Foraging of Parachartergus fraternus (Hymenoptera: Vespidae: Epiponini) on cloudy and sunny days

Foraging of Parachartergus fraternus (Hymenoptera: Vespidae: Epiponini) on Cloudy and Sunny Days

by

Germi Porto Santos1, José Cola Zanuncio2,5, Evaldo Martins Pires2, Fábio Prezoto3, José Milton Milagres Pereira2 & José Eduardo Serrão4

ABSTRACT

Foraging dynamics of a colony of Parachartergus fraternus (Gribodo) (Hymenoptera: Vespidae, Epiponini) were evaluated in Viçosa, Minas Gerais State, Brazil on cloudy (low brightness) and sunny (high brightness) days from 07:00 A.M. to 06:00 P.M. when the temperature and relative humidity were registered every 15 minutes. The temperature was milder and the rela-tive humidity higher and with lower variations on the cloudy day with the opposite being registered on the sunny days. The combination of the relative humidity and temperature determined foraging dynamics of P. fraternus. In both situations, the temperature had positive effect and the relative humidity negative effect on foraging activity of P. fraternus.

Key words: Wasps, foraging dynamics, behavior, colony activity.

INTRODUCTION

Social wasps are important for studies of alimentary webs because they may feed on plants and herbivores in natural and anthropic communities (Marques 1996, Gonring et al. 2003, Weiss et al. 2004). However, individuals of this group are parasitized by Hymenoptera and Diptera species (Soares et al. 2006; Silva Filho et al. 2007) and their immatures (Martins et al. 2008) as well as their nest characteristics (Silva et al. 2006) were studied.

1EMBRAPA/EPAMIG, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais State, Brazil.2Departamento de Biologia Animal, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais State, Brazil.3Departamento de Zoologia, Universidade Federal de Juiz de Fora, 36036-900 Juiz de Fora, Minas Gerais State,, Brazil4Departamento de Biologia Geral, Universidade Federal de Viçosa, 36570-000 Viçosa, Minas Gerais State, Brazil.5Author correspondent: [email protected]

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Social wasps are biological control agents of insect pests (Andrade & Prezoto 2001; Prezoto & Gobbi 2005), mainly of Lepidoptera larvae to obtain protein to feed their immatures (Gianotti et al. 1995; Richter 2000; Prezoto et al. 2006). Polybia dimidiata (Olivier) (Farinha & Pinto 1996); Polybia ignobilis (Haliday 1936) (Gobbi & Machado 1986); Polybia occidentallis (Olivier) (Gobbi et al. 1984); Polybia inhabitant from São Paulo Ihering (Gobbi & Machado 1985) and Polybia sericea (Olivier, 1791) (Marques 1996) are usually found preying upon Lepidoptera larvae which are pests in agriculture (Leite et al. 2001) and forest (Zanuncio et al. 1993) plantations.

Social wasps are generalist opportunists and they forage for water, vegetable pulp, carbohydrates and protein of animal origin for their survival and nest construction (Elisei et al. 2005). The location, recognition, choice of appro-priate prey and returning route to the nest are characteristics of wasps with high sensorial mechanisms (Prezoto & Gobbi 2005).

Polistinae adults feed, usually, on nectar and honeydew stored in viscous drops inside cells of their nests. Species as Parachartergus fraternus (Grobodo) (Hymenoptera: Vespidae) can obtain the honeydew from insects of the family Aetalionidae (Letourneau & Choe 1987). The genus Parachartergus is small with 16 species distributed from Mexico to the south of Argentina. Ten of the species are found in Brazil and two of them are endemic. The nests of this insect are formed by several layers of cells fixed to leaves or branches that ramify to a lateral pedicel (Letourneau & Choe 1987). Independently of colony age, immatures of P. fraternus are morphologically, indistinguishable and their differences are mainly physiologic ones. This explains the occur-rence of totipotency on their females to determine the castes of P. fraternus (Mateus et al. 2004).

