COMMUNITY AND ECOSYSTEM ECOLOGY Fluctuations in Richness and Abundance of Social Wasps During the Dry and Wet Seasons in Three Phyto-Physiognomies at the Tropical Dry Forest of

1,2 3 1 G. M. DE M. SANTOS, P. C. BISPO, AND C.M.L. AGUIAR

Environ. Entomol. 38(6): 1613Ð1617 (2009) ABSTRACT The social wasp were quantiÞed in three different plant physiognomies (forested Caatinga, shrubby Caatinga, and agricultural systems) to analyze the effect of environmental sea- sonality and plant physiognomy on the richness, abundance, and species composition of social wasps in the region of tropical dry forest of Brazil. The forested Caatinga physiognomy had the greatest richness of species (S ϭ 16), followed by shrubby Caatinga (S ϭ 13) and by agricultural system (S ϭ 12). The Þrst axis of detrended correspondence analysis (DCA) explained 67.8% of the variability and shows a gradient of the fauna from agricultural system and shrubby Caatinga to forested Caatinga. In the Þrst axis, wet season scores were much higher than those for the dry season in forested Caatinga. The second axis explained 18.7% of the variability and shows a separation of samples collected during the wet or the dry periods in shrubby Caatinga. This separation was less evident in the agricultural system. Variations in nest abundance were more intense in arbustive caatinga (45% decrease in number of active nests in the dry period), moderate in forested Caatinga (24% decrease in number of active nests in the dry period), and low in agricultural systems (8% decrease in the dry period).

KEY WORDS Caatinga, , community ecology, species richness

Studies on diversity of social wasps (: colonies can be considered semisessile organisms ) in Brazilian ecosystems are still scarce and (Santos and Gobbi 1998). Studies on nest abundance several refer to the classic studies by Ihering (1904), have shown that seasonality occurs in some neotropical Ducke (1906, 1910), Richards and Richards (1951), social wasps species but not in others (Marques et al. and Richards (1978). Recent research have produced 1992, Ramos and Diniz 1993, Diniz and Kitayama 1998, information on the biodiversity of social wasps in the Santos et al. 2006). Furthermore, the same species may cerrado (Henriques et al. 1992, Diniz and Kitayama present seasonal ßuctuation or not, depending on envi- 1998, Mechi 2005, Elpino-Campos et al. 2007, Santos et ronmental conditions (Ramos and Diniz 1993). al. 2009), rupestrian Þelds (da Silva-Pereira and Santos The semiarid region in the Brazilian Northeast has 2006), caatinga (Santos et al. 2006, Aguiar and Santos two well-deÞned seasons: the dry and the wet seasons. 2007), the Atlantic Forest, mangroves and sandbanks For our purposes, the deÞnition of “dry period” in- (Santos et al. 2007), Araucaria Forest (Hermes and volves scarce food resources for the entomofauna. Ko¨hler 2006), and in agriculture lands (Marques and Conversely, the “wet period,” which extends for 2 mo Carvalho 1993, Hermes and Ko¨hler 2006). after the rain stops, presents intense plant blooming and The diversity and seasonality of species in social abundance of food resources for the entomofauna. wasp communities are usually studied from two per- This study aimed to investigate the relationships spectives: abundance of ßower-visiting wasps (Santos between richness and abundance of wasp species and et al. 1998, 2006; Silva-Pereira and Santos 2006; Hermes plant physiognomies with different levels of complex- and Ko¨hler 2006) or nest abundance (Henriques et al. ity (agricultural systems, shrubby Caatinga, and for- 1992, Marques and Carvalho 1993, Diniz and Kitayama ested Caatinga) in a tropical dry forest region of Brazil 1994, de Santos et al. 2007). This paper is based on nest (Caatinga). It also aimed to understand whether the abundance. ßuctuations in richness and abundance of wasp nests The temporal dynamics of tropical social wasps is in these communities are related to the wet and dry very complex. These contribute signiÞcantly seasons. for their colonies and do not abandon them easily; the

