneath woody shrubs. In addition, we asked whether adult plants occur in association with shrubs more frequently than would be expected by chance and whether this distribution could be explained by seed dispersal patterns. Seeds were germinated, ex situ, in a factorial experiment with leaf litter and shade as main effects. In a separate experiment, to determine the effect of shrub cover on seedling establishment, 144 Curtiss’ Milkweed seedlings were planted into a total of twelve fenced plots within Lyonia Preserve, Deltona, fl. Within each plot, six seedlings were planted in sandy gaps, and six were planted in close association with existing woody shrubs. We assessed survival over a five-month period. We also measured the distance to the nearest woody stem from extant adult plant locations and compared these to the distance of random points around those extant plants. Similarly, we released 70 milkweed seeds from extant plant locations and measured the distance from the spot where they landed to the nearest woody stem and compared this to the distance between random points and woody stems. We found that seed germination was significantly enhanced by shade (P < 0.0001) but not by leaf litter, and that seedlings growing in the shade of close neighboring shrubs had significantly higher rates of survival (P < 0.001) than those seedlings planted in gaps. Extant plants tended to grow close to shrubs, and seeds tended to land near shrubs, but neither of these distances were less than would be expected by random chance (P > 0.10 in both cases). The facilitation of seedling establishment by woody plants has been documented in other arid environments, but not in Florida scrub. Introduction Facilitative or positive interactions among individuals of different plant species can influence community composition (Bertness and Callaway 1994) through positive effects on individual plant growth and survival (see reviews in Brooker et al. 2008, Callaway and Walker 1997). For an interaction between two plants to be considered facilitative, the competitive effects of the heterospecific neighbor must be outweighed by the positive effects of the microenvironment created by that neighbor (e.g., Holmgren et al. 1997). 1Department of Biology, Campus Box 8264, Stetson University, DeLand, fl32723. 2The LowCountry Institute, 40 Mobley Oaks Lane, Okatie, SC 29909. *Corresponding author - cbenning@stetson.edu. 260 Southeastern Naturalist Vol. 9, No. 2 The best-known examples of the positive effects of “nurse plants” come from studies of seedling establishment in desert succulents (e.g., Cody 1993, Franco and Nobel 1988, Jordan and Nobel 1979, McAuliffe 1984, Shreve 1931, Turner et al. 1966). Subsequent studies have centered on arid and other stressful environments, with the expectation that the positive effect of plant neighbors will increase, relative to competitive or negative interactions, with increasing abiotic stress (e.g., Bertness and Callaway 1994, Callaway and Walker 1997, Callaway et al. 2002, Tewksbury and Lloyd 2001). Although some experiments have failed to find evidence for increasing facilitation with increased stress (e.g., Riginos et al. 2005, Smit et al. 2007, Tielbörger and Kadmon 2000), facilitative interactions among plants have been documented in stressful environments such as tundra (Callaway et al. 2002) and dry grasslands (Greenlee and Callaway 1996) in addition to deserts. Established adult plants can buffer new recruits against environmental extremes in a variety of ways (Bertness and Callaway 1994). In xeric habitats, nurse plants can provide microhabitats in which stress experienced by a seedling is reduced through increased shade (Franco and Nobel 1989) and reduced transpiration losses (Prider and Facelli 2004), increased nutrient availability through increased litter deposition (Callaway et al. 1991, Franco and Nobel 1988, Shumway 2000), or protection from herbivory (McAuliffe 1986, Rousset and Lepart 2000, Smit et al. 2007). Occurring on well-drained, sandy, nutrient-poor soils (Myers 1990), Florida scrub is a xerophytic ecosystem in which many of the same environmental stresses that account for facilitation in desert ecosystems may be found. Because scrub is a pyrogenic ecosystem, however, there are two important differences that could affect facilitative interactions. First, frequent disturbance through fire results in significant temporal variability in the size and spatial distribution of plants (e.g., Menges and Hawkes 1998). Thus, the aboveground canopy provided by a nurse plant may be highly variable over a relatively brief time period. Secondly, the high-intensity fires that are common in scrub can create open sandy patches in what can otherwise be a dense competitive community. For this reason, the literature on perennial plant distribution and seedling establishment in this ecosystem has emphasized the importance of gaps (e.g., Hawkes and Menges 1996, Johnson and Abrahamson 1990, Menges et al. 2008, Petrü and Menges 2003, Weekley and Menges 2003). Hawkes and Menges (1996) found that 55% of variation in herbaceous plant density was explained by the presence of open space in scrub habitat. In addition, a number of scrub perennials appear to be gap specialists (Menges and Hawkes 1998, Menges and Kimmich 1996, Menges et al. 1999, Petrü and Menges 2003, Quintana-Ascencio and Morales-Hernandez 1997). The association of herbaceous species with gaps has been observed in other dry shrublands as well (e.g., Shmida and Whittaker 1981). These gaps may provide space free of competition for light, nutrients, or water (Forseth et al. 2001, Hawkes and Menges 1996, Weekley and Menges 2003). 