Solidago canadensis impacts on native plant and pollinator communities in different-aged old-fields

Accepted Manuscript Title: Solidago canadensis impacts on native plant and pollinator communities in different-aged old fields Author: Annam´ aria Fenesi Csongor I. V´ ag´ asi Monica Beldean Rita F¨ oldesi Levente-P´ eter Kolcs´ ar Julie Teresa Shapiro Edina T¨ or¨ ok Anik´ oKov ´ acs-Hosty´ anszki PII: S1439-1791(15)00042-0 DOI: http://dx.doi.org/doi:10.1016/j.baae.2015.03.003 Reference: BAAE 50871 To appear in: Received date: 27-8-2014 Revised date: 26-2-2015 Accepted date: 12-3-2015 Please cite this article as: Fenesi, A., V´ ag´ asi, C. I., Beldean, M., F¨ oldesi, R., Kolcs´ ar, L.- P., Shapiro, J. T., T¨ or¨ ok, E., and Kov´ acs-Hosty´ anszki, A.,Solidago canadensis impacts on native plant and pollinator communities in different-aged old fields, Basic and Applied Ecology (2015), http://dx.doi.org/10.1016/j.baae.2015.03.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. Page 1 of 34 Accepted Manuscript 1 Solidago canadensis impacts on native plant and pollinator communities in different-1 aged old fields 2 3 Annamária FENESIa,b,*, Csongor I. VÁGÁSIc,d, Monica BELDEANb, Rita FÖLDESIe, 4 Levente-Péter KOLCSÁRb, Julie Teresa SHAPIROe,f, Edina TÖRÖKb, Anikó KOVÁCS-5 HOSTYÁNSZKIe 6 7 aDepartment of Ecology, University of Debrecen, Egyetem tér 1, H–4032 Debrecen, Hungary 8 bHungarian Department of Biology and Ecology, Babeş-Bolyai University, Republicii street 9 42, RO–400015 Cluj-Napoca, Romania 10 cEvolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeş-Bolyai 11 University, Clinicilor street 5–7, RO–400006 Cluj-Napoca, Romania 12 dMTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary 13 Zoology, University of Debrecen, Egyetem tér 1, H–4032 Debrecen, Hungary 14 eMTA ÖK, Lendület Ecosystem Services Research Group, Alkotmány út 2–4, H–2163 15 Vácrátót, Hungary 16 fSchool of Natural Resources and Environment and Department of Wildlife Ecology and 17 Conservation, University of Florida, Gainesville, FL 32611, USA 18 19 *Corresponding author. Tel.: +40 744916952; fax: +40 264431858. 20 E-mail address: [email protected] 21 22 *Manuscript Page 2 of 34 Accepted Manuscript 2 Abstract 23 24 Secondary succession in former arable fields (i.e. old fields) might be altered by the 25 colonization of invasive alien species, with possible community-wide impacts, hindering the 26 ability old fields to become species-rich communities. However, the effects of invasive 27 species on local communities have rarely been addressed in the light of secondary succession. 28 Therefore, we studied the impact of the highly invasive Solidago canadensis on plant and 29 pollinator communities along a gradient of invasion severity in old fields with different ages 30 (1–20 years since last ploughing) in Southern Transylvania, Romania. We asked whether the 31 invasion of S. canadensis causes shifts in (1) the composition and diversity of plant 32 communities, and (2) pollinator communities along the successional gradient. Further, we 33 asked (3) to what extent the presence of S. canadensis affected flower visitation of native 34 plant species by pollinators. According to our results, the invasion reduced the native plant 35 species richness throughout succession, although the most profound negative effect on plant 36 diversity and vegetation naturalness was exerted in older successional communities. The 37 invasion of S. canadensis had a negative effect on the abundance of bees irrespective of the 38 old field age; however, there was no similar negative effect on hoverflies. Native flowers 39 experienced reduced visitation by wild bees, honey bees and hoverflies due to the augmented 40 presence of S. canadensis. Therefore, the invasion of this perennial plant species diverts the 41 trajectory of vegetation succession, alters the mutualistic links between the native elements of 42 these old fields, and causes a non-desired alternative stable states to be installed. 43 44 Keywords: Canada goldenrod; plant invasion; plant–pollinator interaction; fallow; set-aside; 45 Apis; Romania; Natura 2000; biodiversity conservation 46 47 Page 3 of 34 Accepted Manuscript 3 Introduction 48 49 Over the last few decades, various social and economic changes have driven the abandonment 50 of extensive areas of formerly arable lands in several parts of the world. If these areas are left 51 alone and propagule sources are available, secondary succession takes place and diverse semi-52 natural vegetation can be formed in short time (Stoate et al. 2009). Former arable lands 53 (hereafter old fields) may support farmland biodiversity and provide valuable ecosystem 54 services (e.g. pollination) at the beginning of secondary succession (Tscharntke, Batáry & 55 Dormann 2011) and their conservation value may increase in the later stages (Corbet 1995). 