Nest Maintenance Activity of
Dinoponera quadriceps
in a Natural Environment
Jeniffer C. Medeiros1&Dina L. O. Azevedo1& Melquisedec A. D. Santana1&Arrilton Araújo1
Revised: 24 February 2016 / Accepted: 1 March 2016 / Published online: 7 March 2016
# Springer Science+Business Media New York 2016
Abstract In social insects, task allocation can be more complex than workers merely falling into discrete task groups. Any activity performed by the colony cannot be fully understood in isolation from other activities because they may be interrelated. Inves-tigating activities other than foraging is crucial to understanding the global functioning and organization of ant colonies. This study attempts to characterize the nest mainte-nance activity of the ponerine queenless ant, Dinoponera quadriceps, in its natural environment to determine the effects of environmental variables on the variations in both seasonal and daily rhythms and to discuss its differences and possible relationships to foraging. Four colonies of D. quadriceps were observed in an area of Atlantic Forest in northeastern Brazil. Data collection was performed over a period of 72 h every three months during an entire annual cycle. Nest maintenance activity in D. quadriceps colonies was observed during both the light and dark phases of the day. There was no significant difference between the day phases in the number of workers involved in this task. On the other hand, D. quadriceps colonies exhibited seasonal variation in nest maintenance activity, peaking in the early rainy season. The seasonal rhythm of nest maintenance was positively correlated with relative humidity and negatively correlated with prey availability and rainfall. Our results indicate the existence of an annual variation in the nest maintenance activity of D. quadriceps associated with environ-mental variables. However, it occurs equally both at night and day, countering the hypothesis that there is a daily rhythm.
Keywords Ponerinae . ants . seasonality . environmental factors
* Arrilton Araújo arrilton@gmail.com
1
Laboratório de Biologia Comportamental, PPG em Psicobiologia, Universidade Federal do Rio Grande do Norte, Natal, RN 59078-970, Brazil
Introduction
Although foraging is probably the most important activity performed by ants outside the nest and the one in which workers invest most of their extra-nest time (Araújo and Rodrigues2006; Azevedo et al.2014; Medeiros and Araújo2014), it cannot be fully understood in isolation from other activities performed by the colony because they may be interrelated (Gordon1986). Task allocation can be far more complex than workers merely falling into discrete task groups; moreover, it can be plastic to enable colonies to withstand social perturbations (Pinter-Wollman et al.2012). In one of the best-studied species in this regard, Pogonomyrmex barbatus, a perturbation in some given activity has an associated effect on the number of workers engaged in other activities and on temporal activity patterns (Gordon1986). In P. barbatus, foraging and nest mainte-nance activity have a reciprocal relationship. An increase in one activity, caused by some experimental interference, is accompanied by a decrease in the other (Gordon 1986). However, when both of these activities are subjected to experimental interfer-ence, the colony invests more in foraging instead of nest maintenance, indicating that foraging is indeed a higher priority activity (Gordon1986).
In ant species with age-related division of labor, the workers responsible for nest maintenance are usually younger than foragers because younger workers usually perform activities inside the nest before moving on to perform tasks outside the nest when they are older (Gordon and Hölldobler1987; Jeanson and Weidenmüller2014). The age-related division of labor is derived from individual temporal changes in the behavioral repertoire and the propensity to perform certain tasks (Jeanson and Weidenmüller2014). Therefore, in young P. barbatus colonies, when the demand for nest maintenance activity is experimentally intensified, previously inactive individuals from inside the nest are recruited to increase the number of workers performing nest maintenance tasks. On the other hand, workers engaged in nest maintenance activity are more likely to switch to foraging than they are to continue performing nest maintenance tasks, whereas foragers display very strong task fidelity and are unlikely to switch activity (Gordon1989). These results indicate a possible temporal relation-ship between foraging and nest maintenance regarding the workers that perform these activities in a colony.
