Ecological life history of the facultative woodland biennial Arabis laevigata variety laevigata (Brassicaceae): Survivorship

Bloom, Thomas C

1,2THOMAS C. BLOOM, 1JERRY M. BASKIN, AND 1,3CAROL C. BASKIN (‘School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506-0225, (2)1209 Glade Street, College Station, TX 77840, and 3Department of Agronomy, University of Kentucky, Lexington, KY 40546-0091). Ecological life history of the facultative woodland biennial Arabis laevigata variety laevigata (Brassicaceae): survivorship. J. Torrey Bot. Soc. 128:000000. 2001-Survivorship was studied over an 8.5-year period in a population of the facultative biennial Arabis laevigata var. laevigata in a rocky deciduous woodland (Scott’s Grove) in northcentral Kentucky, where most individuals of this species are associated with rock outcrops. Of the 2,269 seedlings marked in 1986 and 814 in 1987, only 101 (4.5%) and 35 (4.3%), respectively, survived 1 year, and only 24 (0.78%) of the 3,083 plants bolted before they died. In a separate study, only about 64% of the plants that bolted produced seeds. Thus, only about 15 (0.49%) of the 3,083 plants marked as seedlings in 1986 and 1987 actually reproduced. Cohorts exhibited a Deevey Type III survivorship curve. Small plants had a greater probability of dying than large ones. Survival was higher in microsites (on and near rock outcrops) with a thin, patchy leaf litter than in those with a moderate leaf cover; plants were not found in sites with a thick and persistent litter cover. Rosette herbivory also was a cause of mortality. Plants at Scott’s Grove may flower in their second, third, fourth, fifth, or even a later year of life. Survivorship of A. laevigata in its woodland rock outcrop habitat is similar to that of facultative biennials of various other habitat types.

Key words: Arabis laevigata var. laevigata, desiccation and survival, herbivory and survival, life tables, plant litter and survival, survivorship curves, woodland “biennial”.

Kelly (1985) suggested that facultative biennials are normally found in fertile, open, disturbed, or early successional habitats, while obligate biennials may be found in infertile or undisturbed sites. Indeed, most population studies of biennials have been done on weedy species that are not native to North America (e.g. Werner 1975a; Baskin and Baskin 1979a; van der Meijden and van der Waals-Kooi 1979; Gross 1981; Hirose and Kachi 1982; Gross and Werner 1983; Klemow and Raynal 1981, 1985; de Jong and Klinkhamer 1986; Byers and Quinn 1998), and relatively few studies have been done on native North American biennials of stable habitats (e.g., Baskin and Baskin 1979b; Baskin et al. 1986; Spira and Pollock 1986; Bender et al. 2000). The purpose of this study was to extend knowledge about native North American facultative biennials by studying the population biology of Arabis laevigata (Muhl.) Poir. var. laevigata (Brassicaceae; hereafter A. laevigata), which is interesting because, unlike most other facultative biennials, it occupies stable woodland habitat. The study had three objectives: (1) to characterize the habitat of the species, (2) to describe the demography of the population, and (3) to identify the factors affecting germination, survival, and reproduction of this population. Two characteristics of the species make it an ideal organism for such a study: it is native to a large portion of eastern North America, and its major habitat, woodland rock outcrops, differs from that of other biennials that have been studied. A population in a central Kentucky woodland was studied over an 8.5-year period, November 1985-May 1994.

Previous papers published from this study dealt with habitat description (Bloom et al. 1990b) and seed germination ecology (Bloom et al. 1990a) of A. laevigata. This paper presents results of the study on survivorship. Survivorship of A. laevigata plants was monitored intensively between November 1985 and March 1988 in an attempt to characterize the environment of rosettes most likely to survive. The three environmental factors of leaf litter cover, herbivory, and substrate were studied. The relationships of temperature and precipitation to mortality rate also were analyzed. Because relative size may be the best indicator of plant vigor (Harper 1977) and has been shown to correspond with mortality rate in many monocarpic species (e.g., Werner 1975a; Gross 1980; Klemow and Raynal 1985; deJong and Klinkhamer 1986), three measures of plant size were made in this study (rosette diameter, root crown diameter, and leaf number). Also, the interactions of environmental factors, size, and mortality were examined. In addition, all plants (rosettes) still alive in the four cohorts at the end of the 2.5-year period of intensive study were monitored for survivorship in autumn 1988 and in springs of 1989-1994, by which time all of them had died, either with or without producing a flowering stalk.

