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Neighbor leaf-cutting ants and mound-building termites: Comparative nest micromorphology
Geoderma 141 (2007) 224 – 234 www.elsevier.com/locate/geoderma
Neighbor leaf-cutting ants and mound-building termites: Comparative nest micromorphology Marcela I. Cosarinsky a,⁎, Flavio Roces b,1 a
Laboratorio de Icnología, Museo Argentino de Ciencias Naturales “B. Rivadavia”, Angel Gallardo 470, (1405) Buenos Aires, Argentina Behavioral Physiology and Sociobiology (Zoology II), Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
b
Received 2 January 2006; received in revised form 1 June 2007; accepted 1 June 2007 Available online 12 July 2007
Abstract The nest micromorphology of the leaf-cutting ant Atta vollenweideri and the mound-building termite Cortaritermes fulviceps, both species occurring in frequently flooded plains of the NE of Argentina, was comparatively studied. In spite of being located in the same type of soil, the nests showed different micromorphology, related to different nesting behaviors adapted to seasonal rains. Termites construct exclusively epigean mounds combining soil and fecal material arranged in a very massive microstructure. Soil particles excavated from the A horizon are frequently packed as lens-shaped pellets probably moulded in the termites' buccal cavity, and then regurgitated and coated with fecal matter. Many distinct fecal micro-features occur, such as bands crossing the walls or surrounding pellets, and gallery coatings. Conversely, the ants inhabit underground chambers excavated in the Bt horizon, which displays a very porous microstructure, showing voids equal to or smaller than 100 μm. This could be one of the reasons why water may be retained by capillary forces within the soil, being unable to inflow into the chambers during flooding. No micromorphological features composed of fecal matter were observed at any part of the ant nest, and contrary to previous claims, no coating in galleries or chamber walls was observed. During digging, workers remove the soil material and transport it through subterranean tunnels to the soil surface. Individual loads are recognized as rounded pellets that conserve the micromorphology of the excavated horizon, and are dropped on the surface of a large mound. The ant mound represents the epigean part of the nest, and displays a combination of very porous types of microstructure, composed of sand grains weakly cemented with clay, originated in weathered and amalgamated pelletal material with abundant plant fragments. The external nest architecture does not only result from a passive deposition of the excavated material, since ants employ soil pellets and plant fragments to construct conspicuous turrets, a number of which are closed and re-opened with seasonal periodicity. Turrets may protect the nest openings from water inflow and also enhance wind-driven nest ventilation. © 2007 Elsevier B.V. All rights reserved. Keywords: Neotropical; Chaco; Soil-nesting insects; Ants; Termites; Atta vollenweideri; Cortaritermes fulviceps; Soil micromorphology
1. Introduction Humid grasslands in the Gran Chaco region are inhabited by several soil-nesting species of ants and termites. Because of the seasonal rains and frequent floods, nests are expected to have particular adaptations to cope with the high water levels, in order to avoid water inflow into the structure. Ants of the species Camponotus punctulatus, for instance, construct ⁎ Corresponding author. Tel.: +54 11 45528490. E-mail addresses: [email protected] (M.I. Cosarinsky), [email protected] (F. Roces). 1 Tel.: +49 931 8884311; fax: +49 931 8884309. 0016-7061/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2007.06.006
compact and large mounds, and the entire colony was reported to move to the higher parts of the mounds during flooding (Bonetto et al., 1960). Fungus-growing ants of the tribe Attini are the dominant herbivores in the Chaco region, particularly the leaf-cutting ant Atta vollenweideri (Hymenoptera: Formicidae), which is not only important as food consumer, mainly grasses, but also as soil modifier (Bucher and Zuccardi, 1967; Jonkman, 1978, 1980a; Röschard and Roces, 2003). In the Chaco region, the influence of Atta ants on soil includes alteration of soil horizons through digging (nesting) behavior and soil removal, as well as the redistribution of nutrients contained in their underground chambers (Bucher, 1982). A mature nest of this species is easily recognized by its
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large and conspicuous conical- or ellipsoid-shaped mound, uncovered of vegetation, commonly 6 to 8 m in basal diameter and about 0.80 m high (Fig. 1). During the rainy season, mounds often look like round islands surrounded by water. A mature nest of A. vollenweideri may contain up to 2000 underground chambers for rearing a symbiotic fungus on the grass fragments harvested by the foragers, and a small number of very large refuse chambers (Jonkman, 1980c). Chambers, mostly located in the Bt horizon, are interconnected by a complex network of underground tunnels, a number of which connect to the surface. A mature nest may contain up to 200 nest openings (Jonkman, 1980c). Most of them are particularly large, with diameters up to 10 cm. The peripheral nest openings are used as entrances and connect with up to 100 m-long foraging trails, whereas the central nest openings often possess a turret or chimney (Jonkman, 1980b,c). The shape of the mound promotes the ventilation of the underground chambers via a passive mechanism driven by wind (Kleineidam and Roces, 2000; Kleineidam et al., 2001). The mound itself is not inhabited, and it results from the deposition of excavated soil during colony growth that originates from deep horizons. The mound, however, is not only a passive accumulation of excavated soil, since workers import material to reinforce and stabilize the construction, as observed for other ant species (McCook, 1877; Cowan et al., 1985), and also build structures with defined function like ventilation turrets (Jonkman, 1980b).
Fig. 1. Top: mound of the leaf-cutting ant, Atta vollenweideri. Bottom: mound of the termite Cortaritermes fulviceps. Note different scale bars.
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Mound-building termites are also very common and their nests can be found in the close vicinity of large leaf-cutting ant nests. The species Cortaritermes fulviceps (Isoptera: Termitidae) constructs epigean, very hard, dome-shaped nests (Fig. 1). Mounds are about 20 to 50 cm large in basal diameter, and 30 to 70 cm high, and include tussock grasses or little shrubs that frequently jut out from their surface (Talice et al., 1969; Cosarinsky, 2004b). The mound is composed of an intricate inner net of convolute galleries, 1.5 to 5 mm in diameter, which are connected with a diffuse net of subterranean galleries. The mound is entirely inhabited by the colony. In the rainy season, mounds are isolated refuges surrounded by water, and the colony moves to the upper region of the mound (personal observations). Even though the feeding habits of Neotropical termites are not completely understood, soil-feeding termites are recognized in the field by the dark grey color on their abdomens, and because they construct hard, dark mounds, rich in organic matter. These features are common in many Nasutitermitinae, including C. fulviceps. Soil-feeding termites characteristically feed in galleries located in the upper 10 cm of the A horizon, so it is supposed that the same horizon is the source of their building materials (Brauman et al., 2002). Field observations of sympatrically occurring nests of leafcutting ants, A. vollenweideri, and of mound-building termites, C. fulviceps, suggested that they were composed of different materials, even though they were located in the same type of soil. Since both species are seasonally affected by flooding, their nesting behavior and nest morphology may reflect an adaptation to protect the inhabitants against incoming water. The aims of the present study were: 1) to characterize comparatively the micromorphological features of nests constructed by two neighboring social insect species phylogenetically distant, but facing similar ecological conditions; 2) to investigate the selection of building materials and their spatial arrangement in relation to that of the surrounding soil; 3) to explore plasticity in termites' building behavior by comparing the micromorphology of nest constructed with different materials. For that, an inquilinous colony of C. fulviceps nesting on an Atta leaf-cutting ant mound, i.e., the colony used material from the ant mound for building, was comparatively investigated. In social insects, the micromorphology of soil nests was first studied for African and Australian termites (Stoops, 1964; Lee and Wood, 1971; Sleeman and Brewer, 1972; Mermut et al., 1984; Eschenbrenner, 1986; Jungerius et al., 1999). Recently, Cosarinsky (2003, 2004a,b, 2005) and Cosarinsky et al. (2005) studied the nest micromorphology of several Neotropical termite species including the micromorphology of nests of C. fulviceps located in different soil types in Argentina (Cosarinsky, 2004b). Regarding ants, Wheeler (1907) reported that workers of the fungus-growing ant Trachymyrmex turrifex line the underground tunnels and nest chambers with a thin layer of clay. But to our knowledge, the only studies reporting detailed micromorphological nest features in ants are those focusing on Lasius neoniger, one of the most abundant species
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of temperate regions of North America that inhabits subterranean galleries (Wang et al., 1995), and on mound-building fire ants in the Southeastern of the United States, Solenopsis invicta and S. richteri (Green et al., 1999). Recently, Cosarinsky (2006) studied the mound-building Neotropical ants, C. punctulatus and Solenopsis sp. nesting in flooded fields in Argentina, comparing their nest micromorphology with that of the surrounding soil. The present study, therefore, contributes to our knowledge about nesting behavior of ants and provides comparative information on the use of materials for nest building by neighboring social insect species, termites and ants, nesting on similar soils. 2. Area descriptions, methods and material studied 2.1. Nest characteristics and material sampling Nest micromorphology in the leaf-cutting ant A. vollenweideri Forel, 1893 and the mound-building termite C. fulviceps (Silvestri, 1901) Fontes, 1998, was studied using thin sections. Nests and surrounding soil were sampled at the “Reserva Ecológica El Bagual” (26° 10’ S, 58° 56’ W), located in the eastern (humid) Chaco region, Province of Formosa, Argentina. Based on morphological data, their surrounding soil profile was determined as a Typic Haplustalf (Alfisol). In the field, we investigated one mature leaf-cutting ant nest, one mature termite nest, and one inquilinous termite nest located directly on the ant mound. The nest of A. vollenweideri was excavated and sectioned from the top of the mound downwards to 2.50 m deep in the Bt horizon, where fungus and refuse chambers were found. The ellipsoidal-shaped mound
measured 6.60 m and 5.80 m (perpendicular diameters), and was 0.86 m high. Three fungus chambers were sampled in Bt horizon, 20 to 70 cm deep from the central base of the mound (Fig. 2). In the same horizon, but 200 cm deep, a large, heartshaped refuse chamber was found, positioned laterally to the mound perimeter. Undisturbed samples of the mound and its crossing tunnels were taken from the top to the base. The basal and upper walls of both fungus and refuse chambers were sampled, as well as walls of underground tunnels, removing 5 to 8 cm of material from the surface to the adjacent soil. Open and closed turrets were also sampled on the nest mound, taking the surface wall, the wall of opened tunnels, as well as the infilling for those turrets that were closed. The investigated nest of C. fulviceps was found 50 m apart from the A. vollenweideri nest. It was also longitudinally sectioned, and samples were taken from both its peripheral and inner walls. The inquilinous nest of C. fulviceps located on the mound of A. vollenweideri was entirely sampled. The nest showed an epigean and a hipogean portion, the latter included into the ant mound just as a diffuse net of galleries. The nest was 10 cm high over the ant-mound surface, 15 cm in diameter and deepened 15 to 20 cm into the ant mound. A control pit was dug 10 m away from both nests, and A (0–9 cm), E (9–11 cm), B1 (11–25 cm) and B2t (25–200 cm) horizons of the surrounding soil were also sampled. Soil located below the mound of A. vollenweideri was sampled, in order to study the micromorphological modifications of its horizons. The A horizon widened (0–15 cm) and was followed by the E horizon (15– 20 cm), and a homogeneous Bt horizon (20–200 cm, the excavation limit). Fig. 2 shows the location of nests and soil samples.
