Ecography 33: 538 544, 2010 doi: 10.1111/j.1600-0587.2009.05875.x # 2010 The Authors. Journal compilation # 2010 Ecography Subject Editor: John R. Spence. Accepted 21 July 2009
Developmental changes in factors limiting colony survival and growth of the leaf-cutter ant Atta laevigata
Ernane H. M. Vieira-Neto and Heraldo L. Vasconcelos
E. H. M. Vieira-Neto ([email protected]) and Heraldo L. Vasconcelos, Inst. de Biologia, Univ. Federal de Uberlaˆndia (UFU), C.P. 593, 38400-902, Uberlaˆndia, MG, Brazil. (Present address of E. H. M. V.-N.: Dept of Wildlife Ecology and Conservation, Univ. of Florida, Gainesville, FL 32611-0430, USA).
Many species of leaf-cutter ants (Atta and Acromyrmex) increase in abundance following natural or anthropogenic disturbances in the vegetation. However, the mechanisms responsible for such an increase are still poorly understood. We evaluated the effects of nesting site and the availability of palatable forage on survival and growth of Atta laevigata colonies at different developmental stages. Foundress queens transplanted into man-made clearings (dirt roads) had a much higher survival than those transplanted into the adjacent undisturbed savannah vegetation. Similarly, incipient colonies (]3-months old) had significantly greater survival and growth rates in dirt roads. In contrast, nesting site did not influence performance of young colonies (]15-months old). Both incipient and young colonies responded strongly and positively to experimental supplementation of palatable forage, and this effect was independent of the nesting habitat. Colonies that received extra food grew faster and had a significantly greater survival rate than control colonies. These results suggest that performance of A. laevigata is affected by the generally greater availability of suitable nesting sites and palatable vegetation in disturbed habitats. This may explain how these ants maintain high densities in these habitats, and since the relative importance of these factors changed with colony ontogeny, our findings highlight the importance of evaluating potential limiting factors throughout the full range of an organism’s developmental stages.
Several mechanisms can potentially affect the performance of ecosystem properties (Costa et al. 2008). Many leaf-cutter individuals and, ultimately, regulate natural populations ant species increase in abundance following natural or (Murdoch 1994). However, different mechanisms may anthropogenic disturbances in the vegetation (reviewed in operate at different life stages (Wilbur 1980, Jonsson and Wirth et al. 2008). However, the mechanisms driving these Ebenman 2001). For instance, colonies of most ant species increases are poorly understood. are founded by solitary queens and must pass through a series Because many plants in undisturbed habitats have of developmental stages before reaching maturity (reviewed effective defence mechanisms against leaf-cutter ants in Ho¨lldobler and Wilson 1990). Mortality is typically much (Hubbell et al. 1984), palatable plants are relatively rare. higher for colonies in the early stages and therefore the forces In contrast, disturbed habitats are dominated by pioneer acting on these colonies are likely to differ from those vegetation, which are more palatable to both mature affecting older colonies (Wetterer 1994). Studies that (Farji-Brener 2001) and young (Wetterer 1994) leaf-cutter account for different stages of colony development are colonies. The higher availability of palatable vegetation in relatively rare and most have focused on ontogenetic changes disturbed habitats is thought to decrease foraging costs, in morphology and behaviour (Tschinkel 1988, Wetterer thus increasing the net rate of energy gain for the colony 1994) rather than on factors affecting colony survival or (Farji-Brener 2001). In contrast, others have proposed that growth. availability of nesting sites limits leaf-cutter ant popula- Leaf-cutter ants of the genus Atta and Acromyrmex are tions (Jaffe and Vilela 1989). Founding queens actively among the most prevalent herbivores of the Neotropics, search for clearings in the vegetation to land and establish consuming far more vegetation than any other group of a new colony (Vasconcelos 1990, Vasconcelos et al. 2006). animals with comparable taxonomic diversity (Fowler et al. Human disturbance in vegetation provides new clearings 1989, Ho¨lldobler and Wilson 1990). In addition to and thus facilitates establishment of new leaf-cutter ant impacting plant communities, leaf-cutter ants transfer colonies (Jaffe and Vilela 1989, Wetterer 1994). tons of plant biomass below ground and through these Although these two hypotheses have permeated the activities can alter the spatiotemporal dynamics of carbon ecological literature for more than three decades (Rockwood stocks, nutrient availability, susceptibility to fire, and other 1973, Jaffe and Vilela 1989, Vasconcelos 1990, Wetterer