The objective of this work was to observe the foraging dynamics of P. frater-nus on a cloudy and a sunny day on the campus of the Federal University of Viçosa in Viçosa, Minas Gerais State, Brazil.

MATERIAL AND METHODS

This research was developed with a colony of P. fraternus on the Campus of the Federal University of Viçosa in Viçosa, Minas Gerais State, Brazil in a plant of Codiaeum variegatum (Euphorbiaceae). The nest of this wasp was fixed to a vertical stem in the central part of this plant at 1.8 meters above

433 Santos, G.P. et al. — Foraging of Parachartergus fraternus

the soil with east exposure. Foraging activity of P. fraternus

was observed from 07:00 A.M. to 06:00 P.M. in September 18 and 19, 2002 at 3.5 meters from this nest. The number of individuals of this wasp, leaving and returning to the nest, and the temperature and relative humidity were registered every 15 minutes with a thermohygrograph at one meter from the colony. The first day of evaluation was cloudy without sun and the second

one had clouds until 10:00 A.M. (sunny day). Behavior aspects of P. fraternus were observed, analyzed and registered.

Foraging activity of P. fraternus in the cloudy and sunny days was submitted to the variance analysis at p< 0.05. The temperature and relative humidity were correlated (Spearman correlation) to their effects on the activity of these wasps. These analyses were made with the statistical program R (R Develop-ment Colors Team 2006) considering a significance level of p< 0.05.

RESULTS

Morphological traits of Parachartergus fraternusThe dorsal and ventral parts of the body of P. fraternus workers are black-

ish, which can help in the identification of this species. The abdomen of this wasp is of fusiform shape, covered with short hairs which can be seen under a stereomicroscope and it is linked to the thorax by a pedunculum. The mesothoracic wings, when resting, are, longitudinally bent and with dark color with the last distal part colorless and with a clear appearance, almost white, being the main characteristic to identify P. fraternus (Fig. 1). The metathoracic wings of this wasp are translucent with very pronounced veins. The compound eyes of P. fraternus are big with large number of facets while the antennae are geniculate. The mouth parts are orange and the width and length of their bodies were 20 and 10 mm respectively.

Fig. 1. Parachartergus fraternus worker. Viçosa, Minas Gerais State, Brazil.


Behavior of the population of Parachartergus fraternusThe activity of the colony of P. fraternus started about 06:00 A.M. with

four individuals walking over the nest during approximately one hour and with a single one in constant surveillance during the rest of the day (Fig. 2A). This situation was only modified when birds that landed on the plant made more individuals of this wasp to leave the nest with aggressive behavior (Fig. 2B). As this disturbance decreased, most individuals returned to the interior of the nest after an interval of 45 minutes and only the scout stayed outside. Intense disturbances made some individuals to assume positions near the entrance hole of the colony but they returned to the interior of the nest if the disturbance did not increase.

Daily rhythm of Parachartergus fraternus foragingTemperature and relative humidity differed between the two days of

evaluation, with more accentuated oscillations in the sunny one. The rela-tive humidity was 75.75 ± 1.27% and 54.77 ± 1.14%, respectively, between 07:00 A.M. and 01:00-02:00 P.M. with daily average of 61.22 ± 0.99% and variation interval of 25.4% on the cloudy day. Lower and maximum tempera-tures were 21.13 ± 0.48 and 25.65 ± 0.36 oC between 07:00-08:00 A.M. and

Fig. 2. Parachartergus fraternus. A, Nest with a scout wasp as sentinel; B, Nest with individuals showing defensive behavior after the colony is disturbed.


from 01:00-02:00 P.M. with daily average of 23.87 ± 0.26 oC and variation interval of 7.5 oC. On the sunny day, maximum and minimum peaks of the relative humidity were found between 07:00-08:00 A.M. and from 12:00 A.M.-01:00 P.M. with 78.25 ± 1.43% and 31.67 ± 0.68%, respectively and with daily average and variation interval of 45.33 ± 2.29 oC and 51.0%. The minimum and maximum temperatures were found at 07:00-08:00 A.M. and 00:00-01:00 P.M. respectively with daily average of 26.75 ± 0.62 oC and variation interval of 14.8 oC (Table 1).

