ABSTRACT. by Agda Alves da Rocha 1 & Edilberto Giannotti 2

813 Foraging Activity of Protopolybia exigua (Hymenoptera, Vespidae) in Different Phases of the Colony Cycle, at an Area in the Region of the Médio S...
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Foraging Activity of Protopolybia exigua (Hymenoptera, Vespidae) in Different Phases of the Colony Cycle, at an Area in the Region of the Médio São Francisco River, Bahia, Brazil by Agda Alves da Rocha1 & Edilberto Giannotti2

ABSTRACT In this work, the foraging activity of Protopolybia exigua (de Saussure) was studied, aiming to verify the amplitude of the foraging time, the relation between the physical factors of weather (temperature, relative air humidity, luminosity and wind speed) and the daily activity of searching for resources, as well as to analyze the influence of the colony development phases and the number of individuals (adults and immatures) engaged in such activity. The study was carried out in two areas of the city of Bom Jesus da Lapa, Bahia, Brazil, during the period from January to June 2006, when the observation of 12 colonies of P. exigua was performed. The results revealed this species presented an amplitude of activity of almost 13 hours. There was an average of 44.4 nest exits and 37.6 returns a day by the nest workers and the Returns with Resources Index for this species was 93.5%. The foraging activity increased as of 10:01, and became more intense, with the peak from 1:01 p.m. to 4:00 p.m., when the highest temperatures (ºC) and the lowest values of relative air humidity (%) were observed. The colonies that had a larger number of larvae presented a higher average number of trips to the field per hour (10.94) and the number of females in the colony tends to induce foraging activity. There were no differences between the numbers of nest exits by the workers regarding the three phases of colony development. Keywords: social wasps, Epiponini, amplitude of foraging, physical factors of weather, Protopolybia exigua

Instituto de Biociências, Departmento de Biologia, Universidade Estadual Paulista (UNESP), C.P. 199, CEP 13506-900 Rio Claro, SP, BRAZIL email [email protected]; 2 [email protected]

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INTRODUCTION Protopolybia exigua exigua (de Saussure) is a neotropical social wasp that, in Brazil, occurs from Acre to Rio Grande do Sul States (Richards 1978). The first comb of its nest is stelocyttarus (pedunculate) and the others are built directly on the former combs (phragmocyttarus) (Wenzel 1991, Santos 2000). The early development of the colonies is performed by a group consisting of several fertile females (queens), followed by dozens of sterile females (workers and intermediates) (Machado 1974). Many studies were done with the objective of verifying several aspects related to the feeding habits of social wasps, such as daily and seasonal activity of searching for resources, individual ability, items collected, influence of colony and environment factors, and foraging activity behavior patterns (Machado 1974, Simões 1977, Simões & Zucchi 1980, Gobbi & Machado 1985, 1986, Giannotti et al. 1995, Silva & Noda 2000, Andrade & Prezoto 2001, Silva 2002, Paula et al. 2003, Cruz et al. 2006, Prezoto et al. 2006). The foraging activity of these wasps varies throughout a day and throughout the seasons. The amplitude may vary according to the period of the year, but also according to the place where the study is carried out. Probably, as observed by Silva (2002), wasps may have a greater amplitude of activity as the latitude of the region where they are decreases. That is, the closer they are to the Equator, the greater their amplitude of activity. Usually in the hot and humid season the amplitude of the foraging time is greater than in the cold and dry season and, generally speaking, social wasps leave the nest in the hottest, least humid times of the day, apart from Angiopolybia pallens (Lepeletier), that showed preference for twilight periods in its foraging activity (Cruz et al. 2006). In the city of Juiz de Fora, Minas Gerais, it was recently observed that the foraging activity of P. exigua, in the hot and humid season, is greater than in the cold and dry season, when there is a decrease in the number of active nests (Ribeiro-Júnior et al. 2006). Paula et al. (2003) stated that foraging activity results from a complex interaction between the phase of colony development and climatic factors. According to Spradbery (1973), although the predominant social conditions in the colony play a role in the process of the foraging activities, the conditions that establish the limits where foraging is possible are mainly physical, such