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 261 Here, we assess the facilitation by shrubs, if any, in the establishment of an endangered plant, Asclepias curtissii Gray (Curtiss’ Milkweed), endemic to Florida scrub (Coile and Garland 2003). Putz and Minno (1995) reported that Curtiss’ Milkweed plants tend to be found along roadsides, but they were unable to explain adult plant distribution based on the amount of shrub cover or bare soil. Our casual observations at one field site, however, suggested that Curtiss’ Milkweed tends to be found growing amongst shrubs and, unlike some other scrub perennials, is unlikely to be found in open gaps. We tested the hypothesis that facilitation by shrubs is occurring in this species by asking: 1) are seed germination and early seedling establishment positively affected by the microsite provided by a shrub canopy?, 2) are adult plants, in fact, found in association with shrubs more often than expected by chance?, and 3) could such an association be explained by the retention of wind-dispersed seeds by shrubs? Methods Study species Curtiss’ Milkweed is a long-lived perennial that dies back to the tap root each fall and resprouts in spring (Putz and Minno 1995; C.C. Bennington, pers. observ.). In our population, we have observed aboveground shoots typically persisting into October and new shoots appearing in early April. In addition, plants frequently resprout several times during the growing season following herbivory by an animal (based on fecal evidence, we suspect rabbits) that clips the stem back to the ground. Anecdotal evidence presented by Putz and Minno (1995) suggests that individual plants can live 25 years or more. While they have opposite leaves, the foliage of adult plants generally resembles that of the scrub oaks, making plants very cryptic when not in flower. Flower production typically begins in June and reaches a peak in late July (Putz and Minno 1995; C.C. Bennington, pers. observ.). The flowers of Curtiss’ Milkweed are visited by a variety of insects, including a large number of skipper butterflies (Putz and Minno 1995; C.C. Bennington, pers. observ.). Most members of the genus Asclepias are self-incompatible or show inbreeding depression (Ivey et al. 1999, Lipow et al. 1999), but the breeding system of Curtiss’ Milkweed has not been investigated. In our population, individual plants frequently produce a large number of flowers (mean = 152.2, s.d. = 110.1, n = 22, in 2006), but the proportion that set fruit can be quite low (mean = 0.018, s.d. = 0.029, n = 22). We have not attempted to quantify spontaneous seedling recruitment at our field site, and the cryptic nature of the plants makes them difficult to spot through casual observation, but we have only recorded three seedling recruits in five years. Field site description Lyonia Preserve, located in Volusia County, fl(28°55'N, 81°13'W), is a 146-ha area of preserved scrub habitat surrounded by suburban development. 262 Southeastern Naturalist Vol. 9, No. 2 The dominant woody species include three species of oak (Quercus geminata Small [Sand Live Oak], Q. myrtifolia Willd. [Myrtle Oak], and Q. chapmanii Sarg. [Chapman Oak]), Lyonia ferruginea (Walt.) Nutt. (Rusty Lyonia), Ceratiola ericoides Michx. (Florida Rosemary or Sand Heath) and, in some sections, Pinus clausa (Chapman ex Engelm.) Vasey ex Sarg. (Sand Pine). Before the first restoration activity in 1994, the site was dominated by Sand Pine and scrubby oaks. At that time, a variety of methods (i.e., controlled burning, root raking, roller chopping, and harvesting) were used to remove the large trees and to encourage the regeneration of scrub shrubs. The area continues to be managed to maintain a scrub community that likely existed on the site prior to human habitation of the area. Seed germination In the fall of 2004, we recovered between 40 and 99 seeds per follicle from eight different parent plants, for a total of 512 seeds. At the same time, we collected field soil and filled thirty-two 6-cm2 plastic cells in each of sixteen 26-cm x 53-cm plastic trays. One seed was added to each plastic cell with no attempt made to ascertain viability prior to planting. Within each flat, half of the cells were randomly assigned to a “litter” treatment. In these cells, litter (mostly leaves, twigs, and organic matter) collected from Lyonia Preserve was scattered to a depth of approximately 1 cm. On 29 October 2004, plastic flats were moved from the greenhouse to a sunny, grassy field on the Stetson University campus. Once in place, 8 of the 16 flats were randomly assigned to a shade treatment. Shade cloth that reduced light by 50% was placed 10 cm above each of those eight trays in the shade treatment. For the first five weeks, trays were supplementally watered to keep the soil moist and to prevent water availability from limiting germination. Trays remained in their original positions throughout the six months of the experiment. Between 29 October and 3 December 2004, cells were censused every three or four days