56 However, reaching a stage of diverse secondary vegetation is not free from challenges, as old 57 fields are highly susceptible to invasion by alien plant species (Catford et al. 2012). Non-58 native invasive species are likely to colonize the freshly abandoned croplands because of 59 increased soil nutrient availability associated with previous fertilizer applications, and limited 60 competition for resources (Standish, Cramer & Hobbs 2008). Longer-lived alien species can 61 persist until the later stages of succession, therefore perturbing natural succession pathways 62 and altering the pattern of vegetation recovery (Meiners, Pickett & Cadenasso 2002). By 63 preventing the establishment of late-successional species, alien plant invasion may cause the 64 invaded habitats to remain in the early successional stages for a long time (Cramer, Hobbs & 65 Standish 2008). 66 The establishment of invasive plants may influence not only the native flora and the 67 trajectory of its secondary succession, but can also have an impact on the related invertebrate 68 communities, such as pollinator insects (van Hengstum et al. 2014). Former studies presented 69 highly controversial results, reporting either positive (Bartomeus, Vilà & Santamaría 2008) or 70 negative effects (de Groot, Kleijn & Jogan 2007; Moroń et al. 2009) on pollinator abundance 71 and diversity. Invasive plants are reported to influence the abundance and diversity of smaller, 72 Page 4 of 34 Accepted Manuscript 4 mostly solitary wild bees (Apoidea) of limited dispersal ability (Gathmann & Tscharntke 73 2002), as well as hoverflies (Syrphidae) and bumblebees, which generally have larger 74 foraging ranges (Greenleaf et al. 2007). Therefore, invasive species might threaten 75 biodiversity not only at the local level, but at the landscape scale as well (Hejda, Pyšek & 76 Jarošík 2009). Moreover, invasive plant species can also act indirectly on ecological 77 communities by weakening the mutualistic links between native plants and their pollinators 78 (Aizen, Morales & Morales 2008) by luring pollinators away from native plants, either 79 partially (Baskett, Emery & Rudgers 2011) or completely (Bartomeus, Vilà & Santamaría 80 2008). This expansion of plant preference for pollination can result in fewer pollinator visits, 81 pervasive interspecific pollen transfer (Baskett, Emery & Rudgers 2011), and consequently, 82 decreased reproduction success and diversity of the native flora. Despite these possible 83 detrimental effects, the direct effect of invasive plant species on secondary succession of old 84 fields is relatively understudied (Flory and Clay 2010), while the effects of invasive species 85 on the pollinator communities along the successional trajectory has so far never been studied. 86 Here, we focus on a large-scale biological invasion phenomenon in southern 87 Transylvania, Romania. Large-scale abandonment of arable lands has occurred over the last 88 two decades due to a significant class of absentee landowners and the decreasing profitability 89 of traditional subsistence agriculture (Fischer, Hartel & Kuemmerle 2012). Solidago 90 canadensis L. (Canada goldenrod) is the most successful invasive colonizer of these old 91 fields, often becoming dominant even at the landscape scale. Its impact on the species 92 richness of vascular plants and pollinators has already been studied in other countries (de 93 Groot, Kleijn & Jogan 2007; Moroń et al. 2009). However, these studies analysed only the 94 final stage of invasion, when the invasive species had already established dominance in the 95 community, and compared this stage with non-invaded, semi-natural communities, 96 representing only the two contrasting extremes of the invasion gradient. 