Fig. 2. Schematic profiles of Atta vollenweideri and Cortaritermes fulviceps nests, and surrounding soil (not in scale). On the left, a C. fulviceps mound and the soil profile below with A, E, B1 and B2t horizons. On the right, an A. vollenweideri mound with an open and a closed turret, and a small inquilinous mound of C. fulviceps. Below the mound, the soil profile with A, E and Bt horizons, fungus chambers and a refuse chamber, and tunnels. Black stars: location of the material sampled.
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2.2. Methodology of soil thin sections Samples were qualitatively analysed using a petrographic microscope. Most micromorphological features were observed under transmitted plain light, whereas the iso- and anisotropism of the materials, and the birefringence fabrics of the fine material, were observed under polarized light. Sections were prepared from the undisturbed samples, after impregnation with stained polyester blue resin (Murphy, 1986). In addition, the hindgut content of 20 termite workers, embedded in glycerin, was also analysed under the same microscope for comparisons with some nest micromorphological features that were supposed to have fecal or stomodeal origin. The nomenclature used in micromorphological descriptions and comparative tables was taken from Bullock et al. (1985) and Fitzpatrick (1984). The frequency of coarse components was estimated by a visual system (Fitzpatrick, 1984). 3. Results and analysis 3.1. Mineralogy and granulometry of soil and nest samples The nest samples of A. vollenweideri, C. fulviceps and their surrounding soil were composed of the same coarse mineral materials: sand grains, mostly very fine (75 μm), abundant fine (125 μm) and silt (b 50 μm). All samples also shared the same “well to moderately” size sorting. Grains were dominantly quartz (fresh and altered) and scattered hematite and feldspar. In all samples, fine material was clay with iron oxide, with the
Fig. 4. Micromorphology of the mound of A. vollenweideri. Top: a superficial sample showing areas with very loose aggregation alternating with areas showing more aggregated material arranged in a spongy structure. Bottom: detail of the area poorly aggregated (SpS: spongy structure; PAM: poorly aggregated material; Q: quartz grain; IO: iron oxide mottle; C: clay cement; H: hematite grains; S: silt). Stars: voids (all voids in blue).
exception of the mounds of C. fulviceps and the A, E, and B1 horizons from the surrounding soil profile, where the clay was mixed in variable proportions with fine, organic matter. There were abundant iron oxide mottles and much altered amorphous, milky white volcanic glass. 3.2. Micromorphological descriptions — A. vollenweideri The following descriptions focus on the most distinct micromorphological features observed in samples taken from the longitudinal section of the nest of the leaf-cutting ant A. vollenweideri, including the soil profile under the mound.
Fig. 3. Micromorphology of mound turrets from the A. vollenweideri nest. Top: a turret wall (LG: loose grains; PF: plant fragment; Ag: aggregate). Bottom: an infilling of a closed turret with spongy pelletal structure (Pe: pellets partially welded). Stars: mammillated voids (all voids in blue).
3.2.1. Mound turrets They showed a very porous microstructure, with numerous, frequently interconnected, irregularly shaped and mammillated voids, about 0.3 to 1.5 mm in axe (spongy structure). Larger voids were frequently infilled with loose silt and sand grains (single grain structure). In the aggregated material, grains were cemented by thin clays (pellicular grain structure) or were partially welded by narrow clay bridges (bridge grain structure). Abundant plant fragments were also included, without any particular orientation (Fig. 3). When the turret opening was found closed, the tunnel infilling looked like an intrincate net of moniliform chains composed of partially welded, round aggregates (pellets), with a diameter ranging from 0.25 to 0.75 mm, separated by large, very distinct, mammillated voids (spongy, pelletal structure) (Fig. 3).
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3.2.3. A horizon (0–15 cm) In the A horizon grains were loosely aggregated by microaggregates of amorphous, fine, organic matter mixed with clay particles (intergrain microaggregated structure). 3.2.4. E horizon (15–20 cm) The E horizon was composed of parallel layers orientated to the ground level, and distinct perpendicular interfingerings running into the Bt horizon. Layers and interfingerings showed grains weakly aggregated with thin, organic coatings and microaggregates (pellicular grain and microaggregated intergrain structures, respectively). Parallel fissures, frequently infilled with loose grains, separated the layered material. 3.2.5. Bt horizon (20–200 cm-excavation limit) The Bt horizon displayed alternating compact and porous types of microstructure. In the compact type, grains were densely cemented with clay, (massive, intergrain cemented structure),
Fig. 5. Micromorphology of the fungus-chamber wall in the A. vollenweideri nest showing a non-coated surface and a microporous structure (C: clay cement; IO: iron oxide mottle, Q: quartz grain). Stars: voids (all voids in blue).
3.2.2. Mound In the upper region, the mound showed a very porous structure similar to that described for the turrets (spongy structure), alternating with areas displaying very poor aggregation (Fig. 4). In those latter areas, grains were weakly cemented by thin clay (pellicular grain structure) and clay bridges (bridge grain structure) or were loosely adhered by clay microaggregates (intergrain microaggregated structure). Many rounded voids and fissures were infilled with loose silt and sand grains. Downwards, the mound microstructure gradually compacted, showing voids of less than or equal to 100 μm (microporous structure). Abundant plant fragments were included in the whole mound, fresh in the superficial level and rather decomposed in the inner part. The mound surface was covered with loose, rounded soil pellets. They showed a variable composition, microstructure and size. Most were composed of silt and sand cemented with clay, whereas a few were cemented with organic matter mixed with scattered clay particles, or they were almost exclusively composed of clay or silt grains. Clay birefringence fabrics were granostriated, reticulate striated or dotted, showing variable bright. Minor pellets were almost opaque. The frequency of their coarse components varied from few to frequent-common classes (5% to 30%). Most pellets showed massive or microporous structures, but some displayed a loose intergrain microaggregated structure. Pellets occurred as single rounded aggregates (0.5 to 4 mm in diameter), or were clustered in compound pellets. Abundant plant fragments, thin stems and grass fragments with sharp contours and 5 to 10 mm in length, extended among them.
Fig. 6. Micromorphology of the mound of Cortaritermes fulviceps. Top: massive pelletal (PS) and intergrain cemented structures (ICS). Middle: soil pellets (P) surrounded by thin organic pelletal coatings (PC). Bottom: inquilinous termite gallery crossing the adjacent ant-mound material (G) showing organic coating (OC) and adjacent pellets (P). All voids in blue.
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Table 1 Nest of the leaf-cutting ant Atta vollenweideri Nest structure
Turrets
Mound
Features Microstructure
Spongy structure with abundant mammillated voids
Spongy, single, bridge and pellicular grain structures in the upper region; microporous and spongy structures in the inner region Frequency (%) of coarse Common to very Common to very mineral material dominant (30 to N70%) dominant (40 to N70%) Coarse organic material Abundant plant fragments Abundant plant fragments Fine material Clay Clay Birefringence fabric Granostriated and reticulate striated Granostriated and reticulate striated Other features When the tunnel opening is closed, the infilling shows Loose pellets above the a spongy, pelletal structure surface
whereas in the porous type, numerous voids of less than or equal to 100 μm occurred in the aggregated material (microporous structure), or were located between grains partially welded by thin clays (pellicular grain structure), or between microaggregates situated in the intergrain space (intergrain microaggregated structure). 3.2.6. Fungus and refuse chambers, and tunnels Chambers and tunnels were found in the Bt horizon, and showed the same micromorphology as the surrounding horizon. Tunnels and chambers, both for fungus and refuse, showed undulated, smooth, and non-coated surfaces (Fig. 5). 3.3. Micromorphological descriptions — C. fulviceps The same micromorphological features presented above were described for the nests of the termite C. fulviceps: one epigean nest, with subterranean galleries situated in the A
Underground fungus and refuse chambers, and tunnels Microporous and massive, intergrain cemented structures alternated with pellicular and intergrain microaggregated structures Common to dominant (50–70%) Absent Clay Granostriated and reticulate striated, very diffuse in the surface of refuse chambers No coated chambers nor tunnels
horizon, and the other nest of the inquilinous colony located on the mound of A. vollenweideri. In the latter case, the adjacent ant mound wall surrounding the base of the termite nest was also described, including some termite galleries. 3.3.1. Epigean nest and subterranean galleries The mound showed a massive microstructure, dominantly composed of much fitted, piled, lens-shaped pellets (massive, pelletal structure). Each pellet was 430 to 700 μm long and 130 to 220 μm wide, and was lined by a thin coating of organic matter and clay, about 20–70 μm thick (Fig. 6). The inner pelletal microstructure displayed variable aggregation, showing grains densely cemented or weakly adhered by microaggregates. Grain cement and intergrain microaggregates were composed of organic matter and clay. In many areas the pelletal structure was not so remarkable, but walls were crossed by undulated, organic bands of similar composition and thickness
Table 2 Nests of the mound-building termite Cortaritermes fulviceps Nest type Features
Epigean nest and subterranean galleries located in the soil
Nest of an inquilinous colony located on the mound of Atta vollenweideri Termite nest
Microstructure
Massive pelletal structure alternated with Massive pelletal structure intergrain cemented structure Frequency (%) of coarse Frequent to common (30–40%) Frequent to common (30–40%) mineral material Coarse Abundant plant fragments Scattered plant fragments organic material Fine material Amorphous organic matter and clay Amorphous organic matter and clay Birefringence fabric Other features
Adjacent ant mound substratum and termite galleries Microporous structure Common to dominant (40–50%) Scattered plant fragments
Slight dotted and granostriated
Slight dotted and granostriated
Dominantly clay. In many areas the clay is mixed with organic matter Dotted and granostriated
Lens shaped, single and compound pellets lined by a thin organic-clayish coatings. Mound galleries lined by simple organic coatings and compound coatings composed of pellets coated by thick organic bands. Subterranean galleries lined by a very thin organic coating
Lens shaped, single and compound pellets lined by a thin organic-clayish coatings. Galleries lined by simple organic coatings and compound coatings composed of pellets coated by thick organic bands
Scattered, sinuous, organic bands, crossing the groundmass showing a diffuse lenticular drawing. Termite galleries lined by simple organic coatings and adjacent pelletal structure
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Table 3 Profile of the surrounding soil Horizon
A horizon
E horizon
B1 horizon⁎
B2t horizon
Pellicular, intergrain microaggregated and single grain structures Very dominant (N70%)
Microporous and massive, intergrain cemented structures alternated with pellicular and intergrain microaggregated structures Common to dominant (40–70%)
Microporous and massive, intergrain cemented structures alternated with pellicular structure Common to dominant (40–70%)
Absent
Absent
Absent
Features Microstructure
Single grain, intergrain microaggregated and cemented structures Frequency (%) of coarse Very dominant (N70%) mineral material Coarse organic material Abundant plant remains Fine material Amorphous, organic matter Birefringence Undifferentiated fabric Other features Absent
Amorphous, organic Amorphous, organic matter mixed with clay matter mixed with clay Slight dotted Dotted
Clay
Planar aggregates separated by broad horizontal fissures
Mottles of iron oxides
Absent
Granostriated and reticulate striated
⁎Absent below the mound of Atta vollenweideri.