for germination. Between 3 December and 15 May 2005, trays were censused once every two weeks. Because it is possible that a seed germinated during this time but that the seedling died before being detected in a census, we recognize that any effects we observed could have been due to very early seedling mortality, rather than a lack of germination. Seedling transplants Seeds of Curtiss’ Milkweed were collected from mature follicles of three plants in the fall of 2006 and 2007. Seeds from both collection years were germinated in pots containing soil brought back to the greenhouse from Lyonia Preserve. In December 2007, seedlings were transplanted into Cone-tainers (4 cm diameter by 20 cm depth; Stuewe and Sons, Corvallis, OR) in field soil. In March 2008, seedlings were transplanted into plots in Lyonia Preserve. We transplanted 144 plants into twelve 3-m x 2-m plots, surrounded by 1-m tall plastic fencing to reduce mammalian herbivory. All of the plots were located along the edge of a sandy gap, and plots were 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 263 oriented so that one half (3 m x 1 m) had woody vegetation providing shrub cover while the other half lacked woody vegetation (Fig. 1). Within each half of the plot, seedlings were spaced 0.5 m apart. The number of aboveground Curtiss’ Milkweed seedlings remaining was evaluated five times between March 2008 and August 2008. We performed a final census in May 2009 to determine which plants had successfully overwintered and resprouted. In June 2009, we measured soil temperature at one point under shrub cover and one point in open sand in each of the twelve plots using a Li-Cor 1000 data logger (Li-Cor, Lincoln, NE). At those same points, we collected soil samples to a depth of 8 cm. All data were collected in the morning of a single day following a week of typical afternoon showers. Soil samples were weighed to the nearest 10 mg and then dried at 60 °C for one week before being reweighed. The difference between weights was used to calculate percent soil-water availability. Adult plant locations We have monitored the population of adult Curtiss’ Milkweed plants since 2004 and continue to do so. Although not every plant can be found as an adult in each year, we have documented over 50 plant locations over five years. We measured the distance to the nearest woody stem (herein referred to as DNWS) from the stem of the Curtiss’ Milkweed plant for each plant for which an aboveground shoot was identified in the summer of 2008 and for which the flag and tag remained intact through the fall of 2008 (n = 29). To determine whether plants are closer to woody shrubs than would be expected Figure 1. Diagram of the 3-m x 2-m fenced plots used in the survivorship experiment. The shaded area represents the portion of the plot that had natural shrub cover. The other half of the plot lacked woody vegetation. 264 Southeastern Naturalist Vol. 9, No. 2 by chance, we also recorded DNWS for four random points within a 3-m radius of each extant plant. Although many of our plants are located along trails, we did not include random points that fell within a trail or sand road. Seed dispersal Seeds from three different Curtiss’ Milkweed follicles were used to determine whether seeds are more likely to land and settle near a shrub than in open sand. To perform this portion of the study, we chose seven extant plant locations that included a mixture of open sand and closed shrub canopy. At each of these sites, we placed one to three seeds at a time on the open palm of a hand held at approximately 1 m above the soil surface until the wind took them. Wind speeds varied from 3–9 km/hr for these trials. We followed each seed for 10 minutes, being careful not to interfere with its movement. At the end of 10 minutes, we marked the final resting place of each seed with a wire stake flag. If the plume was still attached, we collected the seed and reused it. Once 10 seeds had been released from a particular location, the DNWS for each was recorded. To determine whether DNWS for dispersed seeds was less than would be expected by chance, we determined DNWS for random points that were within the observed range of seed resting places given the wind speed and direction at the time. Thus, rather than considering the entire area within a circle with 3-m radius around a plant as possible sites, we only considered points that were within the seed shadow that contained all 10 of the seed landing sites. Approximately every 30° in the arc, we extended a transect to the distance travelled by the farthest-flying seed at that site. At five random points along each of these transects, we measured DNWS. Statistical analysis To determine the effect of shade and leaf litter on seed germination, we calculated percent germination for each of the litter treatments within each tray. Percentages were transformed using the arcsine square root to improve normality. A two-way analysis of variance (JMP, ver 6.0.2, SAS Institute Inc., Cary, NC) was conducted to determine the effect of light, litter, and their interaction on germination. For each of the dates for which we surveyed seedling presence in the 12 fenced plots, we conducted a loglikelihood test (JMP, ver 6.0.2, SAS Institute Inc., Cary, NC) with main effects of plot and cover (shrub cover versus open sand). We used paired