bioRxiv preprint doi: https://doi.org/10.1101/2020.04.30.070268; this version posted April 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license.

1 The mistletoe Struthanthus flexicaulis reduces dominance and increases diversity of

2 in campo rupestre

3 Graziella França Monteiro 1,2*, Milton Barbosa1, Yasmine Antonini 2, Marcela Fortes de 4 Oliveira Passos 2,3, Samuel Novais 1, G. Wilson Fernandes 1*. 5 6 7 1 Ecologia Evolutiva & Biodiversidade/DGEE, Universidade Federal de Minas Gerais, Belo

8 Horizonte – Minas Gerais, 30270-971, Brazil.

9 2 Laboratório de Biodiversidade/DEBIO/ICEB/Universidade Federal de Ouro Preto, Ouro

10 Preto – Minas Gerais, 35400-000, Brazil.

11 3 Graduate Program in Applied Ecology /DBI-Universidade Federal de Lavras/UFLA, Lavras

12 – Minas Gerais, 37200-000, Brazil.

13

14 *Corresponding author: [email protected]

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23 ABSTRACT

24 The interaction between hemiparasites and their host plants is an important structuring 25 mechanism for communities. The mistletoe Struthanthus flexicaulis (Loranthaceae) is 26 widely distributed in the campo rupestre ecosystem and likely has an important role in 27 structuring the communities of which its hosts are part. The main goals of this study were to 28 investigate the effects of parasitism by S. flexicaulis on host plants in a degraded area of 29 campo rupestre and to determine how parasitism affects characteristics of the structure of this 30 plant community over time. We found that parasitized plants had smaller crowns and branch 31 growth, and suffered lower mortality compared to non-parasitized plants. Parasitism by S. 32 flexicaulis decreased dominance and increased the diversity and evenness of plants in the 33 community over time. Parasitism leads to competition with the host for water and nutrients, 34 which may decrease the performance of the host and, consequently, leading to host death. 35 The high mortality of the most abundant plant species led to a restructured woody plant 36 community. These results reinforce the importance of parasitic plants as key species for 37 maintaining species diversity in plant communities.

38

39 Key words: plant-plant interaction; parasitism; community structure, Espinhaço Mountain 40 Chain

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50

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52

53 INTRODUCTION

54 Identifying the factors that control the distribution, abundance and diversity of species

55 is important to understand the structuring of ecological communities. Communities are

56 structured according to climatic and historical variations (e.g. dispersion and speciation,

57 migration and extinction), local physical conditions and interactions among species [1, 2].

58 On a local scale, abiotic factors have an important influence on the structuring of plant

59 communities, such as the availability of water and soil nutrients [34] in addition to

60 interactions with other organisms, such as microbes and arbuscular mycorrhizal fungi [5, 6,

61 7]. In turn, the distribution of plant communities strongly affects the community structure of

62 other organisms that directly depend on them as resources, such as herbivores and parasitic

63 plants [8, 9, 10].

64 Among parasitic plants, hemiparasites are those capable of photosynthesis, but

65 depend on their hosts for water and nutrients [11]. The susceptibility to attack by

66 hemiparasitic plants (determined by chemical, physiological and physical processes at the

67 parasite-host interface) varies between plant species, and therefore, local abundance and the

68 degree of susceptibility of plants in a community are key factors for the successful

69 colonization of hemiparasites in the environment [12, 13, 14]. In addition, the seeds of the

70 hemiparasitic plants are mostly dispersed by birds, which can lead to a differential deposition

71 of seeds on the host plants according to the preferences of the birds for certain perches [15,

72 16, 17]. Generally, larger plants with more branched tops are more attractive perches for

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73 birds, leading to a greater abundance of hemiparasitic plants on these hosts [15, 18, 16, 19,

74 20].

75 Once the hemiparasitic plants are established, they can affect the host plant both

76 directly and indirectly [21, 22, 23, 9] and, consequently, affect the structure of plant

77 communities [14]. Directly, the hemiparasite decreases the growth and branching of the host

78 plant [23], as they obtain water and nutrients directly from the xylem, decreasing the

79 resources available for the metabolism of the host itself [11, 24, 25], which may ultimately

80 lead to death [19, 26, 9]. Indirectly, the parasite can make the host plant more susceptible to

81 attack by natural enemies [23] and to environmental stress [12, 11], which can also accelerate

82 the death of the host. Therefore, once the most abundant plant species in the environment are

83 more frequently parasitized, the hemiparasitic plant can play an important role in the

84 structuring of plant communities, since by promoting a higher mortality of individuals of

85 dominant species, it would lead to greater uniformity in the number of individuals among

86 plant species in the community [11, 27, 28, 29, 30, 31].

