Seed Germination and Seedling Recruitment of

RESEARCH NOTE

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Seed Germination and Seedling Recruitment of Japanese Honeysuckle in a Central Arkansas Natural Area Sherry P. Fowler Department of Biology University of Central Arkansas 201 Donaghey Avenue Conway, Arkansas 72035

Katherine C. Larson1 Department of Biology University of Central Arkansas 201 Donaghey Avenue Conway, Arkansas 72035

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1

Corresponding author: [email protected]

Natural Areas Journal 24:49–53

Volume 24 (1), 2004

ABSTRACT: Nonindigenous plant species are an increasingly common problem in natural areas and effective management of invasive plants depends in part on accurate information about the life history of the invading species. The negative impact of Lonicera japonica, Japanese honeysuckle, on native plant communities is well known, as is this species capacity for prolific vegetative spreading by trailing stems. Surprisingly, despite being known for impressive floral displays, the capacity of L. japonica for establishment by seed is not known. We found that natural seedling recruitment rate in a L. japonica invaded state park in central Arkansas was only 0.002 seedlings per m2 germinating and surviving one year. Results from experimental seed sowings indicated that germination of L. japonica seeds was patchy, but not significantly different in a shady forest interior and a sunnier forest edge, or impacted by predation or ground cover. Overall, 13.8% of the 2400 seeds sowed germinated from early spring to summer during the first year; no seeds germinated from the experimental plots the following spring, indicating no evidence of a seed bank in our study. Of the seeds that germinated, 14.4% survived one year in the forest interior, while no seedlings survived one year at the forest edge. Index terms: invasive plants, seed germination, seedling recruitment, Lonicera japonica, nonindigenous plant

INTRODUCTION Managers of most natural areas face decisions not about whether to battle nonindigenous species, but which species to direct limited financial resources toward. Information on community-wide impacts of each non-indigenous species as well as the feasibility of control can be critical in making management decisions and in pointing out future research areas (Hiebert 1997). One invasive species with welldocumented impacts in eastern and southeastern states is the woody twining vine, Japanese honeysuckle (Lonicera japonica Thunb.). It can suppress ground vegetation and foliage production of understory vegetation in deciduous forests (Handley 1945, Thomas 1980, Friedland and Smith 1982, Hardt 1986), reduce the growth of trees by root competition (Whigham 1984), and cause crown deformation when it climbs shrubs and small trees in forest gaps (Thomas 1980). This leads to long-term dominance by L. japonica and alteration of the native species composition (Thomas 1980, Friedland and Smith 1982). While the negative impacts of Lonicera japonica on native communities are well documented, and it is clear that L. japonica has a strong capacity for vegetative spread through the production of horizontal stems or stolons, its potential for sexual reproduction is not well known. In her review, Nuzzo (1997) concluded that L. japonica can create a vast seed bank from its prolific production of bird and mammal dispersed berries, and that its seeds were

capable of germinating and surviving in shaded environments. In contrast, the USDA Plants database cites a low fruit abundance and slow seed spread rate for L. japonica (USDA 1999). In this study, we examine natural recruitment rates and field germination rates for L. japonica in a natural area in Arkansas. Specifically, we address the following questions: (1) what is the germination rate and one-year survival rate of experimental field seed sowings of L. japonica; (2) how is germination rate and survival influenced by predation, cover, and site; and (3) what is the natural rate of seedling recruitment of L. japonica in a natural area? METHODS We examined the natural seedling recruitment rate of Lonicera japonica in a temperate oak-hickory forest with an abundance of mature Japanese Honeysuckle in the immediate area and in the surrounding landscape. The research area was in an oak-hickory forest in Woolly Hollow State Park in central Arkansas (Faulkner County, 35°10’ N, 92°27’ W). To quantify natural levels of seedling recruitment in Woolly Hollow State Park, we monitored seedling germination and survival in 45 randomly placed 1 m radius circular plots along a small creek. We counted and mapped all seedlings, regardless of species, that germinated in each subplot at four sample times in the spring and summer of 1998. Seedlings identified as L. japonica were then monitored for the Natural Areas Journal 49