1 Laborato´rio de Entomologia, DCBIO, Universidade Estadual de Materials and Methods Feira de Santana, 44031-460 Feira de Santana, Bahia, Brazil. 2 The study was conducted in the municipalities of Corresponding author, e-mail: [email protected]. Њ Ј Њ Ј Њ Ј 3 Faculdade de Cieˆncias e Letras de Assis, Universidade Estadual Itatim (12 42 S and 39 41 W), Itaberaba (13 32 S and Paulista Ju´ lio de Mesquita Filho, Sa˜o Paulo, Brazil. 40Њ18Ј W), and Milagres (12Њ52Ј S and 39Њ51Ј W), State

0046-225X/09/1613Ð1617$04.00/0 ᭧ 2009 Entomological Society of America 1614 ENVIRONMENTAL ENTOMOLOGY Vol. 38, no. 6

Table 1. Number of social wasp nests registered in three Caatingas physiognomies during the wet and the dry seasons in Brazil

Agricultural Shrubby Forested Species system Caatinga Caatinga Dry Wet Dry Wet Dry Wet 01 Apoica pallens (Fabricius, 1804) 3 4 1 2 1 1 02 lecheguana (Latreille, 1824) 16 16 8 8 1 1 03 Clypearia angustior Ducke, 1906 ÑÑÑÑÑ 1 04 Mischocyttarus cassununga (Ihering, 1903) Ñ Ñ Ñ 6 1 4 05 Mischocyttarus cerberus Ducke, 1918 ÑÑÑÑÑ 1 06 Mischocyttarus drewseni Saussure, 1857 ÑÑÑÑÑ 3 07 Parachartergus pseudapicalis Willink, 1959 1 2 Ñ 3 3 6 08 billardieri (Fabricius, 1804) 2 3 Ñ 1 Ñ Ñ 09 Polistes c. canadensis (L., 1758) 35 33 11 22 8 8 10 Polistes v. versicolor (Olivier, 1791) 7 9 1 10 2 2 11 Polybia ignobilis (Haliday, 1836) 22 21 5 9 1 1 12 Polybia o. occidentalis Richards, 1951 18 27 1 5 2 1 13 von Ihering, 1896 3 6 Ñ 2 1 Ñ 14 Polybia sericea (Olivier, 1791) 19 14 24 27 4 4 15 sylveirae (Saussure, 1854) 2 2 4 4 1 1 16 Protopolybia e. exigua (Saussure, 1854) 1 3 Ñ 1 1 1 17 Synoeca cyanea (Fabricius, 1775) ÑÑÑÑ 2 2 Total (N) 129 140 55 100 28 37 of Bahia, northeastern Brazil. This is a semiarid trop- used to evaluate the relationship between complexity ical region with high risk of drought. The landscape is of the habitat (Euclidian distance among the samples a mosaic of agricultural environments and several based on a scale of habitat complexity) and the fauna physiognomies of the natural caatinga vegetation. (Morisita-Horn similarity index). The scale of habitat Samples were collected at all three locations from complexity varied from 1 to 3. The value 1 was attrib- each of the following physiognomies: FC, forested uted to agricultural systems, 2 to shrubby Caatinga, caatinga, seasonally dry tropical semideciduous forest, and 3 to forested Caatinga. The Mantel test was done open sclerophyllous forest, 6Ð16 m high; SC, shrubby with 5,000 permutations in NTSYS 2.1 (Rohlf 2000). Caatinga, open physiognomy with predominance of medium-sized vegetation (Ͻ2 m high), important Results presence of cactuses and palm trees; AS, agricultural systems, where the natural vegetation was partially Three hundred nineteen nests of 17 species of social replaced by pasture or small plots of crops (cowpea, wasps were observed. Some of these nests were active Vigna unguiculata; beans, Phaseolus vulgaris; corn, Zea in both dry and wet seasons; thus, we had 489 nests mays). registered (Table 1). The forested Caatinga physiog- The number of nests with active colonies in each nomy had the greatest richness of species (S ϭ 16), physiognomy was used as measure of abundance. Two followed by shrubby Caatinga (S ϭ 13) and the agri- data collectors searched for nests of social wasps with cultural system (S ϭ 12) (Fig. 1). The most abundant active colonies in each physiognomy, during the wet species were Polistes canadensis canadensis (L. 1758), period (January, February, and July 1998) and the dry Polybia sericea (Olivier, 1791), Polybia ignobilis (Ha- period (September, October, and November 1998). liday 1836), occidentalis (Rich- Each collector searched for 80 h in each physiognomy, ards, 1951), Brachygastra lecheguana (Latreille, 1824), a total of 160 h of sampling for each physiognomy. Five and versicolor (Olivier, 1791); they to 10 specimens from each colony were registered and identiÞed. Individuals of all species were deposited in the Entomological Collection Johann Becker of the Museu de Zoologia of the Universidade Estadual de Feira de Santana (MZUEFS). Because of the important variation in number of nests among plant physiognomies, we used rarefaction curves to compare the richness of species for the same number of nests. K individuals were randomly re- moved from the sample to estimate the taxa number. The procedure was repeated 1,000 times with the program Ecosim 5 (Gotelli and Entsminger 2000). The abundance matrix was logarithmized before the analysis. This matrix was submitted to detrended correspondence analysis (DCA) (Gauch 1995, Leg- Fig. 1. Rarefaction curves of social wasps registered in endre and Legendre 1998) using the program PCORD three plant physiognomies of Brazilian Steppe (Caatinga). (McCune and Mefford 1999). The Mantel test was ConÞdence intervals (95%). December 2009 SANTOS ET AL.: SOCIAL WASP COMMUNITIES IN THE TROPICAL DRY FOREST 1615