87 Loranthaceae is one of the most representative families of parasitic plants in Brazil,

88 with 10 genera and approximately 100 species described [32, 14]. In the Cerrado biome, 36

89 species have been described, all of which are hemiparasites [33]. Among them, the mistletoe

90 Struthanthus flexicaulis is a common generalist hemiparasite in campos rupestres, with more

91 than 60 species recorded as hosts within at least 24 families of woody plants [25, 9]. The

92 campo rupestre ecosystem is subject to significant anthropic pressure such as mining and

93 road construction [3, 34], and in degraded areas the native pioneer shrub, Baccharis

94 dracunculifolia, whose populations form patches, often dominates the plant community [3,

95 10].

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96 Casual observations indicated a high incidence of the mistletoe S. flexicaulis on the

97 patches of B. dracunculifolia, therefore representing an excellent experimental model to test

98 whether the plant community can be shaped by the presence of a plant parasite. This study

99 aimed to evaluate the factors related to the host plants that affect the distribution and

100 abundance of this important and widespread mistletoe, and the effects of hemiparasitism on

101 host plants in a degraded area of campo rupestre, in southeastern Brazil. We tested whether

102 the presence of the S. flexicaulis affects the structure of this community over time. First, we

103 determined the effect of the frequency and architecture of the woody host plants on parasitism

104 by S. flexicaulis. Predictions of the following hypotheses were tested: (1) More common

105 plant species in the environment are more attacked by the S. flexicaulis; (i) more abundant

106 host plants would present a greater intensity of infection (number of parasites per host) by S.

107 flexicaulis; (2) Structurally more complex host plants would be more parasitized by S.

108 flexicaulis; (i) host plants with more complex architecture (plant height and crown, number

109 of primary and secondary branches and maximum branching) would present a higher

110 intensity of infection by S. flexicaulis; (ii) Branches in greater diameter classes would be

111 more parasitized by S. flexicaulis compared with smaller diameter classes. In a second step,

112 we determined the impact of parasitism by S. flexicaulis on host plants and the woody plant

113 species community. The predictions of the following hypotheses were tested: (1) Parasitized

114 plants show lower growth and suffered higher mortality than non-parasitized plants: (i)

115 parasitized plants would show lower growth (plant height and crown, number of primary and

116 secondary branches, and maximum branching) over time compared to non-parasitized plants;

117 (ii) parasitized plants would have a higher proportion of individuals killed over time

118 compared to non-parasitized plants; (2) Parasitic plants favor the diversity of woody plants,

119 reducing the abundance of dominant species over time: (i) the dominance of species in the

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120 woody plant community with the presence of the mistletoe S. flexicaulis would decrease over

121 time, while diversity and evenness would increase.

122

123 MATERIALS AND METHODS

124 Study area

125 The study was conducted at Reserva Vellozia (19°16’45.7” S 43°35’27.8”W), in

126 Serra do Cipó, southern portion of the Espinhaço Range, in Minas Gerais, Brazil. Reserva

127 Vellozia is located at an altitude between 900-1355 meters, where the vegetation of campos

128 rupestres is predominant. The vegetation of campo rupestre in Serra do Cipó is characterized

129 by a high richness of plant species, with about 125 families of phanerogams with more than

130 2000 species of plants listed [35]. In addition, it presents high levels of endemism and several

131 endangered species [3, 36, 34, 37]. The soil is shallow and often prevents large species

132 from being established [38].

133 Sample design

134 In March 2017, eight 2 m x 50 m transects were established over 4 km, at least 500

135 m apart. The transects were located in areas under anthropic pressure due to the construction

136 of roads, with a high incidence of the mistletoe S. flexicaulis. In each transect, all woody

137 plants (parasitized and non-parasitized) taller than one meter were marked (plants shorter

138 than one meter are generally not parasitized; [23] and the richness (number of species) and

139 abundance (number of individuals) were recorded. Specimens of all the plant species marked

140 were identified to the lowest possible taxonomic level. In addition, the number of S.

