Acessibilidade / Reportar erro

Behavioral and olfactory antennal responses of Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) workers to their dufour gland secretion

Respuestas comportamentales y olfatorias de obreras de Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) a sus secreciones de la glándula de dufour

Abstracts

Behavioral and electrophysiological tests were performed to evaluate the responses of workers of the ant Solenopsis geminata (Fabricius) from different size categories to Dufour gland extracts. Morphometric measures based in head widths across eyes were used to determine worker sizes. Trail following response of different worker sizes to Dufour gland extract from workers of different sizes was assessed. For each worker size category olfactory responses to Dufour gland extracts were determined using electroantennography (EAG). Gas chromatography and mass spectrometry (GC-MS) were used to determine the chromatographic profile of Dufour gland secretion for each worker size. Morphometric measures permitted to classify the workers of S. geminata as large, medium and small workers. Medium S. geminata workers displayed a significantly higher behavioral response to Dufour gland extracts produced by medium size workers. Similarly, medium workers showed a significantly higher EAG response to Dufour gland extracts produced by medium sized workers. Chromatographic profile of Dufour gland secretions produced by workers showed that each size category exhibited a characteristic profile of the three main components considered as potential trail pheromone constituents. This work showed that medium workers of S. geminata exhibited a high trail-following behavior as well as a high antennal response to Dufour gland secretion. This and their relative abundance in field foraging areas, suggest that medium-sized workers are specialized in foraging activities.

Trail-following behavior; electroantennography


Se efectuaron pruebas comportamentales y electrofisiológicas para evaluar las respuestas de obreras de Solenopsis geminata (Fabricius) de diferentes tamaños a extractos de la glándula de Dufour. Se usaron medidas del ancho de la cabeza para determinar el tamaño de las obreras. Se evualuó la respuesta de seguimiento de ruta de obreras de diferentes tamaños a extractos de la glándula de Dufour proveniente de obreras de diferentes tamaños. Para cada grupo de obrera de determinado tamaño se le determinó la respuesta olfatoria por medio de electroantenografía (EAG). Se utilizó Cromatografía de Gases acoplada a Espectrometría de Masas (GC-EM) para determinar el perfil cromatográfico de la secreción de la glándula de Dufour para cada grupo de obreras. Las medidas morfométricas permitieron clasificar a las obreras de acuerdo a su tamaño en grandes, medianas y pequeñas. Las obreras medianas de S. geminata exhibieron una respuesta comportamental alta a los extractos glandulares de hormigas medianas. Las obreras medianas mostraron también una alta respuesta antenal a los extractos de obreras medianas. El perfil cromatográfico de la secreción de la glándula de Dufour producida por obreras muestra que cada tamaño exhibió un perfil característico de los tres componentes potenciales como feromona de ruta. Concluimos que las obreras de tamaño mediano exhibieron altas respuestas tanto comportamentales como olfatorias a la secreción de la glándula de Dufour. Lo anterior y el hecho de que sean las más abundantes en el área de forrajeo sugieren que este grupo de obreras está especializado en actividades de forrajeo.

Comportamiento; seguimiento de ruta; electroantenografía


ECOLOGY, BEHAVIOR AND BIONOMICS

Behavioral and olfactory antennal responses of Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) workers to their dufour gland secretion

Respuestas comportamentales y olfatorias de obreras de Solenopsis geminata (Fabricius) (Hymenoptera: Formicidae) a sus secreciones de la glándula de dufour

Yolanda BrindisI; Jean P. LachaudI, II; Benigno Gómez Y GómezI; Julio C. RojasI; Edi A. MaloI; Leopoldo Cruz-LópezI

IEl Colegio de la Frontera Sur (ECOSUR), Carretera Antiguo Aeropuerto km 2.5, C. postal 30700, Tapachula, Chiapas, Mexico

IICentre de Recherches sur la Cognition Animale (CRCA), CNRS-UMR5169, Univ. Paul-Sabatier, 118 route de Narbonne, 31062 Toulouse cedex 9, France