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as light and temperature intensity. Temperature (positively) and air relative humidity (negatively) seem to have great influence on the foraging activity of Brazilian social wasps (Giannotti et al. 1995, Andrade & Prezoto 2001, Resende et al. 2001), though luminosity is also recognized as an important stimulant (Silva & Noda 2000, Silva 2002). The aim of this study was to answer the following questions, concerning the foraging activity of P. exigua in the region of the Médio São Francisco River, Bahia: 1. What is the time amplitude of the foraging activity? 2. What is the relation between the physical factors of weather (temperature, relative air humidity, luminosity and wind speed) and the daily activity of search for resources? 3. What is the influence of the phases of colony development and the number of individuals (adults and immatures) on the foraging activity?

MATERIAL AND METHODS Location of the Study Area

The São Francisco River basin is commonly divided into four physiographical regions: Alto São Francisco (the Upper São Francisco), which extends from its source to a little beyond the city of Pirapora, Minas Gerais; Médio São Francisco (the Middle São Francisco), which goes from Pirapora, where the navigable portions begin, to Remanso, Bahia; Sub-médio (the Sub-Middle São Francisco), from Remanso to Paulo Afonso, Bahia; and Baixo (the Lower São Francisco), from Paulo Afonso to the mouth of the river, between the states of Sergipe and Alagoas (MMA 2006). The study was carried out in two areas comprised in the city of Bom Jesus da Lapa, in the region of the Médio São Francisco River, Bahia (Fig. 1). One area was on a 120 ha farm, Fazenda Itibiraba (13º11’35”S and 43º24’01”W), located on the right side of the river. The vegetation structure of this area comes from a contact between the Brazilian Caatinga and the Seasonal Forest. The other area was a 33 ha country house, Chácara Nossa Srª Aparecida (13º15’46”S, 43º27’34”W), located within the boundaries of the Extractive Reserve of São Francisco, belonging to the city of Serra do Ramalho, Bahia. It is on the left side of the São Francisco River, and its vegetation consists of semi-decidual and decidual seasonal forest. The climate in the city of Bom Jesus da Lapa ranges from semi-arid and dry to sub-humid, and the rainy season lasts from November to March (SEI

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Fig. 1. Location of the study areas.

2006).

Data Collection

During the period from January 25 to June 2, 2006 (part of the rainy season and the beginning of the dry season) the observation of 12 colonies of P. exigua was done. According to the classification of Jeanne (1972), three colonies were at the pre-emergence stage and eight were at the post-emergence stage. However, according to Noll (1995) one colony (number 9) was at the “post-swarming” stage. Each colony was observed for 45 minutes per hour, from 6 a.m. to 7 p.m., totaling 9h45 of observation per colony and 117h of observation of the 12 colonies. In the intervals, the number of nest exits and returns by the workers were quantified. Two records of the following data were made for each hour of observation (every 30 minutes): temperature (ºC) and relative air humidity (%), using a digital thermo-hygrometer; luminosity (lux), using a light meter; and wind speed (m/s), with an anemometer. At the end of each observation, after the sunset, the nests were collected along with the adult individuals for quantification, as well as the cells and



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the immatures. The adult females were dissected in order to set the degree of ovarian development and insemination, and hence determine the castes. In the colonies that had more than 300 females, 40% of them were dissected and a projection of the total was calculated based on the results obtained. The degree of ovarian development was defined according to Noll et al. (1996).

Data Analysis

The average of the data of the physical factors of weather was related to the frequency of nest exits, by means of Regression Analysis, in order to verify the influence of such factors on the gathering of different resources. Spearman Correlation Analysis was used to check the existence of correlation between the number of immatures (eggs, larvae and pupae) and adults (males, workers, intermediates and queens) present in the nest and the average frequency of nest exits by the workers. All the analyses described above were performed with the statistical software Bioestat 4, at a level of significance of p < 0.05. The Returns with Resources Index (RI), also called Efficiency Index (EI) (Giannotti et al.1995), was calculated using the following formula: RI = no. of foragers that return with resources X 100/ no. of foragers that return to the nest