Recently, there has been a notable increase in the number of studies focused on the foraging behavior of Dinoponera species, which are characterized by solitary foragers that generally scavenge dead animals (mainly arthropods) and maintain individual directional fidelity during foraging, with different individuals specializing on certain areas in the vicinity of the nest (Fourcassié et al.1999; Fourcassié and Oliveira2002; Araújo and Rodrigues 2006; Peixoto et al.2010; Medeiros et al. 2012; Nascimento et al. 2012; Azevedo et al.2014; Medeiros and Araújo 2014; Medeiros et al.2014; Tillberg et al. 2014). The foraging activity in these ant species is known to vary both daily and seasonally, and the factors that affect these rhythms depend on the specific season, habitat and species (Fourcassié and Oliveira 2002; Peixoto et al. 2010; Medeiros et al.2012; Medeiros and Araújo,2014; Medeiros et al.2014).
Nevertheless, the specifics of nest maintenance behavior have received very little attention from myrmecologists, and all that we know about it in Dinoponera species is restricted to the scarce information presented in studies that were focused primarily on other questions (Fourcassié and Oliveira 2002; Peixoto et al. 2010). Fourcassié and
Oliveira (2002) observed that in D. gigantea most of the very frequent but brief trips in the vicinity of the nest, which lasted only 5 min or less, comprised nest maintenance activities such as the removal of refuse and the clearing of sticks and leaves from the nest entrance. Workers engaged in nest maintenance activity are responsible for the displacement of loose soil and sometimes twigs, which is characteristic of the most active nest entrances of D. quadriceps (personal observations; Paiva and Brandão 1995). In D. lucida, nest maintenance activity occurs at any time of day with workers removing soil, leaves and sticks from the excavation of galleries and chambers in the nest. However, this behavior is more frequent following rain showers or in nests that are not well protected from the rain (Peixoto et al.2010). This study aims to charac-terize the nest maintenance activity pattern of the queenless ant, D. quadriceps, in its natural environment and determine the effects of environmental factors on the varia-tions in both seasonal and daily rhythms. Because we already have a large amount of information about foraging behavior in D. quadriceps, investigating other activities performed by the colonies is crucial for obtaining a full picture, and understanding the global functioning and organization of this queenless, monomorphic and solitary foraging ant species will certainly be helpful.
Materials and Methods
Colonies
We observed four D. quadriceps colonies in a secondary Atlantic Forest area at the Floresta Nacional de Nísia Floresta (06°05’S, 35°12’W), Instituto Chico Mendes de Conservação da Biodiversidade, northeastern Brazil. The same four colonies were observed throughout the study, and they presented the same vegetation and luminosity conditions. The colonies were located at distances ranging anywhere from 15 to 35 m apart. Each colony had one to three entrances to the nest. The entrance with the highest worker activity was determined by preliminary observations and chosen as the focus of data collection for the current study. In addition to being the main access to the nest, the selected entrances were those to which foragers brought all of the food. The other entrances were secondary, presenting a greatly reduced traffic of workers. Thus, the missing data from the secondary entrances might not significantly affect the results based on the main entrances.
Before the first data collection period, as many workers as possible from the four colonies were marked, including all workers that left of their own volition or were induced to leave by probing the nest with a stick. The workers were marked using a colored plastic tag with an alphanumeric code affixed to the thorax with a cyanoacry-late ester-based adhesive according to a technique based on Corbara et al. (1986). Before each subsequent data collection period, any unmarked worker collected was marked using the same marking process. Unmarked workers may have lost their mark, or they may not have been collected previously (i.e., because they were not active at the nest entrance or not born yet). A total of 453 individual workers were marked from all four colonies (colony I: 54; colony II: 131; colony III: 105; colony IV: 163), and 304 workers were observed during the data collection periods throughout the study (colony I: 35; colony II: 94; colony III: 57; colony IV: 118).
Data Collection Behavioral Observation
Observational data were collected in all four colonies during the same continuous period lasting 72 h every three months and coinciding with the full moon over an entire annual cycle. Thus, data were collected in four separate months, namely November 2010, February 2011, May 2011 and August 2011. A group of observers working in three or four pairs took discrete shifts to cover each 72-h data collection period. Each colony was observed continuously for 20 min/h; then, each observer of a pair was able to collect the data from two colonies with an interval of 10 min between them. During night observation periods, flashlights with a red light were used to minimize observer interference on normal worker activity.