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141 flexicaulis individuals established (with green leaves and fixed on the stem of the host plant)

142 on all parasitized hosts was recorded.

143 The following measurements of the architecture of all marked plants (parasitized and

144 non-parasitized) were taken (using a measuring tape): height of the plant (from the ground to

145 the top of the crown), height of the crown (first branch to the top), number of primary

146 branches, number of secondary branches and maximum level of branching (maximum

147 number of branching levels that a plant has; methodology adapted from [39]. We measured

148 the diameter (Mitutoyo caliper: mm) of each parasitized branch, which was grouped

149 according to five diameter classes (0-2 mm, 3-5 mm, 6-9 mm, 9-15 mm and >15 mm). To

150 compare mortality and growth between parasitized and non-parasitized plants, we performed

151 a new measurement, in July 2019 (28 months after the first one), of the same architectural

152 parameters (height, number of primary branches, number of secondary branches, maximum

153 branching) and we quantified the living and dead plants. The proportion of dead parasitized

154 and non-parasitized individuals per transect was calculated. The growth of each individual

155 was calculated by the difference in plant height and crown height between the years 2017

156 and 2019. The same was done for the increase in the number of primary branches, secondary

157 branches and maximum branching, as they were calculated by the difference between the

158 measurements of the years 2017 and 2019.

159 Data analysis

160 To assess whether the most frequent host plant species in the environment show a

161 higher intensity of infection (number of parasites per host) by S. flexicaulis, a mixed

162 generalized linear model (GLMM) [40] was used. The response variable was the average

163 number of individuals of S. flexicaulis per individual of each species of host plant per

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164 transect, the fixed variable was the frequency of each host plant species per transect and the

165 random variable was the sampled transects.

166 A GLMM was used to assess whether individuals from structurally more complex

167 host plants have a higher intensity of S. flexicaulis infection. The response variable was the

168 total number of individuals of S. flexicaulis per individual of the host plant, the fixed variables

169 were height, crown height, number of primary and secondary branches and maximum

170 number of branches of the individuals of the host plants, and the random variable was the

171 sampled transects. To observe if branches with larger diameters are more parasitized, a

172 GLMM was created, where the response variable was the abundance of the parasitic plants

173 per transect, the fixed variable was the size classes and the random variable was the transects.

174 To evaluate the mortality of the host plants, a GLMM was performed, where the response

175 variable was mortality after 28 months, the fixed variable was the presence or absence of the

176 mistletoe S. flexicaulis in the plants and the random variable was the sampled transects. The

177 variables of plant height and plant crown were used as covariates to observe the effect on

178 mortality. To evaluate whether the presence of the mistletoe S. flexicaulis affects the growth

179 of host plants after 28 months, GLMMs were performed. The growth measures were the

180 response variables of each model, the fixed variable was the presence or absence of the

181 mistletoe S. flexicaulis, and the random variable was the transects. We performed all analyzes

182 in the R Software [41]. Finally, to determine if there are differences in the structure of the

183 plant community with the presence of the mistletoe S. flexicaulis between the years 2017 and

184 2019, we used Simpson’s dominance index, Pielou's evenness index, and Shannon’s diversity

185 index [42]. As the objective of evaluating how the structure of the plant community would

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186 behave over time without the presence of the parasite, the same indexes were calculated

187 separately for the group of non-parasitized plants between the years 2017 and 2019.

188

189 RESULTS

190 In the first year of study (2017) 271 individuals belonging to 11 families and 20

191 species of plants were recorded in the eight sampled transects. The most representative

192 families in number of species were Asteraceae (four species) and Fabaceae (three species;

193 Table 1). Among all sampled species, Baccharis dracunculifolia was the most abundant (n =

194 189), followed by Callisthene sp (n = 17) and Mimosa maguirei (n = 11; Table 1). Among

195 the 271 individuals and 20 recorded species, 151 individuals (55%) and nine species (45%)

196 were parasitized by S. flexicaulis. The greatest abundance of individuals from S. flexicaulis

197 parasitizing a single host plant (n = 9) was found in B. dracunculifolia. Less frequent species,

198 such as M. maguirei (n = 11) and Solanum lycocarpum (n = 6) were not parasitized (Table

199 1).