t-tests (JMP, ver 6.0.2, SAS Institute Inc., Cary, NC) to compare soil temperature and soil moisture between shrub cover and open sand microsites within the twelve plots. We also used paired t-tests to determine whether: a) adult plants tend to occur closer, and b) hand-dispersed seeds tend to land nearer to woody shrubs than expected by chance. To compare DNWS between extant adult plant locations and random points within a 3-m radius, we paired the DNWS for each plant and the average DNWS for the four random points sampled at 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 265 the same plants. For the seed-dispersal experiment, the average DNWS for the 10 seeds dispersed at each of the seven plant sites was paired with the average for the random points sampled within the dispersal shadow at each of those sites. In both cases, we used one-tailed tests since we predicted both adult plants and seeds to be closer to shrubs than random points. Results Of the 512 seeds that were planted in October 2004, only 36 had germinated at the end of five weeks. By 15 May 2005, however, a total of 111 of the 512 seeds had germinated. Eighty-five of these 111 seeds were in the shade treatment, representing a significant positive effect of shade on germination (F1,28 = 54.8, P < 0.0001; Fig. 2). Litter did not affect germination rate (F1,28 = 0.68, P = 0.41), and there was no differential effect of litter between light treatments (shade x litter interaction: F1,28 = 0.73, P = 0.40). Shrub cover had a strong positive effect on seedling survival in the field (Table 1). Percent survival of seedlings was approximately ten times greater under the shrub canopy than in the open sand throughout the months following their transplant (Fig. 3). At the final census, more than one year after transplant, only two of the 22 seedlings that survived more than one year were from the open sites within plots. Soil temperatures were, on average, Figure 2. Average percent germination (± 1 s.e.) of Curtiss’ Milkweed seeds planted into field soil in individual cells of 16 plastic trays, eight of which were covered with 50% shade cloth. In each tray, the seed and soil in 16 of the 32 cells was covered with leaf litter to a depth of 1 cm. 266 Southeastern Naturalist Vol. 9, No. 2 2.85 °C warmer and soil moisture was approximately 5% lower in microsites with open sand compared to those under shrub canopy in our seedling transplant plots (Table 2). Although our initial observations led us to hypothesize that Curtiss’ Milkweed plants tend to occur close to shrubs, we were unable to demonstrate Table 1. Results of log-likelihood tests comparing aboveground presence of Curtiss’ Milkweed seedlings planted under shrub cover or in open sand in each of 12 fenced plots at each of six census dates. This is a conservative estimate of survival since some individuals were counted as dead (not aboveground) at one census date prior to 31 August 2008, but then resprouted to be found aboveground in the following census. At the final census, all plants found aboveground were also aboveground in August of the previous year. χ2 (P-value) Effect d.f. 5/16/08 5/30/08 7/09/08 Plot 11 18.14 (0.08) 18.82 (0.06) 22.81 (0.02) Habitat 1 56.03 (0.0001) 56.39 (0.0001) 38.60 (0.0001) χ2 (P-value) Effect 8/01/08 8/31/08 5/15/09 Plot 19.31 (0.06) 16.46 (0.12) 29.66 (0.01) Habitat 41.58 (0.0001) 29.53 (0.0001) 23.29 (0.0001) Figure 3. Percent aboveground presence of Curtiss’ Milkweed seedlings transplanted into plots in either open sandy areas or under a shrub canopy. This graph presents a conservative estimate of survival because several plants died back to the tap root and then resprouted between censuses. Log-likelihood tests at each of the six census dates following transplant revealed significantly higher remaining seedlings among those planted under shrub cover (P < 0.001 in all cases). 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 267 that this association is greater than would be expected by chance. While the average distance from an extant milkweed plant to the nearest shrub was less than the average distance between random points and the nearest shrub, this difference was not significant (Table 3). Furthermore, the wind-dispersed seeds of Curtiss’ Milkweed tended to settle close to shrubs, but this difference was not greater than would be expected by chance (Table 3). Discussion We found strong evidence for facilitation of Curtiss’ Milkweed seed germination and seedling establishment by the shrubs of Florida scrub. Previous studies in stressful environments have demonstrated positive effects of nurse plants through the amelioration of extremes in soil fertility, water availability, temperature, and light (see reviews in Brooker et al. 1998, Callaway 1995). In Florida scrub, where soils are characterized by low fertility (e.g., Kalisz and Stone 1984), leaf litter that accumulates beneath shrubs may enhance nutrient levels (e.g., Callaway et al. 1991). Litter tends to build up under shrubs of Florida scrub (Schmalzer and Hinkle 1996), and nitrogen levels have been demonstrated to be higher under shrub canopy than in gaps in this ecosystem (Maliakal-Witt et al. 2005). We found no evidence for a positive effect of leaf litter on seed germination, but did not measure litter depth or nutrient levels in our seedling transplant plots. However, while