Microsoft Word - 25-Bio_27339- 1501 Original Article Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 TEMPORAL DYNAMIC OF FORAGING OF EPIGEIC ANTS IN AN URBAN FOREST FRAGMENT DINÂMICA TEMPORAL DO FORRAGEAMENTO DE FORMIGAS EPIGÉICAS EM UM FRAGMENTO FLORESTAL URBANO Denise LANGE 1 ; Andréa A. VILELA 2 ; Graziella D. V. M. ERDOGMUS 1 ; Andréia B. BARBOSA 3 ; Suelen C. COSTA 3 ; Vanessa STEFANI 1 1. Pós-Doutoranda, Universidade Federal de Uberlândia, LECI (Laboratório de Ecologia, Comportamento e Interações), Uberlândia, MG, Brazil; 2. Doutoranda. Pós-Graduação em Ecologia e Conservação de Recursos Naturais. Universidade Federal de Uberlândia, LECI (Laboratório de Ecologia, Comportamento e Interações), Uberlândia, MG, Brazil; 3. Bióloga, Universidade Presidente Antônio Carlos, Campus Araguari, Araguari, MG, Brazil. ABSTRACT: The present study aimed to investigate the foraging dynamic of an ant community in an urban semideciduous mesophitic forest. A total of 4,297 individuals, distributed in 23 species, seven genera and four subfamilies were sampled in January, April, July and October of 2010. Four ant species guilds were found: leaf cutters, soil-dominant omnivores, soil and vegetation opportunists and large-sized epigaeic predators. There were no significant differences in total of species richness and abundance of individuals in samples among the months evaluated. However, there was a clear substitution (turnover) of species over the months. Nine species were sampled exclusively in the rainy period and five species were present only during the dry period. Thus, the species turnover over the months support the hypothesis that ant communities present a temporal dynamics in their foraging activities even in an urban forest fragment. In general, the abundance of ants foraging on soil was greatest during the months with greater rainfall. However, two species belonging to the guild of opportunistic ants from soil and vegetation doubled the number of foraging individuals in period during the months with less precipitation. These findings support that ant communities, independent of isolation and environment (urban or natural), have temporal dynamics that arise from factors relating to the biology and behavior of the group. KEYWORDS: Ant guilds. Cerrado. Fragmentation. Species richness. INTRODUCTION Ants constitute one of the most successful groups of insects (HÖLLDOBLER; WILSON, 1990). They are ubiquitous and diverse and their abundance has been widely recognized (ALONSO; AGOSTI, 2000; RICO-GRAY; OLIVEIRA, 2007). In tropical ecosystems, ants represent up to 80 % of animal biomass (ANDERSEN, 2000; DAVIDSON et al., 2003), and they are an example of successful colonizers of terrestrial environments (FITTKAU; KLINGE, 1973; STRINGER et al., 2009). This success may be related to their great ability to cooperate in the exploitation of natural resources, as hunters, herbivores or detritivores, and their capacity to establish symbiotic relationship with other organisms such as plants (JOLIVET, 1996; GIANOLI et al., 2008), bacteria and fungous (MUELLER et al., 2005), and other arthropods (see RICO-GRAY; OLIVEIRA, 2007). Thus, ants interact with the community in a general way, influencing the population dynamics of a great number of organisms that live there (FOLGARAIT, 1998; RICO-GRAY; OLIVEIRA, 2007). Due to the wide variety of functions that ants play, the composition and abundance of their assembly are associated with floristic and climatic characteristics of each region (HÖLLDOBLER; WILSON, 1990), as well as environmental disturbances (CERDÁ et al., 2002; ANDERSEN et al., 2002; BRÜHL et al., 2003), which make them good bioindicators of environmental monitoring (ALONSO, 2000; ANDERSEN, 2000; SCHMIDT et al., 2013). According to Delabie and Fowler (1993), striking factors of ant communities, like structure and temporal dynamics of foraging may be influenced by modifications of environment structure, and, therefore, provide important information about conservation of a determined area. In this sense, studies have been searching to understand the impacts caused by the simplification of natural ecosystems through ant community analyses (MAJER, 1996; ANDERSEN, 2000; BROWN JR., 2000), including studies about the impact of urbanization on both structure and functioning communities (LÓPEZ-MORENO et al., 2003). Ants present a variety of strategies and places for foraging, which makes it possible to separate them into functional groups (SILVESTRE et al., 2003). In general, the activity of food search by ants can be classified by foraging stratum, naming species that forage over the soil and litter as epigeic, those that forage on vegetation as arboreal, Received: 08/08/14 Accepted: 21/05/15 