The number of wasps foraging (leaving and returning to the colony) was lower in the cloudy day than the sunny day (F= 13.91; p= 0.0003) (Table 2).

The Spearman correlation showed positive (temperature) and negative (relative humidity) effects on the foraging activity of P. fraternus (Table 3).

A total of 235 exits and 241 returns of individuals of P. fraternus were registered during the cloudy day, with larger number of exits up to 12:00 P.M. and the inverse, except from 01:00-02:00 P.M., during the rest of the day. The foraging rhythm of P. fraternus reached 56.1% from 11:00 A.M. to 03:00 P.M. coinciding with the lowest values of relative humidity and increasing temperature (Fig. 3).

Parachartergus fraternus had 449 exits and 474 returns on the sunny day which was practically double that on the cloudy one and with higher numbers

Table 1 - Mean temperature (oC) and relative humidity (%) every hour from 07:00 A.M. to 06:00 P.M. Viçosa, Minas Gerais State, Brazil

Cloudy day Sunny dayInterval Temperature Relative humidity Temperature Relative humidity

7-8 h 21.13 ± 0.48 75.75 ± 1.27 19.15 ± 0.24 78.25 ± 1.438-9 h 22.20 ± 0.33 67.82 ± 1.28 21.07 ± 0.24 68.67 ± 1.00

9-10 h 23.33 ± 0.05 62.75 ± 0.78 24.85 ± 0.77 53.95 ± 2.2210-11 h 24.37 ± 0.16 58.85 ± 0.13 28.10 ± 0.59 42.82 ± 2.2211-12 h 25.15 ± 0.27 55.97 ± 0.69 31.70 ± 0.53 32.00 ± 0.4412-13 h 24.75 ± 0.16 57.20 ± 0.37 32.12 ± 0.59 31.67 ± 0.6813-14 h 25.65 ± 0.36 54.77 ± 1.14 29.50 ± 0.19 34.87 ± 0.5514-15 h 25.43 ± 0.08 55.82 ± 0.44 29.47 ± 0.16 34.90 ± 0.2315-16 h 25.33 ± 0.27 56.13 ± 0.78 28.35 ± 0.27 35.62 ± 0.4016-17 h 23.80 ± 0.22 61.33 ± 0.88 26.05 ± 0.25 39.05 ± 0.6717-18 h 22.50 ± 0.30 67.05 ± 1.40 23.97 ± 0.34 46.90 ± 2.19Mean 23.87 ± 0.26 61.22 ± 0.99 26.75 ± 0.62 45.33 ± 2.29


of exits than returns up to 12:00 A.M. Contrarily, the number of individuals that returned to the colony was higher than those of exits in the remainder of the day. The relative humidity decreased and the temperature increased, strongly, between 07:00 A.M. and 12:00 A.M. and staying practically stable up to 01:00 P.M. In this period, the foraging rhythm was more intense, with 63.5% of exits and returns. Foraging rhythm decreased from 02:00 to 06:00 P.M. when the relative humidity increased and the temperature decreased (Fig.4).

Differences between the number of individuals that left to forage and those returning to the colony was bigger in the sunny (5.25%) than in the cloudy (2.48%) days.

DISCUSSION

Differences in foraging rhythm of P. fraternus between cloudy and sunny days show that the combination of relative humidity and temperature deter-mines foraging dynamics of this species. The high relative humidity and mild and low oscillations of temperature on the cloudy day reduced the foraging activity of P. fraternus. Conversely, the increase of temperature and decreasing relative humidity increased this activity, which was similar to results for this

Table 2 - Number of wasps (means ± errors) in foraging activity sampled every 15 minutes. Viçosa, Minas Gerais State, Brazil

Wasp exits Wasp returns

Cloudy day 5.34 ± 0.80 b 5.47 ± 0.54 b

Sunny day 10.20 ± 1.29 a 10.77 ± 1.40 a

Means followed by the same letter, per column, are similar for the test F with p< 0.05.