increased soil fertility under shrubs may provide positive effects on seedling growth (e.g., Armas and Pugnaire 2005, Carlsson and Callaghan 1991, Gomez-Aparicio et al. 2005, Moro et al. 1997, Pugnaire et al. 2004, Tirado and Pugnaire 2003), seedling survival of plants with a well-developed tap Table 3. Average distance to the nearest woody stem (DNWS) for a) extant adult Curtiss’ Milkweed plants and random points within a 3-m radius of the plants and b) landing sites of handdispersed Curtiss’ Milkweed seeds and random points within the area of the dispersal shadow. Average DNWS (cm) Paired t-test (± 1 s.d.) results Plant locations Adult plant position 17.62 (± 14.28) t6 = 0.90, Prob > t = 0.19 Random points (within 3-m radius around plants) 20.52 (± 10.85) Seed dispersal Seed landing point 17.35 (± 12.87) t6 = 0.85 Prob > t = 0.22 Random points (within seed dispersal shadow) 19.05 (± 13.28) Table 2. Average soil temperature and soil water availability under shrub canopy and in open sand within 12 plots that incorporated both microsites. Microsite Soil temperature (°C) (± 1 s.d.) Soil moisture (%) (± 1 s.d.) Open sand 30.67 (± 2.89) 4.4 (± 0.022) Shrub canopy 27.82 (± 1.80) 9.6 (± 0.042) Paired t-test results t11 = 4.11, P = 0.002 t11 = 3.89, P = 0.003 268 Southeastern Naturalist Vol. 9, No. 2 root such as Curtiss’ Milkweed is unlikely to be significantly affected by soil nutrient levels. The presence of nurse plants may also benefit seedlings through protection against the effects of herbivory (Acuña-Rodríguez et al. 2006, Garcia et al. 2000, Graff et al. 2007, Jaksic and Fuentes 1980, McAuliffe 1986, Rebollo et al. 2005, Rousset and Lepart 2000), but we eliminated the possibility that a reduction in herbivory could be responsible for any observed facilitation in this study by fencing our seedling plots. The seedlings in this experiment originated from just three maternal plants and therefore represent a potentially small fraction of the genetic variability in the population. It is possible that seedlings from a greater number of parents would reveal increased variability in the response to nurse plants. However, at least for the genotypes we investigated, there were very large positive benefits to establishing under shrub cover. The results of the seed germination experiment suggest that shading by shrubs is the most likely explanation for the positive effect of shrub cover in this study. This effect, however, could be a result of a decrease in solar radiation and reduction in photo-inhibition (Armas and Pugnaire 2005, Egerton et al. 2000) or due to an associated reduction in soil temperature and evaporation (Franco and Nobel 1988, Prider and Facelli 2004, Turner et al. 1966, Valiente-Banuet and Ezcurra 1991). Under shade cloth in our seed germination experiment, reductions in evaporation may have increased water available to germinating seeds and new seedlings, resulting in the positive effect that we observed. Although increases in soil water availability under shrub canopy have been measured in natural communities (Castro et al. 2004a, b.; Egerton et al. 2000; Holzapfel and Mahall 1999; Pugnaire et al. 2004), previous research in Florida scrub suggests that soil moisture may be either lower (Marshall Mattson and Putz 2008) or higher (Maliakal-Witt et al. 2005, Weekley et al. 2007) in gaps than under shrub cover depending upon the relative rates of transpiration and evaporation. While we only measured soil moisture and temperature at one point during one rainy season, our data suggest that young seedlings establishing under a shrub canopy would experience higher water availability and lower temperatures than to those growing in open sand. This difference may be a result of reduced evaporation coupled with an increased accumulation of organic matter under shrubs and consequent improvements in water-holding capacity (e.g., Armas and Pugnaire 2005, Pugnaire et al. 2004). Given that Florida has distinct wet and dry seasons, the facilitative effects of shrubs on seedling establishment may be temporally variable. In dry months, transpiration rates that exceed precipitation inputs may reduce soil water availability beneath the shrub canopy such that the facilitative effects of shrubs on Curtiss’ Milkweed seedlings are lost, or become competitive effects. Not only can temporal variability in the physical environment shift the effect of shrubs from facilitative to competitive (Greenlee and Callaway 1996, Ibáñez and Schupp 2001, Kitzberger et al. 2000, Tielbörger 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 269 and Kadmon 2000), but, in this fire-adapted community with fire-return intervals ranging from 15 to 100 years (Myers 1990), the shrub canopy can be variable in both spatial pattern and size over time (Menges and Hawkes 1998, Petrü and Menges 2004). Unlike desert habitats where established shrubs are very persistent, and nurse plant effects are likely to be observed in the current distribution of adult plants, the shifting shrub canopy typical of Florida scrub may be responsible for the fact that our data on the current distribution of adult plants appears to provide little or no information on the effects of facilitation. Because both Curtiss’ Milkweed and the majority of dominant scrub shrub species at our study site resprout following fire or other disturbance, and