Effects of Camponotus punctulatus ants on plant community compositionand soil properties across land-use histories

P.J. Folgarait1,*, S. Perelman2, N. Gorosito1, R. Pizzio3 and J. Fernández3

1Unidad de Investigación en Interacciones Biológicas, Centro de Estudios e Investigaciones, UniversidadNacional de Quilmes, Roque Sáenz Peña 180, Buenos Aires, Bernal 1876, Argentina; 2IFEVA, Facultad deArognomía, Universidad de Buenos Aires, Av. San Martín 4453, Capital Federal, 1417, Argentina; 3EstaciónExperimental INTA-Mercedes, Casilla de Correo 38, Mercedes, 3470, Corrientes, Argentina; *Author forcorrespondence (e-mail: pfolgarait@unq.edu.ar)

Received 19 January 2001; accepted in revised form 15 February 2001

Key words: Agroecosystems, Edaphic changes, Formicidae, Indicator species, Multivariate analysis, Succession

Abstract

Populations of the ant Camponotus punctulatus undergo demographic explosions after agricultural activities,building conspicuous, vegetation-covered soil mounds. We investigated the effects of C. punctulatus on floristiccomposition and soil properties along a gradient of agricultural disturbance in Northeastern Argentina. Wesampled vegetation and soil “on” and “off” anthills in, at least, three replicate plots of each of the followingsituations that represent an increasing gradient of soil disturbance: natural grasslands, sown pastures of Digitariadecumbens, sown pastures of Setaria sphacelata, and recently abandoned rice fields. Sets of characteristic plantspecies for each of the land use histories, for “on” and “off” anthills as well as for anthills of different sizes wereidentified through Indicator Species Analysis. 64% of the variation in plant community composition was mainlyexplained by land-use history which was associated to the first 2 axes of a Correspondence Analysis based on thefrequency of 126 species across all sites. At the replicate scale, Correspondence Analyses revealed patterns ofplant species composition related to the presence and size of anthills. Larger mounds became enriched in species,especially herb weeds, in comparison to smaller mounds or samples gathered outside the anthills. A PrincipalComponent Analysis of soil data revealed that 71% of the variation in soil properties was explained by the pres-ence of anthills. Soils from “on” anthills were more fertile than soils from “off” anthills, independent of land-usehistory. The fertility effect of C. punctulatus mounds in addition with the vegetation patterns observed along thegradient of anthill-sizes highlights the importance of these ants at the landscape and local scales.

Introduction

Mound-building ants can be considered one of thesoil ecosystem engineers (Folgarait 1998), as theymodulate the availability of resources and create ormodify habitats for other species (Jones et al. 1994).Anthills, or mounds, may affect the floristic compo-sition and relative abundance of plant species grow-ing on them (Rogers and Lavigne 1974; King 1977a;Culver and Beattie 1983). Ant disturbance producedby soil heaping increases as the mound grows, settingthe stage for a succession of plant species with dif-ferent life-history traits (King 1977b). In addition, the

construction of anthills also affects soil propertiessuch as porosity, drainage, and the concentration ofnutrients and organic matter (Baxter and Hole 1967;Lockaby and Adams 1985; Carlson and Whitford1991; Mc Gingley et al. 1994). Edaphic changes ofthis kind could also affect the soil fauna (Lavelle etal. 1997).

Despite the world-wide distribution of ants andtheir prominence in terms of number and biomass incomparison to other soil fauna (Hölldobler and Wil-son 1990), very little attention has been paid to therole of ants in ecosystem functioning (Folgarait1998). This is unfortunate given that (1) ants can be

1Plant Ecology 163: 1–13, 2002.© 2002 Kluwer Academic Publishers. Printed in the Netherlands.

very abundant even where soil is disturbed (Lobry deBruyn 1993), (2) ants can invade and establish suc-cessfully as “pests” in agricultural landscapes (Cher-ret 1986) and forest plantations (Vilela 1986; Folgar-ait et al. 1996a), and (3) ants can affect nutrient cy-cling and water infiltration (Haines 1978; Lugo et al.1973; Lobry de Bruyn and Conacher 1994).

Camponotus punctulatus (Mayr) is a native antspecies with a broad geographical distribution in Ar-gentina, ranging from the frontier with Brazil, Para-guay, and Bolivia to latitude 40° S (Patagonia), andranging from the coast of the Atlantic ocean up toheights of 4000 m (Kusnezov 1951). This ant specieseither builds large mounds or nests underground at thebase of tussocks, rosettes, or under rocks (Kusnezov(1951); P.J. Folgarait, pers. obs.). The presence offlooded areas (Lewis et al. 1991) and an increase inagricultural activities (P.J. Folgarait, unpublished)have been correlated with mound building. The antsdo not represent a direct hazard to crops, as they areneither herbivores nor granivores (Gorosito et al.1997). Nonetheless, farmers need to incur into higheconomic costs in order to destroy these hard-packedand large mounds built by C. punctulatus.