1502 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 and those that forage in the subsoil as hypogeic. In addition, there is an ant species classification according to the hierarchy of resource dominance (ant mosaic – LESTON, 1978). Each species is associated with a foraging stratum, and their individuals possess a search-for-food area that is around the nest (TRANIELLO, 1989; BELCHIOR et al., 2012). However, according to Traniello (1989), the variation in food availability relating to seasonal factors can alter the path and the distance of ants’ search for food. Beside this, the richness and abundance of a species that forage in a specific stratum may also vary. This high sensibility of ants to the environmental characteristics highlights the importance of this group for testing hypotheses about species richness (e.g. KASPARI et al., 2003) and community dynamics (BRONSTEIN, 1998; GOTELLI; ELLISON, 2002; RICO-GRAY; OLIVEIRA, 2007). In general, food production varies with seasonal rainy patterns in tropical environments. The plant resource consumers, including ants, track this production in space and time, adjusting their foraging activities with food availability (e.g. CARROLL; JANZEN, 1973; POL et al., 2011; BELCHIOR et al., 2012). In the Brazilian savannah (Cerrado), precipitation is seasonally discontinuous and yields high temporal heterogeneity in food production, primarily of vegetal origins (FRANCO, 2002). This scenario can significantly affect both patterns of foraging and feeding of Cerrado insects, including ants, during the whole year (YAMAMOTO; DEL-CLARO, 2008; MARQUES; DEL-CLARO, 2010; BELCHIOR et al., 2012). An examination of foraging patterns in a whole year allows narrowing the range of factors affecting the activity levels in assemblages of ants (HANN; WHEELER, 2002). In this sense, this study aimed to evaluate the dynamics of epigeic ant community foraging in an urban forest fragment looking for changes in foraging patterns due to temporal variations. The hypothesis is that ant communities vary throughout the year in relation to abundance of individuals, richness and composition of species. Besides, it is expected a turnover of species over the months and that in periods with lower precipitation occur a greater number of species due to decrease of food availability and the intensification of foraging activity. MATERIAL AND METHODS The present study was carried out in Parque Municipal Bosque John Kennedy (PMBJK), a municipal park located in the urban perimeter of Araguari city (48°11’19” W and 18°38’35” S) in the state of Minas Gerais, Brazil. The park area of 11.2 ha is occupied by a primary and secondary semideciduous mesophitic forest with trees up to 25 m high. Its vegetal community is similar to the native reserves of the region; that is, it possesses closed areas, with high trees and a dense canopy, next to gaps that are forming and in a recovering phase. Despite being an urban forest subjected to anthropic actions, according to Araújo et al., (1997), and Souza and Araújo (2005), the PMBJK still retains a high natural floristic diversity. As shown in Fig. 1, the study region presents two distinct periods: a rainy period with high temperatures (January, February, and October to December) and another period that is drier with low temperatures (March to September). Figure 1. Mean temperature (°C) in bar and monthly precipitation (mm) in line during 2010, from the nearest city of Araguari, Minas Gerais, Brazil. 1503 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 In sampled months (January, April, July and October of 2010), 50 pitfall traps were distributed in 10 parallel rows, distant at least 50 m from each other. In each row, traps were separated 10 m from each other. In all sampled period, the rows were randomly distributed throughout the area of the PMBJK. In order to achieve the study’s goals, all traps were placed at the same points in the four samplings. The traps consisted of a plastic pot of a volume of 1 L and diameter of 15 cm filled with 200 ml of alcohol to 70 %, 5 ml formol to 10 % and liquid detergent (added to break the surface tension of the solution). Each trap was covered with a plastic cover located 7 cm above the pot edge and sustained by wooden sticks. After 5 days of permanence in the field, the traps were removed and the material was sorted in Petri dishes with the aid of a stereo microscope. Then, the ants were identified using keys of Bolton (2003) and after separated by guilds according to the methodology for Cerrado species by Silvestre et al., (2003). After these proceedings, specimens were deposited in the reference collection of the Laboratório de Zoobotânica da Universidade Presidente Antônio Carlos (UNIPAC), Campus Araguari, Minas Gerais, Brazil. Climatic data (temperature and precipitation) were obtained in the climatology station nearest the study area, in Universidade Federal de Uberlândia, in Uberlândia, Minas Gerais, located 30 km from the PMBJK. The pitfall traps method was chosen due to their efficiency for capturing ants are rarely sampled through traditional methods of active search. In addition, these traps allow uniform sampling of individuals that forage during day and night. As the objective of this study was not to measure the ant diversity of fragment, but the temporal variation of foraging in one local inside of the fragment, the collection method using pitfall traps was sufficient. EstimateS software version 8.2 (COLWELL, 2013) was used to generate species accumulation curves in terms of the sampling effort employed. The estimated species richness was calculated for each area using the Jackknife 2 index. This index is based on the numbers of species that occur only once in a sample and those occurring twice. In order to analyze the data, each sample corresponded to a row including five traps, totaling 40 samples evaluated to the end of the study period. Analysis of variance (ANOVA) for repeated measures was used to compare both individual abundance and species richness among the four months. The analysis was carried out using the Systat 13.0 program. A log(x+0.5) transformation was first applied to the data of ant abundance to normalize the data. In addition, to verify the similarity among the months sampled the Bray- Curtis index was used, starting from a matrix of individual abundance for each ant species using the program BioDiversity Professional version 2. RESULTS A total of 4,297 individuals were sampled, belonging to 23 ant species, seven genera, and four subfamilies (Table 1). Analyze of the accumulated richness curves (observed and estimated) indicated that sampling of the ant fauna was achieved in the second evaluation (Figure 2). This result proves that the sampling effort was satisfactory and the variations in the occurrence of species found among the months evaluated in this study are due to the temporal variation in foraging species. Table 1. Abundance and relative frequency (% in parentheses) of ant species found in trimonthly samples evaluated in the Bosque Municipal de Araguari, MG, Brazil. The letter in “Guild” column mean: (lc) leaf cutters, (so) soil-dominant omnivores, (svo) soil and vegetation opportunists, and (lep) large-sized epigeic predators. Subfamily/Species Guild January April July October Total Ponerinae Odontomachus chelifer (Latreille, 1802) lep 96(14.30) 32(8.33) 4(5.55) 8(5.88) 140(8.20) Odontomachus meinerti Forel, 1905 lep - - 20(5.55) - 20(1.64) Pachycondyla verenae Forel, 1922 lep 57(7.14) 25(8.33) 16(11.12) - 98(6.56) Pachychondyla (gp. harpax) sp 1 lep 2(7.14) - - - 2(1.64) Pachychondyla (gp. harpax) sp 2 lep 122(14.30) 36(8.33) 13(5.55) 14(5.88) 185(8.20) Ectatomminae Ectatomma lugens Emery, 1894 lep - - - 4(11.78) 4(3.28) Gnamptogenys sp 1 lep - - - 3(5.88) 3(1.64) 1504 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 Myrmicinae Pheidole megacephala (Fabricius, 1793) so - 24(8.33) - - 24(1.64) Pheidole longicornis Emery, 1888 so - - - 31(5.88) 31(1.64) Pheidole sp 1 so - - 1(5.55) - 1(1.64) Pheidole sp 2 so 55(7.14) 17(8.33) 41(5.55) 20(5.88) 133(6.56) Pheidole sp 3 so - - 178(5.55) - 178(1.64) Pheidole sp 4 so - - 40(5.55) - 40(1.64) Pheidole sp 5 so 7(7.14) - - - 7(1.64) Pheidole sp 6 so - - - 2(5.88) 2(1.64) Pheidole sp 7 so - - - 63(5.88) 63(1.64) Acromyrmex sp 1 lc 213(7.14) 16(8.33) 105(5.55) 135(5.88) 469(6.56) Formicinae Camponotus sericeiventris (Guérin- Méneville, 1838) svo 68(7.14) 9(8.33) 22(11.12) 6(5.88) 105(8.20) Camponotus lespesii Forel, 1886 svo 6(7.14) 7(8.33) 9(11.12) 1(5.88) 23(8.20) Camponotus crassus Mayr, 1862 svo 31(7.14) 217(16.68) 188(11.12) 86(11.78) 522(11.48) Camponotus gp. bidens Mayr, 1970 svo - - - 7(5.88) 7(1.64) Camponotus sp 1 svo 264(7.14) 1069(16.68) 747(11.12) 2(5.88) 2082(9.84) Camponotus sp 2 svo 6(7.14) - - 152(5.88) 158(3.28) Total abundance 838 1420 1384 526 4,297 Figure 2. Observed richness and estimated richness (Jack 2 index) of ant species found in forty samples evaluated in January, April, July and October of 2010 in the Bosque Municipal de Araguari, MG, Brazil. Out of the 15 guilds of ant species described by Silvestre et al., (2003) for the Cerrado Biome, four were found in this study: leaf cutters (Acromyrmex sp), soil-dominant omnivores (Pheidole spp), soil and vegetation opportunists (Camponotus spp), and large-sized epigeic predators (genera species of Odontomachus, Pachycondyla, Ectatomma, and Gnamptogenys) (Table 1). The guild with the highest abundance of individuals was soil and vegetation opportunists, with six species and 2,897 individuals (Figure 3). The soil-dominant omnivore guild, represented by the Pheidole genus, was the second most abundant, with 479 individuals distributed in nine species. These two guilds/genera together encompassed about 78.4 % of all the individuals collected. Both leaf cutters and large soil predators were also abundant; 469 and 452 individuals were found foraging through the year distributed in one and seven species, respectively. 