because individual milkweed plants and shrubs may live for more than twenty years, the presence and size of the current shrub canopy may differ substantially from that which was present at the time of seedling establishment. Thus, our measures of the distance from an extant adult plant to the nearest woody stem do not likely reflect the distance that existed at the time of seedling establishment. Furthermore, if the benefit of the shrub canopy changes over the course of the life span of Curtiss’ Milkweed (Callaway and Walker 1997, Cody 1993, Holzapfel and Mahall 1999, Rousset and Lepart 2000), extant plant distribution may reflect both the environmental history of the site as well as the age of an individual and the life history of the species. While fire-created gaps benefit the establishment and survival of some endemic scrub perennials (Hawkes and Menges 1996, Menges and Kimmich 1996, Petrü and Menges 2003, Weekley and Menges 2003), we found that A. curtissi germination and seedling establishment are positively affected by the presence of a shrub canopy. The taproot and long narrow leaves of Curtiss’ Milkweed seedlings suggest that this species is well-adapted to establishment in the hot, sunny, dry conditions characteristic of Florida scrub. Even so, the large, positive effect of shrubs on seedling survival distinguishes Curtiss’ Milkweed from the many scrub perennials that benefit from gaps (e.g., Hawkes and Menges 1995, Menges and Kimmich 1996, Menges et al. 2006, Quintana-Ascencio and Morales-Hernandez 1997, Quintana-Ascencio et al. 2003). Although we have not yet investigated the effect of shrubs on the subsequent growth and reproduction of adult milkweed plants, the same environmental factors that benefit seedlings (i.e., increased leaf litter, increased water availability, decreased soil temperatures, and decreased herbivory) may also benefit adult plants. For example, mammalian herbivory is common at our study site (C.C. Bennington, pers. observ.), and we previously quantified a positive effect of mammalian herbivore exclusion (using wire mesh cages) on Curtiss’ Milkweed reproduction (C.C. Bennington, unpubl. data). Ongoing studies are aimed at determining the extent to which shrubs afford protection from herbivores. Alternatively, facilitative effects of shrubs may diminish over the life span of the plant. Benefits of shrubs to Curtiss’ Milkweed seedlings may become negative effects on growth and reproduction of 270 Southeastern Naturalist Vol. 9, No. 2 adult plants if shade limits plant growth and/or flower and fruit production or if the physical structure of shrubs reduces pollinator visitation or the ability of seeds to disperse away from the parent plant. Weekley and Menges (2003) found no evidence that fire affects adult survival of Curtiss’ Milkweed, but long-term studies are needed to determine whether changes in the shrub layer affect growth and reproduction in adult plants resprouting from a taproot. If, in fact, the facilitative effect of nurse shrubs seen at the seedling stage shifts to a competitive effect later in life, regular disturbance (i.e., prescribed fire or management techniques designed to mimic the effects of fire) that reduces the density of the shrub canopy may have positive effects on the growth and reproduction of adult Curtiss’ Milkweed plants. While the results of this study illustrate the potential importance of accounting for facilitative interactions in habitat restoration (e.g., Padilla and Pugnaire 2006), more research is needed on the long-term effect of shrubs on this rare plant before management recommendations can be made. Acknowledgments We would like to thank the Plant Ecology (BY 450) class of 2007 at Stetson University for their help collecting seeds. We would also like to thank Volusia County Land Acquisition and Management for allowing us to locate our experiments within Lyonia Preserve. Finally, we thank Terry Farrell, Peter May, and two anonymous reviewers for insightful comments that improved earlier versions of the manuscript. Literature Cited Acuña-Rodríguez, I.S., L.A. Cavieres, and E. Gianoli. 2006. Nurse effect in seedling establishment: Facilitation and tolerance to damage in the Andes of central Chile. Revista Chilena de Historia Natural 79:329–336. Armas, C., and F.I. Pugnaire. 2005. Plant interactions govern population dynamics in a semi-arid plant community. Journal of Ecology 93:978–989. Bertness, M.D., and R. Callaway. 1994. Positive interactions in communities. Trends in Ecology and Evolution 9:191–193. Brooker, R.W., F.T. Maestre, R.M. Callaway, C.L. Lortie, L.A. Cavieres, G. Kunstler, P. Liancourt, K. Tielborger, J.M.J. Travis, F. Anthelme, C. Armas, L. Coll, E. Corcket, S. Delzon, E. Forey, Z. Kikvidze, J. Olofsson, F. Pugnaire, C.L. Quiroz, P. Saccone, K. Schiffers, M. Seifan, B. Touzard, and R. Michalet. 2008. Facilitation in plant communities: The past, the present, and the future. Journal of Ecology 96:18–34. Callaway, R.M. 1995. Positive interactions among plants. The Botanical Review 61:306–349. Callaway, R.M., and L.R. Walker. 1997. Competition and facilitation: A synthetic approach to interactions in plant communities. Ecology 78:1958–1965. Callaway, R.M., N.M. Nadkarni, and B.E. Mahall. 1991. Facilitation and interference of Quercus douglasii on the understory productivity in central California. Ecology 72:1484–1499. 