to pelletal linings. Other areas showed a dense microstructure with grains embedded in dark, fine organic matter (intergrain cemented structure) (Fig. 6). Mound galleries were lined with a distinct organic coating, 50 to 100 μm in thickness, or by a compound coating, 300 to 400 μm thick, composed of superposed, flattened pellets enclosed by alternated, bow-shaped organic bands. Abundant plant fragments occurred randomly distributed. Subterranean galleries were lined by a very thin organic coating, about 50 μm thick. 3.3.2. Nest of the inquilinous termite colony located on the mound of A. vollenweideri Externally, the small inquilinous termite nest looked similar to a closed turret from the ant mound, but it was harder and more consistent. In thin section, it showed an external wall composed of the same materials and micromorphology as the upper region of the ant mound. It possessed an internal, dark brown portion, mostly included inside the mound, composed of a net of galleries similar to that of common epigean nests, from which numerous dark and sinuous galleries extended downwards and laterally into the ant mound. The inquilinous termite nest evinced an internal micromorphology (above and inside the ant-mound surface) similar to that of the large epigean nest located in the soil, except for the rare presence of very small plant fragments. The adjacent ant-mound wall presented numerous voids of less than or equal to 100 μm (microporous structure). The wall material was composed of grains adhered by microaggregates of organic matter and clay, or cemented by thin clays. Scattered, sinuous, organic bands, 20 μm thick, crossed the ant-mound walls, sometimes showing a diffuse lenticular drawing. Termite galleries running across the ant-mound were lined by a dark brown, organic coating, 75 to 200 μm thick and adjacent, superimposed, lensshaped pellets surrounded by thin, organic coatings (Fig. 6).
coarse mineral material, presence of coarse organic materials, qualitative analysis of fine materials and their birefringence fabrics, and other features. The micromorphology of nests of C. fulviceps, both the epigean one with its subterranean galleries, and the inquilinous nest located on the leaf-cutting ant mound, is comparatively summarized in Table 2, as for the nest of A. vollenweideri. This comparison extends to the adjacent substratum of the termite nest included into the ant mound. The same micromorphological features of the surrounding soil are presented comparatively in Table 3. 3.5. Hindgut content of workers of C. fulviceps The hindgut content of termite workers was mostly composed of amorphous, fine, organic matter mixed with clay, including scattered silt particles and few sand grains showing a maximum size of 100 μm (very fine-sized). 4. Discussion and conclusions In spite of being located in a frequently-flooded soil, the nests of neighbor leaf-cutting ants, A. vollenweideri, and mound-building termites, C. fulviceps, showed notably different macro- and micromorphologies. Ants and termites construct their nest mounds with the same soil coarse components: sand grains, mostly very fine sized, and silt, preserving the same soil particle size. They do not select any kind of coarse particles from the soil at the point of soil excavation, but their constructions show many particular micromorphological features such as different types of microstructure and frequency of coarse components, presence of pellets, organic coatings and banded intercalations.
3.4. Comparative soil and nest micromorphology
4.1. Nest micromorphology and building behavior in Atta leafcutting ants
The micromorphology of each part of the A. vollenweideri nest is comparatively presented in Table 1, which summarizes different features related to nest microstructure, frequency of
In A. vollenweideri, the underground structures resulting from the excavation, i.e., chambers (both for fungus and refuse) and tunnels, however, showed the same micromorphology as
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that observed in the surrounding Bt horizon, lacking any distinct, particular feature, which suggests that those cavities are simple and non plastered soil excavations. Ant workers carry the excavated material between their mandibles and pile it around the first nest entrance. Individual loads are small, single or welded soil balls in clusters of 0.5 to 4 mm. They are named pellets herein because of their similarity with the micromorphological term employed for termites and defined by Sleeman and Brewer (1972) as “common micromorphological features of termite constructions recognized as spheroidal or ovoid bodies composed of organic and mineral soil materials or various combinations of both”. Whereas pellets in the termite nests are commonly in the size range of 0.3 to 1 mm and are welded or cemented with fine materials, forming the structural wall units or “bricks” (Stoops, 1964; Mermut et al., 1984; Eschenbrenner, 1986; Sleeman and Brewer, 1972), in the ant nest they are generally bigger soil balls loosely dispersed over the mound, and partly welded in the infillings of the closed turrets. The pelletal composition, microstructure, frequency of coarse components, and clay birefringence fabrics are very variable because those features depend on the horizon from which the pellets were removed. Most pellets were composed of silt and very fine sand grains cemented with clay, the same coarse and fine components of the Bt horizon, suggesting that they have been removed during the excavation of fungus and refuse chambers. This view is supported by the fact that most pellets on the uppermost layer of the mound showed the same types of microstructure and birefringence fabrics observed in the Bt horizon. However, in spite of being micromorphologically similar to that horizon, pellets showed a notably lower value in the frequency of coarse components. The maximum frequency of coarse components shown in the pellets was 30%, whereas in the Bt horizon, the minimum frequency averaged 50%. This difference could result from a posterior incorporation of clay to the removed soil, or from the way pellets are formed. There are, regrettably, no descriptions about digging behavior of ants excavating natural soil, with its original microstructure and fine and coarse components, so that we can only speculate about this discrepancy. In laboratory studies, Sudd (1969) described the excavation and removal of soil by single ants under controlled conditions, and recognized three steps: 1) the mandible grab during removal of sand from the work-surface, 2) the movements of the forelegs for the collection of the load, and 3) the transport of the load between the mandibles towards the end of the tunnel, which could be a single, large sand grain or a crumb of small sand grains. Observations on laboratory colonies of the leaf-cutting ant A. vollenweideri indicate that single workers dig in soil by pulling out small pieces with their mandibles. These pieces are usually not carried to the outside by the same workers, but placed and piled close to the digging site, where other workers may also be involved in digging. A different set of workers is often involved in the transport of the pieces to another place, where items from different digging sites accumulate, or to the exterior. This kind of “transport chains” during removal of digging material resembles that observed in the context of foraging in this species (Röschard and Roces, 2003).
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The final formation of the pellets, for which workers use their forelegs to collect the load together before transporting it between the mandibles, may therefore involve the mixing of soil particles from different sites. This could be one of the reasons for the observed dissimilarity in composition between pellets and soil from the Bt horizon. The large ant mound mainly results from the deposition of the excavated material, and it shows a combination of many porous types of microstructures in its upper region, whereas denser types of microstructures gradually predominate at depth. Both the upper mound material and the percolated rain probably contribute to weld the pelletal material concentrated on the ground surface. In the mound, the frequency of coarse components was higher than in the Bt horizon (its principal source), probably because of the lixiviation of the clay mound. Those few clay particles that had not been lost in the lixiviation process are retained in the intergranular space welding the coarse grains as thin, surrounding grain coatings and bridges. As the mound growths, the lixivial clay gradually concentrates at the base of the mound and in the wide A horizon located under the mound. The final structure of the mound does not only result from a passive amalgamation of pelletal materials, but also from the import and inclusion of abundant thin twigs and grass fragments. Plant fragments show sharp contours and roughly similar size, suggesting that they represent plant or grass fragments cut by the ants, carried and then deposited on the mound surface. In fact, leaf-cutting ant workers were observed to collect plant fragments as building material, especially after rains, for the construction of turrets or the closing of nest openings (Kleineidam and Roces, 2000). As the mound enlarges and compacts, these plant fragments are also amalgamated with the pelletal material, probably helping to reinforce the porous mound structure. The ventilation turrets showed the same porous microstructure observed for the mound, but the infilling of closed turrets evinced a remarkable pelletal structure. Those infillings were composed of easily recognized masses of pellets partially welded and separated by large mammillated voids, suggesting that this type of porous structure could be the consequence of a rapid occlusion employing wet and plastic, recently-excavated soil pellets. The size of the pellets used for turret occlusion ranged from 0.25 to 0.75 mm in diameter, whereas those deposited by the ants on the mound ranged from 0.5 to 4 mm. Since a correlation between worker body size and particle size would be expected, as reported for other ants (Sudd, 1968), this phenomenon suggests that turret occlusion may be carried out by small workers. The closing of nest openings is a rapid, collective colony response to heavy rains (Kleineidam and Roces, 2000), which takes place in quite a few minutes to one or two hours, and this response is also observed in winter (dry season), when colonies close up to 80% of the existing openings (Jonkman, 1980c), probably to avoid the inflow of cold air. Contrary to the assumption of Jonkman (1980c), who argued that chamber walls in A. vollenweideri might be lined with cement to avoid ground-water penetration, tunnel walls and nest chambers were not coated, neither with fecal nor with other fine
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materials. The underground tunnels and chambers of the leafcutting ant nest can therefore be regarded as simple excavations, since no impermeable coating lines their surface. Several authors have focused on the question whether the walls of tunnel and chambers of ant nests are coated. Green et al. (1999) and Cosarinsky (2006) observed that mound galleries of Solenopsis fire ants were not coated. Bruch (1916) described a distinct, firm coating of the nest chamber walls of the Neotropical ant Forelius chalybaeus, but only mentioned a fine composition without giving more details. Wang et al. (1995) observed in the nest walls of L. neoniger a compact microstructure because of the presence of dark infillings of an unidentified colloidal material among sand grains. Cosarinsky (2006) described a distinct soil coating plastering the galleries of C. punctulatus, composed of silt particles embedded in a compact mass of clay with iron oxides and fine organic matter. Both, Gorosito et al. (2006) and Cosarinsky (2006) suggested that the compact structure observed in the walls of galleries and nest chambers was necessary to stabilize the walls and to support the high mass of the Camponotus mound. Lining of nest galleries with clay or “glaze” was also reported for Trachymyrmex turrifex and Camponotus intrepidus, respectively, although its function remains elusive (Wheeler, 1907; Cowan et al., 1985). The employment of fecal matter in ant constructions or excavations has not been reported in the literature. The question arises, why nest do not inundate during floods, even when the soil is totally submerged. Mounds are inhabited islands in the flooded ground and colonies and fungus keep safe in underground chambers during the rainy season. Considering the porous types of microstructure observed in the surrounding Bt horizon, two hypotheses could be advanced. First, it is conceivable that the horizon microstructure only allows the percolation of small amounts of infiltrating water. Second, thousands of voids measuring less than 100 μm are expected to generate large capillary forces that may retain the water out of the chambers during the floods. But these hypotheses need to be evaluated with experiments employing undisturbed, field soil samples. 4.2. Nest micromorphology and building behavior in Cortaritermes termites In contrast to leaf-cutting ants, mounds of C. fulviceps are inhabited, very compact above-ground constructions that protect their residents from infiltrating rainwater. Their walls showed a massive, pelletal microstructure composed of piled, much fitted, lens-shaped, soil pellets covered by undulated layers of fine, organic matter and clay particles. Galleries and chambers were plastered with a distinct, dark brown coating, also composed of fine, organic matter with scattered silt and clays. Very frequently, gallery coatings were compound features composed of superimposed, small soil pellets surrounded by thick organic bands. In some areas, the lens-shaped pellets were not so distinguishable, and undulated organic bands intercalated among elongate parcels of soil. In many areas, soil grains were entirely embedded by fine organic matter. All these organic features were composed of the same components found in the worker's hindgut content: fine organic matter mixed with clay