During the observation periods, each event of a worker leaving or entering the nest was recorded, and each individual identified by its tag with a unique alphanumeric code (adapted from Retana et al.1990). A worker was considered to have left the nest only when it moved more than 15 cm away from the entrance. The 15-cm minimum distance criterion enabled the observers to be certain about what the ants were doing and the ants’ identities because they can move fast while performing nest maintenance and because the immediate vicinity of the nest entrances was surrounded by leaves and twigs, rendering night observations difficult. A worker was considered to have engaged in nest maintenance activity whenever it left the nest carrying soil or waste and returned within two minutes. In general, while executing nest maintenance, the workers do not move more than 30 cm away, depositing material removed from the nest in the area surrounding the entrance and returning quickly. During the observations, trips lasting more than two minutes always involved foraging activity.
Measurement of Environmental Factors
The availability of potential prey throughout the year was estimated by collecting invertebrates using pitfall traps. Six groups of pitfall traps were installed in the forest 80 m away from the observed colonies but still in the same habitat. The traps were installed at this safe distance to prevent any of the ants under observation from being accidentally captured. Three groups of traps were placed on both the east and west sides of the colonies and arranged in transects of 40 m in length and 20 m apart. The traps remained open in the field for 72 h during each month of data collection. Each group comprised five pitfall traps arranged in a cross shape with one meter in between and connected with 100 × 15-centimeter (length x height) plastic fences to form a total sample area of 4 m2. The material collected in the pitfall traps was preserved in 70 % alcohol and identified later in the laboratory. Based on the known diet composition of D. quadriceps presented by Araújo and Rodrigues (2006) and Medeiros et al. (2014) who had identified the food items captured by D. quadriceps workers at the same Atlantic forest area of this study, we considered potential prey items for D. quadriceps to be invertebrates of the following taxa: Blattodea (including Isoptera suborder), Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Orthoptera, Araneae, Chilopoda, Diplopoda, Oligochaeta, Gastropoda and the pupae and larvae of uniden-tified Insecta.
During the intervals between the 20 min/h observation periods, we recorded tem-perature and relative humidity using a digital thermohygrometer and luminosity with a digital luximeter at a distance of approximately 10 cm from the nest entrance being observed. Rainfall data from the observation days were obtained from the Empresa de Pesquisa Agropecuária do Rio Grande do Norte (EMPARN).
Data Analysis
For the analyses of daily rhythm, the nest maintenance activity of each colony was estimated as the total number of worker departures and returns recorded during each 20-min observation period. Thus, for each collection month, the data comprised 72 records of nest maintenance activity for each colony. These data were classified as belonging to the light or dark phase of the day based on the time of sunrise and sunset obtained from the United States Naval Observatory. We used generalized linear mixed models to analyze the influence of the light and dark phases of the day (fixed factor) on the variation in nest maintenance activity (response variable). We used a negative binomial error structure, and the colony was incorporated into the models as a random factor. This mixed model analysis was performed for each collection month separately. For seasonal analyses, we used the daily total sum of nest maintenance activity data and the daily averages for the temperature, humidity and luminosity measurements. Thus, the data used in seasonal analyses comprised 3 records for each colony, one for each collection day for each collection month. According to the rainfall data obtained from EMPARN, November was classified as the early part of the dry season (EDS), February as the late dry season (LDS), May as the early rainy season (ERS) and August as the late rainy season (LRS). For the analysis of variation among EDS, LDS, ERS and LRS we used a generalized linear mixed model with daily nest maintenance activity as a response variable, season as a fixed factor and colony as a random factor. To analyze the influence of environmental factors on the seasonal variation in nest maintenance, another generalized linear mixed model was performed in which daily nest mainte-nance activity was the response variable; temperature, humidity, luminosity, rainfall and prey availability were the fixed factors; and colony was incorporated into the model as a random factor. A negative binomial error structure was specified for the models because the count data presented overdispersion. The statistical software IBM SPSS Statistics 21 was used in all of the data analyses.
