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An Invasive Plant Species Decreases Native Plant Reproductive SuccessAuthor(s): Brenda Molano-FloresSource: Natural Areas Journal, 34(4):465-469. 2014.Published By: Natural Areas AssociationDOI: http://dx.doi.org/10.3375/043.034.0408URL: http://www.bioone.org/doi/full/10.3375/043.034.0408
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Volume 34 (4), 2014 Natural Areas Journal 465
Natural Areas Journal 34:465469
An Invasive Plant Species Decreases
Native Plant Reproductive
1Illinois Natural History SurveyChampaign, IL 61820
R E S E A R C H N O T E
2 Corresponding author: firstname.lastname@example.org; 217-265-8167
ABSTRACT: Invasive plants may have negative, positive, or neutral effects on the reproductive success of native plant species. In this study, I investigated the impact of the rhizomatous invasive species Securigera varia (Fabaceae; crown vetch; synonym: Coronilla varia) on the reproductive success of the native prairie species Tradescantia ohiensis (Commelinaceae; Ohio spiderwort). In particular, I examined how T. ohiensis plant height, fruit set, seed set, and stigma pollen load differed inside or at the edge of crown vetch patches and within native prairie not invaded by crown vetch. A significant reduction in reproductive success and pollen deposition was detected among T. ohiensis plants in the interior of a crown vetch patch compared to those at the edge of a crown vetch patch. These, in turn, had lower reproductive success and pollen deposition than plants in the native prairie areas. Also, T. ohiensis plants were taller inside crown vetch patches. The results of this study suggest that rhizoma-tous invasive species such as Securigera varia can have direct and indirect impacts on the reproductive success of native species.
Index terms: invasion front, invasive, reproductive success, rhizomatous growth, self-incompatible, Tradescantia ohiensis
In the last decade, numerous studies (e.g., Larson et al. 2006; Traveset and Richard-son 2006 [and citations therein]; Nielsen et al. 2008; Montgomery 2009a, 2009b; Dietzsch et al. 2011; Thijs et al. 2012 [and citations therein]; Sun et al. 2013) have addressed the question: Do invasive plant species compete with native plant species for pollinators? These studies have shown negative, positive, and neutral effects re-garding the impact of invasive species on the reproduction of native species. This range of observed effects can be explained by various factors that can influence the abundance and behavior of pollinators available to native and invasive plant spe-cies. These include habitat and blooming overlap, plant species abundance (popula-tion size and population density), shared pollinators (including flower similarity and rewards [pollen and nectar]), and plant breeding system (e.g., self-compatible or self-incompatible).
Growth form and the rate of expansion of an invasive species can also influence the seriousness of its impact. For example, invasive species that spread by rhizomes or stolons can form solid mats overgrowing and overcrowding native species and, due to their rate of expansion (Cousens and Mortimer 1995), can overtake the habitat of native species in a relatively short amount of time (e.g., kudzu [Pueraria montana (Lour.) Merr. variety lobata (Willd.)]; Forseth and Innis 2004). Cousens and Mortimer (1995) noted that an invasive species patch can grow by half the dis-tance of the previous year as long as there
is successful recruitment and a constant expansion rate. As such, native species are continually competing with these invasive species for resources.
How good of a competitor a native spe-cies is against other native species has not been evaluated in most existing native and invasive plant species studies (i.e., com-munity level, but see Lopezaraiza-Mikel et al. 2007; Dietzsch et al. 2011). The great majority of these studies have determined whether or not a native species is receiv-ing enough pollen (i.e., is pollen limited) by conducting supplemental pollinations (e.g., Powell et al. 2011), or by detecting the presence of heterospecific pollen from invasive species (e.g., Brown et al. 2002). Determining how good of a competitor the native species is in the absence of the invasive species is also important, as this can improve our understanding of the true impact of the invasive species. In the present study I investigate spatial overlap and native species competitive ability by determining how native plant height, fruit set, seed set, and stigma pollen load differ inside an area dominated by an invasive species, at the edge of this area, and within an area of native prairie in which the in-vasive species is not present.