and scattered silt particles, suggesting a common fecal origin. It is likely that the addition of fecal matter to the construction, leading to a very compact mound microstructure, would protect the nest from both rain splash and infiltrating water. Lee and Wood (1971) and Sleeman and Brewer (1972) named as “lenticular structure” a similar pelletal type of microstructure observed in thin sections of nest of many Australian mound-building termites. They also found some variations in samples where the lenticular structure was not so clear, and described them as undulate organic bands surrounding elongated soil aggregates. Other samples showed patches of organic matter randomly distributed among soil minerals. They assigned a fecal origin for those organic coatings, bands and patches considering the studies by Emerson (1938) on termite building behavior. He observed workers placing their single soil loads, moistened with saliva, and then excreting a drop of fecal matter over the recently placed parcel of the soil. Similar fecal micromorphological features were also observed in thin sections of mounds of Neotropical termites. In Cornitermes cumulans, Cosarinsky (2003) observed organic gallery coatings and undulate bands crossing the walls of mounds located in sandy soils. The mound of Termes saltans and C. fulviceps located in sandy soils with abundant humus were composed of irregular shaped soil pellets and coarse sand grains entirely surrounded by thick layers of organic matter (Cosarinsky, 2004a,b). The fecal addition to soil material is not the only termite behavior that leads to cohesion and therefore stabilization of the construction. Many mound-building termites moisten with saliva the soil particles carried in the buccal cavity (Noirot and Darlington, 2002). The moistening with saliva could explain in C. fulviceps why the birefringence fabric is granostriated in the mound, while it is undifferentiated in the A horizon, where this species is supposed to feed and collect the building material. In the A horizon, humus masks the clay birefringence, but when the soil particles are removed and mixed with saliva, the clay particles probably decant from the suspension of saliva as very thin streaks or domains arranged around the sand grains, displaying a granostriated birefringence fabric (Aylmore and Quirk, 1960; van Olphen, 1977). The addition of clay and organic matter to the mound is also reflected by a notable decrease in the frequency of coarse components when compared with the A horizon: in the mound the frequency is 30–40% whereas it is N 70% in the A horizon. The inquilinous colony of C. fulviceps located on the mound of A. vollenweideri constructed a small nest employing available materials (from the ant mound), but adding a lot of fecal matter. Its massive, pelletal microstructure was very similar to that found in the mature mound located on the soil surface. The largest difference was that sections of this small nest did not show so many and large plant fragments as they occur in non-inquilinous nests constructed around tussock grasses. Only small plant fragments were observed irregularly distributed within the nest walls, in size of the fragments collected by ants and deposited on their mound. The adjacent ant-mound material surrounding the base of the termite nest was reinforced by many distinct micromorphological
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fecal features, being more concentrated near the subterranean net of galleries, such as undulated, dark, banded intercalations, gallery coatings, and pelletal linings. The wall displayed more aggregation than in the rest of the upper portion of the mound, showing microporous structure similar to that observed in the basal region of the ant mound. The frequency of coarse components decreased to 40–50% in the adjacent ant mound material from more than 70% in the upper portion of the ant mound, probably as a consequence of the addition of fecal matter and a higher concentration of clay that could not lixiviate, because it was retained by the termite nest. 4.3. Comparative nest micromorphology To conclude, the comparative study of nest micromorphology of these neighboring soil-nesting social insects provided information about many processes involved in the formation of their nests. In A. vollenweideri leaf-cutting ants, such processes are: (1) the excavation of chambers and tunnels by digging the soil profile, (2) the concentration of the excavated material on the ground around the tunnel openings as similarly-shaped pellets with a probable addition of clay, (3) the resulting formation of a large, porous mound with weathered and welded pelletal materials and added plant fragments cut and carried by the workers, (4) the building of ventilation turrets in the mound surface by piling and welding moist pellets, and (5) the clay lixiviation taking place from the upper region of the mound, leading to its accumulation in the basal portion and in the wide A horizon below the mound. In C. fulviceps termites, two distinct main processes are involved: (1) the construction of a solid, epigean mound employing abundant fecal materials to cement sand grains or soil pellets molded and moistened with saliva in the worker’s buccal cavity, and (2) the plastering of mound and underground galleries. The same processes are shown for the inquilinous termites nesting on the ant mound, even though the available materials for building, compared with colonies nesting directly on the soil, completely differed. The inquilinous colony also employed abundant fecal matter to reinforce the loose substratum, only composed of sand and clay but lacking any organic matter except by those plant fragments imported by the ants and included in the mound. Plasticity in termite building behavior is therefore emphasized by two facts: first, inquilinous and freely-nesting colonies, although dealing with very different building materials, construct nests with similar micromorphology; second, depending on the available material in the soil, C. fulviceps workers may either mould pellets in their buccal cavities and use no cement for building, or may cement the pellets with fecal material (Cosarinsky, 2004b). Even though the nest micromorphology represents a kind of “frozen” behavioral record of the digging and building efforts of the nest inhabitants, it is, however, not enough to understand all the processes involved in soil-nesting behavior. Micromorphological studies should be extended with edaphological quantitative analyses (such as soil water content; clay and organic matter contents) and behavioral observations both in the field and laboratory.
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Acknowledgements We thank two anonymous reviewers for helpful comments that improved the manuscript. Field work was performed at the wonderful Reserva Ecológica El Bagual (Alparamis SA — Aves Argentinas) in eastern Chaco, Province of Formosa, Argentina. We are very much indebted to the ornithologist Alejandro G. Di Giacomo, his field assistants, and especially Götz family for providing facilities at the Biological Station, daily help during our stays and invaluable logistical support throughout the past ten years of ant (and recently termite) research. Martin Bollazzi helped during material sampling. Thanks to Ulrich Mueller for indicating the reference of Wheeler's paper. Many thanks also to Dr. Luiz Fontes for the taxonomic identification of the termites, and to Dra. Daniela Villegas for her help with soil taxonomy. Financial support was provided by the DFG, Germany (SFB 554). References Aylmore, L.A.G., Quirk, J.P., 1960. Domain or turbostratic structures of clays. Nature 187, 1046–1048. Bonetto, A.A., Manzi, R., Pignalberi, C., 1960. Los tacurúes de Camponotus punctulatus (Mayr) Notas ecológicas. Physis 12, 217–224. Brauman, A., Bignell, D.E., Tayasu, I., 2002. Soil-feeding termites: biology, microbial associations and digestive mechanisms. In: Abe, T., Bignell, D.A., Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, pp. 233–259. Bruch, C., 1916. Contribución al estudio de las hormigas de la provincia de San Luis. Rev. Mus. La Plata 23, 291–357. Bucher, E.H., 1982. Chaco and caatinga — South American savannas, woodlands and thickets. In: Huntley, B., Walkers, B. (Eds.), Ecology of Tropical Savannas. Springer Verlag, Berlin, pp. 48–79. Bucher, E.H., Zuccardi, R.B., 1967. Significación de los hormigueros de Atta vollenweideri Forel como alternadores del suelo de la provincia de Tucumán. Acta Zool. Lilloana 23, 83–95. Bullock, P., Fedoroff, N., Jongerius, A., Stoops, G., Tursina, T., 1985. Handbook for Soil Thin Section Description. Waine Research Publications, England. Cosarinsky, M.I., 2003. Micromorphology of the nest of Cornitermes cumulans (Kollar) (Isoptera: Termitidae). In: Buatois, L.A., Mangano, M.G. (Eds.), Icnología: Hacia una convergencia entre geología y biología. Publicación especial no. 9 de la Asociación Paleontológica Argentina, Buenos Aires, pp. 53–64. Cosarinsky, M.I., 2004a. Nest micromorphology of the neotropical termite Termes saltans (Isoptera: Termitidae). Sociobiology 43, 501–511. Cosarinsky, M.I., 2004b. Nest micromorphology of the termite Cortaritermes fulviceps in different types of soil (Isoptera; Termitidae). Sociobiology 44, 153–170. Cosarinsky, M.I., 2005. Comparative micromorphology of arboreal and terrestrial carton nests of the neotropical termite Nasutitermes aquilinus (Isoptera:Termitidae). Sociobiology 45, 839–852. Cosarinsky, M.I., 2006. Nest micromorphology of the neotropical mound building ants Camponotus punctulatus and Solenopsis sp. Sociobiology 47, 329–344. Cosarinsky, M.I., Bellosi, E.S., Genise, J.F., 2005. Micromorphology of modern epigean termite nests and possible termite ichnofossils: a comparative analysis. Sociobiology 45, 745–778. Cowan, J.A., Humphreys, G.S., Mitchell, P.B., Murphy, C.L., 1985. An assessment of pedoturbation by two species of mound-building ants, Camponotus intrepidus (Kirby) and Iridomyrmex purpureus (F. Smith). Aust. J. Soil Res. 22, 95–107. Emerson, A.E., 1938. Termite nests: a study of the phylogeny of behavior. Ecol. Monogr. 8, 247–284.
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Eschenbrenner, V., 1986. Contribution des termites à la micro-agrégation des sols tropicaux. Cahier ORSTOM, Série Pedologie, vol. 22, pp. 397–408. Fitzpatrick, E.A., 1984. Micromorphology of Soils. Chapman & Hall, London. Fontes, L.R., 1998. Novos aditamentos ao “Catalogo dos Isoptera do novo Mundo”, e uma filogenia para os gêneros neotropicais de Nasutitermitinae. In: Fontes, L.R., Berti Filho, E. (Eds.), Cupins. O desafio do conhecimento. FEALQ, Piracicaba, SP, Brasil, pp. 309–412. Forel, A., 1893. Note sur les Attini. Ann. Soc. Entomol. Belge. 37, 586–607. Gorosito, N.B., Curmi, P., Hallaire, V., Folgarait, P.J., Lavelle, P.M., 2006. Morphological changes in Camponotus punctulatus (Mayr) anthills of different ages. Geoderma 132, 249–260. Green, W.P., Pettry, D.E., Switzer, R.E., 1999. Structure and hydrology of mounds of the imported fire ants in the southeastern of United States. Geoderma 93, 1–17. Jonkman, J.C.M., 1978. Nests of the leaf-cutting ant Atta vollenweideri as accelerators of succession in pastures. Z. Angew. Entomol. 86, 25–34. Jonkman, J.C.M., 1980a. Average vegetative requirement, colony size and estimated impact of Atta vollenweideri on cattle raising in Paraguay. Z. Angew. Entomol. 89, 135–143. Jonkman, J.C.M., 1980b. The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym, Formicidae) part I. Z. Angew. Entomol. 89, 158–173. Jonkman, J.C.M., 1980c. The external and internal structure and growth of nests of the leaf-cutting ant Atta vollenweideri Forel, 1893 (Hym, Formicidae) part II. Z. Angew. Entomol. 89, 217–246. Jungerius, P.D., van der Ancker, J.A.M., Muncher, H.J., 1999. The contribution of termites to the microgranular structure of soils on the Uasin Gishu Plateau, Kenya. Catena 34, 349–363. Kleineidam, C., Roces, F., 2000. Carbon dioxide concentrations and nest ventilation in nests of the leaf-cutting ant Atta vollenweideri. Insec. Soc. 47, 241–248. Kleineidam, C., Ernst, R., Roces, F., 2001. Wind-induced ventilation of the giant nests of the leaf-cutting ant Atta vollenweideri. Naturwiss 88, 301–305. Lee, K.E., Wood, T.G., 1971. Termites and Soils. Academic Press, London, New York.