Results
Throughout the study, 675 nest maintenance trips were recorded (1350 records of leaving and entering the nest, Table1). 95.56 % of the nest maintenance activity was correlated with soil removal, whereas only 2.37 % was correlated with rubbish removal. 2.07 % from the material removed was not identified. Although we had marked as many workers as possible before each data collection period, some un-marked ants were observed performing nest maintenance, and in these cases worker identification was not possible. Thirty-nine marked workers performed nest mainte-nance. Among these, 36 workers (92.31 %) also performed foraging during the same data collection period, whereas 3 workers (7.69 %) performed only nest maintenance.
Only 11 (28.21 %) out of the 39 marked individuals were observed across different periods; most of them (63.64 %, 7 individuals) performed only foraging in the subsequent period (three months later) after they had performed nest maintenance and foraging. Only one individual (9.09 %) continued to perform nest maintenance and foraging across two different periods, and two individuals (18.18 %) were observed only in foraging activity before they were observed in nest maintenance and foraging activity. One individual (9.09 %) was observed across three different periods and performed only foraging before and after nest maintenance and foraging.
Nest maintenance activity was observed during both the light and dark phases of the day. Throughout the year, there was no detectable difference between the phases of the day in terms of the number of workers involved in this task (EDS: F1,28 = 2.089,
p = 0.160; LDS: F1,1 = 0.028, p = 0.889; ERS: F1,5 = 0.625, p = 0.466; LRS:
F1,87= 1.063, p = 0.305). However, it was possible to verify the occurrence of seasonal
variation throughout the year. The colonies of D. quadriceps exhibited seasonal variation in nest maintenance activity (F3,14 = 13.850, p < 0.001), which began to
increase in the late dry season, peaked in the early rainy season and suddenly declined at the end of this season (Fig.1). The seasonal rhythm of nest maintenance activity was explained by a negative relationship with prey availability (F1,4= 34.927, p = 0.003), a
positive relationship with relative humidity (F1,8= 14.775, p = 0.005), and a negative
relationship with rainfall (F1,5 = 13.818, p = 0.012). Temperature (F1,2 = 0.089,
p = 0.789) and luminosity (F1,1= 27.568, p = 0.120) did not have significant effects
on the seasonal fluctuation of nest maintenance activity.
Discussion
D. quadriceps colonies did not present a daily rhythm for nest maintenance activity as evidenced by the lack of a difference between the phases of the day. Nest maintenance activity occurring at any time of day, during both the light and dark phases, was also Table 1 Number of records (events of leaving and entering the nest) of foraging and nest maintenance activity of Dinoponera quadriceps workers per colony in each season (72-h observation period)
Early Dry Season Late Dry Season Early Rainy Season Late Rainy Season Colony #1 Foraging 306 234 69 127 Nest maintenance 8 8 4 8 Colony #2 Foraging 301 205 161 126 Nest maintenance 2 20 226 0 Colony #3 Foraging 156 78 115 176 Nest maintenance 0 0 228 4 Colony#4 Foraging 351 90 203 274 Nest maintenance 10 464 358 10 Total Foraging 1114 607 548 703 Nest maintenance 20 492 816 22
observed in D. lucida (Peixoto et al. 2010). The lack of a daily pattern in nest maintenance activity differs from the observation of foraging activity in D. quadriceps, which exhibits a daily, mainly diurnal rhythm despite also occurring at a lower level at night (Medeiros et al.2014).
