A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae)
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A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae)



Author(s): Denise Monique Dubet da Silva Mouga and Paulo Nogueira Neto ...

Author(s): Denise Monique Dubet da Silva Mouga and Paulo Nogueira Neto



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    A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae) A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae) Document Transcript

    • BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae) Author(s): Denise Monique Dubet da Silva Mouga and Paulo Nogueira Neto Source: Journal of the Kansas Entomological Society, 85(4):295-308. 2012. Published By: Kansas Entomological Society DOI: http://dx.doi.org/10.2317/0022-8567-85.4.295 URL: http://www.bioone.org/doi/full/10.2317/0022-8567-85.4.295 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
    • A High Grassland Bee Community in Southern Brazil: Survey and Annotated Checklist (Insecta: Apidae) DENISE MONIQUE DUBET DA SILVA MOUGA 1 AND PAULO NOGUEIRA NETO 2 ABSTRACT: The native bee community in a high grassland area in Santa Catarina State, Southern Brazil, was studied during 2001 and 2002, using entomological net sampling on flowering plants. The goals were to know the potential bee pollinators in this particular habitat, their abundance and diversity and to fill the gaps in their geographic distribution. Sixty-three bee species in 4 families were collected. Six bee species are new state records. Representatives of Colletidae were not sampled and Halictidae was strongly represented (65% of the species, mainly Dialictus and Augochloropsis). Megachilidae was sampled (5 species) as well as Andrenidae (3 species). The decreasing sequence of importance was almost the same for species and individuals, without the introduced species Apis mellifera L. Threatened (Bombus spp) and specific bee species of this environment were of particular interest. The total number of sampled taxa represent nearly thirteen percent of the bee species known to occur in Santa Catarina State. Capture rates for different bee genera varied temporally as the bees’ activity was strongly influenced by the cold season. The bee species composition found shows similarity of 35% to distant but similar environments. The high grasslands in Santa Catarina State conform to an archipelago framework, that likely corresponds to an island biogeographical pattern in terms of apifauna composition and dynamics. KEY WORDS: Biodiversity, pristine fauna, species richness, biogeography, apifauna, Santa Catarina The state of Santa Catarina (SC), which has one of the steepest altitudinal profiles in Brazil, has, as its original vegetation coverage, Rain Forest (generically known as the Atlantic Forest), the Araucaria Forest, the Semi-Deciduous Rain Forest accompanying the Uruguay River basin, and the highlands (IBGE, 1990). The latter occur above the forest limits, sometimes interweaving forest areas with grass and undergrowth shrubs. Their structure and floristic composition are similar to the grassy-woody steppe and to the herbaceous component of the savanna. These grasslands develop in a peculiar combination of environmental conditions: the high altitude causes lower temperatures with intense winds, and the rugged terrain causes shallow soils, thus forming a mosaic of micro-habitats (Rizzini, 1979). Available data indicate that the occurrence of these grasslands among the surrounding forest formations is primarily due to climatic factors and only secondarily to soil conditions (Ribeiro and Medina, 2002). High grasslands hold physiognomic and ecological similarities with rocky lands, but differ in flora species composition and in the dominant lithology (Doumenge et al., 1995). The high altitude grasslands of the northern region of Santa Catarina are inserted in the complex of the Atlantic Forest biome (Figure 1). They also occur in the higher portions of the Serra do Mar-in the states of Parana´, Sa˜o Paulo and 1 Departamento de Cieˆncias Biolo´gicas, Universidade da Regia˜o de Joinville -UNIVILLE, Rua Paulo Malschitzki 10, Campus Universita´rio, Joinville-SC, Brazil, CEP 89219-710. 2 Departamento de Ecologia, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo - USP, Rua do Mata˜o 277, Cidade Universita´ria, Sa˜o Paulo-SP, Brazil, CEP 05508-900. Accepted 4 September 2012; Revised 12 September 2012 E 2012 Kansas Entomological Society JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 85(4), 2012, pp. 295–308