200

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206

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207

208

209

210 Table 1. Plant community parasitized and not parasitized by Struthanthus flexicaulis in a 211 disturbed area of campos rupestres, in Serra do Cipó MG, Brazil. Host abundance: the total 212 abundance of each species of parasitized and non-parasitized plants. Mistletoe abundance: 213 the abundance of parasites by plant species. % Infected: the proportion of individuals of each 214 species infected with at least one individual of S. flexicaulis. Host mortality: the abundance 215 and percentage of dead plants.

Family Species Host Mistletoe % Host abundance abundance Infected mortality

Asteraceae Baccharis dracunculifolia 189 132 0,67 117 - 0,61 Asteraceae Eremanthus erythropappus 1 1 1,00 0 - 0,0 Asteraceae Eremanthus incantus 2 0 0,00 0 - 0,0 Asteraceae Vernonanthura scorpioides 2 0 0,00 0 - 0,0 Clusiaceae Kielmeyera petiolaris 5 1 0,25 2 - 0,50 Clusiaceae Kielmeyera scorpioides 5 0 0,00 2 - 0,40 Fabaceae Stryphnodendron adstringens 1 0 0,00 0 - 0,0 Fabaceae Dalbergia miscolobium 4 0 0,00 0 - 0,0 Fabaceae Mimosa maguirei 11 0 0,00 0 - 0,0 Lamiaceae Hyptidendron asperrimum 2 3 1,0 2 - 1,0 Lamiaceae Hyptidendron canum 1 0 0,00 0 - 0,0 Lythraceae Diplusodon orbicularis 8 3 0,25 4 - 0,50 Malpighiaceae Byrsonima verbascifolia 1 0 0,00 0 - 0,0 Malpighiaceae Byrsonima 8 2 0,25 3 - 0,37 Myrtaceae Psidium firmum 1 0 0,00 1 - 1,0 Salicaceae Casearia sylvestris 3 0 0,00 1 - 0,33 Solanaceae Solanum lycocarpum 6 0 0,00 0 - 0,0 pachystachya 1 1 1,0 0 - 0,0

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Vochysiaceae Callisthene 17 7 0,35 7 - 0,41 Vochysiaceae Vochysia thyrsoidea 3 4 0,66 1 - 0,33

216

217

218

219 The host species that were more frequent in the environment showed a greater

220 abundance of parasitic plants per individual (intensity of infection; Tables 1 and 2; Fig 1a).

221 Positive associations between the abundance of S. flexicaulis and the height of the plants (Fig

222 1b), the height of the crowns (Figure 1c) and the maximum level of branching (Table 2; Fig

223 1d) were recorded. On the other hand, the number of primary and secondary branches of the

224 plants did not affect the abundance of S. flexicaulis per plant (Table 2). In addition, the

225 abundance of S. flexicaulis was higher in the diameter classes 2 and 3 (Table 2; Fig 2a).

226 Table 2. Results of generalized linear mixed models (GLMM) testing the effect of host plant 227 frequency and architecture on the abundance of the mistletoe Struthanthus flexicaulis, and 228 the effect of this parasite on the growth and mortality of host plants in campos rupestres, in 229 Serra do Cipó, MG, Brazil. Response variables Fixed variables Family DF Deviance p-Value Mean mistletoe abundance Host frequency Gaussian 7 71.010 0.0017* (Intensity of infection) Mistletoe abundance Host total size Poisson 7 337.72 <0.001* (Intensity of infection) Height of the crowns Poisson 7 336.28 0.001* Primary branches Poisson 7 0.001 0.980 Secondary branches Poisson 7 508.49 0.329 Maximum level of Poisson 7 474.20 <0.001* branching Mistletoe abundance Classes branches Binomial 7 189.21 <0.001* Host growth Mistletoe presence Gaussian 7 167.86 0.103

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Increment of crown size Mistletoe presence Gaussian 7 142.90 <0.001*

Increment of primary branches Mistletoe presence Gaussian 7 259.80 0.405 Increment of secondary branches Mistletoe presence Gaussian 7 2.234 0.135 Increment of branching levels Mistletoe presence Gaussian 7 8.603 0.003* Mortality Mistletoe presence Binomial 7 1.4031 0.028* Host total size Binomial 6 1.669 0.147 Crown size Binomial 5 0.237 0.578

230 Fig. 1. Relationship between intensity of infection (abundance of individuals per host plant) 231 by mistletoe Struthanthus flexicaulis and (a) host frequency (y= -0.1348 + 33.3566*x), (b) 232 host height (y= exp(-2.1663 + 0.7923*x)), (c) height of the crowns (y=exp (-1.7705 + 233 0.7827*x)), and (d) maximum level of branching (y=exp (-1.50740 + 0.36442*x)), in 234 campos rupestres, in Serra do Cipó, MG, Brazil.