538 1994, Farji-Brener 2001, Wirth et al. 2007), they have abandoned dirt road (hereafter ‘‘dirt roads’’). These latter never been addressed using field experiments. Most sites were ca 4 m wide and ca 2 km in length. Soon after evidence of food limitation in leaf-cutter ants is based on mating flights (14 November 2005 and 17 November measures of the relative availability of pioneer vegetation 2006) we collected queens that had just settled on the (Wetterer 1994, Farji-Brener 2001). Although such mea- ground and placed them in polyvinyl chloride (PVC) tubes sures of natural resource availability can be useful, they may (20 cm in height and 10 cm in diameter; open at both ends) be inaccurate because not all available resources are edible. that had been placed in plots haphazardly spread within the In contrast, experimental supplementation of food can two study habitats prior to the flight. We used a plot design, reveal the existence of food limitation (Merriman and Kirk instead of randomly spreading tubes in the sites, to be able 2000). The purpose of this study was to assess the relative to calculate claustral survival as a continuous rather than a importance of nesting habitat and the availability of binary value. Plots were either square- or rectangular-shaped palatable forage for Atta laevigata colonies. Our main with 4 8m2 in area, depending on the number of PVC questions were: 1) do nesting site and food supplementation tubes placed in it (5 8 tubes, with 2-m spacing). Each plot affect the survival and/or growth of A. laevigata colonies? was separated from the other by a minimum distance of 2) Are these effects dependent upon colony developmental 50 m. We took digital photographs of the canopy (cf. stage? Engelbrecht and Herz 2001) in each plot, with the camera fixed on a tripod 0.5 m above the ground, and used these to measure canopy openness. The PVC tubes had been sunk Material and methods 3 cm into the soil, after removal of any debris from the soil surface. All tubes were covered with a nylon mesh (2 Study site and species 2 mm) to protect the queens from predation by scarabeid beetles (Vasconcelos et al. 2006). The following day, we We conducted this study at the Estac¸a˜o Ecolo´gica do Panga checked all tubes to determine which queens had built a (19810?S, 48823?W), a 404-ha reserve located 30 km south new nest and sealed its entrance with soil or died. After two of Uberlaˆndia, in Brazil. Our observations and experiments months, we inspected each tube (which were not removed) were conducted in the southern portion of the reserve, every week for 8 weeks to determine which colonies which is covered by a woodland savannah (locally known as survived the claustral phase. This experiment was performed cerrado sensu stricto). The area has a canopy cover of 619 in two consecutive years. A total of 170 queens were 2% (mean9SE, based on 60 measurements with a spherical transplanted to 11 plots in the dirt roads and to 22 plots in densiometer) and a sparse cover of grasses and herbs. The the savannah vegetation in 2005, whereas in 2006 a total of tree and shrub canopy reaches a height of ca 6 m. 175 queens were transplanted to 11 plots in dirt roads and Atta laevigata is the most common leaf-cutter ant species to 24 in the vegetation. at this reserve (Costa et al. 2008). As is typical for other Atta species, a new colony of A. laevigata is founded after a mated queen finishes digging her nest (up to 15 cm deep into the soil) and seals its entrance with soil removed during Survival and growth of incipient and young colonies nest building. After that, the colony enters into what is Using naturally established colonies of A. laevigata (i.e. known as the claustral phase, which lasts for about three colonies not used in the experiment above), we performed a months. During this period the nest entrance remains factorial experiment to test the effects of nesting site (dirt completely sealed, and the queen raises her first brood and roads vs savannah vegetation) and food supplementation grows a new fungus culture using nutrients derived from her (with or without extra fungal substrates) on the survival and wing muscles and fat reserves. The claustral phase ends as soon as the first ant workers emerge and start foraging growth of colonies ca 3-month old (hereafter ‘‘incipient’’) outside the nest. At this time, small pellets of soil are and ca 15-month old (hereafter ‘‘young’’) after establish- deposited by the ants around the nest entrance forming a ment. Colony age was estimated based on the above dates of small, circular mound of ca 2 cm in diameter. More soil is nuptial flights in 2005 and 2006. A total of 258 incipient deposited on the nest mound as the ants enlarge the initial (119 in roads and 139 in the vegetation) and 111 young nest chamber. A second chamber, however, is only built colonies (71 in roads and 40 in the vegetation) were when the colony is approximately one year old. This randomly marked across both sites in late January 2007. All chamber is much larger than the first one and is located marked colonies were at least 5 m from each other. We determined the initial size (volume of excavated soil ‘‘v’’ in deeper (ca 1 m) into the soil. Its construction is followed by 3 a rapid and noticeable increase in nest mound size due to cm ) of each nest mound using the formula for a half- the deposit of soil excavated from the new chamber. ellipsoid (v 4 p r1 r2 h/6), where ‘‘h’’ is the Therefore, based on nest mound size, it is possible to height and ‘‘r1’’ and ‘‘r2’’ are the maximum and minimum distinguish colonies that are less than one year old from radius of the mound. those that are older. About half of the colonies from each habitat type were randomly assigned to each dietary treatment (with or without a food supplement). This food supplement was Colony survival at the claustral phase composed of a mixture (1:1) of oat and corn flakes, chosen because they are very attractive to leaf-cutter ants and could We determined the survival rate of claustral colonies in be obtained year-round. The availability of young leaves undisturbed savannah vegetation and in human-made (often preferred in natural settings) varies much during the clearings, including two fire break corridors and an year. To facilitate retrieval by the small workers characteristic