    • Rio de Janeiro-and of the Serra da Mantiqueira-in Sa˜o Paulo, Minas Gerais and Rio de Janeiro, with a total area estimated at 350 km2 (Tonhasca, Jr., 2005). The causes of the formation of these grasslands are complex and originate from an ancient landscape, dating to the late Pleistocene, when cold and dry weather dominated southeastern South America (Safford, 1999b). Palaeobotanical evidence suggests that the highlands have covered the summits of southeastern Brazil continuously since the late Pleistocene (Behling and Lichte, 1997). In Brazil, the highlands have been free of major anthropization because of their inhospitable conditions and difficult access; they represent some of the few natural environments still preserved in this part of the country. The high levels of endemism observed in the few studies accomplished in the highland environment, the uniqueness of the highland’s ecological processes and their restricted occurrence (being distributed only by patches of a few tens of square kilometers), indicate the need for action to conserve of this environment (Almeida and Carneiro, 1998). As bees establish a close and specific relationship with the flora they visit, the apifauna also reflects the latitudinal and altitudinal variation in its geographic distribution, thus providing an added indicator of biodiversity. By virtue of their sensitivity to environmental changes, bees have also been used as indicators of the need for conservation action (Kevan, 1999). The apifauna the State of Santa Catarina likely consists of more than 500 species (Mouga, 2009). Included are the most frequently occurring taxa (Apis mellifera L., 1758, Trigona spinipes (Fabricius, 1793), Bombus morio (Swederus, 1787), among others), and typical groups of this latitudinal range (families Halictidae and Andrenidae in general) as well as rare or endemic bees. In biogeographic terms, this apifauna is probably one of the richest in terms of diversity as it reflects the transition between tropical and temperate zones that occurs in this region, containing species of both (Alves-dos-Santos, 1999). Previous research about bees in this kind of environment in Brazil was carried out by Silveira and Cure (1993), Martins (1994), Faria-Mucci et al. (2003), Araujo et al. (2006) and Pinheiro et al. (2008). Aiming to complete the knowledge about the Fig. 1. Topographic profile of diverse formations of the Atlantic Forest (after Tonhasca, Jr., 2005, with permission). 296 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
    • biological diversity of bees and their geographic pattern of distribution as well as to provide tools for conservation, we have conducted a survey of the composition of the melissofauna in an area of highland in southern Brazil. Materials and Methods The high grassland is located in the municipality of Garuva, in the northeastern region of Santa Catarina, locally named ‘‘Alto do Quiriri’’, which is located at the geographic coordinates 26u029130S, 48u579290W, at an average altitude of 1283 m (IBGE, 1992). Rocks are abundant on the tops and steeper slopes; between are both dry and damp flats, the latter related to shallow soils with a low water retention capacity (Gonc¸alves et al., 2002). The highland is included within the Rain Forest, which bounds the eastern coast, together with spots of Fog Forest in places more sheltered from the winds. It is adjacent to Araucaria Forest in the west, which possesses