Dispersal Characteristics of Two Native and Two Nonnative Fleshy ...

CASTANEA 79(2): 88–99. JUNE Copyright 2014 Southern Appalachian Botanical Society

Dispersal Characteristics of Two Native and Two Nonnative Fleshy-Fruited Sympatric Shrubs Laura J. McCall1 and Jeffrey L. Walck1* Department of Biology, Middle Tennessee State University, Murfreesboro, Tennessee 37132

ABSTRACT Aspects of the dispersal characteristics of two nonnative shrubs, Elaeagnus umbellata and Ligustrum sinense, were compared with those of two native shrubs, Cornus amomum and Frangula caroliniana, to identify factors that contribute to successful invasion of the nonnative species. For each species, the following aspects were examined: shrub abundance, physical characteristics and nutritional values of fruits, arrangement of fruits along the stem and number of fruits per branch, phenology of fruit maturation and foliage coloration, and animal interactions. The two native shrubs and E. umbellata were similar in abundance, but L. sinense was significantly more abundant than the others. Cornus amomum and F. caroliniana present bicolored displays of fruits that are rapidly dispersed during autumn avian migration. Elaeagnus umbellata produces moisture- and protein-rich fruits during summer that are also rapidly removed. In contrast, L. sinense produces high numbers of fruits in late autumn that remain available to frugivores throughout the winter. The large quantities and prolonged availability of L. sinense fruits enable the dispersal of this shrub by a diverse array of frugivores and contribute at least partially to its successful invasion of new habitat and its observed abundance. Key words: Bicolored display, exotic species, fruit nutrition, fruit phenology, seed dispersal, seed production.

INTRODUCTION Many factors influence the degree to which a nonnative species will invade new territory as well as the scale of the effects that such species will have on natural communities (Maron and Vila` 2001, Ghersa et al. 2002). One of the most important components of the life history of plants that influences establishment to new areas and replacement and rearrangement of plants within habitats is seed dispersal (Harper 1977). Many nonnative woody plants, like native ones, produce fleshy fruits that depend on frugivores for seed dispersal (Drummond 2005). As such, various attributes of both the fruit and whole shrub would be important for attracting frugivores and affecting the dispersal ability and geographic spread of nonnative plants (Aslan and Rejma´nek 2012). Nutritional qualities of fruits presumably reflect requirements of dispersers: summer fruits being sugar rich to provide quick energy when insects offer protein, whereas autumn fruits are

fat rich to meet energy demands of migrating or winter-resident birds (Stiles 1980, Herrera 1982, Howe and Smallwood 1982). While fruits of some plants are retained on the plants over winter, those of other plants are rapidly removed (Baird 1980, White and Stiles 1992). The arrangement of fruits on branches influences dispersal by affecting frugivores’ cost of foraging and risk of predation (e.g., Denslow et al. 1986, Snow and Snow 1986). On the other hand, large quantities of fruit may be more important in attracting dispersers than arrangement. For example, a positive correlation between crop size and number of fruits removed was found for six autumn-fruiting temperate plants (Davidar and Morton 1986). Colors of fruits, especially in relation to foliage, allow plants to advertise to choice dispersers while remaining inconspicuous to ineffective dispersers and to seed predators, which is the case with ‘‘bird fruits’’ (Wheelwright and Janson 1985). Altogether, color, composition, maturation, and presentation of fruits are key for explaining differences in dispersal ability among plants.

*email address: [email protected] Received February 14, 2013; Accepted June 2, 2014. DOI: 10.2179/13-005