ABSTRACT

Behavioral and electrophysiological tests were performed to evaluate the responses of workers of the ant Solenopsis geminata (Fabricius) from different size categories to Dufour gland extracts. Morphometric measures based in head widths across eyes were used to determine worker sizes. Trail following response of different worker sizes to Dufour gland extract from workers of different sizes was assessed. For each worker size category olfactory responses to Dufour gland extracts were determined using electroantennography (EAG). Gas chromatography and mass spectrometry (GC-MS) were used to determine the chromatographic profile of Dufour gland secretion for each worker size. Morphometric measures permitted to classify the workers of S. geminata as large, medium and small workers. Medium S. geminata workers displayed a significantly higher behavioral response to Dufour gland extracts produced by medium size workers. Similarly, medium workers showed a significantly higher EAG response to Dufour gland extracts produced by medium sized workers. Chromatographic profile of Dufour gland secretions produced by workers showed that each size category exhibited a characteristic profile of the three main components considered as potential trail pheromone constituents. This work showed that medium workers of S. geminata exhibited a high trail-following behavior as well as a high antennal response to Dufour gland secretion. This and their relative abundance in field foraging areas, suggest that medium-sized workers are specialized in foraging activities.

Key words:Trail-following behavior, electroantennography

RESUMEN

Se efectuaron pruebas comportamentales y electrofisiológicas para evaluar las respuestas de obreras de Solenopsis geminata (Fabricius) de diferentes tamaños a extractos de la glándula de Dufour. Se usaron medidas del ancho de la cabeza para determinar el tamaño de las obreras. Se evualuó la respuesta de seguimiento de ruta de obreras de diferentes tamaños a extractos de la glándula de Dufour proveniente de obreras de diferentes tamaños. Para cada grupo de obrera de determinado tamaño se le determinó la respuesta olfatoria por medio de electroantenografía (EAG). Se utilizó Cromatografía de Gases acoplada a Espectrometría de Masas (GC-EM) para determinar el perfil cromatográfico de la secreción de la glándula de Dufour para cada grupo de obreras. Las medidas morfométricas permitieron clasificar a las obreras de acuerdo a su tamaño en grandes, medianas y pequeñas. Las obreras medianas de S. geminata exhibieron una respuesta comportamental alta a los extractos glandulares de hormigas medianas. Las obreras medianas mostraron también una alta respuesta antenal a los extractos de obreras medianas. El perfil cromatográfico de la secreción de la glándula de Dufour producida por obreras muestra que cada tamaño exhibió un perfil característico de los tres componentes potenciales como feromona de ruta. Concluimos que las obreras de tamaño mediano exhibieron altas respuestas tanto comportamentales como olfatorias a la secreción de la glándula de Dufour. Lo anterior y el hecho de que sean las más abundantes en el área de forrajeo sugieren que este grupo de obreras está especializado en actividades de forrajeo.

Palabras claves: Comportamiento, seguimiento de ruta, electroantenografía

Fire ants constitute a large group of species belonging to the genus Solenopsis and native to the New World; many of them are of considerable economic importance due to their action as potential biological control agents or as pests (Smith 1936, Travis 1941, Risch & Carroll 1982, Way et al. 2002). They exhibit an efficient foraging behavior which involves a sophisticated system of communication to orientate and recruit other members of the colony towards food sources and to find new nesting sites (Wilson 1959, 1962; Bell & Cardé 1984). Communication is performed utilizing a trail pheromone produced in the Dufour gland of workers, which has been studied at both chemical and behavioral levels in various species of Solenopsis, including S. invicta (Buren), S. xyloni (McCook), S. geminata (Fabricius)and S. richteri (Forel) (Barlin et al. 1976, Vander Meer et al. 1988). Nevertheless, despite the interesting attempt by Brand et al. (1973), a clear relationship level of perception and responsiveness to trail substances and worker subcastes, has not been investigated so far. Moreover, field observations (Brindis et al. personal observation) suggest that the medium size classes of S. geminata display some more differentiated activities related with foraging and food provisioning compared to minor and large workers. The objectives of this study are: 1) Evaluate an eventual difference in behavioral and olfactory responses to the Dufour gland secretion in function of the releaser and receptive worker size, and 2) Establish the existence of a relationship between the chemical profile of the Dufour gland secretions and the different worker sizes.

Material and Methods

Ants. Workers of S. geminata were collected in the foraging area of 13 nests in the municipality of Cacahoatán (14° 59' N, 92° 10' W), Chiapas, Mexico. They were transported to the laboratory and maintained in plastic containers under a relative humidity of 70 ± 5% and a temperature of 25 ± 3°C. Food provided every 24h consisted of a 10% sugar solution soaked onto cotton wool.