On the other hand, the nest maintenance activity of D. quadriceps in the studied area of secondary Atlantic Forest habitat varied seasonally, peaking in the late dry season and early rainy season. This pattern was the opposite of what was observed for foraging activity in the same species both in areas of the Atlantic Forest (Medeiros et al.2014) and the Caatinga habitat (Medeiros et al.2012), which peaks between the late rainy season and the early dry season. Medeiros et al. (2014) used the same data collection methodology and sampling size we adopted here; thus, the studies are entirely compa-rable. In the study in the Caatinga habitat, another methodology was used to estimate foraging activity based on the number of workers captured in pitfall traps (Medeiros et al. 2012); however, Medeiros et al. (2014) showed that the seasonal variation of workers captured in pitfall traps is directly related to the foraging activity of the observed colonies; hence, it is also quite comparable.
There are three possible explanations that are not mutually exclusive for the seasonal pattern of nest maintenance activity. The observed pattern might be explained by (1) a reallocation in the colony workforce, (2) temporal polyethism along with seasonal offspring production, and (3) an increasing need for nest maintenance. The first possible hypothesis is that the alternation between the peaks of foraging and nest maintenance activity throughout the year may indicate the occurrence of a displacement in the colony workforce to other tasks when the necessary level of foraging activity is diminished. The seasonal variation in nest maintenance activity had an inverse relationship with prey availability such that the lower the availability of food in the environment, the less demand for foraging activity and the greater the allocation of workers to the task of nest maintenance activity. Muscedere et al. (2011) observed changes in task allocation within the nests of Acromyrmex octospinosus when
LRS ERS
LDS EDS
Nest maintenance activity per day
200 150 100 50 0 a ab b a
Fig. 1 Seasonal variation of nest maintenance activity in Dinoponera quadriceps colonies. Median, first and third quartiles and non-outlier range of the data are presented. EDR early dry season, LDS late dry season, ERS early rainy season, LRS late rainy season. Different letters represent significant results (Estimated Means Pairwise Contrasts, p < 0.05)
they were deprived of foraging opportunities. When foraging is available, minor workers perform mostly brood care and garden maintenance while major workers are mostly involved leaf processing. However, when foraging is withheld, there are no differences in task frequencies between major and minor workers. Similarly, in Pogonomyrmex barbatus, interference with normal foraging behavior, nest mainte-nance activity or both causes changes in the temporal patterns of all activities observed outside of the nest, indicating that various activities are interrelated. More specifically, when foraging or nest maintenance activities are impeded experimentally, they are of reciprocal priority. That is, when colonies respond to the experimental influence with an increase in foraging activity, there is an associated decrease in nest maintenance activity and vice versa (Gordon1986).
The second hypothesis is that the alternation of foraging and nest maintenance activity peaks in a colony could be related to temporal polyethism and the seasonal variation in offspring production. If the production of offspring in D. quadriceps varies seasonally, as it does in D. lucida (Peixoto et al.2010) and D. australis (Paiva and Brandão 1995), and is further linked to the time of year when foraging activity increases, as in D. australis (Paiva and Brandão1995), the new workers will initiate their adult lives engaged in tasks inside of the nest, such as caring for offspring, before switching to nest maintenance, leading to the observable peak in this activity. At more advanced ages, these same workers become foragers, causing the observable peak in foraging activity, which is also associated with a new peak in offspring production. Indeed, previous studies of D. quadriceps have shown that the increase in foraging activity occurs by way of an increase in the total number of foragers in the colony and not the number of foraging trips being executed by each worker (Medeiros and Araújo 2014; Medeiros et al. 2014). Furthermore, evidence of temporal polyethism was observed in D. lucida, in which a division exists between two main groups, the young workers that care for immature individuals and the older foragers (Peixoto et al.2008). Nest maintenance workers may be in a transitional phase from interior tasks to exterior ones, such as foraging (Gordon and Hölldobler,1987). Indeed, in P. barbatus, new nest maintenance workers are recruited from inactive workers inside the nest, but later these same workers often switch tasks to foraging or patrolling (Gordon1989). Although most of the D. quadriceps ants that performed nest maintenance were also foraging in the same observation period, they were mostly just foraging in the subsequent period, suggesting that performing both nest maintenance and foraging might be an intermediate situation.