I used the native prairie species Tradescan-tia ohiensis Raf. (Commelinaceae; Ohio spiderwort) in this study for the following reasons: (1) it is a perennial self-incompat-ible species (Owens and McGrath 1984), (2) its flowers open early in the morning and wilt by midafternoon (Runkel and Roosa 1989), (3) it shares pollinators (long-tongued bees [especially bumblebees] and
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honey bees) with Securigera varia (L.) Lassen (Fabaceae; crown vetch), and (4) it is a common species at the study site. Secu-rigera varia was the invasive species used in this study. It is an herbaceous perennial legume introduced from the Mediterranean region. It is considered a serious manage-ment threat in natural areas because of its seed bank and rapid vegetative spreading that results in monocultures that can com-pletely cover and shade native vegetation (Solecki 1997; Symstad 2004; Losure et al. 2009). The formation of this dense mat is the result of extensive vegetative growth from multibranched rhizomes (Solecki 1997). Aboveground crown vetch stems can spread horizontally up to 1.8 meters (Tu 2003). In flower, crown vetch can grow to a vertical height of 1 m (Gucker 2009; B. Molano-Flores, pers. obs.). In addition to its aggressive vegetative growth, crown vetch plants produce copious amounts of pinkish-white to deep pink flowers in long-stalked clusters. Though crown vetch has been recognized as a management problem for habitats such as prairies and savannas (Solecki 1997), limited research has been published on its impacts at the species, community, and ecosystem levels (e.g., Wheeler 1974; Walck et al. 1999; Symstad 2004).
This study was conducted at the Lost Mound Unit of the Upper Mississippi River National Wildlife and Fish Refuge (Lost Mound) in southwestern Jo Daviess and northwestern Carroll counties in Illinois, USA. Lost Mound is approximately 10,000 ha and includes both floodplain wetlands and uplands. The floodplain wetlands con-sist primarily of floodplain forest, slough, emergent marsh, and wet meadow, while the uplands consist primarily of sand prai-rie, oak-ash savanna, and woodland (U.S. Fish and Wildlife Service 2002; Wenny et al. 2006). At the site, crown vetch is found predominantly in dry and dry-mesic sand prairie as single plants, small patches, or large patches enveloping large sections of prairie. In 20092010, a crown vetch survey conducted at Lost Mound confirmed the
impact of the species at the site. Out of the 2023 ha of sand prairie, crown vetch covered approximately 405 ha (i.e., 20%) and continues to expand (B. Molano-Flores, unpubl. data).
In 2008, five patches of crown vetch that were nearly dominated by this species and were of a similar size (approximately 30-m diameter), flower density/m2 (average 247/m2), and had similar surrounding native sand prairie vegetation, were selected from throughout Lost Mound. These patches were revisited in 2009. In June of each year, 10 Tradescantia ohiensis plants with a single flowering stalk were tagged within each of the five crown vetch patches and 10 at the edge of each of the five crown vetch patches. All plants selected were at least 2 meters apart from each other and plants selected within a crown vetch patch were at least 4 meters from the edge of the patch. Tradescantia ohiensis plants at the edge of a crown vetch patch were located at the perimeter of the patch (i.e., within the boundary between crown vetch and sand prairie). In addition to these crown vetch patches, five native sand prairie areas that had not been invaded by crown vetch but that did have T. ohiensis, were also selected from throughout Lost Mound. These na-tive sand prairie areas had a similar plant composition to the ones found adjacent to the crown vetch patches. In addition, the sizes of these areas were similar to the crown vetch patches (approximately 30-m diameter). In June of 2008 and 2009, 10 T. ohiensis plants with a single flowering stalk were tagged within each of these areas. Tagged plants were at least 2 meters apart from each other. These plants were includeed to determine the overall reproductive success of T. ohiensis in an un-invaded plant community. In August, maximum plant height was measured and the entire flowering stalk was collected to assess fruit and seed set. Fruit and seed set were determined as follows: fruit set = total number of fruits per plant/total number of flowers per plant; seed set = total number of seeds per fruit/six. The total number of seeds per fruit was divided by six because T. ohiensis flowers have six ovules. Deter-mining seed set in T. ohiensis is possible
even if the fruits have dehisced and seeds have been dispersed. Tradescantia ohiensis has a loculicidal capsule (3 locules with 2 ovules per locule) and if a seed is formed, the ovary wall will expand (versus no ex-pansion of the ovary wall in an unfertilized ovule). Also, the unfertilized ovule will be present as a shriveled paper-like ovule in the locule. Lastly, all T. ohiensis plants were selected haphazardly, and on average had 64 flowers per single flowering stalk.