Table 3 - Correlation between foraging activity of Parachartergus fraternus (Hymenoptera: Vespidae) with temperature and relative humidity. Viçosa, Minas Gerais State, Brazil

r pTemperature oC 0.8067* < 0.0001

Relative humidity (%) - 0.7537 < 0.0001


wasp in Matias Barbosa, Minas Gerais State, Brazil that had larger activity in the hottest part of the day, usually, between 12:00 A.M. and 02:00 P.M. (Paula et al. 2003).

Fig. 3. Daily exits and returns of Parachartergus fraternus indivduals on a cloudy day from 7:00 AM to 6:00 PM.

Fig. 3. Daily exits and returns of Parachartergus fraternus indivduals on a sunny day from 7:00 AM to 6:00 PM.


Parachartergus fraternus foraging was more intense on the sunny day but with higher values during certain climatic conditions and being directly proportional to the temperature and, inversely, to relative humidity. The im-pact of climatic factors on the foraging dynamics of P. fraternus was evident because the evaluations were done on subsequent days. This eliminated the interference of other variables such as age, population density and the stress of the colony which could interfere with the results. This result corroborates those of Polistes simillimus Zikán which foraged from 8:08 A.M. to 06:00 P.M. but with larger intensity from 10:30 A.M. to 05:00 P.M. and with positive correlation between the temperature and negative correlation with the relative humidity (Prezoto et al. 1994). Protopolybia exigua (Saussure) presented more intense foraging activity in hot and dry periods with positive and negative correlation, respectively with temperature and relative humidity (Ribeiro Júnior et al. 2006). The foraging activity of Mischocyttarus cerberus styx Richards, showed 79 and 69% positive correlation with temperature, that is, the higher these values, the larger the number of exits of foragers from the nest. The relative humidity showed 70% negative correlation. Larger values of this relative humidity reduced the number of foragers leaving the nest, which demonstrates that these factors are limiting, inducing or inhibiting foraging activity of this wasp (Silva & Noda 2000).

The combination of temperature and relative humidity seems to condition foraging rhythm of most social wasps such as P. lanio lanio in Rio Claro, São Paulo State, Brazil. This wasp exhibited larger numbers of individuals foraging/hour in humid and hot periods, sug-gesting metabolic adjustment to seasonal changes of temperature and relative humidity. Besides, factors such as the photo period and, possibly, the light brightness, atmospheric pressure and the winds can affect foraging rhythm of wasps, with longer days being more favorable for flight (Giannotti et al. 1995). Polistes occidentalis occidentalis (Olivier) (Hymenoptera: Vespidae) requires a temperature from 20.5 to 29.0oC and relative humidity lower than 60% to leave the nest, with a tendency of increasing exits along the day as temperature and heat increase and the relative humidity decreases. The relationship between physical factors of the weather and activity of these wasps is conditioned mainly by extreme values with very low temperatures and/or relative humidity reducing this activity (Resende et al. 2001). Trigona


hyalinata (Lepeletier) forages in the morning, stimulated by temperature, but also in the afternoon, depending on the light brightness (Lerer et al. 1982). Most social wasps forage during the hottest period of the day, but rhe devel-opmental stage of the colony and the substratum type also, interfere, with these dynamics (Andrade & Prezoto 2001).

Lower synchronization between exits of P. fraternus individuals for for-aging and those returning to the colony on the sunny day can be attributed to different factors. The presence of birds near the nest may have interfered with population behavior of this wasp which reduced counting of individuals leaving and returning during this period. Besides, social wasps are exposed to natural enemies with possible higher predation on the sunny day when foraging activity was practically double that on the cloudy day. Individuals of this wasp also may have returned to the nest on subsequent days after foraging, as observed for Polistes canadensis canadensis (Linnaeus) (Santos et al. 1994) and P. occidentalis occidentalis (Resende et al. 2001). Also, the longest distance from the colony to foraging places can increase chances of confounding individuals during the returning flight to the nest as found for Polistes simillimus (Prezoto & Gobbi 2005).