Materials and Methods. STUDY SITE. The study site, known as Scott’s Grove, is an about 20-ha rocky, deciduous woods with sinkholes near Camp Nelson in southern Jessamine County, northcentral Kentucky, above the confluence of Hickman Creek and the Kentucky River. It is located in the Little Hickman USGS 75 quadrangle. Study sites lie between 235 and 255 meters above sea level. Major canopy species in this forest are Acer saccharum, Carya glabra, C. ovata, Fraxinus americana, F. quadrangulata, Quercus alba, Q. muhlenbergii, Q. shumardii, Q. velutina, and Ulmus rubra (Campbell 1980). Most A. laevigata plants in this woods grow in bare mineral soil at the edges of rock outcrops. Here, their most common associates are Bignonia capreolata, Parthenocissus quinquefolia, Toxicodendron radicans, and bryophytes and lichens (Bloom et al. 1990b). Based on USDA aerial photographs taken in 1956 and 1983, it does not appear that the site had been disturbed severely for at least 30 years prior to this study. Bedrock at the site is limestone of the High Bridge Group of the Middle Ordovician Series (Wolcott 1969). Soils are McAfee silt loam, 6-12% slopes and McAfee-Rock Outcrop Complex, 6-20% slopes. The McAfee is a mixed, mesic, Mollic Hapludalf (McDonald et al. 1983).

Mean monthly minimum and maximum temperatures and total precipitation for 24 months of the study period (1986-1987), and the average monthly minimum and maximum temperatures and average monthly precipitation for the 30-year period from 1941 to 1970 were obtained from Bluegrass Field in Lexington, Kentucky (38deg03′ N, 84deg30′ W), the United States Weather Bureau station nearest Scott’s Grove (NOAA 1983). Actual and average monthly precipitation are shown in Figure 1. Daily precipitation and temperature data were obtained from Dix Dam in Mercer County, Kentucky (37deg49′ N, 84deg43′ W, 165 m elevation) for 1986 (NOAA 1986) and 1987 (NOAA 1987). The Dix Dam station is approximately 9 km from Scott’s Grove. Average annual precipitation is 1141 mm. Precipitation was below average from March through June in 1986; total precipitation (1146 mm) was near average only because of a very wet November. Precipitation in 1987 (908 mm) was below average. Photosynthetic photon irradiance (PPI, 400-700 nm) in the woodland was from 10-fold to 100-fold greater in winter than in summer. Very few plots were exposed to a PPI of over 100 (mu)mol m^sup -2^ s^sup 1^ in summer, but most plots received much more than this in winter (Bloom et al. 1990b).

THE SPECIES. Arabic laevigata, smooth Rockcress, is a hemicryptophyte semi-rosette (cauline leaves, radial rosette) without runners (Gibson 1961). The species usually is reported to be a biennial (Hopkins 1937; Rollins 1993), although Radford et al. (1968) say it also is rarely perennial. Immature vegetative plants consist of a flat rosette of leaves that persist through the winter. Mature reproducing plants consist of a stiff, erect flower stalk, 3-9 dm tall, arising from the center of the rosette; the rosette withers and dies soon after bolting. The small, white flowers are produced from late March through July, and the 5-10 cm long siliques are formed from May through September (Hopkins, 1937; Fernald, 1950; Rollins, 1993). The species is diploid, 2n = 14 (Smith 1938; Kovanda, 1978; Rollins 1993) and n = 7 (Rollins 1993). The geographical range of A. laevigata is from Quebec south to South Carolina and Georgia, and west to Oklahoma and Minnesota (Hopkins 1937; Rollins 1993). The extremes of the species’ range are approximately 34deg30′ N latitude, 45deg00′ N latitude, 98deg30′ W longitude, and 71deg00′ W longitude. Forest regions of the Eastern Deciduous Forest in which A. laevigata is found include the Mixed mesophytic, Western mesophytic, Oak– Hickory, Beech-Maple, Oak-Chestnut, and Hemlock-White Pine-Northern Hardwood (sensu Braun 1950). Sixty-four of 80 habitat descriptions gleaned from the literature (Bloom 1988) indicate that the species primarily grows in rocky habitats, i.e., rocky woods, cliffs, ledges, etc.