In addition to fruit and seed set, stigma pollen load (i.e., the number of pollen grains on a stigma) was used as a sur-rogate to determine pollinator visitation and presence of heterospecific pollen. In June 2008 and 2009 at the peak of the T. ohiensis blooming period, flowers (1 per inflorescence) were collected haphazardly from plants no closer than 2 meters apart at each of the study areas (i.e., 5 crown vetch patch interiors, 5 crown vetch patch edges, and 5 native sand prairie areas) and put in formaldehyde-acetic acid. Flower collec-tion was conducted at the end of the day as flowers open early in the morning and wilt by midafternoon. From the collected flowers, 10 stigmas from each study area were dissected and stained with fuchsin, then put on microscope slides with a drop of glycerin, a mounting medium, and covered with a cover slip. Tradescantia ohiensis pollen and heterospecific pollen were counted on a total of 300 stigmas. Pollinator observations during the course of this study confirmed that both species are pollinated primarily by bees (but oc-casional flies will visit T. ohiensis), and that honeybees are the main pollinator shared by both species (Molano-Flores, unpubl. data). When multiple flowers are open within an inflorescence, honeybees will perform geitonogamous pollination (B. Molano-Flores, pers. obs.).
Two-way ANOVAs were conducted to determine differences among study areas and between years for plant height, fruit set, seed set, and stigma pollen load. Only the conspecific stigma pollen loads were analyzed, because heterospecific stigma pollen loads were extremely low preventing any further data analysis. ANOVA analyses
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were followed by Tukey post hoc tests. ANOVAs passed both normality and equal variance tests. Square transformation and a square root transformation were used to meet assumptions of ANOVA for seed set and conspecific stigma pollen load, respectively, and variables were back-trans-formed for the purpose of data presentation. Means SE are reported and all statistical analyses were performed using SYSTAT 13 (SYSTAT, 2009).
Significant differences were found among study areas and year for plant height, fruit set, seed set, and stigma pollen load (Figure 1). Plants were shorter in the native prairie areas than at the edge of or inside crown vetch patches (F2 = 133.34; P < 0.001, Figure 1). Fruit set (F2 = 71.08; P < 0.001) and seed set (F2 = 48.27; P < 0.001) for Tradescantia ohiensis were significantly higher in the native prairie areas, followed by values at the edge of crown vetch patches and then inside crown vetch patches (F2 = 71.08; P < 0.001, Figure 1). Stigma pollen load in the native prairie areas was greater than inside the crown vetch patches, but not greater than at the edge of the crown vetch patches (F2 = 3.60; P = 0.03, Figure 1).
Plants were taller in 2008 than in 2009 (F1 = 59.52; P < 0.001, Figure 1). Also, in 2009 fruit set (F1 = 12.45; P < 0.001) and seed set (F1 = 49.62; P < 0.001) were higher than in 2008, but no significant differences were found for stigma pollen load (F1 = 0.30; P = 0.58) between years (Figure 1). A significant interaction was found for plant height (F2 = 8.30; P < 0.001), but not for fruit set (F2 = 2.53; P = 0.08), seed set (F2 = 2.38; P = 0.10), or stigma pollen load (F2 = 1.60; P = 0.20). The significant interaction for plant height is the result of plants in the native prairie areas having similar plant height in 2008 and 2009, and plants in the native prairie areas and at the edge of crown vetch patches having similar plant height in 2009 (Figure 1).
