Mistletoes (Loranthaceae), a common semi-parasitic shrub in China, are parasites on the stems or branches of host plant (Li et al., 2011; Cui et al., 2014). The family compares more than 1300 species belonging to 65 genera from 2 subfamilies, and is widely distributed in tropical and subtropical areas (Li et al., 2011; Ouyang et al., 2018). In China, 64 species and 10 varieties belonging to 11 genera could be found in many provinces, especially in South China and Southwest China (Qiu and Lin, 1988; Li et al., 2011; Cui et al., 2014). Despite photosynthesis by themselves, mistletoes are failed to growth independently, which cause their dependence to host plant. The seeds of mistletoes are distributed to branches of host plant through their bird dispersers (Li, 1996; Ou et al., 2014;). After sprouting, their haustoriums could connect the vascular system, which is helpful to obtain water, minerals and carbohydrates from the host body (Li, 1996; Ou et al., 2014; Wang and Zhang, 2017). Mistletoes are tolerant to select their host that contains various plants including Moraceae, Betulaceae, Platanaceae, Fagaceae, Rutaceae, Theaceae, and Leguminosae (Cui et al., 2014). However, their selection to host in different regions were clear different due to the factors of climatic environment, bird dispersers and species and numbers of mistletoes (Cui et al., 2014). In the early stage of parasitism, mistletoes show few influence to host, but their excessive reproduction can cause the decreasing fruit and volume, retarded growth, and plant death, which limit the function of natural forest and plantation on ecology, economy and society.

Kunming Haikou Forest Farm located in Central Yunnan has arbor forest of approximate 6026.1 hm², accounting for 90.2% of the forest land area (Xu et al., 2015). Since establishment, the farm has focused on the ecological protection and obtains achievement in closed forest, ecological construction and civilization, which contribute to the first “national ecological civilization education base” in Yunnan province and “national top ten forest farm” (Tie and Li, 2014; Xu et al., 2015). By investigation, mistletoes found in the forest farm was identified to be Taxillus thibetensis that is belonged to genera Taxillus and mostly lives in mountain broadleaf forest (1 700~3 000 m) in Southeast Xizang, Yunnan and Southwest Sichuan (Qiu and Lin, 1988). Although detriment to forest benefit, few studies are interested in T. thibetensis. In this study, we investigated T. thibetensis in the forest farm through sampling surveys and analyzed their distribution characteristics and host selection. The goal was not only to monitor the spread of parasite but also provide a scientific basis for their ecological control.

1 Results

1.1 Distribution and parasitism

Most T. thibetensis were found in M2 that is low canopy density (30%) and large slope (27°). The other quadrats showed a low parasite, suggesting an initial stage of parasite spread (Table 1). T. thibetensis showed a strong host selection. Quercus aliena was found to be host plants in all quadrat, except for that only one Cotoneaster microphyllus with parasitization was found in M2. The percentage of Q. aliena in community and its number with parasitization both showed a maximal value (64.58% and 83.87%) in M2, which were connected to a large number of Q. aliena with parasitization in the region (Figure 1). In adjoining four quadrats, the number of T. thibetensis was unrelated to Q. aliena rate in community. M1 and M4 showed high rate of Q. aliena (33.73% and 39.47%) but low parasite rate (17.86% and 26.67%). In contrast, there were low Q. aliena rates (26.39% and 6.19%) in M3 and M5 that exhibited high parasite rates (47.37% and 50%). These suggested an unclear correlation between Q. aliena percentage in community and T. thibetensis spread in adjoining quadrats.

Table 1 The distribution of Taxillus thibetensis in Kunming Haikou Forest Farm

Figure 1 The ratio of Q. aliena in quadrat and with parasitization

1.2 The preference of T. thibetensis to growth characteristics of Q. aliena

Based on the independent variables of diameter, tree height and crown width of 114 Q. aliena samples in all five quadrats, stepwise regression analysis was used to fit the parasitic intensity of T. thibetensis. As a result, the coefficient of correlation to parasitic intensity of T. thibetensis was highest for crown width at 0.642, followed by diameter at 0.610, which were both significant (Table 2). After introducing the two independent variables into the regression model in turn, there were clear increasing linear relationship and decreasing standard error and the corrected R² fitting were 0.526 (Table 3).

Table 2 Pearson correlation between parasitic intensity of Taxillus thibetensis and growth characteristics of Q. aliena. Note: The left diagonal shows the pearson correlation coefficient; The right diagonal shows the p value

Table 3 The correlation coefficient and fitting degree in different models

A t-test in partial regression coefficient was employed to analyze the effect of host characteristics on parasitic intensity. The result showed that crown width and diameter of host have a significant influence on number of T. thibetensis and that the equation was y=-0.467+0.152x₁+0.110x₂ (Table 4). An F-test was used to examine the slope of the model, and the result showed a well-fitting degree and available regression model (Table 5).

Table 4 A t-test in partial regression coefficient

Table 5 A F-test in regression model

1.3 The parasitic position preference of T. thibetensis to Q. aliena

In the M2 with high T. thibetensis intensity, one Q. aliena sample were found to underwent most parasitic intensity at 19 and the range of parasitic height position ratio was 61.22%~86.73% (Figure 2). The parasitic intensity of other Q. aliena samples was 5 with average height position ratio of 67.84% (ranging from 40% to 80%). The M1 showed a low T. thibetensis intensity and the parasitic position ratio ranged from 42.37% to 68.29%. There was a large range of parasitic position ratio in the M3, M4 and M5, and it was unobvious to major parasitic position.

Figure 2 The parasitic intensity and position of T. thibetensis in host Q. aliena.