97 Page 5 of 34 Accepted Manuscript 5 To fill these gaps in our knowledge regarding the impact of invasion on both plant and 98 pollinator communities over the course of secondary succession on old fields along a 99 continuous gradient of invasion, we initiated a large-scale field study. We aimed to answer the 100 following questions: (1) Does the invasion of S. canadensis cause shifts in the composition 101 and diversity of plant communities over the course of secondary succession of old fields? (2) 102 Does abundance and species richness of pollinators change due to the invasion of the old 103 fields? (3) To what extent does the presence of S. canadensis affect flower visitation of native 104 plant species by pollinators? To answer these questions, we studied the effect of S. canadensis 105 density (0–80% relative cover) in 36 old fields with various ages (1–20 years since the last 106 ploughing). 107 108 Materials and methods 109 The invasive species 110 S. canadensis is a rhizomatous, patch-forming perennial herb of the Asteraceae. It has become 111 an exceptionally successful invasive species since its introduction to Europe in the 18th 112 century and is now widespread throughout the continent (Weber 1998). In addition to its 113 prolific vegetative propagation (Meyer & Schmid 1999), S. canadensis releases chemicals 114 that inhibit the growth, germination and survival of native plants (Abhilasha et al. 2008), and 115 change the soil composition by diverting nutrients and minerals (Zhang et al. 2009). 116 117 Location and study sites 118 Our study area was located in the middle section of the Târnava Mare Valley in Southern 119 Transylvania, Romania (Fig. 1A). Climate is classified as moderate continental. Mean annual 120 rainfall is approximately 650 mm, while mean annual temperature is 8 °C (Drăgulescu 2003). 121 The region has been designated as Natura 2000 Site of Community Interest (Sighişoara-122 Page 6 of 34 Accepted Manuscript 6 Târnava Mare Natura 2000 site, ROSCI0227) because 18 habitats listed in the EU Habitats 123 Directive Annex I can be found in this region. 124 We examined the succession of vegetation and pollinator communities in this site 125 using a chrono-sequence of old fields representing different stages of succession (space for 126 time substitution, sensu Pickett 1989). We chose old fields with a known abandonment date in 127 the vicinity of four villages (Biertan, Laslea, Malâncrav, Richiş; Fig. 1A). Abandonment here 128 can be defined as the cessation of ploughing, though other uses and activities such as mowing 129 or grazing may be present in the fields. These old fields may also be infrequently burned by 130 locals. The 36 fields examined ranged in age from 1 to 20 years since abandonment. These 131 sites were also chosen to represent the whole range of S. canadensis abundance from highly to 132 less invaded areas (relative cover 0–80%). Most sites were quite small (mean area: 1.3 ha, 133 range: 0.08–2.7 ha). The year of last ploughing, and current land-use practices were 134 determined by interviewing landowners, and based on that information, we categorized the 135 old fields as mown, grazed or without management. To determine whether the sites had been 136 recently burned, or not, we looked for local signs of fire (burned trees and shrubs, incinerated 137 litter or grass tussocks) and asked local people. 138 139 Vegetation survey 140 Percent cover of vascular plant species with a resolution of 1% was visually estimated within 141 three 4 × 4 m plots per site (Fig. 1B). We assigned 0.5% to species with a cover smaller than 142 1% (species represented by one small individual or by seedlings only). The level of invasion 143 was characterized in each plot by the relative cover of S. canadensis and averaged over the 144 three plots at site level. The surveys were conducted once per site in May–June 2012. 145 In order to accurately depict compositional changes during the course of succession, 146 we calculated the following variables for each site: 147 Page 7 of 34 Accepted Manuscript 7 1. Native vascular plant species richness and diversity. Species richness was calculated by 148 averaging the number of species in the three plots per site. The Shannon diversity index of 149 each site was calculated based on the proportional cover of each species. S. canadensis was 150 not included in the calculation. 151 2. Naturalness. All plant species were assigned to one of the three naturalness groups 152 according to Sanda et al. (1983): (i) species of natural and semi-natural habitats, hereafter 153 called “grassland species”, (ii) species common to both natural and ruderal communities, 154 hereafter “generalist species”, and (iii) species of ruderal communities, hereafter “ruderal 155 species”. The proportion of each category was calculated for each site and used in subsequent 156 analyses. 