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Trachymyrmex Septentrionalis RESEARCH ARTICLE Bioturbation by the Fungus-Gardening Ant, Trachymyrmex septentrionalis Walter R. Tschinkel1*, Jon N. Seal2 1 Department of Biological Science, Florida State University, Tallahassee, Florida, United States of America, 2 Department of Biology, Center for Environment, Biodiversity and Conservation, University of Texas at Tyler, Tyler, Texas, United States of America * [email protected] Abstract Soil invertebrates such as ants are thought to be important manipulators of soils in temper- a11111 ate and tropical ecosystems. The fungus gardening ant, Trachymyrmex septentrionalis,is an important agent of biomantling, that is, of depositing soil excavated from below onto the surface, and has been suggested as an agent of bioturbation (moving soil below ground) as well. The amount of bioturbation by this ant was quantified by planting queenright colonies in sand columns consisting of 5 layers of different colored sand. The amount of each color of sand deposited on the surface was determined from April to November 2015. In Novem- OPEN ACCESS ber, colonies were excavated and the color and amount of sand deposited below ground Citation: Tschinkel WR, Seal JN (2016) Bioturbation (mostly as backfill in chambers) was determined. Extrapolated to one ha, T. septentrionalis by the Fungus-Gardening Ant, Trachymyrmex deposited 800 kg of sand per annum on the surface, and an additional 200 kg (17% of the septentrionalis. PLoS ONE 11(7): e0158920. doi:10.1371/journal.pone.0158920 total excavated) below ground. On average, this mixes 1.3% of the sand from other layers within the top meter of soil per millennium, but this mixing is unlikely to be homogeneous, Editor: James A.R. Marshall, University of Sheffield, UNITED KINGDOM and probably occurs as "hotspots" in both horizontal and vertical space. Such mixing is dis- cussed as a challenge to sediment dating by optically stimulated luminescence (OSL). Received: February 12, 2016 Accepted: June 23, 2016 Published: July 8, 2016 Copyright: © 2016 Tschinkel, Seal. This is an open access article distributed under the terms of the Introduction Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any A variety of physical, chemical and biological processes contribute to the formation and devel- medium, provided the original author and source are opment of the world's soils. Historically, geologists and soil scientists have emphasized the credited. physical and chemical aspects of this process, but beginning with Darwin [1], there has been – Data Availability Statement: All relevant data are increasing awareness of the importance of biological processes in soil development [1 8]. Soils within the paper and its Supporting Information files. are home to thousands of species, including microbes and plants that facilitate weathering and move soluble materials around, and animals, from earthworms to aardvarks, whose burrowing Funding: This work was supported in part by National Science Foundation grant No. IOS 1021632 brings soil to the surface (biomantling) or mixes different layers below ground (bioturbation) and DEB 1354629. The funder had no role in study [3, 9–11]. These biological processes disrupt or enhance the physical and chemical processes of design, data collection and analysis, decision to soil development. publish, or preparation of the manuscript. In most temperate to tropical zones, ants are among the most abundant soil-dwelling ani- Competing Interests: The authors have declared mals, and are probably the premier turners of soil [12–16], often exceeding the effects of ter- that no competing interests exist. mites and vertebrates [17]. Their burrowing affects many soil characteristics such as water PLOS ONE | DOI:10.1371/journal.pone.0158920 July 8, 2016 1/15 Bioturbation by Trachymyrmex infiltration, grain size distribution and soil texture and mineral dissolution [6, 12–16, 18, 19], all of which can affect the soil's congeniality for organisms. Their effects are magnified because many ant species move their nests frequently [14, 20–22], and some have been shown to remodel their subterranean nests [10, 23–25], which increases bioturbation. The biomantling by ant species, or even entire communities has been studied several times [12–16], primarily by measuring the mounds of soil the ants dump on the surface on a per nest or per m2 basis. Reported rates vary greatly, depending on species and location. A table summarizing the pub- lished rates can be found in Tschinkel [9]. Earlier studies found significant biomantling activity and other soil movements by the Flor- ida Harvester Ant (Pogonomyrmex badius) in a pine forest in northern Florida [9, 10]. While substantial, the amounts of soil surface movement by this species was much lower than bio- mantling in the fungus-gardening ant Trachymyrmex septentrionalis [26]. These results were surprising because P. badius has relatively large colonies (up to 10,000 workers) and volumi- nous