In this study fruit set, seed set, and stigma pollen load were lower when Tradescantia
ohiensis occurred within, or at the edge of, a crown vetch patch than within a native prairie area (Figure 1). The reduction in
the reproductive success of T. ohiensis at the edge of crown vetch patches is of considerable significance as it demonstrates
Figure 1. 2008 (dark bars) and 2009 (white bars) mean ( SE) values for plant height (cm), % fruit set, % seed set, and stigma pollen load (i.e., the number of pollen grains on a stigma) for Tradescantia ohiensis plants at the interior (CVI) and edge (CVE) of crown vetch patches and in native prairie areas (N) found at Lost Mound, Illinois USA.
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that even before an invasive species reaches a habitat (i.e., at the edge of a plant inva-sion), it can have a negative impact on the reproduction of a native species.
One explanation for the low fruit set as-sociated with T. ohiensis in areas invaded by crown vetch could be pollinator-limi-tation at the site, a common phenomenon (Bierzychudek 1981; Knight et al. 2005). However, 97% of the stigmas that were examined for stigma pollen load had pol-len, suggesting that pollinator-limitation may not be an issue. Many studies account for the reduction in fruit and seed set in the presence of an invasive species as the result of changes in the pollen quantity or quality (Traveset and Richardson 2006 [and citations therein]). Although reduc-tions in stigma pollen load were found in the presence of crown vetch (within and at the edge; Figure 1), the reduction in fruit set and seed set cannot be attributed to reduced pollen deposition. Tradescantia ohiensis plants were not pollen limited as stigma pollen loads were always above the minimum required to fertilize six ovules (Figure 1). Because T. ohiensis is self-in-compatible, pollen quality, not quantity, is a more plausible explanation for the reduction in fruit and seed set.
For T. ohiensis, pollen quality (self- vs. cross-pollen) and its movement depend on flower longevity, pollinator effectiveness, and pollinator behavior. In this species, flowers open for just a few hours on only one day, limiting the pollination window. In addition, according to a study by Raf-ferty and Ives (2012) on the effectiveness of pollinators on T. ohiensis (i.e., seed set from a single visit), some types of pollina-tors are better at moving cross-pollen than others. Pollinator observations conducted during this study showed that honeybees, one of the most common visitors of T. ohiensis at this study site, spent much of their time moving between the flowers of an inflorescence (Molano-Flores, unpubl. data). This behavior by the pollinators is more likely to result in geitonogamous pollination (i.e., self-pollination), leading to reduced fruit set.
In contrast to other native-invasive plant pollinator interaction studies, where in-
vasive plant species pollen is frequently found on the stigma of native plants (Brown et al. 2002; Montgomery 2009a, 2009b), almost no crown vetch pollen or any other heterospecific pollen grains were found on T. ohiensis. Morales and Traveset (2008) noted that low invasive pollen deposition on native stigmas in invaded areas could be more common than is assumed. The lack of crown vetch pollen on T. ohiensis stigmas could be the result of different pollen deposition patterns on the pollina-tor (e.g., head, thorax; Beattie et al. 1973; Tepedino et al. 2011) due to the different flower morphologies. A similar explanation was provided by Thijs et al. (2012) for the minimal presence of invasive pollen on the stigmas of two native and one naturalized species. In crown vetch, pollen is deposited on the pollinators back or head due to its position at the tip of the keel and tripped pollination mechanism. In T. ohiensis the style/sigma is fully exposed, providing greater contact to the abdomen of insects (B. Molano-Flores, pers. obs.). Lastly, lack of crown vetch pollen on T. ohiensis stigmas could be the result of differences in pollinator visitation preferences between these two species. At the study site, hon-eybees were the primary flower visitor that was shared by both species. However, honeybees almost exclusively visited only T. ohiensis in the morning (when the flow-ers were open), and then they switched to crown vetch during the afternoon (after the T. ohiensis flowers had wilted).