These results confirm the tendency of the behavior of P. fraternus to be similar to that of most social wasps and indicate that climatic conditions, mainly temperature and relative humidity, are decisive for the foraging dy-namics of this species.

ACKNOWLEDGMENTS

We are grateful to the “Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)” and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” for financial support of this study.

REFERENCESAndrade, 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: 117-128.

Farinha, A.E.C. & N.P.O. Pinto 1996. Natural enemies of Chlosyne lacinia saundersii Doubl. & Hew. (Lepidoptera: Nymphalidae) in the state of São Paulo. Anais da Sociedade Entomológica do Brasil 25: 165-168.


Elisei, T., C. Ribeiro Júnior, D.L.Guimarães & F. Prezoto 2005. Foraging activity and nesting of swarm-founding wasp Synoeca cyanea (Fabricius, 1775) (Hymenoptera, Vespidae, Epiponini). Sociobiology 46: 317-327.

Giannotti, E., F. Prezoto & V.L.L. Machado 1995. Foraging activity of Polistes lanio lanio (Fabr.) (Hymenoptera, Vespidae). Anais da Sociedade Entomológica do Brasil 24: 455-463.

Gobbi, N. & V.L.L. Machado 1985. Material capturado e utilizado na alimentação de Polybia (Myrapetra) paulista Ihering, 1896 (Hymenoptera, Vespidae). Anais da Sociedade Entomológica do Brasil 14: 189-195.

Gobbi, N. & V.L.L. Machado 1986. Material capturado e utilizado na alimentação de Polybia (Trichothorax) ignobilis (Haliday, 1836) (Hymenoptera, Vespidae). Anais da Sociedade Entomológica do Brasil 15: 117-124.

Gobbi, N., V.L.L. Machado & J.A. Tavares-Filho 1984. Sazonalidade das presas utilizadas na alimentação de Polybia occidentalis occidentalis (Olivier, 1791) (Hymenoptera: Vespidae). Anais da Sociedade Entomológica do Brasil 13: 63-69.

Gonring, RA.H., M.C. Picanço, J.C. Zanuncio, M. Puiatti & A.A. Semeão 2003. Natural biological control and key mortality factors of the pickleworm, Diaphania nitidalis Stoll (Lepidoptera: Pyralidae), in cucumber. Biological Agriculture and Horticulture 20: 365-380.

Leite, G.L.D., M. Picanço, R.N. Guedes & J.C. Zanuncio 2001. Role of plant age in the resistance of Lycopersicon hirsutum f. glabratum to the tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae). Scientia Horticulturae 89: 103-113.

Lerer, H., W.G. Baileey & P. Pankim 1982. Pollination activity of Megachile rotunda (Hymenoptera). Environmental Entomology 11: 997-1000.

Letourneau, D.K. & J.C. Choe 1987. Homopteran attendance by wasps and ants: the stochastic nature of interactions. Psyche 94: 81-91.

Marques, O.M. 1996. Vespas sociais (Hymenoptera, Vespidae): características e importância em agroecossistemas. Insecta 5: 18-39.

Martins, G.F, J.C. Zanuncio & J.E. Serrão 2008. Spermatheca morphology of the social wasp Polistes erythrocephalus. Bulletin of Insectology 61: 37-41.

Mateus, S., B.F. Noll & R. Zucchi 2004. Caste flexibility and variation according to the colony cycle in the swarm-founding wasp, Parachartergus fraternus (Gribodo) (Hymenoptera: Vespidae: Epiponini). Journal of the Kansas Entomological Society 77: 470-483.

Paula, L.C., F.R. Andrade & F. Prezoto 2003. Foraging behavior in the neotropical swarm-founding wasp Parachartergus fraternus (Hymenoptera: Vespidae: Polistinae: Epiponini) during different phases of the biological cycle. Sociobiology 42: 735-744.