The third possible explanation relates to two important factors in determining the increase in nest maintenance activity, relative humidity and rainfall. These two factors are associated with each other, with increased relative humidity and rainfall occurring at the same time of the year, the rainy season. Rainfall can force soil and other debris into the nest or damage the nest structure, increasing the need for digging activity and nest repair. However, ants are usually inactive under the rain. Peixoto et al. (2010) assert that rain certainly inhibits D. lucida activities in the external area of the nest. In Cataglyphis iberica, the rain completely restrains its activity (Cerdá and Retana1989). Melophorus bagoti ants generally stop foraging as soon as it starts to rain (Muser et al.2005). The same also occurs in Pachycondyla obscuricornis under intense and long-lasting rainfall (Chagas and Vasconcelos2002). However, immediately after the rain stops, when there is still high humidity, workers can repair the damage caused to the nest by the rain. This
is probably why nest maintenance peaked during the early rainy season; it is associated with increasing humidity despite being negatively correlated with rainfall. In D. lucida, nest maintenance activity is also more frequently observed after rainfall and in nests not protected from rain (Peixoto et al.2010). In D. quadriceps, most of the nest mainte-nance activity was related to soil removal which can represent nest repair. Nevertheless, another cause for the increasing need for digging activity is still possible. Nest maintenance patterns might also be related to the possible rhythms of nest expansion associated with brood production and colony growth. Because we did not have access to the interior of the nests, we could not distinguish whether it represented nest expansion or nest repair.
Our results indicate that there is an annual variation in the nest maintenance activity of D. quadriceps workers that is associated with environmental variables. Nest main-tenance activity increases during months with higher humidity and lower prey avail-ability, and rainfall has an immediate negative effect on the performance of this task. Nest maintenance activity occurs equally both at night and during the day, countering the hypothesis that there is a daily rhythm.
Acknowledgments We thank C. V. M. Azevedo, M. F. Arruda from the Universidade Federal do Rio Grande do Norte (UFRN), J. H. C. Delabie from the Universidade Estadual de Santa Cruz (UESC) and anonymous reviewers for helpful suggestions on the manuscript; M. D. Marques from the Museu de Zoologia da Universidade de São Paulo (MZUSP) for methodological help; and T. R. P. Lopes, W. A. Silva Neto, L. E. F. Carvalho, R. Sobral, N. A. M. Tasso, D. G. Teixeira, G. R. Mantilla, I. A. Medeiros, P. Fernandes, T. Moreira, P. P. Gomes, M. C. Rodrigues, L. A. Silva and C. P. Bauchwitz from UFRN for their help during field work. We also thank the Instituto Chico Mendes de Conservação da Biodiversidade for issuing permits to work at the Floresta Nacional de Nísia Floresta (#26107-1). This study was supported by the Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (PRONEX– FAPESB/CNPq Grant #6994). Financial support was provided to A.A. by CNPq (Grant #307418/2009-0) and to J.M. and D.L.O.A by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).