next two years. We also measured recruitment (germination and survival) from experimentally sowed seeds. We contrasted two habitat types, a sunny forest edge and a shady forest interior. In the forest interior, we randomly selected six of the previously established plots and along the sunny edge we randomly placed an additional six plots. Each plot contained four treatment subplots examining the influence of two factors known to influence germination rate: predation rate (Borchert and Jain 1978, Mittelbach and Gross 1984) and the amount of ground cover, i.e. plant biomass and litter (McPherson and Thompson 1972, Reader 1991). The four treatment subplots per plot were: (1) removing surface litter and protecting the subplot from predators; (2) removing surface litter with the subplot unprotected from predators; (3) leaving surface litter intact and protecting the subplot from predators; and (4) leaving surface litter intact with the subplot unprotected from predators. Each treatment subplot was made by hammering a PVC tube, 9.9 cm in diameter and 8 cm in height, into the ground to a depth of 4 cm creating an open-topped enclosure containing undisturbed forest soil. For the subplots requiring protection from predators, the open tops were covered with 1 mm fiberglass screen. Fifty seeds of Lonicera japonica were sown directly onto the soil of each subplot in mid-December 1998 to allow seed dormancy to be broken naturally. The seed source was a population of L. japonica at Pierce Creek Landing located on Lake Conway near Conway, Arkansas. The seeds were removed by hand from mature berries and cleaned in water before being sown in the subplots. All subplots were checked every week through July 1999 and every two weeks thereafter for emerged seedlings until March 2000. A General Linear Model was run to determine that blocking was not significant for the plots at both sites. When a three-way ANOVA (factors: ground cover, predation, site) showed the interaction term was not significant, the ANOVA test results for the main effects were used to determine significant differences (p < 0.05). The data was LOG10 transformed to obtain normal50

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ity and homogeneity of variances. RESULTS

japonica seedling out of the 45 subplots censused represents 0.002 seedlings per m2 that survived beyond the initial germination phase.

Natural Recruitment A total of 556 seedlings germinated in the 45 1-m radius plots in spring and summer of 1998, but only three of these 556 seedlings were Lonicera japonica. This represents a germination rate for L. japonica of 0.007 seedlings per m2. By December 1998, one L. japonica seedling was missing and by the end of January 1999, one L. japonica seedling had survived. Over the next year this seedling was monitored, and still existed as of March 2000. One established L.

Experimental Seed Sowing Overall, the percent of seeds germinating was somewhat higher in the forest interior (mean ± s.e. = 16.3 ± 3.34%) than at the forest edge (mean ± s.e. = 11.3 ± 4.18%) although the difference was not significant (p = 0.237). We also found no evidence that predation or ground cover were important factors determining germination (Table 1). If the variation in germination rate among subplots was due to heterogeneity of the plots, such as patchy differences in light,

Table 1. ANOVA results on blocking factor and main effects for the experimental field germination of Lonicera japonica.

DF

MeanSquare

F-ratio

p value

Blocking

1

0.226

0.782

0.382

Predation

1

0.070

0.244

0.624

Ground Cover

1

0.007

0.026

0.873

Site

1

0.413

1.439

0.237

Predation* Ground Cover

1

0.087

0.303

0.585

Predation*Site

1

0.074

0.258

0.614

Ground Cover*Site

1

0.122

0.425

0.518

Predation* Ground Cover*Site

1

0.505

1.758

0.192

Figure 1. The number of Lonicera japonica seeds germinating per subplot at the forest edge and in the forest interior. Each point indicates one subplot in which 50 seeds were experimentally sowed.

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moisture, or soil characteristics, the subplots within each plot would be expected to show similar germination patterns. A General Linear Model showed that blocking due to the location of the twelve plots was not significant (p = 0.382, Table 1), indicating that the variation was at the level of the subplots. Seed germination was strongly clumped in some subplots. While most subplots had zero to few L. japonica seeds germinating, a few subplots had high rates of germination (Figure 1). The pattern of observed germination differed significantly from the pattern expected if seeds germinated randomly (calculated from the Poisson distribution, Chi-square = 141.0, df = 46, p < 0.001).

Figure 2. Number of Lonicera japonica seeds that germinated in experimentally sowed plots each month from January 1999 through March 2000.

Most of the Lonicera japonica seeds germinated from late February (149 seeds) through the first week of April in 1999 (296 of the 330 seeds that germinated, Figure 2). No seeds germinated after June 1999, approximately six months after they were sown. The lack of any seed germination in February and March 2000 indicated no capacity for year to year survival of L. japonica seeds in the soil. Seedling survival was higher in the shady forest interior than on the sunny forest edge. At the beginning of August 1999, one seedling had survived at the forest edge, and 55 seedlings were surviving in the forest interior. In October 1999, the forest edge had no seedlings surviving, and the forest interior had 38 surviving seedlings of L. japonica. By March 2000, there were 28 L. japonica seedlings that had survived in the forest interior, or 14.4%, and none at the forest edge (Figure 3). DISCUSSION

Figure 3. Number of Lonicera japonica seedlings surviving in the experimentally sowed sub-plots each month from January 1999 through March 2000. The number of seedlings reported here includes both the addition of new seedling through new germinations (see Figure 2) and the loss of seedlings through mortality.