Morphometric measures for worker size determination. Head width across eyes measures of collected workers were recorded using a binocular microscope (Nikon mod SMZ-U 1:10) with a micrometric ruler. Once the morphometric measurements for different worker sizes in the foraging area were obtained, the number of workers in each size class for the 10 remaining nests was counted in order to establish the distribution of the different worker sizes in the foraging trail.

Sample preparation. The worker ants were immobilized at -20°C for a period of 5 minutes. The Dufour gland was dissected and separated from the poison gland us ng a stereomicroscope and a petri dish containing 10 ml of distilled water. Ten Dufour glands were placed in a glass tube containing 700 µl of hexane (HPLC grade) for five minutes, after that the glands were withdrawn and the extract concentrated with nitrogen to 100 µl, thus resulting in 10 ml for each gland. The extracts were stored at -20°C for later use in bioassays and electroantennography.

Worker behavioral response to Dufour gland secretion. In order to assess worker response to Dufour gland extracts, the protocol described by Pasteels & Verhaeghe (1974) was followed with some minor modifications. A 10 cm diameter circle with 1 cm divisions was drawn onto a piece of filter paper (Whatman No. 1, Maidstone, England) and either 10 ml of extract or hexane (control) were applied along the circumference using a normal graphic pen (Blundell Harbin, Weymouth, England) allowing the solvent to evaporate over 20 seconds. The filter paper was then placed in a circular plastic container (20 cm diameter X 5 cm high). Finally a worker was placed in the centre of the plastic container. The number of divisions over which the ant traveled continually during 5 min was recorded. After each period of 5 min, which was considered as a repetition, both the filter paper and the worker were replaced. For each sample nest, the response of the workers of the different sizes was assessed for extracts from each worker size category. Fifty replicates were carried out for each randomly selected combination. The bioassays were performed the day after the workers were collected.

Electroantennography (EAG). For each worker subcaste, olfactory response to the Dufour gland extracts from the different subcastes previously defined was determined using the electroantennography (EAG) setup described in Malo et al. (2004). In order to assess the EAG response of the three different sizes of workers to the series of Dufour gland extracts, 10 ml of extract (one Dufour gland equivalent) were placed on a piece of filter paper (Whatman no. 1, Maidstone, England) and exposed to the air for 20 seconds, allowing the solvent to evaporate. The sample was placed in a Pasteur glass pipette for 40 seconds before being applied. New pipettes were prepared for each insect tested. The stimulus was applied at intervals of 2 min. The Dufour gland extracts of different sized workers were used for each EAG preparation and randomly selected. The control stimulus (hexane) was presented at the start and at the end of each EAG analysis. We used one antenna per worker in each size class and for each series of tested extracts. At least 20 workers were used for each size class.

Chemical analysis. The chemical analysis on the Dufour gland extracts was performed using a gas chromatography system Varian CP 3800 (Palo Alto, CA, USA) and a mass spectrometer Varian Saturn 4D 2200 (Palo Alto, CA, USA). The compounds were separated with a non-polar capillary column (DB-5 MS, 30 m x 0.25 µm internal diameter, J&W Scientific Folsom, CA, USA). The temperature program used started with an initial temperature of 50°C for 2 min increasing by 15°C per minute, reaching a final temperature of 280°C. The carrier gas was Helium at constant flow rate (1.0 ml/min). The mass spectra were obtained by electronic impact at 70 eV. Extracts (one Dufour gland equivalent) were injected using the "Splittles" mode. The chemical identification of the trail pheromone candidates was carried out by comparing the mass spectra of the natural compounds with published mass spectra (Vander Meer et al. 1981, Cruz-López 1994). The relative amount of the components was calculated from the sum of the areas of each one of the recorded peak. The extracts taken from the Dufour glands were analyzed for different worker size classes. Five replications from two different nests were carried out for each size class.