COHORT ANALYSES. Survivorship (l^sub x^) Curves. Survival of plants from the 2269 and 814 seeds that germinated in the germination phenology study in 1986 and 1987 (Bloom et al. 1990a), respectively, was monitored until death, bolting, or until 6 March 1988. After bolting, a plant dies, either before anthesis, after anthesis but before fruit/seed production, or after fruit/seed production (Bloom 1988). In February 1986, 26 of 104 locations (sites) within the Scott’s Grove woodland where at least one plant of A. laevigata was growing were selected randomly for monitoring seed germination and plant survival. In 1987, 10 additional sites were chosen randomly from the remaining 78. Thus, survival was monitored at 26 sites in 1986 and at 36 sites in 1987. At each site, a plot was laid out to facilitate monitoring of germination (Bloom et al. 1990a) and survival. If one plant was present at a site, the plot was 0.5 m x 0.5 m, with the plant in the center. If more than one plant was present, the plot extended 0.25 m in all directions from the most distal plants. Thus, all plants at a site were included in the plot. The size of each plot remained unchanged from year to year.

Seedlings were ringed with sections of plastic straw, color-coded to identify individual cohorts. Empty markers were counted and removed at each visit, and the number of markers lost was subtracted from the total of the appropriate cohort. Newly-germinated seeds marked on the same day are referred to as a “week cohort,” and all of the week cohorts in a given year are referred to as the “1986 cohort” or the “1987 cohort.” Seedlings were assigned identification numbers on 20 May 1986 and on 6 June 1987. Seedlings were considered to be established rosettes on these dates because most of them had produced two or more leaves. Two additional cohorts were monitored. Plants that germinated in 1986 on outcrops not used for germination phenology were marked and given identification numbers between 22 August 1986 and 4 March 1987. These plants are referred to as the “886” cohort. Also, rosettes of unknown age were marked and given identification numbers as they were discovered between 23 November 1985 and 4 March 1987. They are referred to as the “undetermined cohort.” Thus, a total of four cohorts was monitored. All individually-numbered plants in the population were monitored approximately biweekly for mortality from March through October and monthly from November through February.

Survivorship curves were constructed with a horizontal scale (x-axis) of days from the beginning of the study (23 November 1985) and a vertical scale (y-axis) of logo number alive. Actual numbers of 1986 and of 1987 cohort plants were used. This was not possible for the 886 or for the undetermined cohorts since all plants were not marked at the same time. To obtain a single survivorship curve, percent morality for each observation period was calculated, and these values were used to generate a survivorship curve for a hypothetical cohort beginning with 1000 individuals either at day 0 (undetermined cohort) or day 273 (886 cohort).

ENVIRONMENTAL FACTORS AND SURVIVORSHIP. Effect of Leaf Litter Cover on Survival. In the intensive part of the study, field plots used for germination phenology (Bloom et al. 1990a) and demographic observations (present study) were scored for amount of leaf litter present in March and for type of substrate. Four leaf litter cover scores were used: (1) no leaf litter cover, (2) no leaf litter cover to partial leaf litter cover, (3) partial leaf litter cover to total leaf litter cover, and (4) total leaf litter cover. No leaf litter and total leaf litter are self-explanatory. Partial leaf litter cover refers to surfaces where litter was present but was constantly shifting, mainly due to wind; for the most part it ranged from about 25 to 50%. Survival of rosettes in demographic plots was analyzed with the amount of leaf litter present in the plots in March as the independent variable. In these analyses, categories (1) and (2) were combined, and categories (3) and (4) were combined. Separate analyses were conducted for the 1986 and 1987 cohorts. Two 2 X 2 contingency tables (two litter categories X dead/alive) were constructed for each cohort. The first table compared survival from germination through establishment, and the second one survival from establishment to 4 March 1987 or 6 March 1988.

Individually-numbered rosettes were scored for amount of leaf litter cover on 15 dates, beginning on 20 May 1986 and ending on 6 March 1988. The number of plants observed for leaf litter cover ranged from 168 to 575. Plants were given a score of zero meaning no leaf litter cover, one meaning partial leaf litter cover, or two meaning complete leaf litter cover.

Two analyses were carried out. To obtain adequate sample sizes for calculating chi-square, the 1986, 886, 1987, and undetermined cohorts were pooled for both analyses. In the first analysis, the effect of leaf litter cover on one date on survival until the next leaf litter cover observations was analyzed. A 3 X 2 contingency table (three leaf litter cover scores X dead/alive during the period until the next observation) was constructed for each leaf litter observation date. In the second analysis, the effect of leaf litter cover during winter on survival during the subsequent spring was examined. The mean value of leaf litter cover on 18 November 1986, 18 December 1986, 25 January 1987, and 4 March 1987 was calculated for plants that survived the period and were not observed bolting on 4 March 1987. A 3 X 2 contingency table (three intervals X dead/alive between 4 March 1987 and 6 June 1987) was constructed.