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Lonicera japonica seedling recruitment in a natural forest in Arkansas with an established population of mature L. japonica was only 0.002 seedlings per m2 germinating and surviving two years. We found no other studies documenting the natural recruitment rate of L. japonica in the United States for comparison to our findings. Published comments on seedling establishment, unsupported by empirical data, ranged from

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those reporting abundant reproduction from seed (Bruner 1967, Carter and Teramura 1988) to those reporting low seedling recruitment (USDA 1999). Another invasive honeysuckle, the shrubby Lonicera maackii (Rupr.) Maxim., had much higher recruitment rates in an invaded forest in the eastern U.S., ranging from 5 seedlings to 328 seedlings per m2 from the forest edge to the forest interior, respectively (Luken and Goessling 1995). Low seedling recruitment can be due to low fruit set, low germination, or high mortality of germinated seedlings; all appear to contribute to low rates of recruitment in Arkansas. For example, we found that Lonicera japonica in areas near our study plots averaged only 17% fruit set (Larson et al. 2002). Although germination of field collected seed was 70% under laboratory conditions (Fowler 2000), only 13.8% (330/2400) of field collected seeds germinated in experimental field sowings. Survival of seedlings after germination was also low, with only 8.4% (28/330) of the germinated seedlings surviving one year in this study. These results from our experimental sowing of field-collected seeds were consistent with our survey data on natural rates of recruitment and lead us to conclude that seedling establishment in Arkansas is limited. We found no evidence of seeds surviving in the soil to form a seed bank. The fruits of Lonicera japonica mature in November and persist on the plants through January, with the majority falling to the ground rather than being eaten by potential dispersers (Fowler 2000). Of the 2400 seeds we sowed in December 1999, 2070 seeds remained ungerminated in the soil six months later; none of these seeds germinated the next year. Two other recent studies on germination of L. japonica also have found that seed germination is limited to the first spring following development (Hidayati et al. 2000; Shelton and Cain 2002). We could identify no clear patterns explaining the causes of low germination in our study or the patchiness we found. Germination in a few subplots was similar to the 70% rate that we found in greenhouse germination trials (Fowler 2000), but the

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differences between subplots could not be attributed to seed source, predation, litter cover, or the difference between a sunny edge and shady forest site. Because the pattern of germination was significantly clumped, the low germination in many plots must be due to some as yet unidentified environmental factor that varied among subplots. The low rates of seedling recruitment by Lonicera japonica that we documented in Arkansas have several implications for understanding and managing populations of this invader within natural areas. First, documenting the capacity of any invasive plant to infest or reinfest natural areas through seed dispersal and establishment is necessary for developing sound management plans (Hiebert 1997). Low seedling recruitment has not prevented L. japonica from severely infesting natural areas within Arkansas, apparently due to its capacity for clonal spread following intentional plantings by humans or the relatively rare event of establishment from seed. However, clonal spread is relatively slow, with L. japonica moving an average of 2 m per year (Larson 2000). Decisions about controlling heavy infestations of L. japonica might be very different depending on whether the plant was spreading mainly through clonal growth or through seedling dispersal and establishment. In areas with low seedling recruitment, expensive removal of established plants and monitoring for recolonization may be feasible, while in an area with good seed dispersal and seedling recruitment, removals of established plants may not significantly impact L. japonica populations. Second, a contrast of our results with other published accounts indicates that there is insufficient information to conclude whether there is significant geographic or temporal variation in the capacity of Lonicera japonica to establish from seed. The only other empirical study we found reported a 63% germination rate of field sowed L. japonica seeds on a farm near the University of Tennessee, with an 18% survival rate one year later (Leatherman 1955). Anecdotal comments about high seedling recruitment are from more eastern states (Bruner 1967; Sasek 1985; Carter

and Teramura 1988). Sasek and Strain (1990) suggested that the western edge of the distribution of naturalized populations of L. japonica was set by lack of seedling establishment due to water stress. The years of this study, 1998, 1999, and early 2000, all had lower than normal levels of precipitation (average of 19.3 cm below the normal of 110.2 cm) while the two years before and after our study were slightly above normal (average of 6.4 cm above normal). It is possible that our results are influenced by the lower than average rainfall during the study. If there is significant temporal or geographic variation in the capacity to establish by seed, different management practices will be necessary under different climatic conditions and across the geographic range of L. japonica in the United States. It seems clear to us that the next step is to gather information on the capacity of L. japonica for establishment from naturally dispersed seed from a range of geographic sites and under different climatic conditions. ACKNOWLEDGMENTS We thank the Superintendent and Staff at Woolly Hollow State Park, Greenbrier, Arkansas for permission to carry out this research and their never-ending help, and to Dr. Don Culwell and Dr. Dan Magoulick for their advice. Thanks also to the University of Central Arkansas Graduate Research Fellowship and the Arkansas Native Plant Society who supported this research with grants. Sherry Fowler received her Master of Science in Biology at the University of Central Arkansas working on this project. She currently teaches high school and maintains a research interest in invasive and native plants of Arkansas. Katherine C. Larson is Associate Professor of Biology at the University of Central Arkansas. She is a plant ecologist studying both invasive and native vines and the relationships they establish with native animals.