Fig. 3. Fauna of social wasps registered in three plant Fig. 2. Richness (standardized for 40 nests) of social physiognomies. Standardized richness in the wet (W) and wasps registered in three plant physiognomies (AS, agricul- dry (D) seasons for each plant physiognomy (AS, agricul- tural system; SC, shrubby Caatinga; FC, forested Caatinga). tural system; SC, shrubby Caatinga; FC, forested Caatinga). Bahia, Brazil. ConÞdence intervals (95%). ConÞdence intervals (95%). corresponded to 82.4% of all colonies of social wasps (Table 1). tal heterogeneity allows for a larger number of niches, The number of active nests observed varied among setting the conditions for a larger number of species to physiognomies: 171 in the agricultural system, 105 in coexist (Levins 1962, Stehli et al. 1969, Latham and shrubby Caatinga, and 43 in forested Caatinga. After Ricklefs 1993, Braganc¸a et al. 1998). Data presented in standardization by rarefaction (40 nests), the richness this study only partially agree with the above. On the (Figs. 1 and 2) of agricultural system and shrubby one hand, the greatest richness of social wasps was Caatinga were similar but lower than in forested Caat- found in the physiognomy with the highest heteroge- inga. neity, the forested Caatinga. On the other, although Standardized richness for the same number of col- agricultural systems are structurally simple and com- onies in each plant physiognomy was similar between paratively much more homogeneous than shrubby the wet and the dry periods for the agricultural system Caatinga, both physiognomies presented similar val- and for the forested Caatinga (Fig. 3). However, rich- ues for richness. Agricultural systems have relatively ness in shrubby Caatinga was much greater in the wet simple vegetation structures but high availability of period. food resources (, preys, and water) for social A signiÞcant relationship between the complexity wasps throughout the year. The same does not occur of plant physiognomies and the fauna of wasps was in shrubby Caatinga, where resource availability is observed (Mantel test, r ϭϪ0.584; P ϭ 0.0002; 5,000 highly seasonal. permutations). Species and sample dispersion in a Shrubby Caatinga, the physiognomy with the most bi-dimensional space formed by the two Þrst axes of susceptible fauna to seasonal changes, barely had wa- the DCA are presented in Fig. 4. The Þrst axis of the ter, green vegetation, ßowers, or fruits in the peak of DCA explained 67.9% of variability and shows a spe- the dry period (November); food scarcity led to cies gradient from agricultural system and shrubby smaller numbers of species and nests registered com- Caatinga to forested Caatinga. In the Þrst axis, wet pared with the wet period. In forested Caatinga and in season scores were much higher than those for the dry agricultural systems, food resources for wasps were season in forested Caatinga (Fig. 4). The second axis also available during the driest periods, probably be- explained 18.7% of the variability and shows a sepa- cause of ßora diversity, varied phenological patterns in ration of samples collected in the wet and the dry forested Caatinga (e.g., occurrence of species that periods in the shrubby Caatinga. This separation was bloom during the dry season or throughout the year), less evident in the agricultural system because of the and water management in agricultural systems. As a overlap of samples collected in both seasons (Fig. 4). result of greater stability in resource availability, the The abundance of nests between the dry and the richness e nest abundance of social wasps registered in wet periods varied. Variations were more intense in both physiognomies was less susceptible to local sea- shrubby Caatinga (45% decrease in number of active sonal variations than shrubby Caatinga. nests in the dry period), moderate in forested Caat- Rainfall, frequent during the wet period in the caat- inga (24% decrease in number of active nests in the dry inga, affects the seasonal availability of ßoral resources period), and low in agricultural systems (8% decrease and leads to a seasonal pattern of resource use by in the dry period). wasps (Diniz and Kitayama 1998, Santos et al. 2006, Aguiar and Santos 2007). Wasp foraging activity is intense during the wet season and signiÞcantly de- Discussion creases during the dry season (Santos et al. 2006). Community ecology theory states that complex en- Elpino-Campos et al. (2007) reported that, during the vironments with greater structural heterogeneity can dry season in the Cerrado (another South American keep a larger number of species. Greater environmen- dry forest with a well-deÞned dry season) in central 1616 ENVIRONMENTAL ENTOMOLOGY Vol. 38, no. 6