RESULTS AND DISCUSSION Colonies Studied

There was great variation in the number of individuals in the different castes of P. exigua and, unlike what was observed by Machado (1974), there was a higher proportion of workers than intermediates in all the colonies (Table 1). There was an average of 16.3 ± 27.3 queens, 35.4 ± 41.0 intermediates and 162.9 ± 177.6 workers per nest. The nests observed presented an average of 134.4 ± 132.4 eggs, 91.75 ± 94.1 larvae and 188.8 ± 218.1 pupae (Table 2). Apart from colonies 9 and 11, all others presented nectar stored in the nest cells. This fact had already been reported in this same species (Machado 1974) and in Protopolybia sedula (Saussure, 1854) (Machado 1977). Individuals of Chalcididae (Hymenoptera) were found in the nests 3 and 8, and in the nests 9 and 12 there were pupae of Megaselia sp. (Diptera, Phoridae), a genus already recognized as a predator of hymenopteran im-

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Sociobiology Vol. 50, No. 3, 2007 Table 1. Information about the colonies of Protopolybia exigua studied in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006. Date Local Adults Queens Interm. Workers %% Colony

1 2 3 4 5 6 7 8 9 10 11 12

1/25/2006 1/28/2006 1/31/2006 2/10/2006 2/18/2006 2/21/2006 2/24/2006 2/28/2006 2/25/2006 5/26/2006 5/31/2006 6/2/2006

1 * 1 2** 2 2 2 1 1 2 2 2 2

3 66 32 1 7 1 37 3 3 5 1 36

12 79 56 0 28 3 134 5 2 53 5 48

50 294 135 12 55 21 236 97 14 470 56 515

Stage

0 Post-emergence (pre-male) 165 Post-emergence (post-male) 0 Post-emergence (pre-male) 0 Pre-emergence (egg) 0 Pre-emergence (larva) 0 Post-emergence (pre-male) 0 Post-emergence (pre-male) 0 Pre-emergence (pupa) 0 Post-swarming 67 Post-emergence (post-male) 0 Post-emergence (pre-male) 0 Post-emergence (pre-male)

1* Fazenda Itibiraba farm; 2** Chácara Nossa Sª Aparecida country house. Table 2. Contents of the cells in the colonies of Protopolybia exigua studied, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006. Colony

Contents of the Cells

Eggs Larvae Pupae Nectar Empty

Parasites /Predators

Total



0 0 6* 0 0 0 0 10* 1** 0 0 56**

477 1680 640 122 194 103 1409 269 572 597 99 599

1 2 3 4 5 6 7 8 9 10 11 12

62 367 154 25 100 54 412 105 0 147 10 177

Average ± ST 134.4 ± 132.4



39 220 142 0 84 18 282 40 0 190 37 49 91.7 ± 94.1

199 613 253 0 0 18 550 6 12 228 49 338

14 2 38 4 4 7 42 61 0 5 0 15

163 478 47 93 6 6 123 47 559 27 3 20

188.8 ± 218.1

16.0 ± 20.0

131 ± 188.5

6.1 ± 16.0

563.4 ± 506.6

* Chalcididae (Hymenoptera), ** Megaselia sp. (Diptera, Phoridae)

matures (Solis et al. 2005). The presence of parasites in the nest is common in wasps of the tribe Polistini. Polistes metricus Say, 1831, presented 70% of



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its nests infected (Nelson 1968). Makino (1985) listed the parasitoids of wasps of the family Polistinae, and registered from the literature 68 species, distributed into 14 families, and in 4 orders, among them two species of Brachymeria (Chalcididae) infesting colonies of Polistes instabilis de Saussure, 1853 and Brachygastra augusti (de Saussure, 1854). Besides, he also registered two species of Megaselia in nests of Polistes canadensis (Linnaeus, 1758) Agelaia testacea (Fabricius, 1804), Mischocyttarus labiatus (Fabricius, 1804) and Polistes exclamans Viereck, 1906. The presence of the phorid Megaselia scalaris (Loew, 1866) was responsible for the abandonment of 28.6% of the nests of Mischocyttarus cerberus styx Richards, 1940 (Giannotti 1998). Its larvae destroyed eggs, larvae and pupae of that wasp.