Within the Espinal Phytogeographical Region ofArgentina (Carnevalli 1994), in Corrientes Province,natural grasslands used for cattle ranching since lastcentury, are being converted into new agroecosys-tems, especially sown pastures and rice paddy fields.Sown pastures, Setaria sphacelata (Stapf & Hubbard)and Digitaria decumbens, (Stent) are planted for live-stock forage in areas where cattle ranching remainsthe main economic activity. In large farms, with theincreasing availability of artificial water reservoirs,rice production is becoming a more common agricul-tural activity. In these new agroecosystems, C.punctulatus populations have unexpectedly under-gone a demographic explosion (P.J. Folgarait, unpub-lished). C. punctulatus establishes better and colo-nises faster in certain types of agricultural fields, andthose with greater soil disturbance (e.g., ex-ricefields), have greater anthill densities. Natural grass-lands used only for cattle ranching have the lowestanthill densities, and sown pastures for cattle forageexhibit intermediate densities (P.J. Folgarait, unpub-lished).

Given the fact that soil-ants appear to have an im-portant role as ecosystem engineers, and that moundsof C. punctulatus increase in number after agriculturaldisturbance, we hypothesized that anthills of C.punctulatus may have an important effect on floristic

composition and on soil properties, and that thesechanges would be affected by land-use history.

Methods

Study site

The study was conducted in Mercedes Department,Province of Corrientes, Argentina (29° S, 58° W). Theclimate is wet sub-tropical, without a definite dry sea-son; autumns (March and April) are rainy, springs(October and November) wet, and summers (Decem-ber, January, and February) are hot and frequentlywet. Mean annual precipitation is 1270 mm and meanannual temperature is 20.1° C. Air humidity is high(> 73%) throughout the year (Fernández et al. 1993).Soils have developed on Triassic basalt and sand-stone, with a large contribution of Pliocene fluvialclays. This has lead to the existence of primarilyBrunizem hidromorphic soils (Purnell and Hein1969).

Sampling design

Data were gathered from December 1995 to May1996 in four different situations reflecting land-usehistories with a decreasing gradient of soil disturb-ance: (1) 2–3 year-old abandoned rice fields; (2) 7–8year-old Setaria sphacelata (hereafter “Setaria”)sown pasture; (3) 7–8 year-old Digitaria decumbens(hereafter “Pangola”) sown pasture; and (4) naturalgrasslands. Rice (Oryza sativa, Linneo) is cultivatedunder flooding; these fields had been abandoned for2–3 years after three consecutive years of growingrice and applying fertilisers. Fungicides for rice dis-eases may have been applied, but insecticides werenever used. Sown pastures for cattle ranching wereplanted 7–8 years ago and had one application of fer-tilisers but no pesticides. Setaria was planted fromseeds using machinery, while Digitaria was sownmanually from rhizomes. Natural grasslands domi-nated by Andropogon lateralis (Nees) were present inthe fields before rice or pastures were cultivated. Theregion has such a long history of cattle ranching thatit was not possible to find any type of land use plotwithout livestock. For that reason, we had to use nat-ural grasslands with cattle as a control for the otherland-use history types. For each land-use type we hadthree or four replicate plots (2.5 ha), with each repli-cate plot being located at a different farm within the

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same region. Two, 150-m long, 6-m width permanenttransects, one N–S, and the other E–W, were laid outin each plot. We counted all anthills present pertransect (P.J. Folgarait, unpublished) and marked amaximum of 20 anthills per transect, from which wetook data presented here.

Overall, across transects, replicate plots, and typeof land-uses, we had 418 paired quadrats placed “on”marked anthills and 3 m “off” the same anthills. Werecorded plant species presence and relative cover ineach quadrat of 50 × 50 cm, as previous work has in-dicated that this area captures the majority of localplant diversity across land-use history types (Fernán-dez et al. 1993). The number of paired quadrats ineach replicate plot depended on the density of anthillsalong the transects, the lowest density being in thenatural grasslands (12) and maximum density (40) inabandoned rice fields. Each pair of quadrats wasplaced in the same direction, covering all directions(N, S, W and E) across pairs.

We collected four paired soil samples at each ofthree replicate plots which were combined to makeone pair of composite sample per replicate plot, onerepresenting “on” the anthills and the other “off” themounds. Each of the four paired soil samples per plotwere taken from a different bearing, N, S, E, or W.The soil from the anthill was exhaustively sampled bymaking collections from different layers that werethoroughly mixed and combined. Samples from offthe anthill were taken 3 m away from the mound fromthe soil profile to a depth equal to the height of thepaired anthill. We chose to sample the intermediatesize ( � 300 kg) of anthills as to have greater prob-ability of capturing the effect of ants on soils. Nosamples were taken from “on” the anthills at naturalgrasslands because there were very few anthills of in-termediate size.