a predominance of herbaceous plants and shrubs on the flat parts (Medeiros, 2002). The climate, according Ko¨eppen, is Cfa (subtropical climate), i.e., with the mean temperature of the three coldest months between 23uC and 18uC, with hot summers with average air temperature in the warmest month $22uC, with summer and winter well-defined, with a humid climate, and with the occurrence of precipitation in all months of the year and no dry season (Knie, 2002). Due to its geographical location, this area is subject to the incursion of tropical air masses that collide with the Serra do Mar, causing the so-called frontal orographic precipitation (Rosa, 2002). Data were obtained using the method proposed by Sakagami et al. (1967); the bees were collected on flowers in an area of approximately 30 ha., alongside a predetermined transect of approximately 3000 m that was traveled twice monthly. The transect included trails, abandoned roads and pathways. The observation and sampling period was six hours, between 09:00 h and 16:00 h (time of highest insolation) on days with favorable weather conditions. Bees were captured with entomological nets, sacrificed, and stored in jars labeled with numerical and temporal data. The temperature and relative humidity were also recorded. Specimens were prepared according to Michener et al. (1994), except for Apis mellifera, which were only registered. Twenty four samples were performed (i.e., collections were bimonthly), in 2001 and 2002, resulting in 288 hours of capture effort. Bees were identified by literature (Michener, 2007; Silveira et al., 2002; Moure et al., 2012) and through the collaboration of experts. All material collected is deposited in the LABEL—Bee Laboratory of UNIVILLE-University of Joinville Region, in Joinville, Santa Catarina, Brazil. The sampled apifauna was characterized qualitatively (taxa identified) and quantitatively (number of individuals, species, genera and families). In order to make comparisons of data from this study with other surveys performed in similar environments, the Sørensen Similarity Quotient (QS or SI) (Southwood, 1971) was calculated. Results The samples totaled 1304 individuals belonging to 63 species in 20 genera of four families of Apoidea present in Brazil (Table 1). Data for each month of the two years of sampling were added. VOLUME 85, ISSUE 4 297
    • Table 1. Species list of bee collected during sampling in 2001 and 2002 at the locality Alto do Quiriri, Garuva/Santa Catarina, Brazil and quantity of individuals collected. Quantities represent sum of data for the two years. (J 5 January, F 5 February, M 5 March, etc; S 5 sum). Bee taxa J F M A M J J A S O N D S Andrenidae Anthrenoides sp 4 1 0 0 0 0 0 0 0 0 0 1 4 6 Rhophitulus hartereae (Schlindwein and Moure, 1998) 0 0 0 0 0 0 0 0 1 0 0 0 1 Rhophitulus sp 2 0 0 0 0 0 0 0 0 1 0 1 0 2 Halictidae Augochlora sp 1 2 0 0 0 0 0 0 0 0 0 3 0 5 Augochlora sp 2 0 0 3 0 0 0 0 0 0 0 4 0 7 Augochlora sp 3 0 2 0 0 0 0 0 0 0 4 0 0 6 Augochlora sp 4 0 0 0 1 0 0 0 0 0 0 0 0 1 Augochlora sp 5 0 0 0 0 0 0 0 0 1 0 0 0 1 Augochlorodes turrifaciens Moure, 1958 1 0 0 0 0 0 0 0 0 1 2 0 4 Augochloropsis sp 1 7 0 0 0 0 0 0 0 0 0 0 0 7 Augochloropsis sp 2 0 0 6 0 0 0 0 0 0 0 0 0 6 Augochloropsis sp 3 0 6 0 0 0 0 0 0 0 0 0 0 6 Augochloropsis sp 4 0 0 0 0 1 0 0 0 0 0 0 0 1 Augochloropsis sp 5 0 0 0 6 0 0 0 0 0 0 3 0 9 Augochloropsis sp 6 0 0 0 0 0 0 0 0 0 2 0 0 2 Augochloropsis sp 7 0 0 0 0 0 0 0 0 0 1 0 0 1 Augochloropsis sp 8 0 0 0 0 0 0 0 0 0 0 0 6 6 Augochloropsis sp 9 0 0 0 0 0 0 0 0 0 6 0 0 6 Augochloropsis sp 10 0 0 0 5 0 0 0 0 0 0 0 0 5 Augochloropsis sp 11 0 5 0 0 0 0 0 0 0 0 0 0 5 Augochloropsis sp 12 0 0 3 0 0 0 0 0 0 0 0 0 3 Neocorynura aenigma (Gribodo, 1894) 0 0 0 0 0 0 0 0 0 0 1 1 2 Paroxystoglossa sp 1 0 3 2 0 0 0 0 0 1 4 0 1 11 Paroxystoglossa sp 2 0 2 0 0 0 0 0 0 1 4 3 2 12 Paroxystoglossa sp 3 0 0 1 0 0 0 0 0 0 4 2 1 8 Dialictus sp 1 0 0 0 0 0 0 0 0 0 0 0 1 1 Dialictus sp 2 6 0 0 0 0 0 0 0 0 0 0 0 6 Dialictus sp 3 0 3 0 0 0 0 