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MCCALL, WALCK: NATIVE AND NONNATIVE SHRUB DISPERSAL

Studies that compare nonnative (highly invasive) species with native species provide insight to the question: What makes a species a good invader? By making comparisons, traits that make nonnative species successful in a region can be identified by controlling confounding factors, particularly if the species are sympatric and are members of the same dispersal guild. In middle Tennessee and throughout eastern United States, Ligustrum sinense Lour. and Elaeagnus umbellata Thunb., originally from Asia, have invaded and become dominant plants in many disturbed landscapes (Sather and Eckardt 1987, Swarbrick et al. 1999, Morris et al. 2002). These two exotics occur with the native species Cornus amomum Mill. and Frangula caroliniana (Walt.) Gray. The four species are shrubs that produce fleshy fruits and are presumably dispersed primarily by birds (Stiles 1980, Fowler et al. 1982, Sather and Eckardt 1987, Williams and Karl 1996, Swarbrick et al. 1999, Drummond 2005). Ligustrum sinense is evergreen and capable of sustaining low levels of photosynthesis during winter months, a trait that confers advantages over native deciduous shrubs such as C. amomum and F. caroliniana (Morris et al. 2002). Elaeagnus umbellata is frequently cited as having early leaf-out (Szafoni 1991, Munger 2003). Both plants are quite tolerant to disturbance and resprout vigorously in response to cutting, mowing, or burning (Szafoni 1991, Swarbrick et al. 1999). Also, E. umbellata is among the few nonleguminous plants to contain bacteria (Frankia) that fix nitrogen (Bond 1976, Berry 1994), which may impart significant competitive advantages in disturbed and infertile soils (Nestleroad et al. 1987). Our study species are sympatric and belong to the same dispersal guild. Thus, we predicted that they would have an equal chance of being dispersed and of attracting dispersers, unless their fruit characteristics differed in such a way to enhance dispersal. As such, the objective of our study was to identify dispersal characteristics that might explain why the nonnative species have a higher abundance and invasiveness than native species via the attraction of dispersers. Specifically, we examined (a) shrub abundance; (b) nutritional and physical characteristics of fruits; (c) number and arrangement of fruits on shrubs; (d) phenology of fruit maturation and leaf coloration; and (e) foraging, fecal

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and regurgitation droppings, and predation of fruits.

METHODS Study Area The study was conducted at Camp Forrest, located approximately 3–8 km east of Tullahoma, in Coffee and Franklin Counties, Tennessee, from July 2003 until February 2004 (McCall 2004). Camp Forrest was one of the Army’s largest training bases during World War II, and it also served as a prisoner of war camp (Arnold Engineering and Development Center [AEDC] 2001). The site was closed in 1946; the buildings and the water, sewage, and electrical systems were all torn down or removed, leaving only roads, chimneys, and concrete foundations. Currently, the site consists mostly of thickets, woods, and open fields (Call 1999).

Shrub Abundance Abundance for each of the four plants was quantified along five transects at Camp Forrest. Along each 25-m transect, shrub presence or absence was recorded at points located every 5 m from 0–25 m, inclusive, on both the left and right edges of a roadway, yielding a total of 12 sample points for each transect. A species was recorded as present if one or more (mature reproductive and >1 m tall) individual plants were located within 2 m of the data point. For each species, frequency was calculated as a percentage (number of occurrences along each transect/total sample points) and then mean – SE was calculated for these percentages.

Characteristics of Fruit Fruits were collected from E. umbellata, F. caroliniana, and L. sinense for analysis of nutritional content; C. amomum fruits were not analyzed because insect infestation destroyed many of them. For each of the three species, fully ripened fruits were obtained from at least 10 different shrubs. Seeds were removed, and two samples of fruit pulp, each weighing at least 10 g, were shipped overnight to A & L Laboratories (Memphis, Tennessee). The fruit pulp was analyzed for moisture content, crude protein (mostly protein þ some nonprotein nitrogen), total digestible nutrients (utilizable material ¼ relative energy value), crude fat (mostly fat þ some ether-soluble materials), acid detergent fiber (highly indigestible material), ash (minerals), and total nitrogen (Henning et al.

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1991, Pinkerton et al. 1991, Perry et al. 1999). Analyses were conducted according to Cunniff (1995) and Horwitz (2000) (see also McCall 2004). Ligustrum sinense and F. caroliniana fruit pulp was first dried to a constant weight in an oven at 408C before shipping, but E. umbellata fruit pulp was shipped as fresh (nondried) material and then dried before analyses. From our collection of fruits, we removed a handful of fruits and randomly counted out 50 and numbered them 1 to 50. Then, length and width were recorded for 12 randomly selected (via random numbers table) E. umbellata and 15 L. sinense fruits using Vernier calipers, and diameter was obtained for 15 F. caroliniana fruits, as they are nearly spherical. Masses of the whole fruit, pulp, and seeds were determined from 15 nondried fruits of each species, and the number of seeds in each fruit was recorded. Mass of pulp also was recorded after drying to a constant value in an oven at 408C. Values for fruit and stone characteristics of C. amomum, when available, were taken from the literature to enable comparisons among the four species, even though the validity of using measures of others (e.g., using different methods or instruments) in the literature may be problematic. Relative dry matter yield (RY), a measure of the pulp reward to dispersers, was calculated for each of the four species (Herrera 1982, 1984, 1987): RY ¼