Foraging Activity Pattern

In the region studied, P. exigua started its foraging activity at 6:06 a.m. and stopped in the twilight, at 6:39 p.m., hence the amplitude of activities outside the nest was almost 13 hours. Ribeiro-Júnior et al. (2006), who studied the foraging activity of this species, in Minas Gerais State, in different seasons, found a slightly smaller amplitude: 7:30 a.m. to 5.30 p.m., in the hot and dry season, and 11 a.m. to 3.30 p.m., in the cold and dry season. Besides the season, the geographical region seems to have an influence on the foraging activity of social wasps. According to Silva (2002), the colonies of a same species, located in the north of Brazil, apparently presented greater daily amplitude than the ones located in the southeast and south. She compared the amplitude of the foraging activity of Mischocyttarus drewseni de Saussure, 1857 in São Paulo to the ones in Paraná (Dantas-de-Araújo 1980) and Pará States ( Jeanne 1972) and found this species presented increasing amplitudes as the site latitude decreased. Gobbi (1977), in São Paulo, for Polistes versicolor (Olivier, 1791), registered an amplitude of nine hours (8:00 a.m. to 5:00 p.m.). Prezoto et al. (1994) found, in São Paulo, an amplitude from 8:08 a.m. to 6:01p.m. (10 hours) for Polistes simillimus Zikán, 1951. Polistes lanio (Fabricius, 1775), also in São Paulo, exhibited an amplitude of about nine hours (8:03 a.m. to 5:14 p.m.) in the cold season and 13 hours in the hot season (5:58 a.m. to 6:46 p.m.) (Giannotti et al.1995). Resende et al. (2001), in Bahia, for Polybia occidentalis (Olivier, 1791) found an amplitude from 6:41 a.m. to 5:32 p.m.. Silva (2002)

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Fig. 2. Foraging activity pattern of the colonies of Protopolybia exigua studied in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006.

observed in M. drewseni, in São Paulo, an amplitude of 11 hours of activity (7:00 a.m. to 6:00 p.m.) in the hot season and seven hours (11:00 a.m. to 6:00 p.m.) in the cold season. Polybia sericea (Olivier, 1791), in Bahia, showed an amplitude from 6:00 a.m. to 6:00 p.m. (Bichara-Filho 2003), similar to the value found for Synoeca cyanea (Fabricius, 1775) (6:30 a.m. to 6:30 p.m.) in Minas Gerais (Elisei et al. 2005). The foraging activity of P. exigua in Bahia increased from 10:01 a.m. on, and became more intense, with the peak from 1:01 p.m. to 4:00 p.m., decreasing only after 5:01 p.m., when the number of returns exceeded the number of nest exits (Fig. 2). In the period from 6:01 p.m. to 7:00 p.m. the number of exits was still higher than in the first period of observation (6:00 a.m. to 7:00 p.m.), though the number of returns was higher. This pattern was similar to the one observed by Ribeiro-Júnior et al. (2006) in the hot and humid season. There was an average of 44.4 nest exits and 37.6 returns by the workers of P. exigua a day. There seems to be a disproportional number of wasps that leave the nest throughout the day (Fig 2), in relation to the ones that return after. One of the factors that may have an influence, although slightly, would



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Fig. 3. Average values (%) of temperature (ºC), relative air humidity (%), luminosity (Lux) and wind speed (m/s) throughout the day, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006.

be predation, which would hinder some wasps from returning. Nevertheless, as reported by Resende et al. (2001), it is possible that the wasps had returned to the nest only the day after, and spent the night outside. This is likely to happen more often to younger individuals, which might have greater difficulty regarding orientation upon returning to the nest. The Returns with Resources Index for this species was 93.5%. It is a very high value, if compared to the ones of other species. Silva (2002) found, for M. drewseni, a percentage of wasps returning with resources of 86%. Giannotti et al. (1995), for P. lanio, observed a value of 68.8% in the cold and

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dry season and 83.9% in the hot and humid season. The values of RI may reflect the colony and environment conditions that are predominant in the period of the study, the availability of resources in the environment, but may also indicate intrinsic characteristics of the species.