McCook, H.C., 1877. Mound-making ants of the Alleghenies, their architecture and habits. Trans. Am. Entomol. Soc. 6, 253–296. Mermut, A.R., Arshad, M.A., St-Arnaud, R.J., 1984. Micropedological study of termite mounds of three species of Macrotermes in Kenya. Soil Sci. Soc. Am. J. 48, 613–620. Murphy, C.P., 1986. Thin Section Preparation of Soils and Sediments. A.B. Academic Publishers, London. Noirot, Ch., Darlington, J.P.E.C., 2002. Termite nests: architecture, regulation and defence. In: Abe, T., Bignell, D.A., Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht. Röschard, J., Roces, F., 2003. Cutters, carriers and transport chains: distancedependent foraging strategies in the leaf-cutting ant Atta vollenweideri. Insec. Soc. 50, 237–244. Silvestri, F., 1901. Nota preliminare sui Termitidi sud-americani. Boll. Mus. Zool. Anat. Comp. R. Univ. Torino 16, 1–8. Sleemann, J.R., Brewer, R., 1972. Microstructures of some Australian termite nests. Pedobiologia 12, 347–373. Stoops, G., 1964. Application of some pedological methods to the analysis of termite mounds. In: Bouillon, A. (Ed.), Études sur les termites africains. Université Lovanium, Léopoldville, pp. 379–398. Sudd, J.H., 1968. Selective removal of larger soil particles by ants. Niger. Entomol. Mag. 1, 122–124. Sudd, J.H., 1969. The excavation of soil by ants. Z. Tierpsychol. 26, 257–276. Talice, R.V., Mosera, S.L., Caprio, R., Sprechmann, A.M.S., 1969. I. Estructura de los termiteros de Nasutitermes fulviceps (Silvestri, 1901). Pub. Dpto. Biol. Gen. Exp. Univ. Montevideo, Uruguay, vol. 2, pp. 1–20. van Olphen, H., 1977. An Introduction to Clay Colloid Chemistry. John Wiley and Sons, New York. Wang, D., McSweeney, K., Lowery, B., Norman, J.M., 1995. Nest structure of ant Lasius neoniger Emery and its implications to soil modification. Geoderma 66, 259–272. Wheeler, W.M., 1907. The fungus-growing ants of North America. Bull. Am. Mus. Nat. Hist. 23, 669–807.
Neighbor leaf-cutting ants and mound-building termites: Comparative nest micromorphology Marcela I. Cosarinsky a,⁎, Flavio Roces b,1 a
Laboratorio de Icnología, Museo Argentino de Ciencias Naturales “B. Rivadavia”, Angel Gallardo 470, (1405) Buenos Aires, Argentina Behavioral Physiology and Sociobiology (Zoology II), Biocenter, University of Würzburg, Am Hubland, D-97074 Würzburg, Germany
b
Received 2 January 2006; received in revised form 1 June 2007; accepted 1 June 2007 Available online 12 July 2007
Abstract The nest micromorphology of the leaf-cutting ant Atta vollenweideri and the mound-building termite Cortaritermes fulviceps, both species occurring in frequently flooded plains of the NE of Argentina, was comparatively studied. In spite of being located in the same type of soil, the nests showed different micromorphology, related to different nesting behaviors adapted to seasonal rains. Termites construct exclusively epigean mounds combining soil and fecal material arranged in a very massive microstructure. Soil particles excavated from the A horizon are frequently packed as lens-shaped pellets probably moulded in the termites' buccal cavity, and then regurgitated and coated with fecal matter. Many distinct fecal micro-features occur, such as bands crossing the walls or surrounding pellets, and gallery coatings. Conversely, the ants inhabit underground chambers excavated in the Bt horizon, which displays a very porous microstructure, showing voids equal to or smaller than 100 μm. This could be one of the reasons why water may be retained by capillary forces within the soil, being unable to inflow into the chambers during flooding. No micromorphological features composed of fecal matter were observed at any part of the ant nest, and contrary to previous claims, no coating in galleries or chamber walls was observed. During digging, workers remove the soil material and transport it through subterranean tunnels to the soil surface. Individual loads are recognized as rounded pellets that conserve the micromorphology of the excavated horizon, and are dropped on the surface of a large mound. The ant mound represents the epigean part of the nest, and displays a combination of very porous types of microstructure, composed of sand grains weakly cemented with clay, originated in weathered and amalgamated pelletal material with abundant plant fragments. The external nest architecture does not only result from a passive deposition of the excavated material, since ants employ soil pellets and plant fragments to construct conspicuous turrets, a number of which are closed and re-opened with seasonal periodicity. Turrets may protect the nest openings from water inflow and also enhance wind-driven nest ventilation. © 2007 Elsevier B.V. All rights reserved. Keywords: Neotropical; Chaco; Soil-nesting insects; Ants; Termites; Atta vollenweideri; Cortaritermes fulviceps; Soil micromorphology
1. Introduction Humid grasslands in the Gran Chaco region are inhabited by several soil-nesting species of ants and termites. Because of the seasonal rains and frequent floods, nests are expected to have particular adaptations to cope with the high water levels, in order to avoid water inflow into the structure. Ants of the species Camponotus punctulatus, for instance, construct ⁎ Corresponding author. Tel.: +54 11 45528490. E-mail addresses: [email protected] (M.I. Cosarinsky), [email protected] (F. Roces). 1 Tel.: +49 931 8884311; fax: +49 931 8884309. 0016-7061/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.geoderma.2007.06.006
compact and large mounds, and the entire colony was reported to move to the higher parts of the mounds during flooding (Bonetto et al., 1960). Fungus-growing ants of the tribe Attini are the dominant herbivores in the Chaco region, particularly the leaf-cutting ant Atta vollenweideri (Hymenoptera: Formicidae), which is not only important as food consumer, mainly grasses, but also as soil modifier (Bucher and Zuccardi, 1967; Jonkman, 1978, 1980a; Röschard and Roces, 2003). In the Chaco region, the influence of Atta ants on soil includes alteration of soil horizons through digging (nesting) behavior and soil removal, as well as the redistribution of nutrients contained in their underground chambers (Bucher, 1982). A mature nest of this species is easily recognized by its
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large and conspicuous conical- or ellipsoid-shaped mound, uncovered of vegetation, commonly 6 to 8 m in basal diameter and about 0.80 m high (Fig. 1). During the rainy season, mounds often look like round islands surrounded by water. A mature nest of A. vollenweideri may contain up to 2000 underground chambers for rearing a symbiotic fungus on the grass fragments harvested by the foragers, and a small number of very large refuse chambers (Jonkman, 1980c). Chambers, mostly located in the Bt horizon, are interconnected by a complex network of underground tunnels, a number of which connect to the surface. A mature nest may contain up to 200 nest openings (Jonkman, 1980c). Most of them are particularly large, with diameters up to 10 cm. The peripheral nest openings are used as entrances and connect with up to 100 m-long foraging trails, whereas the central nest openings often possess a turret or chimney (Jonkman, 1980b,c). The shape of the mound promotes the ventilation of the underground chambers via a passive mechanism driven by wind (Kleineidam and Roces, 2000; Kleineidam et al., 2001). The mound itself is not inhabited, and it results from the deposition of excavated soil during colony growth that originates from deep horizons. The mound, however, is not only a passive accumulation of excavated soil, since workers import material to reinforce and stabilize the construction, as observed for other ant species (McCook, 1877; Cowan et al., 1985), and also build structures with defined function like ventilation turrets (Jonkman, 1980b).
Fig. 1. Top: mound of the leaf-cutting ant, Atta vollenweideri. Bottom: mound of the termite Cortaritermes fulviceps. Note different scale bars.
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Mound-building termites are also very common and their nests can be found in the close vicinity of large leaf-cutting ant nests. The species Cortaritermes fulviceps (Isoptera: Termitidae) constructs epigean, very hard, dome-shaped nests (Fig. 1). Mounds are about 20 to 50 cm large in basal diameter, and 30 to 70 cm high, and include tussock grasses or little shrubs that frequently jut out from their surface (Talice et al., 1969; Cosarinsky, 2004b). The mound is composed of an intricate inner net of convolute galleries, 1.5 to 5 mm in diameter, which are connected with a diffuse net of subterranean galleries. The mound is entirely inhabited by the colony. In the rainy season, mounds are isolated refuges surrounded by water, and the colony moves to the upper region of the mound (personal observations). Even though the feeding habits of Neotropical termites are not completely understood, soil-feeding termites are recognized in the field by the dark grey color on their abdomens, and because they construct hard, dark mounds, rich in organic matter. These features are common in many Nasutitermitinae, including C. fulviceps. Soil-feeding termites characteristically feed in galleries located in the upper 10 cm of the A horizon, so it is supposed that the same horizon is the source of their building materials (Brauman et al., 2002). Field observations of sympatrically occurring nests of leafcutting ants, A. vollenweideri, and of mound-building termites, C. fulviceps, suggested that they were composed of different materials, even though they were located in the same type of soil. Since both species are seasonally affected by flooding, their nesting behavior and nest morphology may reflect an adaptation to protect the inhabitants against incoming water. The aims of the present study were: 1) to characterize comparatively the micromorphological features of nests constructed by two neighboring social insect species phylogenetically distant, but facing similar ecological conditions; 2) to investigate the selection of building materials and their spatial arrangement in relation to that of the surrounding soil; 3) to explore plasticity in termites' building behavior by comparing the micromorphology of nest constructed with different materials. For that, an inquilinous colony of C. fulviceps nesting on an Atta leaf-cutting ant mound, i.e., the colony used material from the ant mound for building, was comparatively investigated. In social insects, the micromorphology of soil nests was first studied for African and Australian termites (Stoops, 1964; Lee and Wood, 1971; Sleeman and Brewer, 1972; Mermut et al., 1984; Eschenbrenner, 1986; Jungerius et al., 1999). Recently, Cosarinsky (2003, 2004a,b, 2005) and Cosarinsky et al. (2005) studied the nest micromorphology of several Neotropical termite species including the micromorphology of nests of C. fulviceps located in different soil types in Argentina (Cosarinsky, 2004b). Regarding ants, Wheeler (1907) reported that workers of the fungus-growing ant Trachymyrmex turrifex line the underground tunnels and nest chambers with a thin layer of clay. But to our knowledge, the only studies reporting detailed micromorphological nest features in ants are those focusing on Lasius neoniger, one of the most abundant species
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of temperate regions of North America that inhabits subterranean galleries (Wang et al., 1995), and on mound-building fire ants in the Southeastern of the United States, Solenopsis invicta and S. richteri (Green et al., 1999). Recently, Cosarinsky (2006) studied the mound-building Neotropical ants, C. punctulatus and Solenopsis sp. nesting in flooded fields in Argentina, comparing their nest micromorphology with that of the surrounding soil. The present study, therefore, contributes to our knowledge about nesting behavior of ants and provides comparative information on the use of materials for nest building by neighboring social insect species, termites and ants, nesting on similar soils. 2. Area descriptions, methods and material studied 2.1. Nest characteristics and material sampling Nest micromorphology in the leaf-cutting ant A. vollenweideri Forel, 1893 and the mound-building termite C. fulviceps (Silvestri, 1901) Fontes, 1998, was studied using thin sections. Nests and surrounding soil were sampled at the “Reserva Ecológica El Bagual” (26° 10’ S, 58° 56’ W), located in the eastern (humid) Chaco region, Province of Formosa, Argentina. Based on morphological data, their surrounding soil profile was determined as a Typic Haplustalf (Alfisol). In the field, we investigated one mature leaf-cutting ant nest, one mature termite nest, and one inquilinous termite nest located directly on the ant mound. The nest of A. vollenweideri was excavated and sectioned from the top of the mound downwards to 2.50 m deep in the Bt horizon, where fungus and refuse chambers were found. The ellipsoidal-shaped mound
measured 6.60 m and 5.80 m (perpendicular diameters), and was 0.86 m high. Three fungus chambers were sampled in Bt horizon, 20 to 70 cm deep from the central base of the mound (Fig. 2). In the same horizon, but 200 cm deep, a large, heartshaped refuse chamber was found, positioned laterally to the mound perimeter. Undisturbed samples of the mound and its crossing tunnels were taken from the top to the base. The basal and upper walls of both fungus and refuse chambers were sampled, as well as walls of underground tunnels, removing 5 to 8 cm of material from the surface to the adjacent soil. Open and closed turrets were also sampled on the nest mound, taking the surface wall, the wall of opened tunnels, as well as the infilling for those turrets that were closed. The investigated nest of C. fulviceps was found 50 m apart from the A. vollenweideri nest. It was also longitudinally sectioned, and samples were taken from both its peripheral and inner walls. The inquilinous nest of C. fulviceps located on the mound of A. vollenweideri was entirely sampled. The nest showed an epigean and a hipogean portion, the latter included into the ant mound just as a diffuse net of galleries. The nest was 10 cm high over the ant-mound surface, 15 cm in diameter and deepened 15 to 20 cm into the ant mound. A control pit was dug 10 m away from both nests, and A (0–9 cm), E (9–11 cm), B1 (11–25 cm) and B2t (25–200 cm) horizons of the surrounding soil were also sampled. Soil located below the mound of A. vollenweideri was sampled, in order to study the micromorphological modifications of its horizons. The A horizon widened (0–15 cm) and was followed by the E horizon (15– 20 cm), and a homogeneous Bt horizon (20–200 cm, the excavation limit). Fig. 2 shows the location of nests and soil samples.