References
Araújo A, Rodrigues Z (2006) Foraging behavior of the queenless ant Dinoponera quadriceps Santschi (Hymenoptera: Formicidae). Neotropical Entomol 35:159–164
Azevedo DLO, Medeiros JC, Araújo A (2014) Adjustments in the time, distance and direction of foraging in Dinoponera quadriceps workers. J Insect Behav 27:177–191. doi:10.1007/s10905-013-9412-6
Cerdá X, Retana J (1989) Influencia de los factores ambientales sobre la actividad diaria de recolección de la hormiga Cataglyphis iberica (Em.) (Hym.: Formicidae). An Biol 15:75–82
Chagas ACS, Vasconcelos VO (2002) Comparação da frequência da atividade forrageira da formiga Pachycondyla obscuricornis (Emery, 1890) (Hymenoptera, Formicidae) no verão e no inverno, em condições de campo. Rev Bras Zoociências 4:97–109
Corbara B, Fresneau D, Lachaud J-P, Leclerc Y, Goodall G (1986) An automated photographic technique for behavioural investigations of social insects. Behav Process 13:237–249
Fourcassié V, Henriques A, Fontella C (1999) Route fidelity and spatial orientation in the ant Dinoponera gigantea (Hymenoptera, Formicidae) in a primary forest: a preliminary study. Sociobiology 34:505–524 Fourcassié V, Oliveira PS (2002) Foraging ecology of the giant Amazonian ant Dinoponera gigantea (Hymenoptera, Formicidae, Ponerinae): activity schedule, diet and spatial foraging patterns. J Nat Hist 36:2211–2227
Gordon DM (1986) The dymanics of the daily round of the harvester ant colony (Pogonomyrmex barbatus). Anim Behav 34:1402–1419
Gordon DM, Hölldobler B (1987) Worker longevity in harvester ants (Pogonomyrmex). Psyche 94:341–346 Jeanson R, Weidenmüller A (2014) Interindividual variability in social insects– proximate causes and ultimate
consequences. Biol Rev 89:671–687. doi:10.1111/brv.12074
Medeiros J, Araújo A (2014) Workers’ extra-nest behavioral changes during colony fission in Dinoponera quadriceps (Santschi). Neotropical Entomol 43:115–121
Medeiros J, Araújo A, Araújo HPF, Queiroz JPC, Vasconcellos A (2012) Seasonal activity of Dinoponera quadriceps (Formicidae, Ponerinae) in the semi-arid caatinga of NE Brazil. Rev Bras Entomol 56:81–85 Medeiros J, Azevedo DLO, Santana MAD, Lopes TRP, Araújo A (2014) Foraging activity rhythms of the queenless ant Dinoponera quadriceps in its natural environment. J Insect Sci 14(220). doi:10.1093/jisesa/ ieu082
Muscedere ML, Berglund JL, Traniello JFA (2011) Polymorphism and division of labor during foraging cycles in the leaf-cutting ant Acromyrmex octospinosus (Formicidae; Attini). J Insect Behav 24:94–105 Muser B, Sommer S, Wolf H, Wehner R (2005) Foraging ecology of the thermophilic Australian desert ant,
Melophotus bagoti. Aust J Zool 53:301–311
Nascimento FS, Souza DISA, Tannure-Nascimento IC, Dantas JO (2012) Social facilitation and food partitioning in the queenless ant Dinoponera quadriceps (Hymenoptera: Formicidae). J Nat Hist 46: 1959–1967. doi:10.1080/00222933.2012.700333
Paiva RVS, Brandão CRF (1995) Nests, worker population, and reproductive status of workers, in the giant queenless ponerine ant Dinoponera Roger (Hymenoptera Formicidae). Ethol Ecol Evol 7:297–312 Peixoto AV, Campiolo S, Delabie JHC (2010) Basic information about the threatened ant, Dinoponera lucida
Emery (Hymenoptera: Formicidae: Ponerinae), aiming its effective long-term conservation. In: Tepper GH (ed) Species diversity and extinction. Nova Science Publishers Inc., New York, pp. 183–213 Peixoto AV, Campiolo S, Lemes TN, Delabie JHC, Hora RR (2008) Comportamento e estrutura reprodutiva
da formiga Dinoponera lucida Emery (Hymenoptera, Formicidae). Rev Bras Entomol 52:88–94 Pinter-Wollman N, Hubler J, Holley J-A, Franks NR, Dornhaus A (2012) How is activity distributed among
and within tasks in Temnothorax ants? Behav Ecol Sociobiol 66:1407–1420. doi: 10.1007/s00265-012-1396-2
Retana J, Cerda X, Bosch J, Alsina A (1990) Comparacion de vários metodos de estudio de ritmos de actividad recolectora en hormigas (Hymenoptera: Formicidae). Butll Inst Catalana Hist Nat 58:65–72 Tillberg CV, Edmonds B, Freauff A, Hanisch PE, Paris C, Smith CR, Tsutsui ND, Wills BD, Wittman SE,
Suarez AV (2014) Foraging ecology of the tropical giant hunting ant Dinoponera australis (Hymenoptera: Formicidae)– evaluating mechanisms for high abundance. Biotropica 46:229–237