A field experiment was conducted to determine the effect of leaf litter cover during winter on survival during winter. Sixty healthy rosettes, germinated in a greenhouse in March 1986, were used. Three groups of 20 plants each were planted on 11 September 1986 in 4 X 5 arrangements at three Scott’s Grove sites with a tree canopy but free of understory vegetation. Plants in all three plots were initially free of leaf litter cover. As fresh leaf litter fell, it was cleared from the plants in half of each plot and allowed to accumulate on the plants in the other half of each plot. These leaf litter conditions were maintained during biweekly visits to the site. Mortality was recorded on 6 March 1988. The number of dead plants in each plot was converted into a percentage, arcsin square root transformed, and analyzed using a one-way completely randomized analysis of variance design.

Effect of Herbivory on Survival. Individually-numbered rosettes were scored for the degree of leaf herbivory on 11 dates beginning on 3 June 1986 and ending on 15 January 1988. Number of plants observed for herbivory ranged from 166 to 571. Plants were given a score of zero to five on the basis of how much leaf area had been removed by herbivores: no leaf area removed = 0, 1-20% removed = 1, 21-40% removed = 2, 41-60% removed = 3, 61-80% removed = 4, and 81-100% removed = 5. Percentages were estimated visually. Herbivory scores of three or greater were pooled for the analysis. The 1986, 886, 1987, and undetermined cohorts were pooled. In both cases, pooling was done to obtain adequate sample sizes for calculating chi-square. The effect of herbivore damage on one date on survival until the next herbivory observation was analyzed. A 4 X 2 contingency table (four herbivory scores X dead/alive until the next observation) was constructed for each herbivory observation.

Effect of Substrate on Survival. The substrate designation of demographic plots and those of individually-numbered rosettes were used in these analyses. The two scores for substrate type in the demographic plots were (1) rock or moss, the majority of the plot being rock outcrop and/or a moss colony, and (2) soil, the majority of the plot being shallow or deep soil. The rock and moss categories were pooled to obtain adequate sample sizes. When the work was begun, rock and moss substrates were scored separately. However, it was difficult to distinguish between rock and moss for some plants, e.g., plants growing at the edge of a moss patch on the edge of a rock outcrop. The substrate of each individually-numbered plant was determined at the time of numbering.

The effect of substrate on survival between germination and establishment was analyzed using the demographic plot substrate designations. Separate 2 x 2 contingency tables (two substrate designations x dead/alive during the period) were constructed for the 1986 and 1987 cohorts. A similar set of tables, also using the demographic plot designations, were constructed for the period from establishment to 4 March 1987 or to 6 March 1988. Contingency tables (two or three substrate designations X dead/alive during the specified period) were constructed using the individual plant substrate designations for the following cohorts and periods: the 1986 cohort from 20 May 1986 to 4 March 1987, the 1986 and 886 cohorts from 4 March 1987 to 6 March 1988, the 1987 cohort from 6 June 1987 to 6 March 1988, the undetermined cohort (including only those plants marked on or before 23 March 1986) from 23 March 1986 to 4 March 1987, and the undetermined cohort (including all rosettes) from 4 March 1987 to 6 March 1988. Rock and moss designations were pooled in some analyses to obtain adequate sample sizes for calculating chi-square.

Relationship of Leaf Litter Cover, Herbivory, and Substrate. The relationship of substrate and leaf litter cover designations in the plots used for observations on both germination phenology (Bloom et al., 1990a) and demography (present study) was analyzed with a 2 x 4 contingency table (two substrate designations x four leaf litter cover designations).

On dates when both leaf litter cover and herbivory were observed, a running average (cumulative mean) of leaf litter cover and of herbivory was calculated for each plant by dividing the sum of all the observations, up to and including that date, by the number of observations made. The relationship of mean herbivory and mean leaf litter cover was estimated by calculating Pearson product-moment correlation coefficients for the two values on each of these dates.

Using the substrate designation of individually numbered plants, the relationship between the largest mean cumulative herbivory value calculated for a plant and its substrate was analyzed with a 3 X 2 contingency table (three intervals of maximum values X two substrate categories). The two substrate categories were rock or moss and soil. A similar analysis was conducted for the largest mean cumulative leaf litter value calculated for a plant and its substrate. Data from all cohorts were pooled for all above calculations to obtain adequate sample sizes.