Fig. 2. Schematic profiles of Atta vollenweideri and Cortaritermes fulviceps nests, and surrounding soil (not in scale). On the left, a C. fulviceps mound and the soil profile below with A, E, B1 and B2t horizons. On the right, an A. vollenweideri mound with an open and a closed turret, and a small inquilinous mound of C. fulviceps. Below the mound, the soil profile with A, E and Bt horizons, fungus chambers and a refuse chamber, and tunnels. Black stars: location of the material sampled.
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2.2. Methodology of soil thin sections Samples were qualitatively analysed using a petrographic microscope. Most micromorphological features were observed under transmitted plain light, whereas the iso- and anisotropism of the materials, and the birefringence fabrics of the fine material, were observed under polarized light. Sections were prepared from the undisturbed samples, after impregnation with stained polyester blue resin (Murphy, 1986). In addition, the hindgut content of 20 termite workers, embedded in glycerin, was also analysed under the same microscope for comparisons with some nest micromorphological features that were supposed to have fecal or stomodeal origin. The nomenclature used in micromorphological descriptions and comparative tables was taken from Bullock et al. (1985) and Fitzpatrick (1984). The frequency of coarse components was estimated by a visual system (Fitzpatrick, 1984). 3. Results and analysis 3.1. Mineralogy and granulometry of soil and nest samples The nest samples of A. vollenweideri, C. fulviceps and their surrounding soil were composed of the same coarse mineral materials: sand grains, mostly very fine (75 μm), abundant fine (125 μm) and silt (b 50 μm). All samples also shared the same “well to moderately” size sorting. Grains were dominantly quartz (fresh and altered) and scattered hematite and feldspar. In all samples, fine material was clay with iron oxide, with the
Fig. 4. Micromorphology of the mound of A. vollenweideri. Top: a superficial sample showing areas with very loose aggregation alternating with areas showing more aggregated material arranged in a spongy structure. Bottom: detail of the area poorly aggregated (SpS: spongy structure; PAM: poorly aggregated material; Q: quartz grain; IO: iron oxide mottle; C: clay cement; H: hematite grains; S: silt). Stars: voids (all voids in blue).
exception of the mounds of C. fulviceps and the A, E, and B1 horizons from the surrounding soil profile, where the clay was mixed in variable proportions with fine, organic matter. There were abundant iron oxide mottles and much altered amorphous, milky white volcanic glass. 3.2. Micromorphological descriptions — A. vollenweideri The following descriptions focus on the most distinct micromorphological features observed in samples taken from the longitudinal section of the nest of the leaf-cutting ant A. vollenweideri, including the soil profile under the mound.
Fig. 3. Micromorphology of mound turrets from the A. vollenweideri nest. Top: a turret wall (LG: loose grains; PF: plant fragment; Ag: aggregate). Bottom: an infilling of a closed turret with spongy pelletal structure (Pe: pellets partially welded). Stars: mammillated voids (all voids in blue).
3.2.1. Mound turrets They showed a very porous microstructure, with numerous, frequently interconnected, irregularly shaped and mammillated voids, about 0.3 to 1.5 mm in axe (spongy structure). Larger voids were frequently infilled with loose silt and sand grains (single grain structure). In the aggregated material, grains were cemented by thin clays (pellicular grain structure) or were partially welded by narrow clay bridges (bridge grain structure). Abundant plant fragments were also included, without any particular orientation (Fig. 3). When the turret opening was found closed, the tunnel infilling looked like an intrincate net of moniliform chains composed of partially welded, round aggregates (pellets), with a diameter ranging from 0.25 to 0.75 mm, separated by large, very distinct, mammillated voids (spongy, pelletal structure) (Fig. 3).
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3.2.3. A horizon (0–15 cm) In the A horizon grains were loosely aggregated by microaggregates of amorphous, fine, organic matter mixed with clay particles (intergrain microaggregated structure). 3.2.4. E horizon (15–20 cm) The E horizon was composed of parallel layers orientated to the ground level, and distinct perpendicular interfingerings running into the Bt horizon. Layers and interfingerings showed grains weakly aggregated with thin, organic coatings and microaggregates (pellicular grain and microaggregated intergrain structures, respectively). Parallel fissures, frequently infilled with loose grains, separated the layered material. 3.2.5. Bt horizon (20–200 cm-excavation limit) The Bt horizon displayed alternating compact and porous types of microstructure. In the compact type, grains were densely cemented with clay, (massive, intergrain cemented structure),
Fig. 5. Micromorphology of the fungus-chamber wall in the A. vollenweideri nest showing a non-coated surface and a microporous structure (C: clay cement; IO: iron oxide mottle, Q: quartz grain). Stars: voids (all voids in blue).
3.2.2. Mound In the upper region, the mound showed a very porous structure similar to that described for the turrets (spongy structure), alternating with areas displaying very poor aggregation (Fig. 4). In those latter areas, grains were weakly cemented by thin clay (pellicular grain structure) and clay bridges (bridge grain structure) or were loosely adhered by clay microaggregates (intergrain microaggregated structure). Many rounded voids and fissures were infilled with loose silt and sand grains. Downwards, the mound microstructure gradually compacted, showing voids of less than or equal to 100 μm (microporous structure). Abundant plant fragments were included in the whole mound, fresh in the superficial level and rather decomposed in the inner part. The mound surface was covered with loose, rounded soil pellets. They showed a variable composition, microstructure and size. Most were composed of silt and sand cemented with clay, whereas a few were cemented with organic matter mixed with scattered clay particles, or they were almost exclusively composed of clay or silt grains. Clay birefringence fabrics were granostriated, reticulate striated or dotted, showing variable bright. Minor pellets were almost opaque. The frequency of their coarse components varied from few to frequent-common classes (5% to 30%). Most pellets showed massive or microporous structures, but some displayed a loose intergrain microaggregated structure. Pellets occurred as single rounded aggregates (0.5 to 4 mm in diameter), or were clustered in compound pellets. Abundant plant fragments, thin stems and grass fragments with sharp contours and 5 to 10 mm in length, extended among them.
Fig. 6. Micromorphology of the mound of Cortaritermes fulviceps. Top: massive pelletal (PS) and intergrain cemented structures (ICS). Middle: soil pellets (P) surrounded by thin organic pelletal coatings (PC). Bottom: inquilinous termite gallery crossing the adjacent ant-mound material (G) showing organic coating (OC) and adjacent pellets (P). All voids in blue.
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Table 1 Nest of the leaf-cutting ant Atta vollenweideri Nest structure
Turrets
Mound
Features Microstructure
Spongy structure with abundant mammillated voids
Spongy, single, bridge and pellicular grain structures in the upper region; microporous and spongy structures in the inner region Frequency (%) of coarse Common to very Common to very mineral material dominant (30 to N70%) dominant (40 to N70%) Coarse organic material Abundant plant fragments Abundant plant fragments Fine material Clay Clay Birefringence fabric Granostriated and reticulate striated Granostriated and reticulate striated Other features When the tunnel opening is closed, the infilling shows Loose pellets above the a spongy, pelletal structure surface
whereas in the porous type, numerous voids of less than or equal to 100 μm occurred in the aggregated material (microporous structure), or were located between grains partially welded by thin clays (pellicular grain structure), or between microaggregates situated in the intergrain space (intergrain microaggregated structure). 3.2.6. Fungus and refuse chambers, and tunnels Chambers and tunnels were found in the Bt horizon, and showed the same micromorphology as the surrounding horizon. Tunnels and chambers, both for fungus and refuse, showed undulated, smooth, and non-coated surfaces (Fig. 5). 3.3. Micromorphological descriptions — C. fulviceps The same micromorphological features presented above were described for the nests of the termite C. fulviceps: one epigean nest, with subterranean galleries situated in the A
Underground fungus and refuse chambers, and tunnels Microporous and massive, intergrain cemented structures alternated with pellicular and intergrain microaggregated structures Common to dominant (50–70%) Absent Clay Granostriated and reticulate striated, very diffuse in the surface of refuse chambers No coated chambers nor tunnels
horizon, and the other nest of the inquilinous colony located on the mound of A. vollenweideri. In the latter case, the adjacent ant mound wall surrounding the base of the termite nest was also described, including some termite galleries. 3.3.1. Epigean nest and subterranean galleries The mound showed a massive microstructure, dominantly composed of much fitted, piled, lens-shaped pellets (massive, pelletal structure). Each pellet was 430 to 700 μm long and 130 to 220 μm wide, and was lined by a thin coating of organic matter and clay, about 20–70 μm thick (Fig. 6). The inner pelletal microstructure displayed variable aggregation, showing grains densely cemented or weakly adhered by microaggregates. Grain cement and intergrain microaggregates were composed of organic matter and clay. In many areas the pelletal structure was not so remarkable, but walls were crossed by undulated, organic bands of similar composition and thickness
Table 2 Nests of the mound-building termite Cortaritermes fulviceps Nest type Features
Epigean nest and subterranean galleries located in the soil
Nest of an inquilinous colony located on the mound of Atta vollenweideri Termite nest
Microstructure
Massive pelletal structure alternated with Massive pelletal structure intergrain cemented structure Frequency (%) of coarse Frequent to common (30–40%) Frequent to common (30–40%) mineral material Coarse Abundant plant fragments Scattered plant fragments organic material Fine material Amorphous organic matter and clay Amorphous organic matter and clay Birefringence fabric Other features
Adjacent ant mound substratum and termite galleries Microporous structure Common to dominant (40–50%) Scattered plant fragments
Slight dotted and granostriated
Slight dotted and granostriated
Dominantly clay. In many areas the clay is mixed with organic matter Dotted and granostriated
Lens shaped, single and compound pellets lined by a thin organic-clayish coatings. Mound galleries lined by simple organic coatings and compound coatings composed of pellets coated by thick organic bands. Subterranean galleries lined by a very thin organic coating
Lens shaped, single and compound pellets lined by a thin organic-clayish coatings. Galleries lined by simple organic coatings and compound coatings composed of pellets coated by thick organic bands
Scattered, sinuous, organic bands, crossing the groundmass showing a diffuse lenticular drawing. Termite galleries lined by simple organic coatings and adjacent pelletal structure
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Table 3 Profile of the surrounding soil Horizon
A horizon
E horizon
B1 horizon⁎
B2t horizon
Pellicular, intergrain microaggregated and single grain structures Very dominant (N70%)
Microporous and massive, intergrain cemented structures alternated with pellicular and intergrain microaggregated structures Common to dominant (40–70%)
Microporous and massive, intergrain cemented structures alternated with pellicular structure Common to dominant (40–70%)
Absent
Absent
Absent
Features Microstructure
Single grain, intergrain microaggregated and cemented structures Frequency (%) of coarse Very dominant (N70%) mineral material Coarse organic material Abundant plant remains Fine material Amorphous, organic matter Birefringence Undifferentiated fabric Other features Absent
Amorphous, organic Amorphous, organic matter mixed with clay matter mixed with clay Slight dotted Dotted
Clay
Planar aggregates separated by broad horizontal fissures
Mottles of iron oxides
Absent
Granostriated and reticulate striated
⁎Absent below the mound of Atta vollenweideri.