Soil analyses typically used in anthill soil studies(see Folgarait (1998) and references therein) wereperformed following standard chemical and texturalanalyses (Page 1982). Kurtz and Bray was used forP; Kjeldahl for N; ammonium acetate extraction forK, Ca, Mg, and Na; DTPA extraction for Zn, Fe, Mg,and Cu; NaCl extraction and ammonium titration forcation exchange capacity; Walkley and Black for or-ganic matter; potenciometric method (soil 1: water2.5) for pH; and Bouyoucous hydrometry for deter-minations of sand, lime and clay content.

Statistical analysis

Sets of characteristic species for each of the land usehistories (or on/off anthills) were identified throughIndicator Species Analysis (Dufrene and Legendre1997) and using 500 Monte Carlo random permuta-tions to assign a probability for the observed maxi-mum indicator value for each species. The indicatorvalue for a species was determined by combining aspecies’ relative abundance with its relative frequencyof occurrence in a particular land use history type(hereafter “land-use history indicator species criteri-on”) or on/off anthills (hereafter “anthill indicatorspecies criterion”). The greater the indicator value ob-tained, the more representative the species is of thatparticular habitat. A species was considered to have ahigh indicator value if its maximum value corre-sponded to a particular land-use type or microsite(on/off anthills) and was associated to a p < 0.05.

In order to characterise the plant species from dif-ferent land-use histories, and from on/off anthills, weused indicator species to explore the association be-tween a species belonging to a particular group (landuse history or on/off anthills) and a series of speciescharacters, such as origin (native or exotic), longev-ity (perennial or annual), growth habit (prostrate orerect), life forms (grasses, herbs, or shrubs), growingseason (cold or warm), and forage value (in decreas-ing order: fine, soft, ordinary, hard, and weed). For-age value was determined for each plant species ac-cording to its nutritional value to cattle and how oftenit was eaten by cattle throughout the year (Rosengurtt1949). The association between the number of indi-cator species in each of the groups and the selectedtraits was tested using X2. The expected number ofspecies in each class was calculated as the total num-ber of species for the class in the two groups multi-plied by the proportion of species belonging to thesame class in the total list of species registered(Greig-Smith 1983).

We used descriptive multivariate methods (Digbyand Kempton 1987) to analyze both floristic compo-sition and soil properties. We used correspondenceanalyses (CA) on plant species frequency data on/offanthills from each land use history type. Of the 149species recorded, 23 species were omitted from theanalysis because they appeared in less than threequadrats. We also explored differences in floristiccomposition on/off anthills in a more detailed scaleusing CA for each replicate plot based on the plantspecies cover matrix data. We summarized the results

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from the individual correspondence analyses by plot-ting the ordinations obtained for a given land-use his-tory type after rescaling the axis for uniformity. Ant-hill size classes were superimposed on individual datapoints from the ordination graphs. Anthill sizes weredivided into small, intermediate, big, and old (usingthe 25–75% percentile range for maximum widthand/or height as the best predictor of size classes (Fol-garait et al. in prep.)). For soils, we used principalcomponent analysis (PCA). Supplementary variablessuch as land use history, position regarding the ant-hill, and size of anthills were used to allow interpre-tation of subjacent operating factors in the ordinationdiagrams (Lebart et al. 1984). Multivariate analyseswere carried out using the PC-ORD software system(Mc Cune and Mefford 1997).

Results

We recorded 149 plant species but only 29 were com-mon to all four land-use history types and, 92 wereshared between two or more land-use types. 33% ofthe 149 plant species, were found exclusively on ant-hills, although 71% of these species changed their af-finity towards anthills across different types of landuse history. The number of plant species on and offanthills was not significantly different across types ofland use history (X2 = 0.706, d.f. = 3, P > 0.05) anddecreased in the following order respectively:Pangola (80 and 76) > abandoned rice (77 and 77) �Setaria (66 and 78) > natural grassland (63 and 60).

Floristic composition and land-use history

A correspondence analysis based on the frequency of126 species indicated that 64% of the variation infloristic composition was explained by the first twoaxes, which were associated with differences in landuse history (Figure 1). The presence of anthills didnot explain the variation in floristic composition atthis level of analysis.