157 3. Functional guilds. The proportion of the main functional groups was taken into account by 158 distinguishing (i) graminoid species belonging to the Poaceae, Cyperaceae or Juncaceae, (ii) 159 legume species of the Fabaceae and (iii) forbs, i.e. herbaceous plants belonging to other 160 families. As the presence of tree and shrub species never exceeded 1% average cover at site 161 level, we excluded those species from the calculation of this variable. 162 163 Pollinator sampling 164 We sampled pollinator insects in 22 sites (out of 36 sites with botanical surveys). We selected 165 these sites to cover the whole range of successional age (1 to 20 years) and low to high 166 densities of S. canadensis cover. The sites were at least 250 m from each other. Pollinators 167 were sampled along two 100 m transects per study site; each transect assigned was at least 15 168 m from the field edge and 15 m apart from each other (Fig. 1B). We surveyed the pollinators 169 twice: first during the peak flowering season of indigenous vegetation (21–25 July 2012) and 170 second during the peak flowering of S. canadensis (19–23 August 2012). Transect counts 171 were performed between 9 a.m. and 6 p.m. under favourable weather conditions with little 172 Page 8 of 34 Accepted Manuscript 8 wind and few clouds at most. A pair of observers walked along each transect for 20 min and 173 recorded all insects actively pollinating, flying or perching on the vegetation. In the case of 174 active pollination, the visited plant species was also recorded. Pollinators were hand-netted 175 and preserved in 96% ethanol for later identification at the species level. 176 We distinguished four pollinator groups: honey bee (Apis mellifera L.), bumblebees 177 (Bombus spp.), other wild bees (Apoidea: Collettidae, Melittidae, Halictidae, Megachilidae, 178 Andrenidae, Apidae except Bombus spp. and honey bee), and hoverflies (Syrphidae). 179 Bumblebees and other wild bees were analysed separately because these two groups have 180 different biological traits in terms of floral requirements, flying abilities and sociality 181 (Gathmann & Tscharntke 2002; Greenleaf et al. 2007; Michener 2007), and therefore 182 different responses to landscape and local scale environmental conditions were expected. 183 Although there are some semi-social species and/or genera among the collected bees (e.g. 184 some Halictus spp.), we use ‘solitary bees’ in the current paper for wild bees other than 185 bumblebees. 186 As the presence of pollinators depends on the pollen and nectar supply, we gathered 187 additional botanical information: flowering plant species and the number of flowers at species 188 level were recorded at ten 1 × 1 m quadrates placed equidistantly along the same two transects 189 per site (Fig. 1B). We counted the number of heads in the case of Asteraceae species and 190 simple umbels for Apiaceae, but refer to both as flowers for the sake of simplicity. 191 We calculated several variables to detect potential changes in the pollinator 192 communities during succession: 193 1. Abundance of each pollinator group (bumblebees, solitary bees, honey bee, hoverflies) per 194 transect was calculated as the number of individuals per group per transect; 195 2. Species richness of bumblebees, solitary bees and hoverflies; species data from the two 196 transects per site were pooled because of the relatively low species numbers; 197 Page 15 of 34 Accepted Manuscript 15 S. canadensis is considered one of the most important plants yielding unifloral honey 346 sources in Central Europe (Farkas and Zajácz 2007). Therefore, a highly interesting finding is 347 that the increasing cover of S. canadensis significantly decreased the abundance of honey 348 bees, even during mass flowering. Although honey bees are important pollinators of S. 349 canadensis, they are likely to begin visiting goldenrod flowers only when the abundance of 350 other flowering plant species has declined (Gross and Werner 1983). As the traditionally 351 managed landscape we studied is a diverse mosaic of croplands, old fields and managed 352 grasslands (pastures or hayfields), pollinators can easily find other pollen sources in the 353 vicinity of the invaded old fields. 