1505 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 April and July presented a great abundance of individuals foraging, however, there was no significant difference among all months analyzed (F = 1.484; df = 39; p = 0.241). A similar result was observed with species richness in samples. Great values were observed in July and October but there was no significant difference among the months evaluated (F = 0.450; df = 39; p = 0.718). October presented the highest total species richness of foraging ants (15 species), followed by July and January and April (see Table 1). However, despite having no difference in richness and abundance of individuals in samples among the months, there was a clear substitution (turnover) of species over the months. Considering the 23 species collected, nine were exclusive in sampling of raining period and five species were present only during the dry period. Based on Fig. 4A, it is evident that there was a variation in foraging activities by all ant guilds found in the traps. Only 34 % of the species (eight species) were found in the four months (Table 1). The soil and vegetation opportunist guild was the most abundant group in the four samplings, constituting more than 60 % of all individuals collected in both April and July. The turnover of individuals of different guilds/species foraging in the different months resulted in a similar richness of species within all samplings (Fig. 4B). This result is evidenced in Fig. 5. In this same figure it is also possible verify a greater similarity between the months of April and July (dry period) and a greater difference between October and the other months sampled. Figure 3. Total percentage of individual abundance and species richness of four ant guilds found from January to October in 2010, in Bosque John Kennedy, Araguari, Minas Gerais, Brazil. Figure 4. Percentage of individual abundance (A) and species richness (B) of four ant guilds found during samplings carried out in 2010, in Bosque John Kennedy, Araguari, Minas Gerais, Brazil. 1506 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 Figure 5. Ant community similarity (Bray-Curtis index) among evaluations (months) carried out in 2010, in Bosque John Kennedy, Araguari, Minas Gerais, Brazil. DISCUSSION The data obtained in the present study support the initial hypothesis that ant communities show temporal variation in foraging, represented by variation in abundance of individuals of each species and by substitution (turnover) of species over the months. This turnover of species among the months resulted in lack of significant difference in total of species richness and abundance of individuals and a variation in similarity of ant fauna among the months. Ants of the soil and vegetation opportunists guild were the most frequent in the present study. These guilds have species with a large number of individuals in the nests, massive recruitment to collect food, and display high aggressive behavior, to inhibit the foraging of other species (SILVESTRE; SILVA, 2001). Further, some Camponotus species possess several adaptations for both soil and vegetation and establish mutualistic associations with plants, hemipterans and lepidopterans (OLIVEIRA; BRANDÃO, 1991; BRANDÃO et al., 2000) resulting in the success of the group in diverse environments. The soil-dominant omnivore guild, represented by the Pheidole genus in this study, was the most abundant in number of species. According to Bolton (1995), Pheidole is between the 10 richer genera in number of Formicidae species. This high species richness added to the fact that the nests have many individuals, make this genus ubiquitous in natural or disturbed environments (see ANDERSEN, 2000; BROWN Jr., 2000; WARD, 2000; LANGE et al., 2008). The great species number and low abundance found in the present study for the large- sized epigeic predator guild could be related to foraging strategy, since they have solitary foraging and nests with few individuals (SILVA; BRANDÃO, 1999; SILVESTRE, et al., 2003; VIEIRA et al., 2007). These findings, in turn, reduce the chance of finding them, compared with ant colonies with many individuals and massive foraging. The leaf cutter ant guild was