mean dry mass of pulp mean wet mass of whole fruit

ð1Þ

Number and Arrangement of Fruits For each of the four species, the arrangement of fruit along the branch was quantified when they were fully ripened. One branch was randomly selected from each of 10–12 separate shrubs for L. sinense, F. caroliniana and E. umbellata and from 4 shrubs for C. amomum. Random selection was done by numbering 20 branches on a shrub from 1 to 20 in an orderly fashion to ensure equal dispersion over the shrub, and then using a random numbers table to select the branch. On each branch, the number of fruits was counted within each of eight increments, starting from the branch tip: 0–5, 5–10, 10–15, 15–20, 20–25, 25–30, 30–40, and 40–50 cm. Fruits on lateral stems were counted in the increment where the stem originated. Numbers of fruits in each increment were combined to determine the total number of fruits from 0–50 cm; for all

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species, except L. sinense, this value accurately represents the number of fruits per branch, as most fruiting branches did not bear fruits beyond this point or terminated at the main stem. For L. sinense, the summation underestimates the number of fruits per branch because this shrub continues to produce infructescences past the 50-cm mark.

Phenology of Fruit Maturation and Leaf Coloration On 24 July 2003, 7–12 fruits from separate shrubs of each species were randomly selected and marked with a white thread. When feasible, additional fruits were selected and marked as replacements for ones that fell or were removed prematurely, to maintain adequate sample sizes. For each marked fruit, diameter (to the nearest 0.1 mm) and color characteristics were recorded; the coloration of the foliage along that branch was also noted. Fruit coloration was evaluated based on comparison to a color chart (Grumbachert Color Computer Cat. No. B 420, Leeds, MA) with a visual estimate of percentage surface area that matched each color category. Foliage coloration was determined similarly, except that the percentage estimate was based on all leaves on the branch. Measurements were made at 1–4 week intervals until the fruits were ripe, mostly removed, or severely damaged by insects (as for C. amomum).

Observations on Foraging, Fecal/ Regurgitation Droppings, and Predation Starting on 16 July 2003, transects were visited at 1- or 2-week intervals until November 2003, and then at monthly intervals until February 2004. During visits, we walked along each transect and recorded observations regarding usage of shrubs by animals, particularly birds, mammals, or insects. These visits occurred during any weather condition, except heavy rain, and at various times during the day. We examined fruits and leaves on the shrubs as well as the ground underneath of shrubs for signs of usage, such as regurgitated or defecated seeds/stones, signs of predation on fruits, dispersal (i.e., intact fruits on the ground), or browsing of branches. Results were combined for each species across the entire study period, and the incidence of each type of behavior was categorized as rare, infrequent, occasional, frequent, or common (Table 1).

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Table 1. study

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Criteria used to classify the occurrence of usage behaviors by animals on each shrub species in the

Category

Description

Rare Infrequent

Observed in small numbers on only one occasion, at a single location. Observed in small numbers at a single location on two or three occasions, or observed in small numbers at two or three locations on a single occasion. Observed at multiple locations on two or three occasions. Observed at multiple locations and on several occasions. Usually encountered at nearly all locations.

Occasional Frequent Common

Statistical Analyses

Characteristics of Fruit

Data on shrub abundance, fruit characteristics, fruit number per branch, and phenology of fruit diameter were examined by one-way analyses of variances (ANOVAs) followed by protected least significant difference tests (PLSDs, p ¼ 0.05), or by a t test (SPSS 2000). The arrangements of fruits on branches were examined as a function of number of fruits per increment versus distance from tip of branch. The slopes of the function were compared among the four species by an analysis of covariance (ANCOVA), and then linear regression was used for each species to test for negative, positive, or no trends in fruit arrangement on branches. Log (fruit characteristics, number, arrangement) or arcsine squareroot (shrub abundance, nutrients) transformation corrected for heteroscedasticity.