354 Although plant species richness and composition went through considerable alteration 355 along the 20 years of succession, neither solitary bees nor hoverflies showed any difference 356 among old fields of different age. Therefore, the bimodal species richness distribution of 357 pollinators along secondary succession presented by Steffan-Dewenter and Tscharntke (2001) 358 could not be replicated for bees or for hoverflies in our study. This is because neither the 359 number of flowering species, nor the number of flowers depended on the age of old fields 360 (data not shown). One exception was the honey bee, which seemed to prefer plant species 361 typical of the beginning of succession in younger old fields. 362 363 Indirect effects of invasion: flower visitation of native species 364 Plants and their pollinators are tightly intertwined components of ecological communities, 365 therefore the adverse effect of S. canadensis might have further indirect repercussions as well. 366 Alien plant species can have a strong effect on the pollination success of native species, often 367 competing with them by causing either reduced pollinator visitation rates or increased 368 heterospecific pollination of native flowers. However, in some cases, both at local and 369 Page 16 of 34 Accepted Manuscript 16 landscape scales, these often mass-flowering invasives may facilitate native plant pollination 370 by increasing pollinator densities (Bjerknes et al. 2007). 371 We found a negative correlation between the cover of S. canadensis and flower 372 visitation of native plants (hereafter flowers) by bees and hoverflies. On the one hand this 373 result might be the consequence of an indirect competition for pollination between the 374 superior invasive and suppressed native species, competing possibly for light, space, soil 375 nutrients. On the other hand, the positive effect of S. canadensis on bumblebees and 376 hoverflies suggests also direct competition for pollination between invasive and native species 377 in August due to the large amount of pollen and nectar provided by S. canadensis. The lower 378 frequency of flower visitation induced by invasives can possibly result in a pollination deficit 379 in native species (Chittka & Schürkens 2001). The reduction in the pollinator pool by alien 380 plants might thus corrupt the reproductive success of insect-pollinated native plants (Stout & 381 Morales 2009). Although flowers of S. canadensis are self-incompatible and dependent on the 382 presence of pollinators for seed production (Gross & Werner 1983), it can also vigorously 383 spread locally by rhizomes, thus its reproductive gain is less affected by a decreased 384 pollinator pool. Through this two-way competition by direct and indirect routes, S. canadensis 385 can further propagate its dominance and, therefore, contribute to the development of an 386 alternative, self-perpetuating stable state in which it dominates. 387 388 Conclusions and recommendations 389 Without management interventions, degraded, alternative states driven by S. canadensis, 390 instead of valuable secondary grasslands, might dominate the landscape for decades (this 391 invasive species can persist in the fields for up to 50–75 years; Hartnett and Bazzaz 1983), 392 and could arrest the natural trajectory of secondary succession in an earlier, less diverse 393 phase. Therefore, we cannot allow spontaneous processes to revegetate the old fields invaded 394 Page 17 of 34 Accepted Manuscript 17 by S. canadensis. Instead, active management actions are needed to guide vegetation 395 recovery. 396 Long-term experiments testing the effects of different land-use techniques on 397 controlling S. canadensis are already available from Central-Eastern Europe (Horváth 2012). 398 According to these experiments, a combination of prescribed disturbances, such as regular 399 mowing and extensive autumnal grazing with cattle or sheep, could reduce the target invasive 400 species’ abundance and enhance the recovery of native vegetation. 401 402 Acknowledgements 403 We greatly thank András Báldi, Zoltán Botta-Dukát and Eszter Ruprecht for useful comments 404 and suggestions on the manuscript. Ede Gábos kindly produced the map of the study area and 405 Zsolt Józan identified the bees. A.F. was supported by the European Union and the State of 406 Hungary, co-financed by the European Social Fund in the framework of TÁMOP 4.2.4. A/2-407 11-1-2012-0001 ‘National Excellence Program’. A.K-H. and R.F. were supported by 408 ‘Lendület’ program of the Hungarian Academy of Sciences, OTKA project (101940), A.K-H. 409 was a Bolyai Fellow and a MTA Postdoctoral Fellow. 410 411 Appendix A. Supplementary data 412 Supplementary data associated with this article can be found, in the online version, at 413 XXXXX." 