539 of the incipient colonies, flakes were finely milled. Incipient completing excavation of nests and hence were not included colonies were supplied with 45 g of milled corn and oat in the following analyses. Among queens that successfully flakes once a week, whereas 90 g were offered to young excavated a new nest ca 40% survived the claustral phase colonies. This is more than two times the average plant (2005 43.7%, 2006 34.5%). Survivorship at the claus- biomass consumed daily by a young colony (41.398.2 g, tral phase was significantly greater in dirt roads than in the fresh weight, n 5 colonies) and about six times more vegetation, and this effect was detected during both study the biomass consumed by an incipient colony (7.193.5 g, years (Fig. 1). In 2005 the number of colonies that survived n 6, Vieira-Neto unpubl.). Corn and oat flakes were the claustral phase was two times greater in dirt roads than in poured directly into the nest entrance of each colony to the vegetation (U 221.5; n1 11, n2 22; pB0.001), avoid robbery by other ants. This experiment lasted for one while in 2006 it was approximately 1.5 times greater (U year, and during this period colony survival was determined 207.5; n1 11, n2 24; p 0.007). In addition, within the at 4-month intervals. Colonies were considered dead if there savannah vegetation colony survival was inversely propor- were no signs of ant foraging or nest building activities tional to canopy cover (2005: rs 0.533, n 22; 2006: rs during at least two consecutive surveys. 0.672, n 24, pB0.01 in both cases). As previous Atta studies have shown a positive relation- ship between colony age/size and nest mound size (Hernandez et al. 1999), we determined the growth of Survival and growth of incipient colonies all living colonies by comparing the initial nest size and the size after 8 months of experimental treatment. It was Of the 258 incipient colonies marked in 2007, only 26.7% not possible to compare growth beyond one year since at were still alive one year later (Fig. 2a). The full survival that time most colonies that had no food supplementation model for incipient colonies was strongly significant (like- were dead. lihood-ratio statistic 54.07, DF 3, pB0.001). Colony survival during this period was influenced by both nesting site and food supplementation. Colonies that received a Statistical analyses food supplement had a significantly higher survival rate than those that did not (x2 3.034, p 0.002). Simi- We used the Mann-Whitney U-test to determine the effect larly, and irrespective of the food treatment (habitat of nesting site on colony survival during the claustral phase supplementation interaction, p 0.463), colonies located based on the proportion of surviving colonies in each plot. along the dirt roads had a higher survival than those in the We also evaluated the relationship between tree-canopy vegetation (x2 4.133, pB0.001). However, the effect openness and survival of claustral colonies in the savannah of the food supplementation was stronger than the effect of vegetation using Spearman non-parametric correlations. nesting site. While the chances of survival for colonies in the Data from different sampling years were analyzed separately. savannah vegetation decreased 68% relative to those in the Logistic regressions were used to evaluate the effects of dirt roads (odds-ratio 0.32), colonies not supplied with nesting site and food supplements on the survival odds of fungal substrates had an 83% smaller chance of survival incipient and young colonies. The response variable was the compared to treatment colonies (odds-ratio 0.17). number of colonies alive (coded as ‘‘1’’) or dead (coded as Growth of incipient colonies was strongly increased by ‘‘0’’) after 12 months. Nesting site (0 vegetation, 1 dirt food supplements (F 28.84, pB0.001), but unaffected roads) and food supplementation (0 without, 1 with) 1, 97 were treated as independent categorical variables. The significance of individual independent variables was tested by the Wald x2 statistic, while model goodness-of-fit was determined by the likelihood-ratio test. The magnitude of the effect of the independent variables was determined by interpretation of the odds-ratio, which indicates how much each factor changes the odds of colony survival (Tabachnick and Fidell 2007). Finally, to determine if nest site and food supplements affect growth of incipient and young colonies, we per- formed a two-way ANCOVA, using nest mound size after eight months (in cm3) as the dependent variable, nesting site and food supplementation as categorical factors and initial nest size as the covariate. Data on nest sizes were log- transformed (log10 x 1). Data for incipient and young colonies were analyzed separately.