Percentages of moisture, crude protein and fat, total digestible nutrients, acid detergent fiber, ash, and nitrogen varied significantly among the fruits of F. caroliniana, E. umbellata and L. sinense (1-way ANOVA, p 0.016). Elaeagnus umbellata fruits had significantly higher percentages of moisture, crude protein, nitrogen, and acid detergent fiber than F. caroliniana and L. sinense fruits; F. caroliniana fruits had higher moisture, crude protein, and nitrogen than L. sinense fruits, but L. sinense fruits had higher acid detergent fiber than F. caroliniana (Table 3). Values for moisture and nitrogen of C. amomum fruits were about equal to those of F. caroliniana. On the other hand, percentage of crude fat in fruits (highest to lowest) varied among the species as: L. sinense > C. amomum ¼ F. caroliniana > E. umbellata, and that of ash as: F. caroliniana > L. sinense > E. umbellata. Total digestible nutrients were relatively constant among fruits of F. caroliniana, E. umbellata, and L. sinense. The sizes and masses of fruits differed significantly among F. caroliniana, E. umbellata, and L. sinense (1-way ANOVA, p < 0.001). Fruits of F. caroliniana and E. umbellata were about the same size, and both were significantly

RESULTS Shrub Abundance Frequency of occurrence varied significantly among the four species (1-way ANOVA, p < 0.001). Ligustrum sinense had significantly higher frequency than the other three species; frequency did not differ among C. amomum, F. caroliniana and E. umbellata (Table 2).

Table 2. Frequency of occurrence, number of fruits, and slopes for the function of number of fruits versus distance for native and nonnative shrubs in middle Tennessee Species Native species Cornus amomum Frangula caroliniana Nonnative species Elaeagnus umbellata Ligustrum sinense

Frequency†§

Fruits per Branch†§

Slope

0.350 – 0.116A (0.083–0.667) 0.200 – 0.082A (0.000–0.500)

24.25 – 6.05A 50.80 – 11.87AB

0.0169* þ0.0088ns

0.267 – 0.067A (0.083–0.500) 0.950 – 0.033B (0.833–1.000)

91.00 – 17.60B 414.45 – 87.12C

þ0.0248* þ0.0104ns

†Values with different uppercase letters within columns are significantly different (PLSD, p ¼ 0.05). *Indicates significant difference from zero (p 0.009). ns ¼ not significant. § Frequency (mean – SE; range shown in parentheses) was determined along five transects, and fruit number (mean – SE) and arrangement in the first 50 cm from branch tip were recorded from branches of 4–12 shrubs.

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Table 3. Characteristics (mean – SE) of ripe fruits collected from native and nonnative shrubs in middle Tennessee Native Species

Nonnative Species

Parameter‡

Cornus amomum§

Frangula caroliniana

Elaeagnus umbellata

Ligustrum sinense

Moisture (%) Crude protein (%) Total digestible nutrients (%) Crude fat (%)* Acid detergent fiber (%) Ash (%) Nitrogen (%) Length (mm)** Width (mm)** Whole fruit mass, fresh (mg) Fresh pulp mass (mg) Fresh mass of dispersal unit (mg) Dry pulp mass (mg) Number of dispersal units per fruit Relative dry matter yield

74.62, 79 n.a. n.a. 5.78, 2 n.a. n.a. 0.77 6–9 6–9 203 209 49, 43 16.3, 34 1 0.078

80.29 – 0.18A 4.70 – 0.26A 79.53 – 0.24A 2.51 – 0.32 8.74 – 0.36A 9.20 – 0.47A 0.75 – 0.04A 9.44 – 0.28A 9.44 – 0.28A 444 – 22A 305 – 20A 160 – 35A 64 – 0.2A 3 0.143

85.36 – 1.23B 17.66 – 1.21B 69.00 – 0.00B 0.93 – 0.01 42.45 – 0.05B 2.65 – 0.05B 2.83 – 0.20B 8.80 – 0.15A 7.57 – 0.09B 382 – 16B 276 – 14A 75 – 3B 40 – 4B 1 0.105