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 271 Callaway, R.M., R.W. Brooker, P. Choler, Z. Kikvidze, C. J. Lortie, R. Michalet, L. Paolini, F.I. Pugnaire, B. Newingham, E.T. Aschehoug, C. Armas, D. Kikodze, and B.J. Cook. 2002. Positive interactions among alpine plants increase with stress. Nature 417:844–848. Carlsson, B.Å., and T.V. Callaghan. 1991. Positive plant interactions in tundra vegetation and the importance of shelter. Journal of Ecology 79:973–983. Castro, J., R. Zamora, J.A. Hódar, and J.M. Gómez. 2004a. Seedling establishment of a boreal tree species (Pinus sylvestris) at its southernmost distribution limit: Consequences of being in a marginal Mediterranean habitat. Journal of Ecology 92:266–277. Castro, J., R. Zamora, J.A. Hódar, J.M. Gómez, and L. Gómez-Aparicio. 2004b. Benefits of using shrubs as nurse plants for reforestation in Mediterranean mountains: A 4-year study. Restoration Ecology 12:352–358. Cody, M.L. 1993. Do cholla cacti (Opuntia spp., Subgenus Cylindropuntia) use or need nurse plants in the Mojave Desert? Journal of Arid Environments 24:139–154. Coile, N.C., and M.A. Garland. 2003. Notes on Florida’s Endangered and Threatened Plants. Bureau of Entomology, Nematology, and Plant Pathology–Botany Section. Contribution No. 38, 4th Edition. Florida Department of Agriculture and Consumer Service, Division of Plant Industry, Gainesville, fl. Egerton, J.J. G., J.C.G. Banks, A. Gibson, R.B. Cunningham, and M.C. Ball. 2000. Facilitation of seedling establishment: Reduction in irradiance enhances winter growth of Eucalyptus pauciflora. Ecology 81:1437–1449. Forseth, I.N., D.A. Wait, and B.B. Casper. 2001. Shading by shrubs in a desert system reduces the physiological and demographic performance of an associated herbaceous perennial. Journal of Ecology 89:670–680. Franco, A.C., and P.S. Nobel. 1988. Interactions between seedlings of Agave deserti and the nurse plant Hilaria rigida. Ecology 69:1731–1740. Franco, A.C., and P.S. Nobel. 1989. Effect of nurse plants on the microhabitat and growth of cacti. Journal of Ecology 77:870–886. Garcia, D., R. Zamora, J.A. Hódar, J.M. Gómez, and J. Castro. 2000. Yew (Taxus baccata L.) regeneration is facilitated by fleshy-fruited shrubs in Mediterranean environments. Biological Conservation 95:31–38. Gómez-Aparicio, L., J.M. Gómez, R. Zamora, and J.L. Boettinger. 2005. Canopy vs. soil effects of shrubs facilitating tree seedlings in Mediterranean montane ecosystems. Journal of Vegetation Science 16:191–198. Graff, P., M.R. Aguiar, and E.J. Chaneton. 2007. Shifts in positive and negative plant interactions along a grazing-intensity gradient. Ecology 88:188–199. Greenlee, J., and R.M. Callaway. 1996. Effects of abiotic sress on the relative importance of interference and facilitation. American Naturalist 148:386–396. Hawkes, C.V., and E. Menges. 1996. The relationship between open space and fire for species in a xeric Florida scrubland. Bulletin of the Torrey Botanical Club 123:81–92. Holmgren, M., M. Scheffer, and M.A. Huston. 1997. The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975. Holzapfel, C., and B.E. Mahall. 1999. Bidirectional facilitation and interference between shrubs and annuals in the Mojave Desert. Ecology 80:1747–1761. 272 Southeastern Naturalist Vol. 9, No. 2 Ibáñez, I., and E.W. Schupp. 2001. Positive and negative interactions between environmental conditions affecting Cercocarpus ledifolius seedling survival. Oecologia 129:543–550. Ivey, C.T., S.R. Lipow, and R. Wyatt. 1999. Mating systems and interfertility of Swamp Milkweed (Asclepias incarnata ssp. incarnata and ssp. pulchra). Heredity 82:25–35. Jaksic, F.M., and E.R. Fuentes. 1980. Why are native herbs in the Chilean matorral more abundant beneath bushes: Microclimate or grazing? Journal of Ecology 68:665–669. Johnson, A.F., and W.G. Abrahamson. 1990. A note on the fire responses of species in Rosemary scrubs on the southern Lake Wales Ridge. Florida Scientist 53:138–143. Jordan, P.W., and P.S. Noble. 1979. Infrequent establishment of seedlings of Agave deserti (Agavaceae) in the Northwestern Sonoran Desert. American Journal of Botany 66:1079–1084. Kalisz, P.J., and E.L. Stone. 1984. The Longleaf Pine islands of the Ocala National Forest, Florida: A soil study. Ecology 65:1743–1754. Kitzberger, T., and D.F. Steinaker, and T.T. Veblen. 2000. Effects of climatic variability on facilitation of tree establishment in northern Patagonia. Ecology 81:1914–1924. Lipow, S.R., S.B. Broyles, and R. Wyatt. 1999. Population differences in self-fertility in the “self-incompatible” milkweed Asclepias exaltata (Asclepiadaceae). American Journal of Botany 86:1114–1120. Maliakal-Witt, S.E., E.S. Menges, and J.S. Denslow. 2005. Microhabitat distribution of two Florida scrub endemic plants in comparison to their habitat-generalist congeners. American Journal of Botany 92:411–421. Marshall Mattson, K.D., and F.E. Putz. 2008. Sand Pine (Pinus clausa) seedling distribution and biomechanics in relation to microsite conditions and proximity to potential nurse plants. Forest Ecology and Management 255:3778–3782. McAuliffe, J.R. 1984. Sahuaro-nurse tree associations in the Sonoran Desert: Competitive effects of sahuaros. Oecologia 64:319–321. McAuliffe, J.R. 1986. Herbivore-limited establishment of a Sonoran Desert tree, Cercidium microphyllum. Ecology 67:276–280. Menges, E.S., and C. Hawkes. 