2 Discussion

The spatial distribution pattern of mistletoes in the community is affected by the distribution of the host and the spread method of the dispersers (Overton, 1994; Roxburgh and Nicolson, 2005). The various mistletoes species showed high choice preference to host, and the main host comprised plants from Fagaceae, Moraceae, Euphorbiaceae, Lauraceae, Rutaceae, and Theaceae families, in which Fagaceae plants were easiest to be parasitic (Mathiasen and Daugherty, 2008). The study of Cui et al. (2014) showed that host species of both Loranthus tanakae and Taxillus sutchuenensis was Q. aliena var. acuteserrata in Qinling Mountain. Liu et al. (2014) found that Q. wutaishanica was main host of Loranthus tanakae in Malan forest region of Shaanxi Province. In this study, T. thibetensis found in Kunming Haikou Forest Farm showed a strong host selection and Q. aliena was main host plants. M2 exhibited high parasite intensity, which was an initial stage of spread. The result was consistent with the host selection preference of mistletoes (Qiu and Lin, 1988; Li and Zhang, 2019). Furthermore, Q. aliena was main host in initial spread of T. thibetensis.

The growth characteristics of host could affect the parasitic intensity of mistletoes. A high intensity was related to high tree height and dense power branches because those could provide abundant nutrition for mistletoes (Pang et al., 2012; Zhang, 2015). The study of He (2019) in the Shennongjia of Western Hubei showed that mistletoes were easy to be found in trees with high diameter and crown width, which were supported by the study of Ouyang et al. (2018). The choice preference of mistletoes was related to their bird dispersers. The high tree characterized by large crown width could provide the activity places for birds, which increased spread probabilities of mistletoe seeds in the tree (Xiao and Pu, 1994; Li and Zhang, 2020). Our result was also accord with the choice preference. The parasitic intensity exhibited significant positive correlations with both crown width and diameter, and an optimal fitting regression equation were established to monitor and control of mistletoe parasite. Moreover, some studies revealed the preference of mistletoes to the upper position of host tree due to that enough light could help their developmental growth (Roxburgh and Nicolson, 2005; Liu et al., 2014). In this study, a large of mistletoes were found in upper of host tree in M2, but the height selection were unobvious in M3, M4 and M5, suggesting an initial stage of parasite spread.

Mistletoes play an important role in community because of their significant effect on structure and distribution of community. A number of studies focused on the spread of pollen and seed, parasitic process, host selection and environment influence, but most of which are reported in America and Australia (Watson, 2009). China has rich plant species and complex ecological environment. A number of mistletoes are found in various plant communities, but a few studies were interested in them. As a regulator in community, more attentions to parasitic mechanism of mistletoes were required.

3 Materials and Methods

3.1 A survey for the research region

The research region is located at south slope of western hill in Kunming Haikou Forest Farm (24°50′52.1″N~24°51′4.5″N, 102°33′48.1″E~102°34′9.6″E). Its climate is influenced by the season alternation of southwest monsoon and westerly circulation from the Indian Ocean, and presents a plateau monsoon climate in Southwest China. There is a variety of forest types in the region, including semi-humid evergreen broadleaf forest, coniferous forest and mixed forest. The region is characterized by red soil with medium thickness, high-altitudes (1900 ~2 200 m), lower middle southeastern slope, mild climate, moderate rainfall, distinguishing dry and wet seasons. The annual average temperature is 14.6^°C ranged from -7.8^°C to 34.4^°C. The annual average precipitation is 909.7 mm, in which the summer is the rainy season (accounting for more than 80%). The natural forest comprise a number of plants, such as Weigela japonica var. sinica, Rhododendron simsii, Myrsine Africana, Myrica rubra, Eulalia speciose, Arundinella anomala, Arthraxon hispidus, Gentiana scabra, Ageratina adenophora, Arisaema heterophyllum, Schizachyrium delavayi, Urtica fissa and Pteridophyta. There is a small amount of bare rock in the investigation plot.

3.2 Investigation and identification

We chose randomly five quadrats of 20 m×20 m in the parasite center and its four adjoining areas with an altitude range of 2 000~2 300, and at least 25 m were intervened between quadrats. As showed in Table 1, the parasite center were named M2 (altitude of 1 987 m), and other areas were named M1 (2 071 m), M3 (2 012 m), M4 (2 028 m) and M5 (1 947 m). The forest compass and Vertex IV range finder were used to plan the quadrat of 20 m× 20 m, in which each were further divided into four subquadrats of 10 m×10 m. We investigated the growth characteristic (diameter, tree height and crown width) of all woody plants (more than 2 cm diameter), the canopy density and parasitization in the quadrat.

3.3 Data analysis

The host plants in every quadrat were investigated. The percentage of host species was the number with parasitization of all species in the quadrat, and the parasite percentage of host species was number with parasitization of all individuals in the host species. The parasitic intensity was the sum of parasitic number at different height position of tree. The percentage of parasitic height position was calculated by the parasitization position of the tree height. In analysis of host growth characteristics, the regression equation between parasitic intensity and characteristics (including height, diameter and crown width) was established using stepwise method in SPSS 21.0.

Authors’ contributions

Anpei Zhou designed and performed the experiments, analyzed the data, and authored drafts of the paper. Zhiwei Jin analyzed the data and authored drafts of the paper. Xu Yang was involved in design of experiments and analysis of data. Zhiguang Li is the conceiver and administration of the paper and contributed the experiments design, data analysis and draft and review. All authors read and approved the final manuscript.

Acknowledgments

This work was supported by testing item of the Central Yunnan Plateau Forest Ecosystem National Positioning Research Station (2018-YN-10) and operation subsidy of the Central Yunnan Plateau Forest Ecosystem National Positioning Research Station (2018-LYPT-DW-087).

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