63.66 – 1.10C 1.91 – 0.06C 74.06 – 0.55C 7.02 – 3.41 17.12 – 0.84C 3.52 – 0.17C 0.31 – 0.01C 6.51 – 0.13B 5.53 – 0.10C 94 – 4C 54 – 3B 33 – 1C 16 – 1C usually 1 0.174

n.a. ¼ Values not available. ‡ Moisture content is given as percent fresh mass pulp; other nutritional characteristics are given as percent dry mass pulp. Values with different uppercase letters within rows are significantly different (PLSD, p ¼ 0.05). § Data from Borowicz and Stephenson (1985), Borowicz (1988), Gleason and Cronquist (1991), and Witmer (1996). *A one-way ANOVA detected significant differences among the transformed values for crude fat (p ¼ 0.016), but the PLSD was unable to separate means, probably due to low sample size. **Diameter was determined for C. amomum and F. caroliniana fruits, as they are nearly spherical.

larger than those of L. sinense; diameter of C. amomum fruits spanned nearly the entire range of values for fruits from the other three species (Table 3). Fresh masses of whole fruits and dispersal units and values for dry pulp mass were hierarchically arranged (heaviest to lightest) as F. caroliniana > E. umbellata > C. amomum > L. sinense. Fresh pulp masses for F. caroliniana and E. umbellata were similar, and both had significantly higher values than did L. sinense. Frangula caroliniana was unique in producing fruits with three seeds; all others typically bore only one. The relative yield was highest for fruits of L. sinense, followed by those of F. caroliniana, E. umbellata, and C. amomum.

Number and Arrangement of Fruits Number of fruits in the first 50 cm of branch length varied significantly among the four species (1-way ANOVA, p < 0.001). Ligustrum sinense produced a significantly greater number of fruits than the other three species (Table 2). On the other hand, the number of fruits on F. caroliniana did not differ from that of C. amomum or E. umbellata, but C. amomum

had fewer fruits per branch than did E. umbellata. The arrangement of fruits on branches differed significantly among the four species (ANCOVA, p < 0.001). Cornus amomum fruits were clustered near the tips of fruiting branches, and the number of fruits significantly decreased (linear regression, p ¼ 0.009) as the distance from the tip increased (Figure 1, Table 2). In contrast, numbers of E. umbellata fruits significantly increased (regression, p < 0.001) as distance from the tip of the branch increased. Fruits of F. caroliniana and L. sinense were evenly distributed along the branch (regression, p ‡ 0.052).

Phenology of Fruit Maturation and Leaf Color On 24 July 2003, fruits of C. amomum, F. caroliniana, and L. sinense were in the initial stages of ripening (i.e., they were green or yellow-green), whereas those of E. umbellata were mostly fully ripened (i.e., red; Figures 2–3). Fruits of C. amomum turned bluish when fully ripened in late August to early September, and those of L. sinense turned purple by midNovember. Frangula caroliniana fruits were

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Figure 1. Mean (– SE) fruit arrangement along branches from native (A) and nonnative (B) shrubs in middle Tennessee. See Table 2 for statistical analyses.

mostly red in early August and were beginning to turn black in mid-September. Diameter of E. umbellata fruits did not increase between sampling periods, as fruits were already fully ripened (t test, p ¼ 0.236), but diameters of C. amomum, F. caroliniana, and L. sinense fruits significantly increased from 24 July 2003 until they were mature (1-way ANOVA, p < 0.001; Figure 4). Leaves of L. sinense and E. umbellata remained mostly green during the peak of fruit maturation (Figure 3). In contrast, C. amomum leaves turned red before autumn abscission and F. caroliniana leaves turned yellow (Figure 2). The change in leaf coloration of C. amomum mostly occurred after its fruits were fully ripened, and that of F. caroliniana occurred after its fruits had turned red but before they ripened and turned black.

Observations on Foraging, Fecal/ Regurgitation Droppings, and Predation Observations of usage of C. amomum by birds were scarce (Table 4). However, insect foraging