PLANT SIZE AND SURVIVORSHIP. Rosette and root crown diameters of rosettes were measured on five dates during the intensive part of the study, which ended on 6 March 1988. Number of leaves on most rosettes was counted four times. Rosette diameter was defined as the greatest distance between any two leaf tips to the nearest 0.1 cm. Root crown diameter was defined as the diameter of the plant body immediately below the point of leaf attachment and was measured with a vernier caliper to the nearest 0.1 mm.

On 23 March 1986, rosette and root crown diameters of individuals of the undetermined cohort were measured. On 18 November 1986 and 4 March 1987, all of the 1986 cohort and most of the undetermined cohort were measured. All of the 1986, 1987, and undetermined cohorts were measured on 13 November 1987 and on 6 March 1988.

Pearson product-moment correlation coefficients were calculated for the herbivory means and for the three measures of plant size (In transformed) on 18 November 1986, 4 March 1987, 13 November 1987, and 6 March 1988. Similarly, Pearson product-moment correlation coefficients were calculated for leaf litter cover means and the three measures of plant size (In transformed) on each of the preceding dates. The 1986, 886, 1987, and undetermined cohorts were pooled in these analyses to obtain adequate sample sizes.

A one-way completely randomized analysis of variance with substrate as the classification variable and each of the size measures (In transformed) as the response variable was conducted for each of the 14 sets of size data. Three levels of the classification variable were used: rock, moss, and soil. The 1986, 886, 1987, and undetermined cohorts were pooled for the analyses to obtain adequate sample sizes. Tukey’s HSD was used to compare means.

LONG-TERM SURVIVORSHIP, 1988-1994. Following the intensive part of the study, which ended on 6 March 1988, survivorship was monitored in each of the four cohorts until all marked plants had died, either before or after bolting. Survivorship/bolting of all remaining individuals in the population was determined in October 1988, March 1989, 1990, 1991, 1992, 1993, and May 1994, by which time the last monitored-plant had died.

Results. COHORT ANALYSES. Survivorship (l^sub x^) Curves. Survivorship curves for the 1986 week cohorts are presented in Figure 2, for the 1987 week cohorts in Figure 3, and for the undetermined and 886 cohorts in Figure 4. A total of 489 undetermined cohort rosettes, 2269 1986 cohort seedlings, 218 886 cohort rosettes, and 814 1987 cohort seedlings were marked. The greatest amount of mortality occurred in the first 2 months after germination (Figs. 2, 3). A considerable amount of mortality occurred in all cohorts during days 530-570 (7 May 1987 to 16 June 1987) and days 620-660 (4 August 1987 to 14 September 1987). The lowest rate of mortality occurred during late autumn and winter (days 320-475 and 675-834) (Figs. 2, 3, 4).

There was a significant association between time of germination in 1986 and survival until 4 March 1987 among 1986 week cohorts (chi^sup 2^ = 17.8, df = 7, p0.05). The association between germination date and survival among the week cohorts of 1986 was not seen in their second year (4 March 1987 to 6 March 1988) (chi^sup 2^ = 2.87, df = 6, p>0.05). Survival of the 1986 and 1987 cohorts in their first year of growth was not significantly different (chi^sup 2^ = 0.03, df = 1, p>0.05). The undetermined cohort survived better between 23 March 1986 and 4 March 1987 than did the 1986 cohort between germination and 4 March 1987 (chi^sup 2^ = 576.89, df = 1, p

Only nine of the 2,269 plants in the 1986 cohort were alive on 6 March 1988. Of the 2,260 plants that had died in this cohort, 2,257 (99.9%) did so without bolting. One of the three plants that bolted did so in its second year and two in their third year (Fig. 2). Fifteen plants in the 1987 cohort were alive on 6 March 1988. Only eight of the 799 plants that had died did so after they bolted, all of du= in their second year (Fig 3).

Life Tables. Observations on mortality presented in the previous section are supported by the life table data (Table 1). Killing power (k^sub x^) between x = 0 and x = 1 was higher in 1986 (0.889) than in 1987 (0.281). Killing power during days 530-570 was 0.315 for the 18 March 1986 cohort (x = 14, 15) and 0.375 for the 20 March 1987 cohort (x = 2, 3). Killing power during days 620-660 was 0.368 for the 1986 cohort (x = 17, 18) and 0.606 for the 1987 cohort (x = 5, 6). The greatest rate of mortality (qx or kx) for the 1986 cohort was between x = 0 and x = 1; however, the greatest mortality rate for the 1987 cohort was between x = 5 and x = 6. Mortality during the 1986-1987 winter (x = 7 to x = 10) was low in the 1986 cohort (k. = 0.022). Mortality during the 1987-1988 winter was zero in both the 1986 cohort (x = 19 to x = 22) and the 1987 cohort (x = 7 to x = 10).