Each type of land use history was characterized bya particular combination of species. From 87 speciesfound through the indicator species analyses, 26 spe-cies characterized the abandoned rice land-use type,27 species the Setaria land-use type, 21 species thePangola land-use type, and 18 the natural grasslandstype (“Land use history” column, in Table A1). Theproportion of indicator, prostrate and erect speciesdiffered little across types of land-use history (X2 =

7.31, d.f. = 3, P < 0.06). Prostrate species were morecommon in Pangola and less common in naturalgrassland plots, whereas erect plants were more com-mon in Setaria and less common in Pangola, in com-parison to their proportion in the total flora. Warmgrowing season species were more common in rice,Setaria, and natural grassland plots, and did not differin Pangola in relation to their proportion in the totalflora (X2 = 10.47, d.f. = 3, P < 0.015). Herb indicatorspecies were more represented in Setaria and Pangola,and grasses were more frequent in rice and naturalgrassland (X2 = 10.42, d.f. = 3, P < 0.015). Finally,indicator species with low forage value like weedswere over-represented in Setaria and Pangola whilethe other categories altogether were more common inrice and natural grassland (X2 = 9.12, d.f. = 3,P < 0.028).

Floristic composition and anthills

The correspondence analysis of the floristic composi-tion performed separately for each land-use type pro-duced ordinations that appeared to be associated withpresence and size of anthills. For natural grasslands,the axes explained 23% to 41% of the variation foundin floristic composition (Figure 2a). When data onanthill size was superimposed on the correspondenceanalyses plot, two distinct groups of samplesemerged, one containing samples off the anthills andthe other containing anthills of different size classes(Figure 2a). For rice, the axes explained from 28% to33% of the variation in the floristic composition, andtwo anthill groups can be distinguished as in naturalgrassland (Figure 2b), although small anthills overlap

Figure 1. Correspondence analysis of plant species composition.Each symbol represents a replicate plot and different symbols cor-respond to different types of land-use history, � Rice, � Pangola,‰ Setaria, ™ Natural Grassland. For each type of land-use history,clear symbols represent floristic composition on the anthills,whereas black symbols reflect floristic composition off anthills.

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both groups in the latter. For Pangola, from 32% to45% of the variation in floristic composition was ex-plained by the first axes (Figure 2c). Anthill sizeshowed two distinct groups, one representing the flo-ristic composition from off the mounds and fromsmall mounds, and the other representing the plantcommunity from medium and big anthills. In Setaria,from 31% to 38% of the variation in floristic compo-sition was explained by the first axes (Figure 2d).Again, the anthill sizes superimposed exhibited twogroupings, but were better defined than in Pangola(Figure 2d).

Floristic composition and affınity for anthills

From the species indicator analyses we found 14 spe-cies with high affinity for anthills and 14 with low af-finity for anthills (“Anthills” column, in Table A1).

Grasses and herbs were differentially represented byspecies with high or low affinity for anthills in com-parison to the total flora (X2 = 14.3, d.f. = 1, P <0.0002); herbs were more common among the highaffinity species, whereas grasses were more frequentamong the low affinity species. In comparison to thetotal flora, weeds were over-represented on anthillswhereas the plants with better forage value were morecommon off the anthills (X2 = 28.5, d.f. = 1, P <0.0001). Only perennials were found at both micro-sites; while annuals were very uncommon in the totalflora. Growing season did not differ between plantspecies with high and low affinity for mounds (X2 =0.073, d.f. = 1, P > 0.393), nor did the proportion ofprostrate versus erect plant species (X2 = 0.30, d.f. =1, P > 0.580) in comparison to their proportion in thetotal flora.

Figure 2. Axis I plotted against axis 2 of the correspondence analysis performed at the replicate plot scale. Different symbols are used togive information about each plant sample in relation to anthill sizes and presence/absence of mounds: ✽ from outside the mound; � (small),� (medium), © (big), and ™ (old) from on the anthills, for a) natural grasslands, b) abandoned rice fields, c) Pangola, and d) Setaria.Minimum convex polygons have been drawn around points belonging to data outside the anthills, from small anthills, and from medium, bigand old anthills together.

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Soil, land-use histories, and anthills

The three first ordination axes of the principal com-ponent analysis explained 85% of the total variationin soil properties. The presence of anthills explainedmost of this variation (71%) and was associated withthe first two axes (Figure 3). Pairwise correlationsbetween soil properties and each of these axes sug-gest that soil from anthills mainly had greateramounts of organic matter, carbon, nitrogen, CEC,and phosphorous than soil off the mounds. This pat-tern emerged regardless of the type of land use his-tory or the particular replicate plot. The third axisseemed to be associated with types of land use his-tory (Figure 4). The correlations found between thesoil properties and the third axis suggested that soilsfrom Setaria and natural grasslands had more sandand phosphorous, whereas abandoned rice soils hadmore potassium and clay.

