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Disruption of Ant-Aphid Mutualism in Canopy Enhances the Abundance of Beetles on the Forest Floor

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Disruption of Ant-Aphid Mutualism in Canopy Enhances the Abundance of Beetles on the Forest Floor Disruption of Ant-Aphid Mutualism in Canopy Enhances the Abundance of Beetles on the Forest Floor Shuang Zhang., Yuxin Zhang., Keming Ma* State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing, People’s Republic of China Abstract Ant-aphid mutualism is known to play a key role in the structure of the arthropod community in the tree canopy, but its possible ecological effects for the forest floor are unknown. We hypothesized that aphids in the canopy can increase the abundance of ants on the forest floor, thus intensifying the impacts of ants on other arthropods on the forest floor. We tested this hypothesis in a deciduous temperate forest in Beijing, China. We excluded the aphid-tending ants Lasius fuliginosus from the canopy using plots of varying sizes, and monitored the change in the abundance of ants and other arthropods on the forest floor in the treated and control plots. We also surveyed the abundance of ants and other arthropods on the forest floor to explore the relationships between ants and other arthropods in the field. Through a three- year experimental study, we found that the exclusion of ants from the canopy significantly decreased the abundance of ants on the forest floor, but increased the abundance of beetles, although the effect was only significant in the large ant- exclusion plot (80*60 m). The field survey showed that the abundance of both beetles and spiders was negatively related to the abundance of ants. These results suggest that aphids located in the tree canopy have indirect negative effects on beetles by enhancing the ant abundance on the forest floor. Considering that most of the beetles in our study are important predators, the ant-aphid mutualism can have further trophic cascading effects on the forest floor food web. Citation: Zhang S, Zhang Y, Ma K (2012) Disruption of Ant-Aphid Mutualism in Canopy Enhances the Abundance of Beetles on the Forest Floor. PLoS ONE 7(4): e35468. doi:10.1371/journal.pone.0035468 Editor: Frederick R. Adler, University of Utah, United States of America Received January 7, 2012; Accepted March 16, 2012; Published April 25, 2012 Copyright: ß 2012 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was supported by National Natural Science Foundation of China (30900185, 30870459), Special Fund for Forestry-scientific Research in the Public Interest (200904005), and State Key Laboratory of Urban and Regional Ecology Grant (SKLURE2008-1-02). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] . These authors contributed equally to this work. Introduction or abundance of other arthropod groups on the forest floor [21,22]. Recent studies have highlighted the importance of ants in In addition to predation and competition, mutualism is an structuring the arthropod community in terrestrial ecosystems important factor in shaping community structure and diversity [19,23,24,25], suggesting that variations in ant abundance can lead [1,2]. Ant-aphid mutualism is a common mutualistic interaction in to corresponding changes in the arthropod community on the forest the field, where ants feed on the honeydew excreted by aphids and floor. Therefore, if aphids in the canopy can change the abundance in return protect those insects from predators and parasitoids [3,4]. of ants on the forest floor, the ecological effects of ants on other Aphids lead to a high abundance of ants in the tree canopy [5], and arthropods can also be changed. Most related studies, however, only aphid-tending ants have important ecological impacts for both the focus on the impacts of the ant-aphid interaction on plants host plant and other related insect species on the plant [6,7,8]. [6,7,11,14,26,27,28,29,30], and we know little about the possible Many honeydew-feeding ants are ground rather than canopy impacts of this mutualism extend to the forest floor. dwelling, such as the ant species in the genera Formica and Lasius In this study, we hypothesized that the breakdown of the ant- [9,10,11,12,13] as well as some invasive ants in the genera aphid mutualism in the canopy could decrease the abundance of Anoplolepis, Solenopsis, Linepithema [14,15,16]. Plant-based food (such ants on the forest floor due to a lack of food resources, and increase as extrafloral nectar and honeydew excreted by aphids) may be a the abundance of other ground arthropods. To test this hypothesis, key factor in creating high densities of ants in the field [17,18]. For we