represented by one species in this study, but its abundance was similar to both the soil-dominant omnivore and large-sized epigeic predator guild. Species of leaf cutter ants are exclusive to neotropical regions and their importance in these areas has been largely documented in agroecosystems where they result in great economic losses (BOARETO; FORTI, 1997; BURRATO et al., 2012). In natural environments, the leaf cutters also cause significant damage to plant communities, although, due to the presence of natural enemies, this damage is not so harmful to the whole community (BRAGANÇA et al., 2009). The major number of ants foraging during the months of low precipitation in the present study was influenced mainly by two species (C. crassus and Camponotus sp1). The other species that were found in the four samples had highest abundance in the months of rainy season (January and October). This results may be related to the foraging strategy of each species (PORTER; TSCHINKEL, 1987), to the physical barrier imposed by rain, to the efficiency of the pitfall trap during the rainy months, and to the variation of available resources (NUNES et al., 2011). According to Dos Santos et al., (2012), in the Cerrado biome, during the months with lowest precipitation, the availability and quality of food fall sharply, influencing populations directly, including some ant species (see COGNI; OLIVEIRA, 2004; YAMAMOTO; DEL-CLARO 2008). Consequently, some species that forage on 1507 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 soil and vegetation may intensify their patrolling on soil in searching for food when the resources in the vegetation are scarce. This pattern was evident in this study for C. crassus and Camponotus sp1. Other species, on the other hand, intensified their search for food during the rainy season, such as Odontomachus chelifer, Pachycondyla verenae, Pachycondyla sp2, Acromyrmex sp1, and Camponotus sericeiventris. Therefore, the hypothesis that the decrease in supply of resource intensifies the foraging for food was not evident for most of the ant community studied. One factor, which was not evaluated in this study, but may have influenced the temporal dynamics of foraging ants, is the competitive hierarchy among ant species inside and outside of intra and inter-guilds. A possible evidence of this is the fact that species with massive recruitment usually dominate the resources, inhibiting the presence of other species (SILVESTRE, 2000; PARR; GIBB, 2010). As a result, for the ant community of the present study, the highest presence of the large-sized epigeic predator guild during the period of greatest rainfall may be the temporal reflex of this hierarchy competition by food resources. In other words, the guilds with massive recruitment (the soil and vegetation opportunist guild and soil-dominant omnivore guild) may inhibit foraging in the driest period of the year and reduce this dominance in the wettest periods. Other factors influencing the foraging patterns of ant species are the reproductive period and size of the colony. Larger colonies with massive recruitment, as is the case of minor species, need constant food to maintain all individuals of the colony (TRANIELLO, 1989). Nevertheless, larger species with small colonies increase their foraging in the reproductive period, because the food demand is higher in this period (SILVESTRE, 2000). These characteristics would explain, in part, the foraging pattern observed in the present study, of species abundant in the driest period of the year, like Pheidole and Camponotus. Thus, our initial hypothesis of a temporal dynamics in activity of ants was confirmed. However, the increase in search for food occurred during the rainy season, with an exception of two species of Camponotus. Our findings highlight that ant communities, independent of isolation and environment (urban or natural), have temporal dynamics that arise from factors relating to the biology and behavior of the group. ACKNOWLEDGMENT Thank R. Pacheco for her support in the identification of ant-species. We also thank the Coordenação de Aperfeiçoamento Pessoal de Nível Superior - Plano Nacional de Pós-Doutorado (CAPES-PNPD 2556/2011 - V. Stefani; 20131340- 32006012013P7 – D. Lange) and Programa de Apoio a Projetos Institucionais com a Participação de Recém-Doutores (CAPES-PRODOC 2651/2010 - G. Marques Erdogmus) and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG - A. A. Vilela) for financial support. We also thank the Municipal Government of Araguari, the environmental department, and the employees of the John Kennedy Woodland Park (Parque Bosque John Kennedy) for their assistance in this study. RESUMO: O presente estudo teve como objetivo investigar