Also, studies have shown that invasive spe-cies can affect the growth of native species (Gorchov and Trisel 2003; Vila and Weiner 2004). In this study, T. ohiensis plants were taller in crown vetch than in native prairie areas (inside crown vetch > edge of crown vetch > native prairie), most likely as the result of resource competition (e.g., light). Because crown vetch can grow to a height of 1 m (Gucker 2009; B. Molano-Flores, pers. obs.), T. ohiensis plants need to invest more resources in vegetative growth in order to grow above crown vetch, leav-ing fewer resources for reproduction. A similar explanation was given by Bohnen and Hanchek (1994) in a restored prairie where T. ohiensis grew taller and had very low reproduction due to competition with other prairie species. Alternatively, taller T.
ohiensis plants within crown vetch patches could be the result of a fertilizer effect due to the nitrogen fixing capabilities of crown vetch. However, lack of information about nitrogen levels in the soil within the study areas limits the exploration of this hypothesis. Nevertheless, reproductive output did not benefit from this possible fertilizer effect (i.e., plants within the crown vetch patches had lower reproduc-tive success; Figure 1).
In conclusion, this study found that the rhizomatous invasive plant species, crown vetch, had a negative impact on the repro-ductive success of a native species both within and at the edge of its invasion front. This is of interest because, in this study, many of the plants at the edge of the crown vetch invasion were subsequently incorpo-rated within the crown vetch patch by the following year as the invasion proceeded. In this way, it is possible that the effects of crown vetch on T. ohioensis reproductive success accelerated along the invasion by decreasing T. ohioensis fitness and competi-tive ability prior to their direct competitive interaction in subsequent years. This would represent a direct and indirect competitive impact for this invader.
I thank Daniel Elbert, Katherine Chi, and Clark Danderson for fieldwork assistance. Many thanks to the staff at the Lost Mound Unit of the Upper Mississippi River Na-tional Wildlife and Fish Refuge (Lost Mound) for access to the study area. Thanks to Mary Ann Feist, Jean Mengelkoch, Greg Spyreas, and anonymous reviewers for comments. This study was supported through an Illinois Wildlife Preservation Fund (No. 08-037W).
Brenda Molano-Flores is a plant repro-ductive and conservation biologist at the Illinois Natural History Survey.
Beattie, A.J., D.E. Breedlove, and P.R. Eh-rlich. 1973. The ecology of pollinators and
Volume 34 (4), 2014 Natural Areas Journal 469
predators of Frasera speciosa. Ecology 54:81-91.
Bierzychudek, P. 1981. Pollinator limitation of plant reproductive effort. The American Naturalist 117:838-840.
Bohnen. J.L., and A.M. Hanchek. 1994. Flower-ing and seed yield in three species of prairie plants. HortTechnology 4:255-259.
Brown, B.J., R.J. Mitchell, and S.A. Graham. 2002. Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328-2336.
Cousens, R., and M. Mortimer. 1995. Dynamics of Weed Populations. Cambridge University Press, New York.
Dietzsch, A.C., D.A. Stanley, and J.C. Stout. 2011. Relative abundance of an invasive alien plant affects native pollination pro-cesses. Oecologia 167:469-479.
Forseth, I.N., and A.F. Innis. 2004. Kudzu (Pueraria montana): history, physiology, and ecology combine to make a major ecosystem threat. Critical Reviews in Plant Sciences 23:401-413.
Gorchov, D.L., and D.E. Trisel. 2003. Competi-tive effects of the invasive shrub, Lonicera maackii (Rupr.) Herder (Caprifoliaceae), on the growth and survival of native tree seedlings. Plant Ecology 166:13-24.
Gucker, C.L. 2009. Coronilla varia. In Fire Effects Information System, [Online]. U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, Fire Sciences Laboratory (Producer). Accessed 30 August 2011 .
Knight, T.M., J.A. Steets, J.C. Varmosi, S.J. Mazer, M. Burd, D.R. Campbell, M.O. Dudash, R.J. Johnston, R.J. Mitchell, and T.L. Ashman. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology and Systematics 36:467-497.
Larson, D.L., R.A. Royer, and M.R. Royer. 2006. Insect visitation and pollen deposi-tion in an invaded prairie plant community. Biological Conservation 130:148-159.
Lopezaraiza-Mikel, M.E., R.B. Hayes, M.R. Whalley, and J. Memmott. 2007. The impact
of an alien plant on a native plant-pollinator network, an experimental approach. Ecology Letters 10:539-550.
Losure, D., K. Moloney, and B. Wilsey. 2009. Modes of crown vetch invasion and persis-tence. The American Midland Naturalist 161:232-242.