Fig. 4. Ordination (DCA) of social wasp faunas registered in three Caatingas physiognomies (AS, agricultural system; SC, shrubby Caatinga; FC, forested Caatinga) during the wet season (January, February, and July 1998) and the dry season (September, October, and November 1998). The abundances of the faunas were determined by number of active nests in each sample. Numbers refer to the species listed in Table 1.

Brazil, the decrease in water and food availability tion structure and the seasonal variations in food and (nectar and preys) are limiting factors for colony water availability. survival. Lorenzon et al. (2003) observed that, in caat- inga environments, social bees decreased foraging ac- tivities during the dry season. Considering that euso- References Cited cial colonies of social wasps need a permanent food supply, food storage is the only guarantee for colony Aguiar, C.M.L., and G.M.M. Santos. 2007. Compartilha- survival during scarcity periods. mento de Recursos Florais por Vespas Sociais (Hym- The effects of plant physiognomy and season were enoptera:Vespidae) e Abelhas (Hymenoptera: Apoidea) em uma A´ rea de Caatinga. Neotrop. Entomol. 36: 836Ð important determinants of the wasp fauna because 842. samples collected in the same physiognomy and same Braganc¸a, M.A.L., J. C. Zanuncio, M. C. Picanc¸o, and A. J. season were quite similar. Wasp faunas were different Laranjeiro. 1998. Effects of environmental heterogene- in each of the three phyto-physiognomies studied, ity on Lepidoptera and Hymenoptera populations in Eu- showing the importance of the vegetation mosaic to calyptus plantations in Brazil. For. Ecol. Manag. 103: 287Ð maintain wasp beta diversity. Some wasp species in- 292. crease abundance or occur only in the wet season, Diniz, I. R., and K. Kitayama. 1994. Colony densities and reinforcing the effect of seasonality on wasp fauna. preferences for nest habitats of same social wasps in Mato Grosso State, Brazil (Hymenoptera, Vespidae). J. Hym- Our data showed that, in addition to factors intrinsic enopt. Res. 3: 133Ð143. to each species, such as the ability to forage and store Diniz, I. R., and K. Kitayama. 1998. Seasonality of vespid food, the dynamics of social wasps is strongly inßu- species (Hymenoptera: Vespidae) in a central Brazilian enced by environmental factors such as local vegeta- Cerrado. Rev. Biol. Trop. 46: 109Ð114. December 2009 SANTOS ET AL.: SOCIAL WASP COMMUNITIES IN THE TROPICAL DRY FOREST 1617

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