Discussion

There were three main findings in this study: (1) land-use history was the major factor structuring floristiccomposition across all plots sampled, masking at thisscale the effect of C. punctulatus; (2) within eachland-use history type, the presence and size of anthills

explained distinct amounts of the variation found inplant communities, and (3) the presence of anthillswas the main factor underlying the changes observedin soils and determined similar changes in soil char-acteristics across land-use history types. It seems thatthe effects of C. punctulatus on soils translate to flo-ristic composition within each land-use history typebut in the context of the differential species availabil-ity (Pickett et al. 1987) in each environment. Each ofthese findings is discussed below.

Floristic composition and land-use history type

Total species richness was very similar across typesof land-use history. This result is in accordance withprevious works which found in agroecosystems simi-lar or even greater levels of biodiversity than in natu-ral ecosystems (Swift et al. 1996; Ghersa and León1999), and is in contrast to the common misconcep-tion that plant diversity and complexity are necessar-ily lower in transformed ecosystems.

The multivariate analyses revealed, however, thateach type of land-use history was characterised by aparticular combination of species including specieswith high indicator value. Others have also shown theimportance of land use history to explain presentplant composition (Wells et al. 1976; Motzkin et al.1996). Not surprisingly, the most abundant indicator

Figure 3. First and second axes of a principal component analysisfor edaphic variables (see text for details). The arrows join pairedsamples; the clear symbols represent soil samples from on the ant-hills whereas the black symbols represent paired soil samples fromoff the anthills for plots representing different land-use historytypes, � Rice, � Pangola, ‰ Setaria, ™ natural grassland. Anthillsfrom natural grasslands were not sampled (see text for details).Edaphic variables that best correlated with each axis are shown:OM = organic matter, C = carbon, N = total nitrogen, CEC = cat-ion exchange capacity, Ca = calcium, and Na = sodium.

Figure 4. First and third axes of a principal component analysisfor edaphic variables. Different types of symbols represent differ-ent land-use histories, � Rice, � Pangola, ‰ Setaria, ™ naturalgrassland. Clear symbols represent soil samples from on the ant-hills whereas black ones correspond to samples from off themounds. Anthills from natural grasslands were not sampled (seetext for details). Edaphic variables that best correlated with eachaxis are shown: OM = organic matter, C = carbon, N = total nitro-gen, K = potassium, P = phosphorous and CEC = cation exchangecapacity.

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plant species were in the sown pastures: Digitariadecumbens in Pangola and Setaria sphacelata in Se-taria, and the native grass Andropogon lateralis innatural grasslands.

The traits studied in the indicator plant speciesfrom each type of land-use history showed some dif-ferences between land-use histories and highlightedthe importance of the particular assemblage of plantspecies rather than plant guilds for different land-usehistory types. However, it can be said that in general,more warm-growing season species were found inabandoned rice, Setaria and, natural grasslands. Atboth sown pastures, we found more herbs and moreweed indicator species in comparison to their ex-pected proportion based on frequency in the totalflora. Grasses and species with greater forage valuewere over-represented in abandoned rice and naturalgrasslands.

Floristic composition and anthill size

Conversions of natural ecosystems to agroecosystemsgenerally involve the invasion of herbaceous plantswith rapid growth and wide environmental tolerance(Mc Kinney and Lockwood 1999) and, the develop-ment of pest outbreaks (Swift et al. 1996). In the sys-tem under study, agriculture promotes a demographicincrease in C. punctulatus populations (P.J. Folgarait,unpublished), and in turn, anthills seemed to have aneffect on the vegetation, promoting the invasion ofherb weed indicator species on the anthills. Othershave also shown, changes in the patterns of vegeta-tion due to the presence of mounds in natural systems(King 1977a; Culver and Beattie 1983). Seventy per-cent of the species exclusive to anthills within anytype of land-use history, exhibited a change in theiraffinity towards anthills in different land-use areas.Therefore, land-use histories and anthill presence hadinteractive effects on plant species composition. Infact, the effect of C. punctulatus on floristic compo-sition was best captured within each plot and eachtype of land-use history, when anthill sizes were con-sidered as well as their presence/absence (Figure 2).In natural grasslands, and to some extent in aban-doned rice fields, the plant composition on anthillswas different from that off the mounds, suggestingthat these were different microsites for the plants. Forsown pastures, the floristic composition on small ant-hills was similar to that off the anthills, while mediumand large-sized anthills had their own characteristicplant community. Assuming there is a correlation be-

tween the size of the anthill and its age (Grubb et al.1969; King 1977b), we can hypothesise that a plantsuccession occurs on anthills through time becomingenriched by plant species with high affinity for ant-hills. As a result, the longer the time, the larger theanthill, and the more different the plant communityon anthills will be, as seen on larger anthills in sownpastures. Using the same line of reasoning, the floris-tic composition of small anthills should be more sim-ilar to non-anthill surroundings as less time haspassed for plant succession. Therefore, these antsseem to behave as ecosystem engineers, by changingthe habitat availability for plants.