0 0 0 0 0 0 3 Dialictus sp 4 0 0 0 0 0 0 1 0 0 0 0 0 1 Dialictus sp 5 0 0 0 0 1 0 0 0 0 0 0 0 1 Dialictus sp 6 0 0 0 0 0 0 0 0 0 2 0 0 2 Dialictus sp 7 0 0 0 0 0 0 0 0 3 0 0 0 3 Dialictus sp 8 0 0 0 0 0 0 0 0 0 0 0 8 8 Dialictus sp 9 0 0 0 0 0 0 0 0 0 0 3 0 3 Dialictus sp 10 0 0 0 0 0 0 0 0 0 0 0 8 8 Dialictus sp 11 0 0 0 0 0 0 0 0 0 2 0 0 2 Dialictus sp 12 0 0 0 0 0 0 0 0 0 0 3 0 3 Dialictus sp 13 0 2 0 0 0 0 0 0 0 0 0 0 2 Dialictus sp 14 3 0 0 0 0 0 0 0 0 0 0 0 3 Pseudagapostemon (Brasilagapostemon) fluminensis (Schrottky, 1911) 0 0 0 0 0 0 0 0 0 0 0 2 2 Pseudagapostemon sp 1 0 5 0 1 0 0 0 0 1 1 0 1 9 Sphecodes sp 1 1 0 1 1 1 0 0 0 0 1 0 3 8 Sphecodes sp 2 1 1 1 2 0 0 0 0 0 0 0 4 9 Sphecodes sp 3 0 1 0 1 0 0 0 0 0 0 0 7 9 298 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
    • Several species of bees were identified only as morpho-species because of the lack of dichotomous keys and specialists for some groups (especially for the Halictidae). No individuals of Colletidae were collected. The family with the smallest species composition was Andrenidae (3 species) while Halictidae was represented by 41 species. In the group of the long-tongued bees, Megachilidae was represented by 5 species. Few non-corbiculate Apidae species were collected (4 species) and the corbiculate species added 10 taxa. Six of the species collected in our sampling are new records for Santa Catarina state: Augochlorodes turrifaciens Moure, 1958, Pseudoagapostemon (Brasila- gapostemon) fluminensis (Schrottky, 1911), Rhophitulus hartereae (Schlindwein and Moure, 1998), Ceratina (Crewella) cyanicollis Schrottky, 1902, Neocorynura aenigma (Gribodo, 1894) and Melipona (Eomelipona) marginata Lepeletier, 1836. In terms of species richness, the sequence of decreasing number of species of bees in the families was: Halictidae . Apidae . Megachilidae . Andrenidae. Halictidae, the richest taxon, had 65% of the species, thus showing a prevalence for this Table 1. Continued. Bee taxa J F M A M J J A S O N D S Megachilidae Megachile (Austromegachile) trigonaspis Schrottky, 1913 1 0 0 0 0 0 0 0 0 0 0 1 2 Megachile (Austromegachile) sp 1 0 0 0 0 0 0 0 0 0 0 0 1 1 Megachile (Chrysosarus) sp 1 1 0 0 0 0 0 0 0 0 0 0 0 1 Megachile (Moureapis) maculata Smith, 1853 0 0 0 1 0 0 0 0 0 0 0 0 1 Megachile (Pseudocentron) sp 1 0 0 0 0 0 0 0 0 0 1 0 0 1 Apidae Lophopedia pygmaea (Schrottky, 1902) 0 1 1 0 0 0 0 0 0 0 0 0 2 Xylocopa (N.) brasilianorum (Linnaeus, 1767) 0 1 0 0 0 0 0 0 0 0 0 0 1 Ceratina (C.) cyanicollis Schrottky, 1902 0 0 0 0 0 0 0 0 0 0 2 0 2 Ceratina (Cr.) sp 5 0 0 0 0 0 0 0 0 0 0 1 0 1 Bombus (F.) pauloensis Friese, 1913 2 3 1 0 0 0 0 0 0 1 0 0 7 Bombus (F.) morio (Swederus, 1787) 0 2 0 0 0 0 0 0 0 0 0 0 2 Bombus (F.) brasiliensis Lepeletier, 1836 0 1 0 0 0 0 0 0 0 0 0 0 1 Melı´pona (E.) bicolor Lepeletier, 1836 1 0 0 0 0 0 0 0 0 2 0 0 3 Melı´pona (E.) marginata Lepeletier, 1836 0 0 0 0 0 0 0 0 0 1 0 0 1 Plebeia emerina (Friese, 1900) 6 0 0 0 0 0 0 0 3 2 3 1 15 Plebeia saiqui (Friese, 1900) 0 0 0 0 0 0 0 0 0 0 2 0 2 Schwarziana quadripunctata (Lepeletier, 1836) 0 1 3 1 1 0 0 0 1 2 2 0 11 Trigona spinipes (Fabricius, 1793) 1 0 0 0 0 0 0 0 1 0 0 0 2 Apis mellifera Linnaeus, 1758 52 136 117 16 57 6 7 22 142 434 50 7 1046 Total 86 175 139 35 61 6 8 22 156 475 82 59 1304 VOLUME 85, ISSUE 4 299
    • environment. Apidae had the greatest abundance of individuals. The species Apis mellifera represented 80% of individuals counted. The sequence of decreasing predominance was also constructed without the species Apis mellifera. The results were, for the number of species, the series: Au . H . Me . Mg . An 5 B 5 X . T and for the number of individuals, the series: Au . H . Me . B . An . Mg . X . T (where Au: Augochlorini; H: Halictini; Me: Meliponini; B: Bombini; An: Andrenidae; Mg: Megachilidae; T : Tapinotaspidini and X: Xylocopini). The number of bee species observed through the year shows a strong decrease in the winter (Fig. 2). The locations and abbreviations for the Brazilian’s states