Influence of the Physical Factors of Weather

There was great variation of the physical factors of weather throughout the day. The temperature increased a lot as of 11:01h and remained high until the last periods of observation, unlike what happened to the humidity (Fig. 3). It was noticed that, the higher the temperature, the higher the activity of the wasps, confirmed by Regression Analysis (r= 0.83 p= 0.0001) (Fig. 4). On the other hand, the higher the humidity, the lower the number of nest exits by the foragers (r= - 0.76, p = 0.0002) (Fig. 5), corroborating previous studies (Giannotti et al. 1995, Silva 2002, Andrade & Prezoto 2001, Ribeiro-Júnior et al. 2006). Most colonies found built their nests at spots facing west, which led to higher temperatures during most times of the day. This might explain the high intensity of foraging in the late afternoon, once the sun reflected directly on the nests until the sunset. There was a higher number of wasp exits as luminosity increased, but this factor does not seem to have great influence on the foraging activity of P. exigua throughout the day (r= 0.22, p = 0.0560). This result differs from what seems to occur with M. cerberus styx (Silva & Noda 2000), M. drewseni (Silva 2002) and S. cyanea (Elisei et al. 2005), but it is similar to the results found in P. occidentalis (Resende et al. 2001). In temperate regions, luminosity seems to be an important factor, influencing the beginning and the end of the foraging activity in wasps of the subfamily Vespinae, once the temperature does not vary so much during the day as in tropical regions (Edwards 1980). There was a direct relation between the wind speed and the nest exits by the wasps (r = 0.64 p = 0.0013). However, during the observation of colony 4, there was a day with strong winds, up to 3 m/s, on which there were no Fig. 4. Average frequency of workers of Protopolybia exigua leaving the nest as a function of temperature, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006 (r= 0.83 p= 0.0001). Fig. 5. Average frequency of workers of Protopolybia exigua leaving the nest as a function of relative air humidity, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006 (r= - 0.76 p = 0.0002).

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Fig. 6. Average frequency of workers of Protopolybia exigua leaving the nest as a function of wind speed, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006 (r = 0.64 p = 0.0013).

Fig. 7. Relation between the number of larvae and the average of exits per hour of the workers of Protopolybia exigua studied, in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006.



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nest exits, as it was also observed by Elisei et al. (2005). In those moments, most wasps went into the nest, while few of them stood on the outer part. As the wind speed decreased, some of them went out and performed trophallaxis with the wasps that were outside, probably passing stored nectar on. The activity increased only after 4:01 p.m., when the wind speed decreased, allowing the wasps to leave.

Colony Development and Foraging Activity

Silva (2002) defined that the main internal component that induced foraging activity was the number of larvae, for it was observed that, the higher the number of larvae present in the nest, the higher the average number of trips per hour. This fact was also observed in the present study (Fig. 7). The colonies that did not have larvae presented an average of 0.14 trips per hour; the ones that had between 1 and 100 larvae showed an average of 1.94 exits; colonies containing from 101 to 200 larvae had an average of 3.59 exits; and the colonies that had from 201 to 300 larvae presented an average number of trips to the field per hour of 10.94. According to Spearman Correlation Analysis, there was a positive correlation between the number of larvae present in the nest and the average number of exits per day (r=0.91, p= 0.0001). However, it was also observed that there was a correlation between the number of eggs and the average number of exits per day (r= 0.90, p= 0.0001) and between the same factor and the number of pupae (r= 0.64, p=0.0236). This may be explained by the fact that in colonies in which there is a higher number of larvae, coincidentally with the post-emergence stage, there is growth in the colony, with a higher rate of egg-laying and higher number of pupae developing, hence a higher number of females emerging. There was a positive correlation between the number of females present in the nest (queens: r = 0.77, p = 0.0032; intermediates: r = 0.85, p = 0.0004 and workers: 0.81, p = 0.0014) and the average number of exits per day, but there was no correlation between the number of males (r = 0.53, p = 0.0748). Silva (2002) stated that the presence of females in the colony, whether they are active or potential foragers, influences foraging activity, for they will do the activities of collecting and capturing resources for the colony. Furthermore, there is higher need of energy supplies.

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Fig. 8. Pattern of the Foraging Activity (Average Frequency of Exits) of Protopolybia exigua in different phases of the colony cycle, in the region of the Médio São Francisco River, Bahia, in the period of January to June 2006.