235 Parasitized plants showed lower crown growth and lower increment of branches over

236 time than the non-parasitized plants (Table 2; Fig 2b and c). However, for the other

237 architectural variables measured over time (height, primary, and secondary branches), no

238 statistically significant differences were found between parasitized and non-parasitized

239 plants (Table 2). Plant mortality was intensified by the presence of S. flexicaulis (Table 2;

240 Figure 2d). Out of the 120 non-parasitized plants, 26 individuals (21.66%) died after 28

241 months, while among the 151 parasitized plants, 128 individuals (84.10%) died during the

242 same period. Among the most abundant species (n > 7), B. dracunculifolia and Diplusodon

243 orbicularis suffered higher mortality (Table 1). There was no effect of plant and canopy

244 height on plant mortality (Table 2).

245 Fig. 2. (a) Classes of parasitized branches, (b) increment of crown size, (c) increment of 246 branching levels of plants (d) mortality of plants parasitized and non-parasitized and by the 247 mistletoe Struthanthus flexicaulis in campos rupestres, in Serra do Cipó, MG, Brazil. 248 249 The community structure changed between the years of 2017 and 2019. There was a

250 reduction in species richness from 20 to 18 species, since individuals of Hyptidendron

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251 asperrimum (n = 2) and Psidium firmum (n = 1) died. The plant community showed greater

252 dominance in 2017 (Simpson = 0.495) than in 2019 (Simpson = 0.322). In addition, evenness

253 was lower in 2017 (Pielou = 0.201) than in 2019 (Pielou = 0.274). Species diversity was

254 lower in 2017 (Shannon = 0.603) compared to 2019 (Shannon = 0.793). When we evaluated

255 only the non-parasitized plant group, we observed that the structure of this assemblage

256 remained stable between the years 2017 (Simpson = 0.246; Pielou = 0.0537; Shannon =

257 0.860) and 2019 (Simpson = 0.242; Pielou = 0.0572; Shannon = 0.856).

258 DISCUSSION

259 The abundance of the mistletoe S. flexicaulis depends directly on the abundance of

260 host plants in the studied community, that is, the more frequent host species in the community

261 were more intensely infected (number of hemiparasites per individual). In our study, the most

262 frequent and most parasitized plant species, Baccharis dracunculifolia, is a pioneer plant that

263 occurs in dense patches [43, 44, 45]. Then, these patches may become more visible and

264 represent important resting sites to birds in disturbed areas, increasing the deposition of seeds

265 and consequently the abundance of parasitic plants [46], [19]. In a study carried out in

266 ferruginous campo rupestre, [9] found that Mimosa calodendron was the host plant with the

267 highest proportion of parasitized individuals. The authors suggested that the aggregate

268 populations of this host plant within the community, forming green patches in the landscape,

269 determined its greater use as perches by seed-dispersing birds and, consequently, a greater

270 deposition of hemiparasite seeds. Many individuals of the same species, in dense patches,

271 can also favor the spread of the parasite, since part of the seeds ingested by the birds are left

272 close to the mother plant [46], [47], [25]. In addition, the high density of host plants in patches

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273 can increase the likelihood of individuals receiving branches of the parasite from neighboring

274 infected plants [9].

275 Plants with more complex architecture had more S. flexicaulis. Taller plants with

276 larger and more branched crowns are more likely to be used as perches and offer a greater

277 number of sites for the establishment of S. flexicaulis [19, 20, 23]. Greater abundance of S.

278 flexicaulis on individuals of B. dracunculifolia that presented larger classes of size and with

279 more levels of branching were reported by [23]. In addition, plants with more complex

280 architecture have branches with a greater variety of sizes, which can increase the amount of

281 optimal substrates for the establishment of the hemiparasite. Similarly, to our results,

282 previous studies have shown that branches with intermediate diameters are the most

283 colonized, as in them the parasite’s haustorium penetration is facilitated, while parasitic

284 plants are unable to establish themselves in branches with very small diameters and very

285 large branches have very thick bark that prevents haustorium penetration [48, 18]. Another

286 important factor is that hosts with more complex architecture, probably older ones, have been

287 in the environment for a longer time, and therefore, they were more likely to be infected.