ENVIRONMENTAL FACTORS AND SURVIVORSHIP. Effect of Leaf Litter Cover on Survival. Greater mortality of newly-germinated seedlings between germination and establishment was associated with less leaf litter cover on demographic plots in March in 1986 (chi^sup 2^ = 93.82, df = 1, p

Mortality of individually numbered plants was not associated with leaf litter cover during any period of the study. There were no significant associations between leaf litter cover during the 1986-1987 winter and mortality between 4 March 1987 and 6 June 1987 (chi^sup 2^ = 1.23, df = 2, p>0.05). Winter leaf litter cover had no significant effect on mortality during the 19871988 winter leaf litter cover experiment (F = 4.39; df = 1, 4; p>0.05).

Effect of Herbivory on Survival. Frequencies of herbivory scores on each observation date are given in Table 2. A score of zero (no leaf area removed) was the most common score observed in June and August, and a score of one (1-20% leaf area removed) was the most common score observed on all other dates. No herbivores were observed or identified. There was an association between herbivory and mortality during the interval until the next herbivory observation for 18 December 1986, 4 March 1987, 8 April 1987, 6 June 1987, 4 August 1987, 13 November 1987, and 15 January 1988 (Table 2).

Effect of Substrate on Survival. Survival from germination to establishment was higher in demographic plots with a soil substrate designation for 1986 cohort plants (chi^sup 2^ = 85.55, df = 1, p0.05). From establishment until the end of the first year of growth (4 March 1987 or 6 March 1988), survival was higher in plots with a rock or moss substrate designation (1986 chi^sup 2^ = 7.16, df = 1, p0.05).

Relationship of Leaf Litter Cover, Herbivory, and Substrate. There was a strong association between none to partial leaf litter cover and a rock or moss substrate and between partial to total leaf litter cover and a soil substrate in demographic plots (chi^sup 2^ = 72.8, df = 1, p

Similarly, for individually numbered plants, there was a greater than expected association between a higher cumulative leaf litter cover mean and a soil substrate (chi^sup 2^ = 91.44, df = 2, p

There were significant positive correlations between the cumulative leaf litter cover mean and the cumulative herbivory mean on each of the ten dates for which it was possible to calculate a correlation coefficient; the lowest correlation coefficient was 0.127 (n = 430, p

PLANT SIZE AND SURVIVORSHIP. Each mean probability of fate for rosettes in each size intervals in Table 3 is the average of the proportion in 1986-1987 and 1987-1988; thus, n = 2 (two 1-year transitions). This is completely age– independent because plants were assigned to size classes regardless of their age. In Table 4, mean probability of transition into different size intervals in the first year of growth, n also is 2 (first-year of growth for the 1986 cohort and first-year growth for 1987 cohort). This is agedependent since only first-year plants were included. Likewise in Table 5, mean probability of transition among different size intervals during the March to March period between measurements, n = 2, i.e., the transition from 1986 to 1987 for the undetermined age cohort and the transition from 1987-1988 for undetermined age and 1986 cohorts.

Smaller plants had a greater probability of dying during the intervals between size measurements but few plants grew to the largest sizes (Table 3). This was true regardless of the size measure examined. Some mortality was observed even in the largest size intervals. No consistent pattern of transition between size intervals was observed. After 1 year of growth, plants were found in almost all size intervals (Table 4). Established plants were observed to move into smaller size intervals, remain in the same size interval, and move into larger size intervals (Table 5).

Cumulative leaf litter cover means on dates when sizes were measured were significantly negatively correlated with all three size measures. The correlation between cumulative leaf litter cover mean and root crown diameter ranged from r = -0.307 (n = 118, p

Substrate had a highly significant effect on all size measures observed on all dates. The minimum F value in the 14 analyses of variance was 10.0 (p