Results
Colony survival at the claustral phase Figure 1. Percentage of colonies surviving the claustral phase in two contrasting nesting sites (dirt roads and woodland savannah). In total 345 queens were experimentally transplanted. About Box-plots in grey represent colonies observed in 2005, while in 19% of these (2005 21%, 2006 17%) died before white are those observed in 2006.
540 Discussion
To our knowledge this study represents the first experi- mental evaluation of the widely accepted hypothesis explaining increased leaf-cutter ant abundance in disturbed habitats. Our results indicate that the survival and growth of A. laevigata colonies is affected both by nesting site and food supplementation. Furthermore, we demonstrate that there is a developmental change in factors affecting colony survival, reinforcing the view that in ants different life stages can be limited by different factors.
Nesting site limitation
Colonies at both the claustral and incipient phases survived much longer in dirt roads than in the adjacent undisturbed savannah, whereas once colonies reached the young phase subsequent survival was not significantly affected by nesting site. Several mechanisms may explain the greater survival of claustral and incipient colonies in dirt roads. One possibility
Figure 2. Effects of nesting site (dirt roads and savannah vegetation) and experimental food supplementation (with or without a weekly supplement of food) on the survival of (a) incipient and (b) young A. laevigata colonies. by nesting site (F1, 97 0.67, p 0.416). The interaction between nesting site and food supplementation was only marginally significant (F1, 97 3.61, p 0.061). Overall, colonies that received additional food grew on average 3.3 times faster than those that did not receive (Fig. 3a).
Survival and growth of young colonies
Of the 111 young colonies marked in 2007, only 29.7% were still alive one year later (Fig. 2b). The full survival model for young colonies was only marginally signifi- cant (likelihood-ratio statistic 7.39, DF 3, p 0.060). Survival of young colonies was significantly affected by food supplementation (x2 2.271, p 0.023) but not by nesting site (x2 0.020, p 0.984), and there was no interaction between these two factors (p 0.660). The chances of survival for colonies not supplied with food were 72% lower than that of supplied colonies (odds-ratio 0.28). Similarly, food supplements (F1, 38 14.03, pB0.001) Figure 3. Mean (9SE) nest mound size of incipient (a) and but not nesting site (F1, 38 1.20, p 0.280) affected the growth of young colonies. The interaction between nesting young (b) A. laevigata colonies located in dirt roads and in the savannah vegetation 8 months after the beginning of the food site and food supplementation was also not significant supplementation experiment. Grey bars represent colonies that (F1, 38 0.37, p 0.548). Overall, colonies receiving a received a weekly supplement of oats and corn flakes and white food supplement grew 4 to 6 times faster than control bars represent control colonies. Data on nest mound size are log10 colonies (Fig. 3b). (x 1) transformed.