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and evidence of arthropod damage to C. amomum shrubs were abundant. Mutilated and partially consumed fruits were commonly observed on F. caroliniana shrubs, and regurgitated or defecated seeds of F. caroliniana fruits were frequently observed on or near the shrubs. Although evidence of bird usage of F. caroliniana fruits, in the form of mutilated fruits as well as regurgitated seeds, was abundant, there was only one occasion when birds were observed carrying out these actions. Evidence of usage of E. umbellata fruits by birds and other animals was ubiquitous (Table 4). Regurgitated seeds were commonly observed on the leaves of the shrub and on the ground below. Signs of seed predation were abundant; cracked and emptied seed husks were commonly found on the ground, and to a lesser extent, on the leaves of the shrubs. Ants and hemipterans were commonly seen foraging on shrubs of E. umbellata, and evidence of arthropod damage was frequently encountered. Seeds of this species also were observed in coyote or fox scat at the site. Birds and small mammals were frequently flushed out of E. umbellata shrubs upon approach. Regurgitated and defecated seeds of L. sinense were frequently found on leaves of L. sinense, on leaves of nearby shrubs of other species, and on the ground (Table 4); however, observations of birds actually handling or eating L. sinense fruits were rare. No evidence of seed predation of L. sinense was observed. Indications of arthropod damage to fruits were frequently observed, in the form of shriveled fruits or webbing around fruit clusters, and soft scale insects were occasionally seen on L. sinense branches. Although birds commonly used L. sinense shrubs when perching or as cover upon retreat, it was not determined whether birds nested or roosted in L. sinense shrubs. Evidence of browsing, presumably by deer, also was abundant and became more so toward the end of winter.

DISCUSSION Among the nutritional parameters evaluated, those associated with the selection of fruits by birds include water content, fat, and protein (Herrera 1982, Johnson et al. 1985). Seasonal trends in fruit nutrition are apparent in the present study: water content was highest for the summer-fruiting species (E. umbellata) and lowest for the late autumn/ winter-fruiting species (L. sinense). This trend

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Figure 2. Phenology of fruit maturation and leaf coloration for native shrubs in middle Tennessee between July 2003 and September 2003.

has been reported in other studies, and may correspond with an increased (summer) water need for dispersers (Stiles 1980; Herrera 1982, 1984). Any pattern in fat composition of the fruits studied is obscured by the highly disparate values for C. amomum; omitting these values allows an increasing trend in fat content from summer to winter. We acknowledge, however, that caution must be applied when comparing results from the literature since the methods of the papers cited varied from our methods. Although this increase corresponds with increased energy demands of dispersers, there is little evidence that avian dispersers prefer lipidrich fruits or remove them at higher rates than lipid-poor fruits (Johnson et al. 1985, Borowicz 1988, Lepczyk et al. 2000). Eleagnus umbellata

fruits had higher protein content, on par with values in Parmar and Kaushal (1982), compared to the other study species. The high protein content of E. umbellata fruits is perplexing, as very few fleshy-fruited species provide such high levels of protein in any season (Herrera 1987). This high protein quantity may entice dispersers that would otherwise feed on insects during the late summer. Fruits of F. caroliniana were rapidly removed (L. McCall, pers. obs.), and literature accounts indicate that those of C. amomum are as well (Stiles and White 1982, Borowicz and Stephenson 1985, Dirr 1995, Drummond 2005). Similarly, E. umbellata fruits do not remain attached to the shrub for very long; they either fall to the ground or are removed quickly, and the few that do

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Figure 3. Phenology of fruit maturation and leaf coloration for nonnative shrubs in middle Tennessee between July 2003 and October or November 2003.

Figure 4. Diameter (mean – SE, SE shown if ‡0.2) of fruits from native (Cornus, Frangula) and nonnative (Elaeagnus, Ligustrum) shrubs in middle Tennessee between July 2003 and November 2003.

remain are damaged by insects or microbes. Apparently, the relatively high temperatures and humidity levels during summer place summerripening fruits at an increased exposure to insect and microbial pests. Thus, quick removal would be advantageous for summer-ripening plants. On the other hand, fruits of L. sinense remain attached to the plant for many weeks following maturation (L. McCall, pers. obs.; also reported in Batcher 2000, Mikowski and Stein 2008) and ripen at a time of the year (late autumn/winter) when microbial and insect attack would be greatly reduced. Although the patterns of fruit presentation along the fruiting branch differed among the four shrub species studied, a more meaningful pattern emerges with a comparison of fruits produced per branch. Ligustrum sinense produced more fruits per branch than did any of the

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Observations of usage by animals of native and nonnative shrubs in middle Tennessee Native Species

Nonnative Species

Observation

Cornus amomum

Frangula caroliniana

Elaeagus umbellata

Ligustrum sinense

Regurgitated/defecated seed/stone (pulp removed)§ Husk of seed/stone only (i.e., seed predation)§ Fruit partially eaten or mutilated§ Handling of fruit‡ Nonfood use of shrub^ Arthropod damage to fruit Insect foraging§§ Intact fruits below shrub Seeds/stones in nonbird feces Evidence of browsing

infrequent not observed infrequent not observed rare common common not observed not observed not observed

frequent not observed common infrequent frequent infrequent not observed infrequent not observed not observed

common common frequent rare common frequent common common occasional rare

frequent not observed occasional rare common frequent occasional common rare frequent