LONG-TERM SURVIVORSHIP, 1988-1994. At the end of the intensive part of the study, 6 March 1988, 74 marked-plants were still alive: 9 in the 1986 cohort; 15 in the 1987 cohort; 41 in the 886 cohort; and 9 in the undetermined cohort. In these four cohorts, the last individuals had died or bolted by spring 1992, spring 1991, spring 1994, and spring 1994, respectively. Plants in the 1986 cohort bolted in spring 1989 (4 plants) and 1990 (1); in the 1987 cohort in 1989 (7) and 1990 (1); in the 886 cohort in 1989 (16) and 1990 (1); and in the undetermined cohort in 1989 (5) and 1991 (1). Thus, 36 of the 74 marked rosettes in the population bolted and then died, and 38 died without bolting. Of the 13 plants that bolted in the 1986 and 1987 cohorts, seven did so in their third year, five in their fourth year, and one in its fifth year. Sixteen of the 17 plants that bolted in the 886 cohort were in their fourth year and one in at least its fifth year. Finally, of the six plants that bolted in the undetermined cohort (age of rosettes unknown when marked) five were in at least their fifth year and one in at least its seventh year.

Discussion. The shape of a survivorship curve gives an indication of when environmental forces act on a population (Harper and White 1974). Cohorts of A. laevigata exhibit Type III survivorship curves (Deevey 1947), indicating that seedlings experience greater mortality than older, established plants (Figures 2, 3). A similar pattern has been reported for other facultative biennials (Werner 1975a; Baskin and Baskin 1979b; Gross 1980; Klemow and Raynal 1985; de Jong and Klinkhamer 1986).

The rate of pre-establishment mortality in A. laevigata appeared to be dependent on amount of precipitation during this period. Days 110– 140 in Figure 2 and days 474-504 in Figure 3 correspond to the calendar period of 12 March to 11 April. Mortality during this period was greater in 1986 than in 1987. A possible cause of this difference was greater precipitation during this period in 1987 (98.81 mm) than in 1986 (63.00 mm) (NOAA 1986, 1987). Mortality of older rosettes also corresponded to low precipitation. More undetermined cohort rosettes died during the 12 March to 11 April period in 1986 than in 1987 (Figure 4). The high mortality experienced by all cohorts between 4 August 1987 and 14 September 1987 (days 620-660) occurred during a period of little precipitation (48.77 mm) (NOAA 1987). During the same period in 1986 (days 255-295), mortality of undetermined cohort rosettes was low, and mortality of 1986 cohort rosettes decreased relative to what it had been before this period. Precipitation during the 1986 period totaled 162.05 mm (NOAA 1986). A third period of increased mortality that corresponded to low precipitation was 7 May 1987 to 16 June 1987. Precipitation during this period in 1986 (days 165-205) totaled 128.17 mm and in 1987 (days 530-570) 28.70 mm (NOAA 1986, 1987).

Klemow and Raynal (1981) reported a Deevey Type II curve for the obligate biennial Melilotus alba when conditions were cool and moist and a Deevey Type III curve when conditions were hot and dry. Survivorship curves for the facultative biennial Polymnia canadensis were Deevey Type III during normal precipitation and Deevey Type I during droughts (Bender et al. 2000). Survival in a population of the facultative biennial Picris hieracioides (Klemow and Raynal 1985) and in the obligate biennial Synandra hispidula (Baskin et al. 1986) were greater in a moist study year than in a dry study year. Thus, not surprisingly, survival of A. laevigata and other biennials appears to correspond to high (normal) amounts and regular distribution of precipitation.

The presence of a leaf litter cover has been shown to cause seedling mortality in several monocarpic species (Gross and Werner 1982, 1983; Tremlett et al. 1984). Gross and Werner (1982) found that the negative effect of a leaf litter cover was greater on the facultative biennials Verbascum thapsus and Oenothera biennis, species with small, flat rosettes easily covered with leaf litter, than on Daucus carota and the facultative biennial Tragopogon dubius, species with larger and taller rosettes. Arabis laevigata seedlings are very small, and a similar effect was expected but not observed. Total leaf litter cover may cause etiolation and increase the probability of mechanical damage, but some cover during the first 2 months of growth may provide a microenvironment in which seedlings are protected from desiccation before they are adequately established. During the interval between the onset of germination in early March (when demographic plot leaf litter conditions were observed) and establishment in late May or early June, the trend was for the amount of leaf litter cover to decrease (Bloom et al. 1990a). In plots with partial to total or total leaf litter cover initially, some litter was removed by wind and investigator disturbance, but enough probably remained to reduce evapotranspiration from the plots. Plots with no or with none to partial leaf litter cover initially would be bare before the end of the period, and evapotranspiration presumably would be greater than in the partially-covered plots.