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LITERATURE CITED Borchert, M.I. and S.K. Jain. 1978. The effect of rodent seed predation on four species of California annual grasses. Oecologia 33:101-113. Bruner, M.H. 1967. Honeysuckle – a bold competitor on bottomland hardwood sites. Forest Farmer 26:9-17. Carter, G.A. and A.H. Teramura. 1988. Nonsummer stomatal conductance for the invasive vines kudzu and Japanese honeysuckle. Canadian Journal of Botany 66:2392-2395. Fowler, S.J. 2000. Fruit set and seedling recruitment in Lonicera japonica, Japanese honeysuckle. M.S. thesis, University of Central Arkansas, Conway. 40 pp. Friedland, A.J. and A.P. Smith. 1982. Effects of vines on successional herbs. The American Midland Naturalist 108:402-403. Handley, C.O. 1945. Japanese honeysuckle in wildlife management. The Journal of Wildlife Management 9(4):261-264. Hardt, Richard A. 1986. Japanese honeysuckle: from “one of the best” to ruthless pest. Arnoldia 46(2):27-34. Hidayati, S.N., J.M. Baskin and C.C. Baskin. 2000. Dormancy-breaking and germination requirements of seeds of four Lonicera species (Caprifoliaceae) with underdeveloped spatulate embryos. Seed Science Research 10:459-469. Hiebert, R. 1997. Prioritizing invasive plants and planning for management. Pages 195212 in Assessment and management of plant invasions, J. Luken and J. Thieret (eds.). Springer, N.Y.

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Larson, K.C. 2000. Circumnutation behavior of an exotic honeysuckle vine and its native congener: influence on clonal mobility. American Journal of Botany 87(4):533538. Larson, K.C., S.J. Fowler, and J. Walker. 2002. Lack of pollinators limits fruit set in the exotic Lonicera japonica. The American Midland Naturalist 148:54-60. Leatherman, A.D. 1955. Ecological life-history of Lonicera japonica Thunb. Ph.D., University of Tennessee, Knoxville. 97 pp. Luken, J.O. and N. Goessling. 1995. Seedling distribution and potential persistence of the exotic shrub Lonicera maackii in fragmented forests. The American Midland Naturalist 133:124-130. McPherson, J.K. and G.L. Thompson. 1972. Competitive and allelopathic suppression of understory by Oklahoma oak forests. Bulletin of the Torrey Botanical Club 99(6):293-300. Mittelbach, G.G. and K.L. Gross. 1984. Experimental studies of seed predation in old-fields. Oecologia 65:7-13. Nuzzo, V. 1997. Element stewardship abstract for Lonicera japonica. The Nature Conservancy, Arlington, Va. Available online . Reader, R.J. 1991. Control of seedling emergence by ground cover: a potential mechanism involving seed predation. Canadian Journal of Botany 69:2084-2087.

Sasek, T.W. 1985. Implications of atmospheric carbon dioxide enrichment for the physiological ecology and distribution of two introduced woody vines, Pueraria lobata Ohwi (kudzu) and Lonicera japonica Thunb. (Japanese honeysuckle). Ph.D. dissertation, Duke University, Durham, N.C. 218 pp. Sasek, T.W. and B.R. Strain. 1990. Implications of atmospheric CO2 enrichment and climatic change for the geographical distribution of two introduced vines in the USA. Climatic Change 16:31-51. Shelton, M.G. and M.D. Cain. 2002. Potential carry-over of seeds of 11 common shrub and vine competitors of loblolly and shortleaf pines. Canadian Journal of Forestry Research 32:412-419. Thomas, L.K., Jr. 1980. The impact of three exotic plant species on a Potomac island. National Park Service Science Monograph No.13. U.S. Department of the Interior, Washington, D.C. 197 pp. USDA, NRCS (Natural Resources Conservation Service). 1999. The PLANTS database: invasive. Available online . Whigham, D. 1984. The influence of vines on the growth of Liquidambar styraciflua L. (sweetgum). Canadian Journal of Forestry Research 14:37-39.

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