541 is that habitat affects predation rates. Armadillos are Rockwood (1973) argued that mature Atta colonies are important predators of small Atta colonies in some sites absent from deciduous forests due to the limited availability (Rao 2000), but during the period of this study we never of suitable vegetation in these areas during the dry season. registered any attacks by armadillos on our focal colonies. Similarly, the greater abundance of Atta nests in early Although the army ant Nomamyrmex esenbeckii is also an successional forests, along anthropogenic edges, or in small important predator of leaf-cutter ant colonies (Swartz 1998, vegetation clearings has been attributed to the higher Powell and Clark 2004), we witnessed only two raids by availability of palatable plant species in these areas N. esenbeckii on our focal colonies. However, unlike (Wetterer 1994, Farji-Brener 2001, Urbas et al. 2007, armadillo attacks, which leave excavation damage, raids by Wirth et al. 2007). Interestingly, we observed that food N. esenbeckii leave little evidence and undetected raids may supplementation had strong and positive effects on the have occurred. Nonetheless, since army ants forage over survival and growth of A. laevigata colonies but did not relatively large areas it is unlikely that differential predation detect a significant interaction between the effects of food pressure could account for the differences between the two supplementation and nesting site. This was surprising given habitats we studied since colonies in both habitats were only that the availability of suitable vegetation, and perhaps the a few meters apart from each other. Consistent with this view intensity of competition for food among colonies, was is the fact that nesting site only affected the survival of thought to be greater in dirt roads than in the undisturbed claustral and incipient colonies, even though young colonies savannah vegetation (cf. Wetterer 1994). Therefore, we had are as likely to be raided by army ants as those from earlier expected to find a proportionally greater effect of food developmental stages (Rao 2000). supplementation on colonies located in the undisturbed Alternatively, differences in abiotic conditions may have areas, but this was not the case (Fig. 3). This suggests accounted for the observed habitat differences in colony that differences in plant resources for leaf-cutter ants survival. In the tropics, clearing of vegetation increases soil between disturbed and undisturbed savannah habitats may density and decreases soil porosity, thus altering soil not be as great as are those between disturbed and properties and, consequently, water flow (Reiners et al. undisturbed tropical forests (Wetterer 1994, Farji-Brener 1994). These changes in soil conditions likely influence 2001, Pen˜aloza and Farji-Brener 2003). ground-nesting species that often select habitats providing Food limitation has been detected in some other insects. enhanced structural and microclimatic conditions to their For instance, ants in the genus Formica showed higher survival and reproduction rates when extra food was offered nests (Ryti and Case 1986). For instance, the ant species (Deslippe and Savolainen 1994), while effects of food Paraponera clavata nests in drier soils and thereby avoids the limitation on ant communities were detected for Mediter- detrimental effects of excessive water in the nest (Elahi ranean ants (Arnan et al. 2007). Similarly, carabid beetles 2005). Similarly, excessive water can have a detrimental (Lenski 1984), grasshoppers (Oedekoven and Joern 2000), effect on leaf-cutter nest survival and has been suggested damselflies (Dmitriew and Rowe 2005), and gerrids that flooding of the nest chamber is the major cause (Spence 1986) were positively affected by food addition. of mortality during the claustral phase (Autuori 1950). Our study of A. laevigata demonstrates food limitation both In addition, vegetation clearings may provide a better for incipient and young colonies, even though colonies at microclimate for development of the colonies and in these different developmental stages employ different particular of the symbiotic fungus, which requires elevated foraging behaviours and forage on different substrates. temperatures (ca 258C) and humidity for optimum growth Incipient A. laevigata colonies, in contrast to young and (Powell and Stradling 1986, Roces and Kleineidam 2000), mature colonies, do not cut leaves directly from the plant since temperature and soil humidity (at 15 20 cm of soil crown. Instead, they rely on pieces of organic material depth) is often greater in clearings than in shaded areas available on the ground, including especially small seeds (Vitousek and Denslow 1986, Becker et al. 1988). There- and flowers, bird faeces, and fragments of dead dry leaves fore, the relationship between colony developmental stage (Vieira-Neto unpubl.). Thus, food limitation appears to be and effect of nesting habitat may relate to nesting depth. a generally important feature of developing leaf-cutter ant Nests of young colonies are located more deeply in the soil ecology in savannah habitats. It is uncertain if colonies that than are those of claustral and incipient colonies and at reach the reproductive phase are also food limited, and these depths abiotic differences between soils of the dirt further studies should evaluate the effect of food addition roads and those of the savannah vegetation are likely to on these colonies. diminish.
Conclusions Food limitation Although we demonstrate that nesting sites and food The availability of plant resources has long been suggested supplements strongly influence survival of A. laevigata as a major factor influencing the density and distribution of colonies, further studies are necessary to determine how herbivores, including leaf-cutter ants. However, studies changes in these resources actually affect the demographic demonstrating resource limitation of insect herbivores patterns of leaf-cutter ant populations. Changes in the through experimental food supplementation are rare (but performance of early life stages, such as those we detected see Oedekoven and Joern 2000). here in response to variation in nesting habitat and food
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