Prezoto, F. & N. Gobbi 2005. Flight range extension in Polistes simillimus Zikán, 1951 (Hymenoptera, Vespidae). Brazilian Archives of Biology and Technology 48: 947-950.

Prezoto, F., E. Giannotti & V.L.L. Machado 1994. Atividade forrageadora e material coletado pela vespa social Polistes simillimus Zikán, 1951 (Hymenoptera, Vespidae). Insecta 3: 11-19.


Prezoto, F., H.H. Santos-Prezoto, V.L.L. Machado & J.C. Zanuncio 2006. Prey captured and used in Polistes versicolor (Olivier) (Hymenoptera: Vespidae) nourishment. Neotropical Entomology 35: 707-70.

R Development Core Team 2006. R: A Language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. ISBN 3-900051-07-0. URL http://www.R-project.org.

Resende, J.J., G.M.M. Santos, C. Bichara Filho & M. Gimenes 2001. Atividade diária de busca de recursos pela vespa social Polybia occidentalis occidentalis (Olivier, 1791) (Hymenoptera, Vespidae). Revista Brasileira de Zoociências 3: 93-104.

Ribeiro Junior, C., D.L. Guimarães, T. Elisei & F. Prezoto 2006. Foraging activity rhythm of the Neotropical swarm-founding wasp Protopolybia exigua (Hymenoptera, Vespidae, Epiponini) in different seasons of the year. Sociobiology 47: 115-123.

Richter, M.R. 2000. Social wasp (Hymenoptera: Vespidae) foraging behavior. Annual Review of Entomology 45: 121-150.

Santos, G.M.M., O.M. Marques & C.A.L. Carvalho 1994. Raio de ação de Polistes canadensis canadensis (L., 1758) (Hymenoptera, Vespidae). Insecta 3: 20-24.

Silva, E.R. & S.C.M. Noda 2000. Aspectos da atividade forragedora de Mischocyttarus cerberus styx Richards, 1940 (Hymenoptera, Vespidae): duração das viagens, especialização individual e ritmos diário e sazonal. Revista Brasileira de Zoociências 2:7-20.

Silva, C.A.D., E.M. Pires, M.C. Lacerda, F. Prezoto, J.C. Zanuncio & J.E. Serrão 2006. Immature stages and nest characteristics of Apoica pallens (Hymenoptera: Vespidae). Sociobiology 48: 365-374. 2006.

Silva-Filho, R., P.C.R. Cassino, O.M. Marques, A.M. Penteado-Dias, W.C. Rodrigues & J.C. Zanuncio 2007. Parasitoids of Polistes lanio lanio (Hymenoptera: Vespidae) larvae in the municipality of Seropédica, Rio de Janeiro State, Brazil. Sociobiology 50: 1191-1198.

Soares, M.A., C.T. Gutierrez, J.C. Zanuncio, L.L. Bellini, F. Prezoto & J.E. Serrão 2006. Pachysomoides sp. (Hymenoptera: Ichneumonidae: Cryptinae) and Megaselia scalaris (Diptera: Phoridae) parasitoids of Mischocyttarus cassununga (Hymenoptera: Vespidae) in Viçosa, Minas Gerais State, Brazil. Sociobiology 48: 673-680.

Weiss, M.R., E.E. Wilson & I. Castellanos 2004. Predatory wasps learn to overcome the shelter defense of their larval prey. Animal Behaviour 68: 45-54.

Zanuncio, J.C., J.B. Alves, G.P. Santos & W.O. Campos 1993. Levantamento e flutuação populacional de lepidópteros associados à eucaliptocultura: VI- Região de Belo Oriente, Minas Gerais. Pesquisa Agropecuária Brasileira 28: 1121-1127.

Foraging of Parachartergus fraternus (Hymenoptera: Vespidae: Epiponini) on cloudy and sunny days

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