In a greenhouse study, Werner (1975b) observed an increased probability of seedling survival in the facultative biennial Dipsacus sylvestris under quackgrass litter. In another greenhouse study, Hamrick and Lee (1987) found that survival of seedlings of the facultative biennial Carduus nutans was enhanced under a light cover of leaf litter; they attributed this effect to the retardation of evapotranspiration from the soil surface. Because there were intervals of very little precipitation during the pre-establishment periods of A. laevigata in both 1986 and 1987, it is not known if leaf litter cover would have a positive effect in all years, particularly years with adequate rainfall throughout this period. If seedlings under a leaf litter cover die from “rotting” (Werner 1975b), a leaf litter cover may be detrimental in a wet year. The absence of any association between leaf litter cover and mortality of established rosettes during spring, summer, and autumn can be explained by the fact that rosettes were never covered by a thick and persistent leaf litter layer during these seasons. Rosettes presumably survived under the limited leaf litter cover because it was transient and not very deep. The absence of any association between leaf litter cover and mortality in winter, when the cover was thicker and more persistent, may indicate that the species is adapted to leaf litter cover during this period. Although leaf litter cover does not directly cause mortality, it does have an indirect effect because a greater frequency of cover was associated with smaller plant sizes, and smaller plants were more susceptible to mortality.

Arabis laevigata grows in two general types of habitats at Scott’s Grove. In the first type, plants grow on a soil substrate that has a relatively high chance of being covered with leaf litter. Plants in this habitat are more likely to become established than they are in the rock or moss habitat in which they grow better. However, unless the leaf litter cover decreases during summer and autumn, they are less likely to survive to 1 year. Herbivory and its associated winter mortality are more likely to occur in this habitat type. In the second habitat type, plants grow on a rock or moss substrate, and they are covered by leaf litter only during late autumn and winter. Chances of establishment are greater if some leaf litter cover persists until seedlings are established in late spring. Plants in this habitat type are more likely to survive to 1 year and beyond than are those on a soil substrate.

The risk of mortality is greater in the soil habitat for two reasons. (1) The degree of rosette herbivory is higher under a leaf litter cover. The effect of herbivory on mortality apparently is independent of size, since herbivory and size are not correlated. (2) Plants on a soil substrate and/ or covered more frequently with leaf litter are likely to be smaller than those on a rock or moss substrate and/or covered less often with leaf litter. The strongest association found in the analysis of survivorship was between small plant size and increased mortality. Size-dependent mortality has been observed in many plant species (Harper 1977), including many that are monocarpic (Werner 1975b; Gross 1981; Gross and Werner 1983; Lee and Hamrick 1983; Kachi and Hirose 1985). Small plants are more susceptible to mortality because they have a longer prereproductive period and are exposed to a longer period of mortality risk, and they are less likely to be buffered from environmental fluctuations in, for example, soil moisture, than large plants (Cook 1979).

Survivorship of A. laevigata, a species of rocky woodlands, is similar to that of facultative biennial species that occupy either stable or unstable open habitats (e.g. Werner 1975b; Baskin and Baskin 1979a,b; Gross 1981; Reinartz 1984). In all three habitat types, mortality is high, and only a very low percentage of plants from seeds that germinate in the population live to the reproductive stage of the life cycle. Thus, for example, as in A. laevigata less than 1% of the seedlings of the facultative biennials Pastinaca sativa (Baskin and Baskin 1979a) and Grindelia lanceolata (Baskin and Baskin 1979b) that grow in fertile, secondary successional habitats and cedar glades, respectively, lived to produce seeds. Further, in the facultative biennial Polymnia canadensis, a species of dry to mesic woodlands in eastern North America, only about 3.5% of 23,063 plants marked as seedlings survived to the seed-producing stage (Bender et al. 2000). Thus, it appears that high mortality, concentrated in the seedling stage, i.e., Deevey Type III survivorship, is a life history characteristic common among facultative biennials, regardless of the habitat they occupy.

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Thomas C. Bloom1,2, Jerry M. Baskin1,4, and Carol C. Baskin1,3

1School of Biological Sciences, University of Kentucky, Lexington, Kentucky 40506-0225

21209 Glade Street, College Station, TX 77840

3Department of Agronomy, University of Kentucky, Lexington, KY 40546-0091

Received for publication August 8, 2000, and in revised form January 18, 2001.

4 Jerry M. Baskin, corresponding author: Telephone: (859) 257-8770; FAX: (859) 257-1717; E-mail: jmbask0@pop.uky.edu

Copyright Torrey Botanical Society Apr-Jun 2001

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