Statistical analysis. The statistical analyses were carried out using the statistical package STATISTICA for Windows, version 7.1, Statsoft, Inc. (2005). Data obtained from both the morphometric measurements (three nests) and chemical analysis (two nests) of the Dufour gland, were pooled because preliminary analysis showed that there was no significant difference between data. These data were analyzed by a principal component analysis. To determine which variables influence group separation, a correlation of the original variables and the principal components used were obtained. The behavioral responses of different size workers to the Dufour gland secretions were analyzed by means of a two-way ANOVA, whereby the first factor is extract origin with three levels (Dufour gland extracts of large, medium and small workers) and the second factor is tested worker subcaste (large, medium and small) assessed in the bioassays. The EAG amplitude values were analyzed using a two-way ANOVA where one factor is the assessed products (hexane, Dufour gland extracts of large, medium and small workers) and the second factor is tested worker subcaste (large, medium and small). When necessary, data were logarithmically or square root (Öx) transformed to meet the assumptions of normality and homogeneity of variances. Those transformed data were obtained applying the Box-Cox family of transformations and transformation of ranks (Conover & Iman 1981). Significant ANOVAs were followed by posthoc Tukey test for multiple comparisons of means (P < 0.05).

Results

Worker size determination. The S. geminata workersdisplay head widths across the eyes ranging from 0.05 mm to 0.15 mm. The workers that fell within the range 0.13 mm to 0.15 mm were classed as "large workers", those which were between 0.l0 mm and 0.12 mm "medium workers" and the remaining, between 0.05 mm and 0.07 mm, "small workers". The latter were statistically different from the two other subcastes (F = 22133; g.l = 2, 1497; P < 0.05) (Fig. 1A).



The number of workers counted within each size class in the 10 different nests showed that it was the medium sized workers who predominated in the foraging area (F = 25.365; df = 2, 27; P < 0.05). No difference occurred between the number of large and small workers present in the same area (Fig. 1B).

Trail following response of S. geminata workers to Dufour gland extracts. Behavioral test showed that the extract origin (from minor, medium or major workers) (nest 1: F = 203.2; df = 2, 441; P < 0.001), the worker size category of the tested ant (nest 1: F = 1190.4; df = 2, 441; P < 0.001), and the extract origin and tested worker size interaction (nest 1: F = 225.6; df = 4, 441; P < 0.001) significantly influenced trail-following responses of workers. Similar results were obtained for nest 2 (extract origin: F = 189.2; df = 2, 441; P < 0.001; tested worker size: F = 1189.2; df = 2, 441; P < 0.001); and the extract origin x tested worker size interaction (F = 219.43; df = 4, 441; P < 0.001).

In each combination, extracts from any worker size elicited higher responses than controls. The workers of the three size categories displayed a significantly higher trail-following response to Dufour gland extracts taken from ants of their own subcaste (Fig. 2A). However, the response to extracts taken from medium sized workers was always highest, independent of the tested worker subcaste (Fig. 2B). Similar results were obtained from nest 2. (data not shown)


Chromatographic profile of the Dufour gland secretions of S. geminata workers. Independent of the worker size category concerned, the secretion of the Dufour gland is composed of a mixture of alkaloids (venom components) and both saturated and unsaturated hydrocarbons (C13–C25) with an even and odd number of carbon atoms. In our study only compounds 1, 2 and 3 (Fig. 3) were considered as potential components of the trail pheromone of S. geminata as suggested by Barlin et al. (1976). Compound 1 has a mass spectrum characteristic of a bishomofarnesene with a M+ 232 molecular ion. The mass spectrum of peaks 2 and 3 possess the M+ 246 molecular ion displaying a fragmentation trishomofarnesene pattern.


When comparing the relative amount of the three components produced in the secretion of the different worker size, a positive correlation was observed between ant size category and relative amount of pheromone components (F = 9.29; df = 4, 81; P < 0.05). Notwithstanding, the principal component analysis of the relative proportions of compounds 1, 2 and 3 shows that there is a natural grouping of these compounds according to the worker size (Fig. 4). The first two principal components explain 96.04% of the variance that exists in compounds 1, 2 or 3.


Electroantennography (EAG). The amplitude of the EAG responses obtained for each worker size to series of Dufour gland extracts showed that assessed products (F = 203.24; df = 3, 264; P < 0.05), worker subcaste (F = 145.; df = 2, 264; P < 0.05) and assessed products x worker size interaction (F = 121.82; df = 6, 264; P < 0.05) significantly influenced the antennal response in workers of the three subcastes (Fig. 5). The workers from each of the subcastes displayed a significantly higher antennal response to Dufour gland extracts produced by ants of their same size (Fig. 5A). Likewise, the workers showed a significantly higher response to Dufour gland extracts produced by medium sized workers rather than large and small workers (Fig. 5B).