to pelletal linings. Other areas showed a dense microstructure with grains embedded in dark, fine organic matter (intergrain cemented structure) (Fig. 6). Mound galleries were lined with a distinct organic coating, 50 to 100 μm in thickness, or by a compound coating, 300 to 400 μm thick, composed of superposed, flattened pellets enclosed by alternated, bow-shaped organic bands. Abundant plant fragments occurred randomly distributed. Subterranean galleries were lined by a very thin organic coating, about 50 μm thick. 3.3.2. Nest of the inquilinous termite colony located on the mound of A. vollenweideri Externally, the small inquilinous termite nest looked similar to a closed turret from the ant mound, but it was harder and more consistent. In thin section, it showed an external wall composed of the same materials and micromorphology as the upper region of the ant mound. It possessed an internal, dark brown portion, mostly included inside the mound, composed of a net of galleries similar to that of common epigean nests, from which numerous dark and sinuous galleries extended downwards and laterally into the ant mound. The inquilinous termite nest evinced an internal micromorphology (above and inside the ant-mound surface) similar to that of the large epigean nest located in the soil, except for the rare presence of very small plant fragments. The adjacent ant-mound wall presented numerous voids of less than or equal to 100 μm (microporous structure). The wall material was composed of grains adhered by microaggregates of organic matter and clay, or cemented by thin clays. Scattered, sinuous, organic bands, 20 μm thick, crossed the ant-mound walls, sometimes showing a diffuse lenticular drawing. Termite galleries running across the ant-mound were lined by a dark brown, organic coating, 75 to 200 μm thick and adjacent, superimposed, lensshaped pellets surrounded by thin, organic coatings (Fig. 6).
coarse mineral material, presence of coarse organic materials, qualitative analysis of fine materials and their birefringence fabrics, and other features. The micromorphology of nests of C. fulviceps, both the epigean one with its subterranean galleries, and the inquilinous nest located on the leaf-cutting ant mound, is comparatively summarized in Table 2, as for the nest of A. vollenweideri. This comparison extends to the adjacent substratum of the termite nest included into the ant mound. The same micromorphological features of the surrounding soil are presented comparatively in Table 3. 3.5. Hindgut content of workers of C. fulviceps The hindgut content of termite workers was mostly composed of amorphous, fine, organic matter mixed with clay, including scattered silt particles and few sand grains showing a maximum size of 100 μm (very fine-sized). 4. Discussion and conclusions In spite of being located in a frequently-flooded soil, the nests of neighbor leaf-cutting ants, A. vollenweideri, and mound-building termites, C. fulviceps, showed notably different macro- and micromorphologies. Ants and termites construct their nest mounds with the same soil coarse components: sand grains, mostly very fine sized, and silt, preserving the same soil particle size. They do not select any kind of coarse particles from the soil at the point of soil excavation, but their constructions show many particular micromorphological features such as different types of microstructure and frequency of coarse components, presence of pellets, organic coatings and banded intercalations.
3.4. Comparative soil and nest micromorphology
4.1. Nest micromorphology and building behavior in Atta leafcutting ants
The micromorphology of each part of the A. vollenweideri nest is comparatively presented in Table 1, which summarizes different features related to nest microstructure, frequency of
In A. vollenweideri, the underground structures resulting from the excavation, i.e., chambers (both for fungus and refuse) and tunnels, however, showed the same micromorphology as
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that observed in the surrounding Bt horizon, lacking any distinct, particular feature, which suggests that those cavities are simple and non plastered soil excavations. Ant workers carry the excavated material between their mandibles and pile it around the first nest entrance. Individual loads are small, single or welded soil balls in clusters of 0.5 to 4 mm. They are named pellets herein because of their similarity with the micromorphological term employed for termites and defined by Sleeman and Brewer (1972) as “common micromorphological features of termite constructions recognized as spheroidal or ovoid bodies composed of organic and mineral soil materials or various combinations of both”. Whereas pellets in the termite nests are commonly in the size range of 0.3 to 1 mm and are welded or cemented with fine materials, forming the structural wall units or “bricks” (Stoops, 1964; Mermut et al., 1984; Eschenbrenner, 1986; Sleeman and Brewer, 1972), in the ant nest they are generally bigger soil balls loosely dispersed over the mound, and partly welded in the infillings of the closed turrets. The pelletal composition, microstructure, frequency of coarse components, and clay birefringence fabrics are very variable because those features depend on the horizon from which the pellets were removed. Most pellets were composed of silt and very fine sand grains cemented with clay, the same coarse and fine components of the Bt horizon, suggesting that they have been removed during the excavation of fungus and refuse chambers. This view is supported by the fact that most pellets on the uppermost layer of the mound showed the same types of microstructure and birefringence fabrics observed in the Bt horizon. However, in spite of being micromorphologically similar to that horizon, pellets showed a notably lower value in the frequency of coarse components. The maximum frequency of coarse components shown in the pellets was 30%, whereas in the Bt horizon, the minimum frequency averaged 50%. This difference could result from a posterior incorporation of clay to the removed soil, or from the way pellets are formed. There are, regrettably, no descriptions about digging behavior of ants excavating natural soil, with its original microstructure and fine and coarse components, so that we can only speculate about this discrepancy. In laboratory studies, Sudd (1969) described the excavation and removal of soil by single ants under controlled conditions, and recognized three steps: 1) the mandible grab during removal of sand from the work-surface, 2) the movements of the forelegs for the collection of the load, and 3) the transport of the load between the mandibles towards the end of the tunnel, which could be a single, large sand grain or a crumb of small sand grains. Observations on laboratory colonies of the leaf-cutting ant A. vollenweideri indicate that single workers dig in soil by pulling out small pieces with their mandibles. These pieces are usually not carried to the outside by the same workers, but placed and piled close to the digging site, where other workers may also be involved in digging. A different set of workers is often involved in the transport of the pieces to another place, where items from different digging sites accumulate, or to the exterior. This kind of “transport chains” during removal of digging material resembles that observed in the context of foraging in this species (Röschard and Roces, 2003).