1998. Interactive effects of fire and microhabitat on plants of Florida scrub. Ecological Applications 8:935–946. Menges, E.S., and J. Kimmich. 1996. Microhabitat and time-since-fire: Effects on demography of Eryngium cuneifolium (Apiaceae), a Florida scrub endemic plant. American Journal of Botany 83:185–191. Menges, E.S., P.J. McIntyre, M.S. Finer, E. Goss, and R. Yahr. 1999. Microhabitat of the narrow Florida scrub endemic Dicerandra christmanii, with comparisons to its congener D. frutescens. Journal of the Torrey Botanical Club 126:24–31. Menges, E.S., P.F. Quintana-Ascencio, C.W. Weekley, and O.G. Gaoue. 2006. Population viability analysis and fire-return intervals for an endemic Florida scrub mint. Biological Conservation 127:115–127. Menges, E.S., A. Craddock, J. Salo, R. Zinthefer, and C.W. Weekley. 2008. Gap ecology in Florida scrub: Species occurrence, diversity, and gap properties. Journal of Vegetation Science 19:503–514. Moro, M.J., F.I. Pugnaire, P. Haase, and J. Puigdefábregas. 1997. Effect of the canopy of Retama sphaerocarpa on its understorey in a semiarid environment. Functional Ecology 11:425–431. 2010 P. Mondo, K.D. Marshall Mattson, and C.C. Bennington 273 Myers, R.L. 1990. Scrub and high pine. Pp. 150–193, In R.L. Myers and J.J. Ewel (Eds.). Ecosystems of Florida. University of Central Florida Press, Orlando, fl. 765 pp. Padilla, F.M., and F.I. Pugnaire. 2006. The role of nurse plants in the restoration of degraded environments. Frontiers in Ecology and the Environment 4:196–202. Petrü, M., and E.S. Menges. 2003. Seedling establishment in natural and experimental Florida scrub gaps. Journal of the Torrey Botanical Society 130:89–100. Petrü, M., and E.S. Menges. 2004. Shifting sands in Florida scrub gaps and roadsides: Dynamic microsites for herbs. American Midland Naturalist 151:101–113. Prider, J.N., and J.M. Facelli. 2004. Interactive effects of drought and shade on three arid-zone chenopod shrubs with contrasting distributions in relation to tree canopies. Functional Ecology 18:67–76. Pugnaire, F.I., C. Armas, and F. Valladares. 2004. Soil as a mediator in plant-plant interactions in a semi-arid community. Journal of Vegetation Science 15:85–92. Putz, F.E., and M. Minno. 1995. The pollination biology and ecology of Curtiss’ Milkweed (Asclepias curtissii). Florida Game and Fresh Water Fish Commission Nongame Wildlife Program Project Report, Tallahassee, fl. 121 pp. Quintana-Ascencio, P.F., and M. Morales-Hernandez. 1997. Fire-mediated effects of shrubs, lichens, and herbs on the demography of Hypericum cumulicola in patchy Florida scrub. Oecologia 112:263–271. Quintana-Ascencio, P.F., E.S. Menges, and C.W. Weekley. 2003. A fire-explicit population viability analysis of Hypericum cumulicola in Florida Rosemary scrub. Conservation Biology 17:433–449. Rebollo, S., D.G. Milchunas, and I. Noy-Meir. 2005. Refuge effects of a cactus in grazed short-grass steppe. Journal of Vegetation Science 16:85–92. Riginos, C., S.J. Milton, and T. Wiegand. 2005. Context-dependent interactions between adult shrubs and seedlings in a semi-arid shrubland. Journal of Vegetation Science 16:331–340. Rousset, O., and J. Lepart. 2000. Positive and negative interactions at different life stages of a colonizing species (Quercus humilis). Journal of Ecology 88:401–412. Schmalzer, P.A., and C.R. Hinkle. 1996. Biomass and nutrients in aboveground vegetation and soils of Florida oak-Saw Palmetto scrub. Castanea 61:168–193. Shmida, A., and R.H. Whittaker. 1981. Pattern and biological microsite effects in two shrub communities, southern California. Ecology 62:234–251. Shreve, F. 1931. Physical conditions in sun and shade. Ecology 12:96–104. Shumway, S.W. 2000. Facilitative effects of a sand dune shrub on species growing beneath the shrub canopy. Oecologia 124:138–148. Smit, C., C. Vandenberghe, J. den Ouden, and H. Müller-Schärer. 2007. Nurse plants, tree saplings, and grazing pressure: Changes in facilitation along a biotic environmental gradient. Oecologia 152:265–273. Tewksbury, J.J., and J.D. Lloyd. 2001. Positive interactions under nurse-plants: Spatial scale, stress gradients, and benefactor size. Oecologia 127:425–434. Tielbörger, K., and R. Kadmon. 2000. Temporal environmental variation tips the balance between facilitation and interference in desert plants. Ecology 81:1544–1564. Tirado, R., and F.I. Pugnaire. 2003. Shrub spatial aggregation and consequences for reproductive success. Oecologia 136:296–301. 274 Southeastern Naturalist Vol. 9, No. 2 Turner, R.M., S.M. Alcorn, G. Olin, and J.A. Booth. 1966. The influence of shade, soil, and water on Saguaro seedling establishment. Botanical Gazette 127:95–102. Valiente-Banuet, A., and E. Ezcurra. 1991. Shade as a cause of the association between the cactus Neobuxbaumia tetetzo and the nurse plant Mimosa luisana in the Tehuacan Valley, Mexico. Journal of Ecology 79:961–971. Weekley, C.W., and E.S. Menges. 2003. Species and vegetation responses to prescribed fire in a long-unburned, endemic-rich Lake Wales Ridge scrub. Journal of the Torrey Botanical Society 130:265–282. Weekley, C.W., D. Gagnon, E.S. Menges, P.F. Quintana-Ascencio, and S. Saha. 2007. Variation in soil moisture in relation to rainfall, vegetation, gaps, and time-sincefire in Florida scrub. Ecoscience 14:377–386.