The antennal response of the S. geminata workers to the different Dufour gland extracts was significantly different when compared with the response elicited with hexane (control). This antennal response varied depending on the subcaste of the worker being assessed and fluctuated within a range of 0.57 mV and 1.97mV.

Discussion

Bioassay results demonstrated that Dufour gland secretion of medium workers released a significantly higher trail following responses to all three subcastes compared with the Dufour gland secretion from the other two subcastes. We also registered that the intensity of the trail-following response in medium-sized S. geminata workers was significantly higher when compared with both major and minor workers. Of particular interest is the fact that medium sized workers of S. geminata show a greater antennal capacity in perceiving trail pheromones. This indicates that there is a direct relationship between trail-following and antennal responses between subcastes. Many other studies describe electrophysiological responses to pheromones (Kern & Bestmann 1993, Andryszak et al. 1990) but none consider electrophysiological responses between subcastes. Highly significant behavioral and antennal responses of medium workers, together with their relative abundance in the foraging area involved in food transport to the nest (Fig. 1 B and unpublished observations) may lead that medium-sized workers are specialized in foraging activities. In other polymorphic ant species a similar relationship has been observed between behavioral specialization and morphological subcaste. For example, in the harvester ant Messor barbarus (L.)the medium sized workers are more involved in food collecting activities (Heredia & Detrain 2000). Similarly, in Acromyrmex lobicornis (Emery) two morphological subgroups each with specific functions can be differentiated: minor workers which take care of the brood and fungus inside the nest and major workers which are usually found outside the nest providing food to the colony (Quirán et al. 2001). However, further behavioral studies are needed to understand the respective role of the different worker subcastes of S. geminata on foraging trails.

The efficacy of a secretion often depends on a mixture of substances, thus the relative proportion of the components may be critical. When comparing the chromatographic profiles of the Dufour gland secretions for S. geminata workers, a positive correlation was observed between ant size and secretion quantity. Interestingly, each worker subcaste show a characteristic profile of the three components considered as being essential in the trail pheromone (Barlin et al. 1976). This could indicate that the relative abundance of the substances is critical to act as an efficient trail pheromone. Therefore, it seems likely that there is a correlation between medium sized worker specialization and chemical composition of the secretion but not with pheromone quantity. Variation in the proportions of secretion components between castes of varying sizes have been reported previously. For example, in S. geminata Brand et al. (1973) found that variations in proportions of cis-2-methyl-6-n-undecylpiperidine (cis C11) with trans-2-methyl-6-n-undecylpiperidine (trans C11), both present in poison gland secretions, were greater in soldiers than in medium workers. Similarly for S. invicta, Deslippe & Guo (2000) reported that the venom alkaloid composition varied across worker size and age. Furthermore, in Myrmica rubra (L.) there was a variation in the proportion of 3-octanol and 3-octanonein worker mandibular glands across worker size (Tricot et al. 1972).

A final point of interest is that minor and major workers are less abundant than median workers in the trail foraging area but they show an antenal response and perception to the Dufour gland secretion; however it seems that they might play a different role to that of forager. In other polymorphic ants different functions have been observed between subcastes, for example in A. capiguara (Gonçalves), two worker subcastes were found on foraging trail, large forager were found transporting grass while minors patrolled the trail area for threats, playing a key role in alarm reaction (Hughes & Goulson 2001). We conclude that medium workers of S. geminata exhibited a high trail following as well as a high antennal responses to Dufour gland secretion. This and their relative abundance in the field foraging area suggest that medium-sized workers are specialized in foraging activities.

Acknowledgments

We thank Antonio Santiesteban and Armando Virgen for technical assistance and Javier Valle-Mora for statistical advice (all at ECOSUR). YB thanks to CONACYT for a master scholarship.

Received 28/II/07. Accepted 09/X/07.