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The final formation of the pellets, for which workers use their forelegs to collect the load together before transporting it between the mandibles, may therefore involve the mixing of soil particles from different sites. This could be one of the reasons for the observed dissimilarity in composition between pellets and soil from the Bt horizon. The large ant mound mainly results from the deposition of the excavated material, and it shows a combination of many porous types of microstructures in its upper region, whereas denser types of microstructures gradually predominate at depth. Both the upper mound material and the percolated rain probably contribute to weld the pelletal material concentrated on the ground surface. In the mound, the frequency of coarse components was higher than in the Bt horizon (its principal source), probably because of the lixiviation of the clay mound. Those few clay particles that had not been lost in the lixiviation process are retained in the intergranular space welding the coarse grains as thin, surrounding grain coatings and bridges. As the mound growths, the lixivial clay gradually concentrates at the base of the mound and in the wide A horizon located under the mound. The final structure of the mound does not only result from a passive amalgamation of pelletal materials, but also from the import and inclusion of abundant thin twigs and grass fragments. Plant fragments show sharp contours and roughly similar size, suggesting that they represent plant or grass fragments cut by the ants, carried and then deposited on the mound surface. In fact, leaf-cutting ant workers were observed to collect plant fragments as building material, especially after rains, for the construction of turrets or the closing of nest openings (Kleineidam and Roces, 2000). As the mound enlarges and compacts, these plant fragments are also amalgamated with the pelletal material, probably helping to reinforce the porous mound structure. The ventilation turrets showed the same porous microstructure observed for the mound, but the infilling of closed turrets evinced a remarkable pelletal structure. Those infillings were composed of easily recognized masses of pellets partially welded and separated by large mammillated voids, suggesting that this type of porous structure could be the consequence of a rapid occlusion employing wet and plastic, recently-excavated soil pellets. The size of the pellets used for turret occlusion ranged from 0.25 to 0.75 mm in diameter, whereas those deposited by the ants on the mound ranged from 0.5 to 4 mm. Since a correlation between worker body size and particle size would be expected, as reported for other ants (Sudd, 1968), this phenomenon suggests that turret occlusion may be carried out by small workers. The closing of nest openings is a rapid, collective colony response to heavy rains (Kleineidam and Roces, 2000), which takes place in quite a few minutes to one or two hours, and this response is also observed in winter (dry season), when colonies close up to 80% of the existing openings (Jonkman, 1980c), probably to avoid the inflow of cold air. Contrary to the assumption of Jonkman (1980c), who argued that chamber walls in A. vollenweideri might be lined with cement to avoid ground-water penetration, tunnel walls and nest chambers were not coated, neither with fecal nor with other fine
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materials. The underground tunnels and chambers of the leafcutting ant nest can therefore be regarded as simple excavations, since no impermeable coating lines their surface. Several authors have focused on the question whether the walls of tunnel and chambers of ant nests are coated. Green et al. (1999) and Cosarinsky (2006) observed that mound galleries of Solenopsis fire ants were not coated. Bruch (1916) described a distinct, firm coating of the nest chamber walls of the Neotropical ant Forelius chalybaeus, but only mentioned a fine composition without giving more details. Wang et al. (1995) observed in the nest walls of L. neoniger a compact microstructure because of the presence of dark infillings of an unidentified colloidal material among sand grains. Cosarinsky (2006) described a distinct soil coating plastering the galleries of C. punctulatus, composed of silt particles embedded in a compact mass of clay with iron oxides and fine organic matter. Both, Gorosito et al. (2006) and Cosarinsky (2006) suggested that the compact structure observed in the walls of galleries and nest chambers was necessary to stabilize the walls and to support the high mass of the Camponotus mound. Lining of nest galleries with clay or “glaze” was also reported for Trachymyrmex turrifex and Camponotus intrepidus, respectively, although its function remains elusive (Wheeler, 1907; Cowan et al., 1985). The employment of fecal matter in ant constructions or excavations has not been reported in the literature. The question arises, why nest do not inundate during floods, even when the soil is totally submerged. Mounds are inhabited islands in the flooded ground and colonies and fungus keep safe in underground chambers during the rainy season. Considering the porous types of microstructure observed in the surrounding Bt horizon, two hypotheses could be advanced. First, it is conceivable that the horizon microstructure only allows the percolation of small amounts of infiltrating water. Second, thousands of voids measuring less than 100 μm are expected to generate large capillary forces that may retain the water out of the chambers during the floods. But these hypotheses need to be evaluated with experiments employing undisturbed, field soil samples. 4.2. Nest micromorphology and building behavior in Cortaritermes termites In contrast to leaf-cutting ants, mounds of C. fulviceps are inhabited, very compact above-ground constructions that protect their residents from infiltrating rainwater. Their walls showed a massive, pelletal microstructure composed of piled, much fitted, lens-shaped, soil pellets covered by undulated layers of fine, organic matter and clay particles. Galleries and chambers were plastered with a distinct, dark brown coating, also composed of fine, organic matter with scattered silt and clays. Very frequently, gallery coatings were compound features composed of superimposed, small soil pellets surrounded by thick organic bands. In some areas, the lens-shaped pellets were not so distinguishable, and undulated organic bands intercalated among elongate parcels of soil. In many areas, soil grains were entirely embedded by fine organic matter. All these organic features were composed of the same components found in the worker's hindgut content: fine organic matter mixed with clay
and scattered silt particles, suggesting a common fecal origin. It is likely that the addition of fecal matter to the construction, leading to a very compact mound microstructure, would protect the nest from both rain splash and infiltrating water. Lee and Wood (1971) and Sleeman and Brewer (1972) named as “lenticular structure” a similar pelletal type of microstructure observed in thin sections of nest of many Australian mound-building termites. They also found some variations in samples where the lenticular structure was not so clear, and described them as undulate organic bands surrounding elongated soil aggregates. Other samples showed patches of organic matter randomly distributed among soil minerals. They assigned a fecal origin for those organic coatings, bands and patches considering the studies by Emerson (1938) on termite building behavior. He observed workers placing their single soil loads, moistened with saliva, and then excreting a drop of fecal matter over the recently placed parcel of the soil. Similar fecal micromorphological features were also observed in thin sections of mounds of Neotropical termites. In Cornitermes cumulans, Cosarinsky (2003) observed organic gallery coatings and undulate bands crossing the walls of mounds located in sandy soils. The mound of Termes saltans and C. fulviceps located in sandy soils with abundant humus were composed of irregular shaped soil pellets and coarse sand grains entirely surrounded by thick layers of organic matter (Cosarinsky, 2004a,b). The fecal addition to soil material is not the only termite behavior that leads to cohesion and therefore stabilization of the construction. Many mound-building termites moisten with saliva the soil particles carried in the buccal cavity (Noirot and Darlington, 2002). The moistening with saliva could explain in C. fulviceps why the birefringence fabric is granostriated in the mound, while it is undifferentiated in the A horizon, where this species is supposed to feed and collect the building material. In the A horizon, humus masks the clay birefringence, but when the soil particles are removed and mixed with saliva, the clay particles probably decant from the suspension of saliva as very thin streaks or domains arranged around the sand grains, displaying a granostriated birefringence fabric (Aylmore and Quirk, 1960; van Olphen, 1977). The addition of clay and organic matter to the mound is also reflected by a notable decrease in the frequency of coarse components when compared with the A horizon: in the mound the frequency is 30–40% whereas it is N 70% in the A horizon. The inquilinous colony of C. fulviceps located on the mound of A. vollenweideri constructed a small nest employing available materials (from the ant mound), but adding a lot of fecal matter. Its massive, pelletal microstructure was very similar to that found in the mature mound located on the soil surface. The largest difference was that sections of this small nest did not show so many and large plant fragments as they occur in non-inquilinous nests constructed around tussock grasses. Only small plant fragments were observed irregularly distributed within the nest walls, in size of the fragments collected by ants and deposited on their mound. The adjacent ant-mound material surrounding the base of the termite nest was reinforced by many distinct micromorphological
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fecal features, being more concentrated near the subterranean net of galleries, such as undulated, dark, banded intercalations, gallery coatings, and pelletal linings. The wall displayed more aggregation than in the rest of the upper portion of the mound, showing microporous structure similar to that observed in the basal region of the ant mound. The frequency of coarse components decreased to 40–50% in the adjacent ant mound material from more than 70% in the upper portion of the ant mound, probably as a consequence of the addition of fecal matter and a higher concentration of clay that could not lixiviate, because it was retained by the termite nest. 4.3. Comparative nest micromorphology To conclude, the comparative study of nest micromorphology of these neighboring soil-nesting social insects provided information about many processes involved in the formation of their nests. In A. vollenweideri leaf-cutting ants, such processes are: (1) the excavation of chambers and tunnels by digging the soil profile, (2) the concentration of the excavated material on the ground around the tunnel openings as similarly-shaped pellets with a probable addition of clay, (3) the resulting formation of a large, porous mound with weathered and welded pelletal materials and added plant fragments cut and carried by the workers, (4) the building of ventilation turrets in the mound surface by piling and welding moist pellets, and (5) the clay lixiviation taking place from the upper region of the mound, leading to its accumulation in the basal portion and in the wide A horizon below the mound. In C. fulviceps termites, two distinct main processes are involved: (1) the construction of a solid, epigean mound employing abundant fecal materials to cement sand grains or soil pellets molded and moistened with saliva in the worker’s buccal cavity, and (2) the plastering of mound and underground galleries. The same processes are shown for the inquilinous termites nesting on the ant mound, even though the available materials for building, compared with colonies nesting directly on the soil, completely differed. The inquilinous colony also employed abundant fecal matter to reinforce the loose substratum, only composed of sand and clay but lacking any organic matter except by those plant fragments imported by the ants and included in the mound. Plasticity in termite building behavior is therefore emphasized by two facts: first, inquilinous and freely-nesting colonies, although dealing with very different building materials, construct nests with similar micromorphology; second, depending on the available material in the soil, C. fulviceps workers may either mould pellets in their buccal cavities and use no cement for building, or may cement the pellets with fecal material (Cosarinsky, 2004b). Even though the nest micromorphology represents a kind of “frozen” behavioral record of the digging and building efforts of the nest inhabitants, it is, however, not enough to understand all the processes involved in soil-nesting behavior. Micromorphological studies should be extended with edaphological quantitative analyses (such as soil water content; clay and organic matter contents) and behavioral observations both in the field and laboratory.
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Acknowledgements We thank two anonymous reviewers for helpful comments that improved the manuscript. Field work was performed at the wonderful Reserva Ecológica El Bagual (Alparamis SA — Aves Argentinas) in eastern Chaco, Province of Formosa, Argentina. We are very much indebted to the ornithologist Alejandro G. Di Giacomo, his field assistants, and especially Götz family for providing facilities at the Biological Station, daily help during our stays and invaluable logistical support throughout the past ten years of ant (and recently termite) research. Martin Bollazzi helped during material sampling. Thanks to Ulrich Mueller for indicating the reference of Wheeler's paper. Many thanks also to Dr. Luiz Fontes for the taxonomic identification of the termites, and to Dra. Daniela Villegas for her help with soil taxonomy. Financial support was provided by the DFG, Germany (SFB 554). References Aylmore, L.A.G., Quirk, J.P., 1960. Domain or turbostratic structures of clays. Nature 187, 1046–1048. Bonetto, A.A., Manzi, R., Pignalberi, C., 1960. Los tacurúes de Camponotus punctulatus (Mayr) Notas ecológicas. Physis 12, 217–224. Brauman, A., Bignell, D.E., Tayasu, I., 2002. Soil-feeding termites: biology, microbial associations and digestive mechanisms. In: Abe, T., Bignell, D.A., Higashi, M. (Eds.), Termites: Evolution, Sociality, Symbioses, Ecology. Kluwer Academic Publishers, Dordrecht, pp. 233–259. Bruch, C., 1916. Contribución al estudio de las hormigas de la provincia de San Luis. Rev. Mus. La Plata 23, 291–357. Bucher, E.H., 1982. Chaco and caatinga — South American savannas, woodlands and thickets. In: Huntley, B., Walkers, B. (Eds.), Ecology of Tropical Savannas. Springer Verlag, Berlin, pp. 48–79. Bucher, E.H., Zuccardi, R.B., 1967. Significación de los hormigueros de Atta vollenweideri Forel como alternadores del suelo de la provincia de Tucumán. Acta Zool. Lilloana 23, 83–95. Bullock, P., Fedoroff, N., Jongerius, A., Stoops, G., Tursina, T., 1985. Handbook for Soil Thin Section Description. Waine Research Publications, England. Cosarinsky, M.I., 2003. Micromorphology of the nest of Cornitermes cumulans (Kollar) (Isoptera: Termitidae). In: Buatois, L.A., Mangano, M.G. (Eds.), Icnología: Hacia una convergencia entre geología y biología. Publicación especial no. 9 de la Asociación Paleontológica Argentina, Buenos Aires, pp. 53–64. Cosarinsky, M.I., 2004a. Nest micromorphology of the neotropical termite Termes saltans (Isoptera: Termitidae). Sociobiology 43, 501–511. Cosarinsky, M.I., 2004b. Nest micromorphology of the termite Cortaritermes fulviceps in different types of soil (Isoptera; Termitidae). Sociobiology 44, 153–170. Cosarinsky, M.I., 2005. Comparative micromorphology of arboreal and terrestrial carton nests of the neotropical termite Nasutitermes aquilinus (Isoptera:Termitidae). Sociobiology 45, 839–852. Cosarinsky, M.I., 2006. Nest micromorphology of the neotropical mound building ants Camponotus punctulatus and Solenopsis sp. Sociobiology 47, 329–344. Cosarinsky, M.I., Bellosi, E.S., Genise, J.F., 2005. Micromorphology of modern epigean termite nests and possible termite ichnofossils: a comparative analysis. Sociobiology 45, 745–778. Cowan, J.A., Humphreys, G.S., Mitchell, P.B., Murphy, C.L., 1985. An assessment of pedoturbation by two species of mound-building ants, Camponotus intrepidus (Kirby) and Iridomyrmex purpureus (F. Smith). Aust. J. Soil Res. 22, 95–107. Emerson, A.E., 1938. Termite nests: a study of the phylogeny of behavior. Ecol. Monogr. 8, 247–284.
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