are presented in Fig. 3. The values of the similarity index (SI) among bee communities are given in Table 2. SI varied from 0.13 to 0.35, with an average value of 0.23. Species composition comparisons of the Quiriri grassland bee fauna with the bee fauna of other grasslands indicated 35% overlap between Quiriri (SC) and the state of MG (at the locality of Ibitipoca, located at 1760 m altitude), as well as 25% at 1000 m altitude and 21% at 1579 m altitude. There was 34% overlap between Quiriri and RJ (1450 m altitude) and 22% between Quiriri and PR (910 m altitude), among other localities. Discussion Bee Species Richness The Quiriri highland is located in a contact zone between two rich formations (Rain Forest and Araucaria Forest), which could result in an apifauna equal to the sum of the respective forest apifaunas. Indeed, the taxa list shows elements of both kinds of formations; however, the apifauna is an impoverished one compared with those of the forests. Some of the bee species encountered in the highland are widely distributed and not specifically associated with certain plant taxa; these include Apis mellifera, Trigona spinipes, Bombus morio and Schwarziana quadripunctata (Lepe- letier, 1836). It should be however emphasized that sampling may be incomplete for bees that live in some scarce dense vegetal formations or that appear at night, a time period for which the sampling methodology was inappropriate. Since bees were also captured in flight, there is evidence of the occurrence of other species than those that were collected in flowers. Fig. 2. Total number of bee species sampled per month at locality Alto do Quiriri, Garuva, Santa Catarina, Brazil. Data for years 2001–2002 combined. 300 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
    • Table 2. SimiIarity (Sørensen Index) among bee communities (Apidae) sampled in grasslands in different areas of Brazil. Author Localities Geographic coordinates Altitude (meters) Sørensen I´ndex Martins, 1994 Lenc¸ois/BA 12u34’S–41u50’W 700 0.13 Faria,1994 Serra do Cipo´/MG 19u17’S–43u36’W 1500 0.16 Faria-Mucci et al., 2003 Lavras/MG 20u28’22’’S–43u33’50’’W 1000 0.25 Araujo et al., 2006 Ouro Preto/MG 20u26’S–43u46’W 1573 0.21 Silveira and Cure, 1993 Ibitipoca/MG 21u09’ S–49u43’’W 1760 0.35 Freitas, 2002 Serra da Bocaina/RJ 22u43’57’’S–44u37’06’’W 1450 0.34 Mouga, this study Garuva/SC 26u02’13’’S–48u57’29’’W 1538 Barbola and Laroca, 1993 Lapa/PR 25u44’S–49u47’W 910 0.22 Bortoli and Laroca, 1997 Guarapuava/PR 25u23’36’’S–51u27’19’’W 1120 0.20 Pinheiro et al., 2008 Viama˜o/RS 30u20’S–50u50’’W 450 0.21 Abbreviations: BA 5 Bahia State, MG 5 Minas Gerais State, PR 5 Parana´ State, RJ 5 Rio de Janeiro State, RS 5 Rio Grande do Sul State, SC 5 Santa Catarina State Fig. 3. Brazil’s states. Abbreviations: BA 5 Bahia, ES 5 Espirito Santo, MG 5 Minas Gerais, PR 5 Parana, RJ 5 Rio de Janeiro, RS 5 Rio Grande do Sul, SC 5 Santa Catarina, SP 5 Sao Paulo. VOLUME 85, ISSUE 4 301
    • Colletidae is a baseline group thought to be approximate to an ancestral group of Hymenoptera—the sphecoid wasps (Michener, 2007). These are especially abundant in xeric areas with sandy soils, where they nest in the ground. The absence of this bee family in this study may prove to be linked to the fact that Quiriri has humid climate and soil. The Andrenidae, the smaller group represented in the study, consists mainly of species with high oligolectia associated with environments of higher latitudes (Michener, 2007), and is better represented in species in the state of Santa Catarina than in Parana. The small species richness of Andrenidae and Colletidae in several study sites in Brazil is possibly related to the geographic distribution of these families. In Andrenidae, Andreninae is largely confined to Holartic region and some genera of Panurginae are found in Neotropical and Neartic regions. Colletidae is essentially Australian, with a few genera occurring in South America (Michener, 1979). The wealth of the family Halictidae