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Fig. 8 displays the pattern of the foraging activity of P. exigua, in different phases of the colony cycle, in the region studied. There is difference in the foraging activity of P. exigua, concerning the phases of colony development. At the pre-emergence stage, there was an average of 29.6 nest exits by the workers and 28.5 returns. At the post-emergence stage, there was an average of 55.4 nest exits and 45.6 returns. The only colony that was at the postswarming stage presented an average of 1.3 exits and 1.4 returns per day. The amplitude was 12 hours for the pre and post-emergence stages, while at the post-swarming stage it was 8 hours a day. According to Andrade & Prezoto (2001), the nourishment needs of a colony of Polistes ferreri Saussure, 1853 at the pre-emergence stage are low, due to the small number of larvae, which demand less foraging efforts. Silva (2002) stated that another factor responsible for the low frequency of foraging activity in this phase, at least in Mischocyttarini, might be the exposure to usurpers and predators, for the small amount of founders would have to provide the colonies with resources as well as defend the nest. In colonies of wasps Epiponini this does not take place, once the nest foundation happens by swarming, hence with a high level of individuals able to defend the colony. This number is, however, much smaller than the one at the post-emergence stage, a phase of the colony cycle when the foraging activity tends to be more intense, when the first imagoes emerge, as it happens to P. exigua. In this phase the colonies grow a lot, along with the number of larvae, requiring greater feeding supplies and consequently a higher number of nest exits by the workers. The foraging activity decreases a lot at the post-swarming stage, which, according to Noll (1995), would be the one characterized by the presence of individuals in the mother nest, after the production of sexed individuals and the swarming. Such few individuals would be immatures, perhaps including a small amount of old queens and some males. The average number of nest exits did not exceed 10 per observation time in this phase, while at the preemergence stage it reached almost 50 and in post-emergence almost 100 nest exits per observation time. All the factors analyzed (Table 3) influenced the foraging activity of P. exigua during the pre-emergence stage. At post-emergence, nevertheless, only temperature (positively) and humidity (negatively) influenced strongly the

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Table 3. Spearman Correlation Analysis between the frequency of nest exits by workers of Protopolybia exigua and physical factors of weather (temperature, humidity, luminosity and wind speed), in the region of the Médio São Francisco River, Bahia, in the period from January to June 2006. Development Stage Temp. (ºC)

Spearman Correlation (frequency of nest exits) Hum. (%)

Lum. (lux)

Speed (m/s)

Pre-emergence r = 0.52 p = 0.0033 r = - 0.58 p = 0.0017 r = 0.79 p = 0.0001 r = 0.29 p = 0.0323 Post-emergence r = 0.82 p = 0.0001 r = - 0.73 p =0.0002 r = 0.08 p = 0.1772 r = 0.15 p = 0.1034 Post-swarming r = 0.06 p = 0.6416  r = - 0.01 p = 0.6257  r = 0.04 p = 0.5127   r = 0.35 p = 0.0185

foraging activity. In this case, the colony factors seem to have an influence stronger than the physical factors of weather. In the decline phase only the wind speed influenced in a positive way, though slightly. Paula et al. (2003) observed that colonies in different phases of Parachartergus fraternus reacted the same way to temperature (increasing the frequency of exits) and humidity (decreasing the frequency of exits).

CONCLUSIONS The foraging activity of Protopolybia exigua reacted to the environment conditions predominant in the region, but also to the colony conditions existent in the nest, such as the high number of larvae and females, which seemed to influence the nest exits by the workers.

ACKNOWLEDGMENTS The authors thank Mr. Guarim Ferreira da Rocha, Alessandra de C. Vaz and Alisson Cardoso R. da Cruz for their help in collecting the data; Messrs Clovis José de Oliveira and Paulo Aubieri for allowing entrance to their properties in order to carry out the work; the company Empresa Baiana de Desenvolvimento Agrícola (EBDA), in Bom Jesus da Lapa, BA, for providing transportation to the areas of study; and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the financial support (Process: 130371/2006-8).

REFERENCES Andrade, F. R. & F. Prezoto, 2001. Horários de atividade forrageadora e material coletado por Polistes ferreri Saussure, 1853 (Hymenoptera, Vespidae), nas diferentes fases de seu ciclo biológico. Revista Brasileira de Zoociências 3 (1): 117-128.



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