414 415 References 416 Abhilasha, D., Quintana, N., Vivanco, J., Joshi, J. (2008). Do allelopathic compounds in 417 invasive Solidago canadensis s.l. restrain the native European flora? J. Ecol., 96, 993–418 1001. 419 Page 18 of 34 Accepted Manuscript 18 Aizen, M.A., Morales, C.L., Morales, J.M. (2008). Invasive mutualists erode native 420 pollination webs. PLoS Biology, 6, e31. 421 Bartha, S., Szentes, S., Horváth, A., Házi, J., Zimmermann, Z., Molnár, C., ... , Molnár, Z. 422 (2014). Impact of mid‐successional dominant species on the diversity and progress of 423 succession in regenerating temperate grasslands. 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The effects of Solidago canadensis cover, age of the old fields and land-use (M – mown, W – without management) on vegetation 525 characteristics according to the linear mixed-effects models. Positive effects are indicated by “+” and negative effects by “–”. Effect sizes (Partial 526 r) and their 95% confidence interval are also shown. P-values of significant effects are in bold. Significant interactions between the covariates S. 527 canadensis cover and old field age have no contrasts but are plotted on Fig. 2. 528 df F p Contrasts Effect size 95% C.I. Richness and diversity Plant species richness S. canadensis cover 1, 29 4.43 0.044 – 0.09 -0.24; 0.43 Old field age 1, 29 32.88 <0.001 + 0.72 0.38; 1.06 SCC × OFA 1, 29 3.09 0.088 D iversity S. canadensis cover 1, 29 20.43 <0.001 – 0.24 - 0.09; 0.58 Old field age 1, 29 6.07 0.019 + 0.61 0.27; 0.95 SCC × OFA 1, 29 15.19 <0.001 -0.58 -0.92; -0.24 Naturalness Grassland species S. canadensis cover 1, 29 0.01 0.956 Old field age 1, 29 53.51 <0.001 + 0.80 0.46; 1.14 SCC × OFA 1, 29 5.30 0.028 -0.39 -0.73; -0.05 Generalist species S. canadensis cover 1, 29 0.94 0.339 Old field age 1, 29 21.43 <0.001 – - 0.72 - 1.06; - 0.38 SCC × OFA 1, 29 10.69 0.002 0.51 0.17; 0.86 Ruderal species Old field age 1, 31 45.09 <0.001 – -0.76 -1.11; -0.42 Functional guilds Graminoids Page 24 of 34 Accepted Manuscript 24 S. canadensis cover 1, 29 1.56 0.221 Old field age 1, 29 9.53 0.004 + 0.21 - 0.12; 0.55 SCC × OFA 1, 29 5.78 0.022 0.40 0.06; 0.74 Legumes S. canadensis cover 1, 27 5.42 0.027 + 0.52 0.18; 0.86 Old field age 1, 27 8.10 <0.008 + 0.68 0.34; 1.02 SCC × OFA 1, 27 8.39 0.007 -0.48 -0.82; -0.14 Land-use 1, 27 4.47 0.021 W>M -0.47 -0.81; -0.13 Forbs S. canadensis cover 1, 30 12.30 0.001 – -0.50 -0.84; -0.16 Old field age 1, 30 38.31 <0.001 – - 0.74 - 1.09; - 0.40 529 530 Page 31 of 34 Accepted Manuscript Figure Page 32 of 34 Accepted Manuscript Figure Page 33 of 34 Accepted Manuscript Zusammenfassung Die sekundäre Sukzession auf ehemaligen Feldern könnte durch die Besiedelung mit invasiven fremden Arten verändert werden, die möglicherweise die ganze Gemeinschaft beeinflussen, indem sie die Entwicklung hin zu artenreichen Gemeinschaften erschweren. Indessen wurden die Einflüsse von invasiven Arten auf lokale Gemeinschaften selten in Hinblick auf die sekundäre Sukzession betrachtet. Wir untersuchten deshalb den Einfluss der hoch-invasiven Kanadischen Goldrute (Solidago canadensis) auf Pflanzenund Bestäubergemeinschaften entlang eines Gradienten unterschiedlich starker Invasion auf alten Feldern unterschiedlichen Alters (1 bis 20 Jahre seit dem letzten Pflügen) in Süd-Transsilvanien (Rumänien). Wir fragten, ob Invasion durch die Goldrute Veränderungen in der Zusammensetzung und Diversität der Pflanzenund Bestäubergemeinschaften entlang des Sukzessionsgradienten hervorruft. Desweiteren fragten wir, inwieweit die Anwesenheit der Goldrute den Blütenbesuch an einheimischen Pflanzen beeinflusst. Die Invasion reduzierte den Artenreichtum der einheimischen Pflanzen über die gesamte Sukzession hinweg, aber der stärkste negative Effekt auf die Pflanzendiversität und die Natürlichkeit der Vegetation erfolgte in den älteren Sukzessionsgemeinschaften. Die Goldruten-Invasion hatte unabhängig vom Alter der Felder einen negativen Effekt auf die Abundanz der Bienen, aber es gab keinen gleichartigen Effekt auf die Schwebfliegen. Einheimische Pflanzen erfuhren einen reduzierten Blütenbesuch durch Wildbienen, Honigbienen und Schwebfliegen, der der vermehrten Anwesenheit der Goldrute geschuldet war. Deshalb ändert die Invasion durch diese ausdauernde Abstract in German Page 34 of 34 Accepted Manuscript Pflanzenart den Verlauf der Vegetationssukzession, ändert die mutualistischen Verbindungen zwischen den einheimischen Arten der ehemaligen Felder und verursacht die Etablierung eines unterwünschten, alternativen stabilen Zustandes.