subterranean nests (up to 10 L), whereas T. septentrionalis has much smaller nests, usually containing a few hundred workers whose average individual live weight is less than a milligram [26, 27]. The biomantling differences are probably the result of the much higher nest density of T. septentrionalis. Despite their small size, T. septentrionalis colonies are extremely abundant. An average hect- are of pine forest contains >1000 nests that collectively excavate >1 metric ton of soil each year [26]. Over the course of a millennium, these ants completely displace the top-most 6.3 cm of soil [26, 28]. As a result, T. septentrionalis is likely an important agent of biomantling in coastal plains forests, a region in which this species has a long evolutionary history [29, 30]. Furthermore, Seal and Tschinkel [26] also reported that these ants move their fungus chambers to deeper levels as the soil warms in the spring and summer, a behavior common in fungus- gardening ants in seasonal environments [30–31]. Because some shallow chambers of colonies excavated in midsummer contained sand, it seemed likely that T. septentrionalis is an impor- tant agent of bioturbation by mixing soil from different levels. The purpose of this study is to confirm and quantify this bioturbation by planting colonies in columns composed of layers of different colored sand and monitoring seasonal deposition of colored sand as well as the loca- tion of the sand in the soil column. Materials and Methods Study site Field site: The study population of the fungus-gardening ant, Trachymyrmex septentrionalis,is located in the same 23 ha site as the Pogonomyrmex badius population of Tschinkel [9]. The lati- tude and longitude of the site are, respectively, 30.3587 and -84.4177, about 16 km southwest of Tallahassee, Florida, USA. This study site is located in the Apalachicola National Forest within the so-called sandhills ecotype [32]. Dubbed Ant Heaven, the soils are excessively drained sand but sloping toward a wetland and stream to the east. The water table is >5 m at the maximum depth to water, creating a droughty site suitable for several drought-resistant species of ants and plants (e.g. Opuntia). The forest is composed of longleaf pines (Pinus palustris) planted ca. 1975, whereas turkey oak (Quercus laevis), bluejack oak (Quercus incana), occasional sand pines (Pinus clausa) and sand live oak (Quercus geminata) occur in the subcanopy. The natural ground cover of wiregrass (Aristada stricta) was absent, replaced by several successional species of grasses, herbs and shrubs. T. septentrionalis nests were easily recognized in the spring by the semi-lunar crescent of excavated soil [33], and occurred at densities of about 1000 per ha. The soil of most of Ant Heaven formed as ridges of sandy marine or dune deposits on marine limestone terraces. This Ortega Sand is strongly acidic, very well-drained and nutrient PLOS ONE | DOI:10.1371/journal.pone.0158920 July 8, 2016 2/15 Bioturbation by Trachymyrmex poor (85% of the nutrients are in the topmost 15cm, unpublished data, WRT). The eastern edge of Ant Heaven slopes to the Fisher Creek wetland with its very poorly drained Donovan Mucky Peat. On the west, the Ortega Sand grades into the extremely acidic Talquin Fine Sand, but little of this is included in Ant Heaven (http://websoilsurvey.nrcs.usda.gov/app/ WebSoilSurvey.aspx). This project was carried out under US Forest Service, Apalachicola National Forest permit number APA56302, Expiration Date: 12/31/2017. Trachymyrmex septentrionalis is not a pro- tected species. Construction of layered soil Sand of six different colors (orange, green, purple, yellow, blue, pink) was purchased from Sand Blast Entertainment (www.coloredsand.com). Using a post-hole digger, 1 m deep, 50 cm diameter holes were excavated and the excavated sand mixed with each color so that the final mixture consisted of about 25% colored sand and 75% native sand. Five different colors of these sand mixtures were layered and packed in 20 cm thick layers ("host" layers) in the exca- vated holes with a 10 cm layer of native sand on the top. Before layering, the sides of each hole were lined with sheer polyester fabric to prevent the ants from excavating outside the layer cake. In three of the ten "layer cakes", yellow was used instead of purple. Ten such 5-color layer cakes were constructed and allowed 2–3 weeks to settle. The order of layers and their approxi- mate depth was native (0–10 cm), orange (10–30 cm), green (30–50 cm), purple or yellow (50– 70 cm), blue (70–90 cm), pink (90–110 cm). In general, the setup of this experiment was simi- lar to that in [23]. Excavation and planting of colonies In mid-April 2015, during the early stages of their annual cycle, active T. septentrionalis colo- nies were carefully excavated, and all ants and fungus were collected. Colonies were all brood- less and contained 500 to 1000 workers. Only queenright colonies were used for the experiment.
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