In sown pastures, the plant community on anthillsbegan to differ from non-anthill areas only when ant-hills were of intermediate/large size. If size of anthillsrepresents different stages of plant succession, thenwe have to ask why smaller and younger anthills fromabandoned rice fields had a floristic compositionsomewhat more similar to intermediate mounds thanto non-anthill areas? In recently abandoned rice fields,anthills are found on contour lines above a height of30–40 cm off the ground. The median height of smallanthills ranges from 10 to 20 cm, depending on thetype land-use history, whereas the medium size of anintermediate anthill is 45 cm for sown pastures (P.J.Folgarait, unpublished). Therefore, small anthills inabandoned rice fields had an effective height of 40 cmor more. Considering that most seeds have a second-ary lateral dispersion phase after they reach theground, the presence of an anthill could represent anobstacle that might affect such lateral transport ofseeds over the ground. If this was the case in our sys-tem, then small anthills built on the ground and areasoff anthills might offer similar resistance to the lat-eral movement of seeds. However, small anthills builton top of contour lines (thus with a greater overallheight) and intermediate or large anthills probably re-present greater barriers for the lateral movement ofseeds. Therefore, the added height from contour linesmay be the reason why small anthills in abandonedrice fields had a floristic composition somewhat simi-lar to larger size-categories. If this hypothesis is true,then we could speculate that a plant succession istriggered by a particular anthill size. The possibilitythat C. punctulatus carried seeds has been disprovedin feeding choice experiments (Gorosito et al. 1997),and no elaiosomes were found in the known seedsfrom our plant list (P.J. Folgarait, unpublished).Therefore, we do not believe that seeds were trans-ported to the mounds by ants.

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Soil characteristics, floristic composition, land-usehistory type, and anthills

Soils from C. punctulatus anthills were more fertilethan soils off the mounds (Figure 3). Other studieshave also shown increases in K, P, and N in moundsof other ant species (Salem and Hole 1968; Czerwin-sky et al. 1969; Petal 1978; Mandel and Sorenson1982). In Corrientes, Argentina, farmers have noticedthat greater crop yields are reached in plots full ofdispersed anthill soil and this effect has also beensuggested for anthills made by other ant species (Th-omas 1962; Woodell and King 1991). In fact, Setariasphacelata plants grown in pots with anthill soil ex-hibited significantly greater productivity than thosegrown in non-anthill soil with the addition of fertilis-ers (P.J. Folgarait, unpublished). Some observationsalso suggest that Setaria sphacelata decomposesfaster on anthills than off them (Folgarait and Somma,unpublished), indicating that soil functioning is af-fected by anthill soil. This information suggests thatC. punctulatus behaves as an ecosystem engineerchanging the availability of resources for other organ-isms. Although, in general, increasing levels of agri-cultural disturbance reduce soil fertility (Daily et al.1997), in our system some of this fertility may be re-stored by the presence of C. punctulatus, as our soilanalyses suggest that the effect of C. punctulatus onsoil properties was consistent among land-use histo-ries.

Some studies have attempted to associate changesin plant composition between anthills and surround-ings with concomitant changes in soil characteristics(Gentry and Stiritz 1972; Rogers and Lavigne 1974;Beattie and Culver 1977; Culver and Beattie 1983;Carlson and Whitford 1991). However, no clear pat-terns have emerged (but see King (1977b)). We ran acanonical correspondence analysis on our data in or-der to explain the variation in floristic composition onand off anthills and across land-use types based onsoil variables. The first two axes of the canonical cor-respondence analysis explained only a 33% of thevariation in plant composition using soil characteris-tics as explanatory variables (Folgarait et al. 1997), acomplementary evidence that changes in soils con-trolled by C. punctulatus have an indirect impact on

community composition probably because it is medi-ated by the differential species availability and thestage of plant succession in each land-use history.Mitchell et al. (1997) have shown that different suc-cessional plant species that invaded heathland siteswere associated with different levels of soil nutrients.It may be possible that intermediate and large C.punctulatus anthills were relatively more fertile thanyoung mounds and that the differences in the plantcommunity on and off the anthills were related to adifferential response by plant species to the nutrientstatus of the microsite.

In summary, at the landscape level, land use his-tory explained most of the variation recorded in flo-ristic composition whereas anthills seemed to be re-sponsible for most of the variation observed in soilcharacteristics. Within each type of land use history,the presence and size of anthills also explained partof the variation detected in the plant community. Wepropose that plant succession occurs on anthills insuch a way that big mounds, above 40 cm height, be-come enriched with plant species, especially herbweeds, which are indicators of anthills.