raised the following questions: 1) Does the exclusion of ants example, the addition of artificial carbohydrates to the forest floor from the canopy impact the abundance of ants and other can largely enhance the foraging activity of ants and intensify their arthropods on the forest floor, and 2) is there a relationship interactions with other arthropods [19]. Therefore, aphids may between the abundance of ants and other arthropods in the field? enhance the abundance of ants in the canopy as well as on the forest floor. However, the magnitude of the dependency of ants on Methods aphids is rarely studied, with most existing studies only evaluating the impacts of ants on aphids [3]. Ethics statement Because of their ubiquity and aggressiveness, ants are likely to No specific permits were required for the described field studies. influence all other arthropod groups on the forest floor, either The location was not privately owned or protected in any way, and directly or indirectly [20]. Ants can depress or enhance the diversity the study did not involve endangered or protected species. PLoS ONE | www.plosone.org 1 April 2012 | Volume 7 | Issue 4 | e35468 Indirect Impact of Aphids on Ground Arthropods Study site as the treatment and the right as the control, as in the conservative The study area is located in the Beijing Forest Ecosystem experimental design in 2009. Research Station (30u57929 N, 115u25933 E, altitude 1,200– In April of each year in the study (before the growing season), an 1,400 m), a member of the Chinese Ecological Research Network adhesive ring was smeared around the trunk (about 1 m above the (CERN), about 100 km northwest of Beijing City, China. This ground, and 5 cm in width) on all trees in the treatment plot to area typically has a warm temperate continental monsoon climate impede the access of ants to aphids on the canopy. The adhesive with average annual precipitation of 500–650 mm. The mean was made of a polymer resin mixture (Beijing Nonghaha S & T annual temperature is 5–10uC. It is an oak (Quercus liaotungensis) CO. LTD) and was nontoxic, harmless to plants, and non- dominated, 80-year-old secondary forest with a few birches (Betula attractive to insects. The adhesive was re-smeared every two spp.), maples (Acer mono.), and shrubs (e.g., Prunus spp., Vitex negundo months during the growing season until the end of the study. Any var. hetertophylla). bridges that could allow ants to climb onto trees were cut off throughout the study. Impacts of excluding ants from the canopy on the Pitfall traps were used for arthropod sampling. This method is a abundance of ants and other arthropods on the forest sampling technique extensively used to sample surface foraging floor invertebrates such as ants, beetles, and spiders [25,34,35]. According to a systematic sampling method, we set up 16 traps We conducted this experiment during three consecutive in each 20*20 m plot, with a 5 m interval between adjacent traps growing seasons (2009, 2010, and 2011) of the oak tree Q. (Fig. 1C). We collected samples only in the three small plots in the liaotungensis, which is the dominant tree species in the study area middle area of the large plot in order to reduce any possible edge [31]. We selected a slope in a small watershed to conduct the effect (Fig. 1B). Starting at the end of May in 2009, 2010, and experiment. We chose this area because the ant Lasius fuliginosus 2011, we sampled the abundance of ground arthropods each was the only active ant species with high abundance in the pitfall month. For each trap, a cup (diameter = 7.9 cm, depth = 9.7 cm) trap sampling in this area. L. fuliginosus is a typical honeydew- with 50 ml of alcoholic solution (5% in concentration) was buried feeding ant that has mutualistic relationships with some aphid under the ground. Two days after the traps were set, we retrieved species [32]. In the study area, L. fuliginosus was attracted by aphids the cups and samples were taken back to the lab for taxonomy. We Lachnus tropicalis and Tuberculatus sp. in the canopy and Stomaphis then classified the arthropods as ants, spiders, beetles, centipedes, japonica on the trunk of Q. liaotungensis. The aphid was the key factor millipedes, caterpillars, and so on, and counted the number of attracting ants in the canopy of Q. liaotungensis in the study site [33]. individual arthropods in each family. The species of ants, spiders, In 2009, we set up four pairs of plots (20*20 m) with a distance and beetles were identified as accurately as possible. of at least 50 m between the adjacent pairs. For each pair, the left plot was set as the aphid exclusion plot and the other as the control plot (Fig.
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