  • Andryszak, N.A., T.L. Payne, J.C. Dickens, J.C. Moser & R.W. Fisher 1990. Antennal olfactory responsiveness of the Texas leaf cutting ant (Hymenoptera: Formicidae) to trail pheromone and its two alarm substances. J. Entomol. Sci. 25: 593-600.
  • Barlin, M.R., M.S. Blum & J.M. Brand. 1976. Fire ant trail pheromones: Analysis of species specificity after gas chromatographic fractionation. J. Insect Physiol. 22: 839-844.
  • Bell, W.J. & R.T. Carde. 1984. Chemical ecology of insects. Chapman and Hale Ltd., London, 524p.
  • Brand, J.M., M.S. Blum & M.R.Barlin. 1973. Fire ant venoms: Intraspecific and interspecific variation among castes and individuals. Toxicon 11: 325-331.
  • Conover, W.J. & R.L. Iman. 1981. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stat. 35: 124-133.
  • Deslippe, R.J. & Y.J. Guo. 2000. Venom alkaloids of fire ants in relation to worker size and age. Toxicon38: 223-232.
  • Heredia, A. & C. Detrain. 2000. Worker size polymorphism and ethological role of sting associated glands in the harvester ant Messor barbarus Insects Soc. 47: 383-389.
  • Hughes, W.O.H. & D. Goulson. 2001. Polyethism and the importance of context in the alarm reaction of the grass-cutting ant Atta capiguara Behav. Ecol. Sociobiol. 49:503-508.
  • Kern, F. & J. Bestmann. 1993. Antennal electrophysiological responsiveness of the ponerine ant Leptogenys diminuta to trail and recruitment pheromones and its structure analogs. Naturwissenschaften80: 424-427.
  • Malo, E.A., L. Cruz-López, V. Castrejón-Gómez & J.C. Rojas. 2004. Antennal sensilla and electrophysiological response of male and female Spodoptera frugiperda (Lepidoptera: Noctuidae) to conspecific sex pheromone and plant odors. Ann. Entomol. Soc. Am. 97: 1273-1284.
  • Pasteels, J.M. & J.C. Verhaeghe. 1974. Dosage biologique de la pheromone de piste chez les fourrageuses et les reines de Myrmica rubra Insectes Soc. 21: 167-180.
  • Quiran, E.M., B.M. Corró Molas, V.E. Caramuti & J. Bernardos. 2001. Determinación preliminar de subcastas en obreras de Acromyrmex lobicornis Emery 1887 (Hymenoptera: Formicidae). Gayana (Concepc) 65: 19-25.
  • Risch, S.J. & C.R. Carroll. 1982. Effect of a keystone predaceous ant, Solenopsis geminata, on arthropods in a tropical agroecosystem. Ecology63: 1979-1983.
  • Smith, M.R. 1936. Consideration of the fire ant Solenopsis xyloni as an important southern pest. J. Econ.Entomol. 29: 120-122.
  • Statsoft, Inc. 2005. STATISTICA (Data analysis software system), version 7.1. www.statsoft.com
  • Travis, B.V. 1941. Notes on the biology of the fire ant Solenopsis geminata (F.) in Florida and Georgia. Fla. Entomol. 24: 15-22.
  • Tricot, M.C., J.M. Pasteels & B. Tursch. 1972. Phéromones stimulant et inhibitant I'aggressivité chez Myrmica rubra J. Insect Physiol. 18: 499-509.
  • Vander Meer, R.K., F. Alvarez & C.S. Lofgren. 1988. Isolation of the trail recruitment pheromone of Solenopsis invicta J. Chem. Ecol. 14: 825-838.
  • Vander Meer, R.K., F.D. Williams & C.S. Lofgren. 1981. Hydrocarbon components of the trail pheromone of the red imported fire ant, Solenopsis invicta Tetrahedron Lett. 22:1651-1654.
  • Way, M.J., G. Javier & K.L. Heong. 2002. The role of ants, especially the fire ant, Solenopsis geminata (Hymenoptera: Formicidae), in the biological control of tropical upland rice pests. Bull. Entomol. Res. 92: 431-437.
  • Wilson, E.O. 1959. Source and possible nature of the odor trail of fire ants. Science129: 643-644.
  • Wilson, E.O. 1962. Chemical communication among workers of the fire ant Solenopsis saevissima (Fr. Smith). 1. The organization of mass foraging. Anim. Behav. 10: 134-147.

Publication Dates

  • Publication in this collection
    16 May 2008
  • Date of issue
    Apr 2008

History

  • Accepted
    07 Oct 2007
  • Received
    28 Feb 2007
Sociedade Entomológica do Brasil Sociedade Entomológica do Brasil, R. Harry Prochet, 55, 86047-040 Londrina PR Brasil, Tel.: (55 43) 3342 3987 - Londrina - PR - Brazil
E-mail: editor@seb.org.br