Acknowledgements

We are indebted to G. Zipeto, P. Zapata, C. Benítezwho helped in the field with data collection; C. Beni-tez’s help with plant identifications was invaluable.We should like to thank the staff of the AgriculturalExperimental Station of INTA-Mercedes, particularlyto C. Frick, O. Royo-Pallarés, and F. Arias for theircontinual support and logistic help. We also thank theowners of the establishments: Aguacerito, El Altillo,Encarnación, Itaá Caabó, Manduré, Napenay, Timbó,Usandizaga, and Yuquerí for allowing us to gather thedata at their farms. We thank M. Aizen and J.P. Rossifor reading the manuscript, and especially S. Emer-son, E. Chaneton, S. Torti, and two anonymous re-viewers for their thoughtful comments and editorialhelp which greatly improved the manuscript. Thiswork was funded by Fundación Antorchas (grant13219/1 to PJF) and by the International Foundationfor Science (grant c/2437-1 to PJF).

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Table A1. A list of plant species, with known associated traits (blanks represent unknown), recorded across types of land use history. Exoticspecies are marked with*. Longevity: P = perennial, A = annual; Habit: P = postrate, E = erect; Type: G = grasses, H = herbs, S = shrubs;Growing season: C = cold, W = warm; Forage value: F = fine, S = soft, H = hard, O = ordinary, W = weed. Anthills’ column shows at whichland-use history type (R = abandoned rice fields, P = Pangola, S = Setaria, and NG = natural grassland) there was (HA) or low (LA) affinityfor anthills by the anthill indicator species criterium. Land-use history column shows at which land–use history type a plant species had ahigh affinity for it according to the indication species criterium.

Species Family Longevity Habit Type Growing

season

Forage

value

Anthills Land-

use

history

Adesmia punctata Fabaceae P P G C F P

Andropogon lateralis Poaceae P E G W O NG

Andropogon selloanus Poaceae P E G W O NG

Apium leptophyllum Apiaceae P E H C W HA: P. NG P

Arachis villosa Fabaceae P P H W O

Aristida venustula Poaceae P E G C O NG

Aster squamatus Asteraceae P E H W W HA: R, S, P P

Axonopus affınis Poaceae P P G W S R

Axonopus argentinus Poaceae P P G W S NG

Axonopus compresus Poaceae P P G W S

Baccharis coridofolia Asteraceae P E H W W NG

Baccharis notosergila Asteraceae P E H W W

Borreria verticiliata Rubiaceae P E H W

Bothrichloa laguroides Poaceae P E G W S NG

Briza sp. Poaceae P E G C R

Bulbostylis sp. Cyperaceae A P G W

Chaptalia piloselloides Asteraceae P P H C W

Chevreulia acuminata Asteraceae P P H C W

Chloris polydctyla Poaceae P E G W O LA: S S

Coelorhachis selloana Poaceae P E G W S S

Commelina virginica Comelinaceae P E H W

Coniza bonariensis Asteraceae A E H W W R

Cuphea glutinosa Lythraceae H W

Cynodon dactylon* Poaceae P P G W O R

Cypella herbetii Iridaceae E H W

Cyperus luzolae Cyperaceae P P G W H R

Desmanthus depresus Fabaceae P P H W O HA: S, P S

Desmodium incanum Fabaceae P P H W S LA: P NG

Deyeuxia splendens Poaceae P E G W O

Dichantrum aristatum* Poaceae P P G W F R

Dichondra repens Convolvulaceae P P H C W HA: S S

Digitaria decumbens* Poaceae P P G W F LA: P P

Dorstenia brasiliensis Moraceae P P H W

Echinochloa sp.* Poaceae A E G W W

Eleocharis bonariensis Cyperaceae E G W R

Eleocharis nodulosa Cyperaceae E G W R

Eleocharis virens Cyperaceae P G W P

Eleusine tristachya* Poaceae P P G W O S

Elyonorus muticus Poaceae P E G W H P

Eragrostis airoides Poaceae P E G W O R

Eragrostis bahiensis Poaceae P E G W O

Eragrostis lugens Poaceae P E G W O LA: S S

Eragrostis neesii Poaceae P E G W O S

9

Table A1. Continued.