§

On plant or ground. By birds. By birds or mammals; examples include use of shrub for cover or as perch. §§ On any part of shrub, including fruit. ‡

^

other shrubs studied; E. umbellata produced the second highest number of fruits per branch, although its values were not significantly different from those of F. caroliniana. Moreover, our fruit number for L. sinense is underestimated since we did not count fruits beyond our 50-cm mark on the branch even though fruits were present. If we consider the number of seeds per fruit, L. sinense still has the highest fecundity but F. carolina might be higher than E. umbellata. However, we should be cautious in our assessment of seed production since we did not (1) determine number of seeds in each fruit, and (2) measure seed viability. Many studies have indicated the large fruit crops of nonnative plants as an important factor in their invasive success (Kolar and Lodge 2001, Ghazoul 2002). Prolific seed production of both nonnative shrubs has not gone unnoticed. Westoby et al. (1983) reported means of 1,300 fruits/m2 and 2,800 fruits/stem in L. sinense; Montaldo (1993) found 990 mature fruits/m2 and calculated the average production to be 13,860 fruits per plant. Studies of E. umbellata have reported that mature specimens are capable of producing 0.9–3.5 kg seed/year (Sather and Eckardt 1987). Fruit count of F. caroliniana was 41% of that of the exotic Rhamnus cathartica (Stewart and Graves 2006). Fruit ripening of the native shrubs corresponded with autumn avian migration, which generally starts in late August and peaks during September and October (Stedman 2004a, 2004b, 2004c). The native shrubs have fruits that are representative

of the ‘‘typical’’ dispersal syndrome of autumnripening, fleshy-fruited, bird-dispersed shrubs: in terms of fruit coloration per se and employing bicolored displays (i.e., fruit color contrasts with foliage or other structures). Utilization of F. caroliniana was abundant, indicating that its fruits can effectively attract frugivores. Observations on animal usage of C. amomum were inconclusive because insects destroyed most of the fruits; however, literature accounts indicate that it, too, is heavily utilized when fruiting (Borowicz and Stephenson 1985, Dirr 1995). The finding that E. umbellata produces summerripening fruits was in contrast to most literature accounts stating that fruits ripen in autumn, generally September to October (e.g., Sather and Eckardt 1987, Dirr 1995). However, Parmar and Kaushal (1982) and Zheng et al. (2004), who describe the plant in different parts of its native range in Asia, report the fruiting season to be mid-July until mid-August, which is consistent with the findings of the present study. Thus, of the two nonnative shrubs studied, E. umbellata presents fruits prior to the beginning of autumn migration that are therefore dispersed primarily by summer residents, while L. sinense fruits ripen after most autumn migrants have departed, remaining available to winter residents. Ligustrum sinense was nearly ubiquitous at the study site, whereas the frequency of E. umbellata was not different from that of the two native shrubs. Elaeagnus umbellata appears to be eaten by a broad array of potential dispersers, yet the persistence of the fruits is limited, which

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distinguishes it clearly from L. sinense. Seed predation may also play an important role in limiting the spread of E. umbellata, as this species was the only shrub in which seed predation was widespread and commonly observed. Dispersal of the native species appears targeted toward avian migrants, whereas that of the nonnative species is mostly by residents. As compared to the two native species and to the nonnative E. umbellata, L. sinense produces an enormous quantity of fruits. These two parameters increase the opportunities for establishment of L. sinense by (1) allowing dispersal by several assemblages of frugivores, and (2) saturating the environment with its seeds. Although we cannot completely rule out other factors that might influence L. sinense (e.g., soil type), its dispersal advantages would seem to play an important role in its distribution and abundance at the study site and throughout eastern North America.

ACKNOWLEDGMENTS Funding was provided by the Thomas C. Hemmerly Research Scholarship from the Department of Biology at Middle Tennessee State University. Special thanks are given to J. Lamb, C. Miller, and K. Fitch for assistance in site selection and allowing access to the Camp Forrest area, and C. Koczaja for aid in data collection. LITERATURE CITED

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