288 Plants parasitized by S. flexicaulis showed lower crown growth and branching than

289 non-parasitized plants, over time. This result was expected once the parasitic plant competes

290 with the host plant for water and nutrients [49]. Other studies have shown that host plants

291 attacked by S. flexicaulis showed lower foliage cover compared to non-parasitized plants [19,

292 23]. In addition to interfering with the vigor of parasitized plants, parasitism can affect the

293 fitness of their hosts [49, 50]. [19] demonstrated that individuals of M. calodendron

294 parasitized by S. flexicaulis produce less fruits and lighter seeds than those not parasitized,

295 suggesting that the viability of these seeds can also be reduced. Particularly, in environments

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296 under water stress, such as the campo rupestre, the negative effects of parasitic plants on host

297 performance can be amplified, leading to a higher mortality rate of parasitized individuals

298 [19, 14]. In fact, in this work, the individuals of the dominant species, B. dracunculifolia,

299 that were parasitized showed a mortality rate of 61% after two years. In another work in the

300 campo rupestre, of the 164 dead individuals of the species M. calodendron, 139 (84%)

301 showed traces of the mistletoe S. flexicaulis [9].

302 The presence of S. flexicaulis altered the structure of the plant community in this study

303 area, leading to decreased dominance and increased diversity and evenness of the plant

304 community over time. This result was determined by the high mortality of parasitized

305 individuals of the most abundant species. If the most parasitized individuals in the

306 community belong to competitively dominant plant species, parasitism can mediate the

307 coexistence of species in the community, allowing inferior competitor species to persist [11,

308 29, 31]. Similar effects of the presence of other aerial parasitic plants on the structure of plant

309 communities have been demonstrated in different ecosystems [29, 51]. An experimental

310 study in a coastal swamp environment demonstrated that the coexistence between plant

311 species was mediated by the parasitism of the vine Cuscuta salina, since its preferred host

312 plant is competitively dominant [29]. In another study, [51] demonstrated that the presence

313 of the parasite Cuscuta howelliana led to an increase in richness and a change in the

314 composition of species of plant communities that inhabit seasonal lakes. Similar results were

315 also found for root hemiparasites [27, 30, 31]. Studies carried out with hemiparasitic species

316 of the genus Castilleja in alpine ecosystems have shown that the presence of these species is

317 associated with an increase in plant species richness and an increase in the evenness of the

318 plants in the community [30, 31].

15 bioRxiv preprint doi: https://doi.org/10.1101/2020.04.30.070268; this version posted April 30, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license.

319 In this study, we determined the factors related to the characteristics of the host plants

320 that affect the distribution and abundance of the mistletoe S. flexicaulis, and the effects of

321 this parasitism on host plants and, consequently, on the structure of the communities they

322 inhabit in the campo rupestre. The aggregate distribution of B. dracunculifolia, the dominant

323 host in the community, seems to contribute to the parasite's success, since dense patches are

324 more visible by birds in the landscape and facilitate the vegetative propagation of the

325 parasite's individuals. In addition, we demonstrate that the architectural complexity of the

326 host plant is an important factor that positively affects the abundance of the parasitic plant.

327 In turn, the parasitism by S. flexicaulis, negatively affects the growth of host plants, which

328 also have a higher mortality rate compared to non-parasitized plants. The high mortality of

329 the most abundant species B. dracunculifolia led to a change in the structure of the plant

330 community over time, with a decrease in dominance and an increase in the diversity and

331 evenness of plant species. These results reinforce the importance of parasitic plants as key

332 species for maintaining species diversity in plant communities.

333 Acknowledgments: We thank two anonymous reviewers for their criticisms on

334 earlier versions of the ms. We also thank the logistic support provided by the Reserva

335 Vellozia and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)

336 for funding this Long-Term Ecological Research (PELD-CRSC-17 - 441515/ 2016-9). We

337 thank Maria Cristina Messias, Thaise Bahia and Hildeberto Caldas de Sousa for help in

338 identifying plant species. We also thank Daniel Vasconcellos for translating this study to

339 English. This study is in partial fulfillment of the requirements for a Doctor in Ecology at

340 Universidade Federal de Minas Gerais (UFMG). CAPES provided scholarships to GFM, MB

341 and SN. CNPq provided scholarships to YA and GWF.

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342

343

344

345

346

347 References

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