Species Family Longevity Habit Type Growing

season

Forage

value

Anthills Land-

use

history

Eryngium sp1 Apiaceae P E H W W

Eryngium sp2 Apiaceae P E H W W

Eryngium echinatum Apiaceae P P H C W P

Eryngium nudicaule Apiaceae P P H C W S

Eryngium paniculatum Apiaceae P E H W W HA: NG NG

Eryngium buniifolium Asteraceae P E H W W P

Eryngium cristiaenum Asteraceae P E H W W

Eupatorium sp1 Asteraceae P E H W W

Eupatorium sp2 Asteraceae P E H W W

Eupatorium sp3 Asteraceae P E H W W

Eupatorium

subaristatum

Asteraceae P E H W W S, NG

Euphorbia selloii Euphorbiaceae W NG

Evolvolus cericeus Convolvulaceae P P H W S

Evolvolus glomeratus Convolvulaceae P P H C W

Facelis retusa Asteraceae A P H C W

Fimbristylis diphilla Cyperaceae P E G O LA: S S

Gamochaeta

pensilvanica

Asteraceae P E H W R

Gerardia communi Geraniaceae A E H W S

Glandularia pulchella Verbenaceae P P H C W HA: S P

Heymia salicifolia Lythraceae P E S W

Hypochoeris

megapotamicus

Asteraceae P P H W HA: S S, P

Indigofera asperifolia Fabaceae P P H W S NG

Kummerowia striata* Fabaceae A E H W F S

Leersia hexandra Poaceae P P G W F R

Lepidium aletes Brassicaceae A E H C W

Ludwigia uruguayense Onagraceae P P H W R

Luziola leiocarpa Poaceae P P G W F R

Mecardonia

montevidensis

Scrophulariaceae P P H W W

Melochia parvifolia Esterculareaceae P P H W W S

Micropsis dacicarpa Asteraceae A P H C W

Micropsis sp. Asteraceae A P H C W

Mitracarpus

megapotamicus

Rubiaceae P P H W W LA: S S

Modiolastrum

malvifolium

Malvaceae P P H W P

Oriza sativa* Poaceae A E W R

Oxalis sexenata Oxalidaceae P P H C W P

Panicum demisum Poaceae P E G W S R

Panicum miliodes Poaceae P E G W S LA: S R

Panicum pilcomayensis Poaceae P E G W O

Paspalum alnum Poaceae P P G W F LA: S, CN R

Paspalum dilatatum Poaceae P P G W F R

Paspalum modestum Poaceae P P G W F R

10

Table A1. Continued.

Species Family Longevity Habit Type Growing

season

Forage

value

Anthills Land-

use

history

Paspalum notatum Poaceae P P G W S LA: R NG

Paspalum pauciciliatum Poaceae P E G W F

Paspalum plicatulum Poaceae P E G W O

Paspalum quadrifarium Poaceae P E G W H

Paspalum urvellei Poaceae P E G W S R

Phaffıa lanata Amarantaceae P E H W W HA: NG NG

Phaffıa sp. Amarantaceae P E H W S

Piptochaetium

montevidensis

Poaceae P E G C F LA: P R

Piptochaetium stipoides Poaceae P E G C S LA: P P

Plantago paralias Plantaginaceae P P H W HA: R, P, NG P

Pluchea sagitalis Asteraceae P E H W W

Polygala australis Polygalaceae A H C W NG

Polygala pulchella Polygalaceae A H C W P

Polygonum punctatum Polygalaceae P P H W W R

Pratia oderacea Campanulaceae P P H W R

Pterocaulon

polystachyum

Asteraceae H W P

Pterocaulon

subvaginatum

Asteraceae P E H W LA: S S

Rebulnium richardianum Rubiaceae P E H W HA: S S

Rhynchospora

megapotamica

Cyperaceae P E G C O P

Rhynchospora praecinta Cyperaceae P E G C O LA: S, NG S, NG

Rhynchospora tenuis Cyperaceae P E G C O NG

Ruellia morongii Acantaceae W NG

Schizachyrium

microstachyum

Poaceae P E G W O S

Scoparia montevidensis Scrophulariaceae P E H W W S

Scutelaria racemosa Labiatae E H W HA: R, P R, P

Setaria geniculata Poaceae P E G W O R, P

Setaria sphacelata* Poaceae P E G W F HA: S S

Sida rombifolia Malvaceae P E H W W S

Sisyrinchium pachyrizm Iridaceae P E W S

Solanum commersonii Solanaceae P H W W

Soliva pterosperma Asteraceae A P H C W

Sorghastrum agrostoides Poaceae P E G W H NG

Spilantes stolonifera Asteraceae P P H C W HA: P P

Sporobolus indicus Poaceae P E G W O LA: S, P, NG S

Staelia thymoides Rubiaceae P H W P

Stenandrium trinervis Acantaceae P H W

Stipa neesiana Poaceae P E G C S

Tragia geraniifolia Euphorbiaceae P E H W S

Tridens hackelli Poaceae P E G O R

Trifolium polymorphum Fabaceae P P H C F

Verbena filiformis Verbenaceae H W HA: R, NG P

Vernonia flexuosa Asteraceae P E H W S

11

Table A1. Continued.

Species Family Longevity Habit Type Growing

season

Forage

value

Anthills Land-

use

history

Whalembergia

linaroides

Campanulaceae P E H W

Nomenclature follows Burkart 1969–1978.

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