Montgomery, B.R. 2009a. Effect of introduced Euphorbia esula on the pollination of Viola pedatifida. Botany 87:283-292.
Montgomery, B.R. 2009b. Pollination of Sisy-rinchium campestre (Iridaceae) in prairies invaded by the introduced plant Euphorbia esula (Euphorbiaceae). The American Mid-land Naturalist 162:239-252.
Morales, C.L., and A. Traveset. 2008. Interspe-cific pollen transfer: magnitude, prevalence and consequences for plant fitness. Critical Reviews in Plant Sciences 27:221-238.
Nielsen, C., C. Heimes, and J. Kollmann. 2008. Little evidence for negative effects of an invasive alien plant on pollinator services. Biological Invasions 10:1353-1363.
Owens, S.J., and S. McGrath. 1984. Self-incom-patibility and the pollen-stigma interaction in Tradescantia ohiensis Rafin. Protoplasma 121:209-213.
Powell, K.I., K.N. Krakos, and T.M. Knight. 2011. Comparing the reproductive success and pollination biology of an invasive plant to its rare and common native congeners: a case study in the genus Cirsium (Astera-ceae). Biological Invasions 13:905-917.
Rafferty, N.E., and A.R. Ives. 2012. Pollinator effectiveness varies with experimental shifts in flowering time Ecology 93: 803-814.
Runkel, S., and D. Roosa. 1989. Wildflowers of the Tallgrass Prairie, the Upper Midwest. Iowa State University Press, Ames.
Solecki, M.K. 1997. Controlling invasive plants. Pp. 251-278 in Stephen Packard and Cornelia F. Mutel, eds., The Tallgrass Res-toration Handbook: For Prairies, Savannas, and Woodlands. Island Press, Washington, D.C.
Sun, S.-G., B.R. Montgomery, and B. Li. 2013. Contrasting effects of plant invasion on pollination of two native species with similar morphologies. Biological Invasions
Symstad, A. 2004. Secondary invasion fol-lowing the reduction of Coronilla varia (crownvetch) in sand prairie. The American Midland Naturalist 152:183-189.
SYSTAT. 2009. SYSTAT for Windows, Ver-sion 13. SYSTAT Software Inc., Richmond, CA.
Tepedino, V.J., W.R. Bowlin, and T.L. Griswold. 2011. Diversity and pollination value of in-sects visiting the flowers of a rare buckwheat (Eriogonum pelinophilum: Polygonaceae) in disturbed and natural areas. Journal of Pollination Ecology 4:57-67.
Thijs, K.W., R. Brys, H.A.F. Verboven, and M. Hermy. 2012. The influence of an invasive plant species on the pollination success and reproductive output of three riparian plant species. Biological Invasions 14:355-365.
Traveset, A., and D.M. Richardson. 2006. Biological invasions as disruptors of plant reproductive mutualisms. Trends in Ecology and Evolution 21:208-216.
Tu, M. 2003. Element stewardship abstract for Coronilla varia L. Wildland Invasive Spe-cies Team, The Nature Conservancy. Davis, CA. Accessed 6 January 2012 .
U.S. Fish and Wildlife Service. 2002. Lost Mound National Wildlife Refuge Savanna, Illinois Interim Comprehensive Conserva-tion Plan. U.S. Department of the Interior, Fish and Wildlife Service, Savanna, IL.
Vila, M., and J. Weiner. 2004. Are invasive plant species better competitors than native plant species? evidence from pair-wise experiments. Oikos 105:229-238.
Walck, J., J. Baskin, and C. Baskin. 1999. Effects of competition from introduced plants on establishment, survival, growth, and reproduction of the rare plant Solidago shortii (Asteraceae). Biological Conserva-tion 88:213-219.
Wenny, D., E. Anderson, and R. Nyboer. 2006. Lost Mound Unit of the Upper Mississippi River National Wildlife Refuge. Meadowlark 15: 51-56.
Wheeler, A.G. 1974. Phytophagous arthropods fauna of crownvetch in Pennsylvania. Cana-dian Entomologist 106:897-908.