a dinâmica temporal do forrageamento da comunidade de formigas de um fragmento de mata mesófila semidecídual urbana. Um total de 4.297 indivíduos, distribuídos em 23 espécies, sete gêneros e quatro subfamílias foram coletados nos meses de janeiro, abril, julho e outubro de 2010. Quatro guildas de espécies de formigas foram encontradas: Cortadeiras, Onívoras dominantes de solo, Oportunistas de solo e vegetação e Predadoras epigéicas grandes. Não houve diferenças significativas na riqueza de espécies e na abundância de indivíduos encontrados nas amostras entre os meses avaliados. Entretanto, houve uma clara substituição (turnover) de espécies ao longo dos meses. Nove espécies foram amostradas exclusivamente no período chuvoso e cinco espécies no período seco. Assim, a substituição das espécies ao longo dos meses reforça a hipótese de que comunidades de formigas apresentam uma dinâmica temporal em suas atividades de forrageamento mesmo em um fragmento florestal em área urbana. No geral, a abundância de formigas forrageando no solo foi maior durante os meses de maior pluviosidade. Entretanto, duas espécies da guilda de formigas oportunistas de solo e vegetação dobraram o número de indivíduos forrageando no período de menor precipitação. Estes resultados comprovam que as comunidades de formigas, independente do isolamento e ambiente (urbano ou natural), possuem uma dinâmica temporal na atividade de forrageamento que surgem a partir de fatores relacionados com a biologia e o comportamento de cada grupo e espécie. PALAVARAS-CHAVE: Guildas de formigas. Cerrado. Fragmentação. Riqueza de espécies. 1508 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 REFERENCES ALONSO, L. E. Ants as indicators of diversity. In: AGOSTI, E. D.; MAJER, J. D. ALONSO, L. E.; SCHULTZ, T. R. (Ed.). Ants: Standard methods for measuring and monitoring biodiversity. Washington: Smithsonian Institution Press, Washington, 2000. p. 80-88. ALONSO, L. E.; AGOSTI, D. Biodiversity studies, monitoring and ants: an overview, In: Ants: Standard methods for measuring and monitoring biodiversity. In: AGOSTI, E. D.; MAJER, J. D. ALONSO, L. E.; SCHULTZ, T. R. (Ed.). Ants: Standard methods for measuring and monitoring biodiversity. Washington: Smithsonian Institution Press, Washington, 2000. p. 1-8. ANDERSEN, A. N. A global ecology of rainforest ants: functional groups in relation to environmental stress and disturbance. In: AGOSTI, E. D.; MAJER, J. D. ALONSO, L. E.; SCHULTZ, T. R. (Ed.). Ants: Standard methods for measuring and monitoring biodiversity. Washington: Smithsonian Institution Press, Washington, 2000. p. 25-34. http://dx.doi.org/10.1046/j.1365-2664.2002.00704.x ANDERSEN, A. N.; HOFFMANN, B. D.; MÜLLER, W. J.; GRIFFITHS, A. D. Using ants as bioindicators in land management: simplifying assessment of ant community responses. Journal of Applied Ecology, London, v. 39, p. 8-17, 2002. ARAÚJO, G. M.; GUIMARÃES, A. J. M.; NAKAJIMA, J. N. Fitossociologia de um remanescente de mata mesófila semidecídua urbana, Bosque John Kennedy, Araguari, MG, Brasil. Revista Brasileira de Botânica, São Paulo, v. 20, p. 67-77, 1997. http://dx.doi.org/10.1590/s0100-84041997000100007 BELCHIOR, C.; DEL-CLARO, K.; OLIVEIRA, P. S. Seasonal patterns in the foraging ecology of the harvester ant Pogonomyrmex naegelii (Formicidae, Myrmicinae) in a Neotropical savanna: daily rhythms, shifts in granivory and carnivory, and home range. Arthropod-Plant Interactions, New York, v. 6, n. 4, p. 571-582, 2012. http://dx.doi.org/10.1007/s11829-012-9208-1 BOLTON, B. A new general catalogue of the ants of the world. Harvard University Press, Massachusetts, 1995. 504 p. BOLTON, B. Synopsis and classification of Formicidae. Memoirs of the American Entomological Institute, Gainesville, v. 71, p. 1- 370, 2003. BRAGANÇA, M. A. L.; TONHASCA, JR. A.; DELLA LÚCIA, T. M. C. Características biológicas e comportamentais de Neodohrniphora elongata Brown (Diptera, Phoridae), um parasitóide da saúva Atta sexdens rubropilosa Forel (Hymenoptera, Formicidae). Revista Brasileira de Entomologia, Curitiba, v. 53, n. 4, p. 600–606, 2009. http://dx.doi.org/10.1590/S0085-56262009000400009 BRANDÃO, C. R. F.; SILVESTRE, R.; REIS-MENEZES, A. Influência das interações comportamentais entre espécies de formigas em levantamentos faunísticos em comunidades de cerrado. Oecologia Brasiliensis, Rio de Janeiro, v. 8, p. 371-404, 2000. BRONSTEIN, J. L. The contribution of ant-plant protection studies to our understanding of mutualism. Biotropica, Florida, v. 30, n. 2, p. 150-161, 1998. http://dx.doi.org/10.1111/j.1744-7429.1998.tb00050.x BROWN, Jr. W. L. Diversity of ants. In Measuring and monitoring biological diversity: standard methods for ground living ants. In: AGOSTI, E. D.; MAJER, J. D. ALONSO, L. E.; SCHULTZ, T. R. (Ed.). Ants: Standard methods for measuring and monitoring biodiversity. Washington: Smithsonian Institution Press, Washington, 2000. p. 45-79. BRÜHL, C. A.; ELTZ, T.; LINSENMAIR, K. E. Size does matter - effect of tropical rainforest fragmentation on the leaf litter ant community in Sabah, Malaysia. Biodiversity and Conservation, New York, v. 12, p. 1371-1389, 2003. http://dx.doi.org/10.1023/A:1023621609102 1509 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 CARROL, C. R.; JANZEN, D. H. Ecology of foraging by ants. Annual Review of Ecology and Systematics, Palo Alto, v. 4, p. 231-257, 1973. http://dx.doi.org/10.1146/annurev.es.04.110173.001311 CERDÁ, X.; DAHBI, A.; RETANA, J. Spatial patterns, temporal variability and the role of multi-nest colonies in a monogynous Spanish desert ant. Ecological Entomology, New Jersey, v. 27, p. 7–15, 2002. http://dx.doi.org/10.1046/j.0307-6946.2001.00386.x COLWELL, R. K. 2013. EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. User's Guide and application published at http://purl.oclc.org/estimates. DAVIDSON, D. W.; COOK, S. C.; SNELLING, R. R.; CHUA, T. H. Explaining the abundance of ants in lowland tropical rainforest canopies. Science, Washington DC, v. 300, p. 969-972, 2003. http://dx.doi.org/10.1126/science.1082074 DELABIE, J. H. C.; FOWLER, H. G. Physical e biotic correlates of population fluctuations of dominant soil and litter ant species (Hymenoptera: Formicidae) in Brazilian cocoa plantations. Journal of the New York Entomological Society, New York, v. 101, n. 1, p. 135-140, 1993. DOS SANTOS, S. R. Q.; VITORINO, M. I.; HARADA, A. Y.; SOUZA, A. M. L.; SOUZA, E. B. A riqueza das formigas relacionada aos períodos sazonais em Caxiuanã durante os anos de 2006 e 2007. Revista Brasileira de Meteorologia, São José dos Campos, v. 27, n. 3, p. 307- 314, 2012. FITTKAU, E. J.; KLINGE, H. On biomass and trophic structure of the Central Amazonian rain forest ecosystem. Biotropica, Florida, v. 5, p. 2-14, 1973. http://dx.doi.org/10.2307/2989676 FOLGARAIT, P. J. Ant biodiversity and its relationship to ecosystem functioning: a review. Biodiversity and Conservation, New York, v. 7, p. 1221-1244, 1998. http://dx.doi.org/10.1023/A:1008891901953 FRANCO, A. C. Ecophysiology of woody plants. In: OLIVEIRA, P. S.; MARQUIS, R. J. (Eds.). The cerrados of Brazil: Ecology and natural history of a neotropical savanna. Columbia University Press, Irvington, 2002. p. 178-197. GIANOLI, E.; SENDOYA, S.; VARGAS, F.; MEJÍA, P.; JAFFÉ, R.; RODRÍGUEZ, M.; GOTELLI, N. J.; ELLISON, A. M. Biogeography at a regional scale: Determinants of ant species density in New England bogs and forests. Ecology, New York, v. 83, p. 1604-1609, 2002. HAHN, D. A.; WHEELER, D. E. Seasonal foraging activity and bait preferences of ants on Barro Colorado Island, Panama. Biotropica, Florida, v. 34, p. 348-356, 2002. http://dx.doi.org/10.1111/j.1744- 7429.2002.tb00548.x HÖLLDOBLER, B.; WILSON, E. O. The ants. Cambridge: Harvard University Press, 1990. 746 p. http://dx.doi.org/10.1007/978-3-662-10306-7 JOLIVET, P. Ants and plants: an example of coevolution. The Netherlands: Backhuys, Leiden, 1996. 303 p. KASPARI, M.; YUAN, M.; ALONSO, L. Spatial grain and the causes of regional diversity gradients in ants. American Naturalist, Chicago, v. 161, p. 459–477, 2003. http://dx.doi.org/10.1086/367906 LANGE, D.; FERNANDES, W. D.; RAIZER, J.; FACCENDA, O. Predacious activity of ants (Hymenoptera: Formicidae) in conventional and in no-till agriculture systems. Brazilian Archives of Biology and Technology, Curitiba, v. 51, n. 6, p. 1199-1207, 2008. http://dx.doi.org/10.1590/S1516-89132008000600015 LESTON, D. A neotropical ant mosaic. Annals of the Entomological Society of America, Annapolis, v. 71, n. 4, p. 649-653, 1978. http://dx.doi.org/10.1093/aesa/71.4.649 1510 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 LOPES, C. T.; VASCONCELOS, H. L. Evaluation of three methods for sampling ground-dwelling ants in the brazilian cerrado. Neotropical Entomology, New York, v. 37, n. 4, p. 399-405, 2008. http://dx.doi.org/10.1590/S1519-566X2008000400007 LÓPEZ–MORENO, I. R.; DIAZ-BETANCOURT, M. E.; LANDA, T. S. Insetos sociales em ambientes antropizados: las hormigas de la ciudad de Coatepec, Veracruz, México. Sociobiology, Feira de Santana, v. 42, p. 605-622, 2003. MAJER, J. D. Ant recolonization of rehabilited bauxite mines at Trombetas, Pará, Brazil. Journal Tropical Ecology, Cambridge, v. 12, p. 257-273, 1996. MAJER, J. D.; BRENNAN, K. E. C.; MOIR, M. L. Invertebrates and the restoration of a forest ecosystem: 30 years of research following bauxite mining in Western Australia. Restoration Ecology, Washington DC, v. 15, p. 104–115, 2007. http://dx.doi.org/10.1111/j.1526-100X.2007.00298.x MARQUES, G. D. V.; DEL-CLARO, K. The ant fauna in a cerrado area: the influence of vegetation structure and seasonality (Hymenoptera: Formicidae). Sociobiology, Feira de Santana, v. 47, n. 1, p. 235-252, 2006. MARQUES, G. V. D.; DEL-CLARO, K. Sazonalidade, abundância e biomassa de insetos de solo em uma reserva de cerrado. Revista Brasileira de Zoociências, Juiz de Fora, v. 12, n. 2, p. 141-150, 2010. MUELLER, U. G.; GERARDO, N. M.; AANEN, D. K.; SIX, D. L.; SCHULTZ, T. R. The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics, Palo Alto, v. 36, p. 563- 595, 2005. http://dx.doi.org/10.1146/annurev.ecolsys.36.102003.152626 NUNES, F. A.; SEGUNDO, G. B.; VASCONCELOS, Y. B.; AZEVEDO, R.; QUINET, Y. Ground-foraging ants (Hymenoptera: Formicidae) and rainfall effect on pitfall trapping in a deciduous thorn woodland (Caatinga), Northeastern Brazil. Revista de Biología Tropical, Costa Rica, San José, v. 59, n. 4, p. 1637-1650, 2011. OLIVEIRA, P. S.; BRANDÃO, C. R. F. The ant community associated with extrafloral nectarines in the brazilian cerrados. In: HUXLE, Y.C.R.; CUTLER, D.F. (Eds.). Ant-Plant Interactions. Oxford University Press, Oxford, 1991. p. 199-212. PARR, C. L.; GIBB, H. Competition and the role of dominant ants. In: LACH, L.; PARR, C.; ABBOTT, K. (Eds.). Ant ecology. Oxford University Press, Oxford, 2010. p. 77-96. POL, R. G.; CASENAVE, J. L.; PIRK, G. I. Influence of temporal fluctuations in seed abundance on the foraging behaviour of harvester ants (Pogonomyrmex spp.) in the central Monte desert, Argentina. Austral Ecology, New Jersey, v. 36, p. 320-328, 2011. http://dx.doi.org/10.1111/j.1442-9993.2010.02153.x PORTER, S. D.; TSCHINKEL, W. R. Foraging in Solenopsis invicta (Hymenoptera: Formicidae): effects of weather and season. Environmental Entomology, Annapolis, v. 16, n. 3, p. 802-808, 1987. http://dx.doi.org/10.1093/ee/16.3.802 RICO-GRAY, V.; OLIVEIRA, P. S. The ecology and evolution of ant-plant interactions. The University of Chicago Press, Chicago, 2007. 331 p. http://dx.doi.org/10.7208/chicago/9780226713540.001.0001 SCHMIDT, F. A.; RIBAS, C. R.; SCHOEREDER, J. H. How predictable is the response of ant assemblages to natural forest recovery? Implications for their use as bioindicators. Ecological Indicators, Atlanta, v. 24, p. 158-166, 2013. http://dx.doi.org/10.1016/j.ecolind.2012.05.031 SILVA, R. R. D. A.; BRANDÃO, C. R. F. Formigas (Hymenoptera: Formicidae) como indicadoras da qualidade ambiental e da biodiversidade de outros invertebrados terrestres. Biotemas, Florianópolis, v. 12, n. 2, p. 55-73, 1999. 1511 Temporal dynamic of foraging… LANGE, D. et al. Biosci. J., Uberlândia, v. 31, n. 5, p. 1501-1511, Sept/Oct. 2015 SILVESTRE, R. Estrutura de comunidades de formigas do cerrado. 2000. Tese (Doutorado em Ciências). Faculdade de Filosofia, Ciências e Letras, Universidade de São Paulo, Ribeirão Preto, 2000. SILVESTRE, R.; SILVA, R. R. Guildas de Formigas da Estação Ecológica Jataí, Luiz Antônio, SP: Sugestões para aplicação do modelo de guildas como Bio-Indicadores Ambientais. Biotemas, Florianópolis, v. 14, n. 1, p. 37-69, 2001. SILVESTRE, R.; BRANDÃO, C. R. F.; SILVA, R. R. Grupos funcionales de Hormigas: El caso de los gremios del Cerrado. In: FERNÁNDEZ, F. (Ed.). Introducción a las Hormigas de la Región Neotropical. Instituto Humboldt, Bogotá, 2003. p. 113-148. SOUZA, J. P.; ARAÚJO, G. M. Estrutura arbustivo/arbórea do subosque de clareiras e áreas sob dossel fechado em floresta estacional semidecidual urbana em Araguari – MG. Bioscience Journal, Uberlândia, v. 21, p. 93-102, 2005. STRINGER, L.; STEPHENS, A.; SUCKLING, D.; CHARLES, J. Ant dominance in urban areas. Urban Ecosystems, New York, v. 12, p. 503–514, 2009. http://dx.doi.org/10.1007/s11252-009-0100-4 TRANIELLO, J. F. Foraging strategies of ants. Annual Review of Entomology, Palo Alto, v. 34, n. 1, p. 191- 210, 1989. http://dx.doi.org/10.1146/annurev.en.34.010189.001203 VIEIRA, A. S.; ANTONIALLI-JÚNIOR, W. F.; FERNANDES, W. D. Modelo arquitetônico de ninhos da formiga Ectatomma vizottoi Almeida (Hymenoptera: Formicidae). Revista Brasileira de Entomologia, Curitiba, v. 51, p. 489-493, 2007. http://dx.doi.org/10.1590/S0085-56262007000400014 WARD, P. S. Broad-scale patterns of diversity in leaf litter ant communities. In: AGOSTI, E. D.; MAJER, J. D. ALONSO, L. E.; SCHULTZ, T. R. (Ed.). Ants: Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, 2000. p. 99-121. YAMAMOTO, M.; DEL-CLARO, K. Natural history and foraging behavior of the carpenter ant Camponotus sericeiventris Guérin, 1838 (Formicinae: Campotonini) in the Brazilian tropical savanna. Acta Ethologica, New York, v. 11, p. 55–65, 2008. http://dx.doi.org/10.1007/s10211-008-0041-6