highlights the need for more taxonomic studies on this family. The large number of species of the genera Augochlora, Augochloropsis and Dialictus reinforce the hypothesis that Halictidae is a group with possibly Gondwanian origin that is prevalent in southern areas of South America (Michener, 2007). With regard to the sampling of many short tongued species, most of which are mainly at the subsocial level of sociality (Michener, 1974), we note that this feature is very suitable for flowers of the flat type, e.g., Asteraceae, that prevail in high grasslands. The smaller presence of Megachilidae in relation to Apidae may be the result of scarcity of nesting suitable material for the first group; the leaves of plants in this environment are adapted to frequent conditions of wind and fire (thickened with silica deposits and reduced) and therefore stiff (Safford, 2001). Michener (1953), and subsequently other authors, observed Megachilidae taking petals to the nest, an apparent replacement of leaves by less leathery material. This choice must often further restrict Megachilidae populations since many plants bloom for short periods of time in the highlands. As to the predominance of certain taxa, Roubik (1989) posits that social species of Apidae and Halictidae can be considered the ecological equivalent of the many solitary species. In the limiting environmental conditions of high altitude grasslands, sociality may be a selective advantage for the division of work and efficient communication, providing better storage of food, which is vital for environments with regular periods of acute scarcity. Of the four bumblebee species found sympatrically in South Brazil, Bombus bellicosus Smith, 1879, a species of conservation concern (Martins and Melo, 2010), is reported to occur in high altitudes (Moure and Sakagami, 1962); it was not, however, collected during this study. The grassland environment, despite its apparent stable botanical composition, reveals a floristic diversity which enables a diverse apifauna to exist. Faria-Mucci et al. (2003) found a depleted apifauna in rocky grasslands (in regional terms), although more than 60% of plant species presented melittophilic features. In addition, they found that the bee fauna encountered was mostly of tropical origin, widely distributed, and not directly associated with rocky grasslands. Possibly the relationships between the flora and fauna of this kind of environment are largely generalistic, with broad adaptive interaction in different areas, which may explain in part the lack of Apidae in relation to resource abundance in this ecosystem. 302 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
    • The total number of sampled taxa represents nearly thirteen percent of the bee species known to occur in Santa Catarina State (Mouga, 2009). As the apifauna of these high grasslands must withstand the severe abiotic factors, the limited availability of places to nest due to the scarcity of hollow trees and the soggy soil caused by the very shallow groundwater, the bee diversity is restrained to taxa that nest in clumps, thickets, cracks in rocks, dry slopes and gullies that intersperse the grasslands. This agrees with Michener (1974) who says there is a decrease in bee species numbers in climatically temperate environment. Bee Species Composition Regarding geographical distribution, some of the taxa found had not previously been recorded for the state of Santa Catarina. This was the case, in Andrenidae, for the species Rhophitulus hartereae (Schlindwein and Moure, 1998), although several species in the genus have been recorded in the nearby states (Moure et al., 2012). In the Halictidae, the species Augochlorodes turrifaciens had been described only for Rio de Janeiro (Moure et al., 2012). For Neocorynura (a genus mainly distributed in South America, with one species reaching North America), the species found in this study, N. aenigma, was not previously known in Santa Catarina but has been documented in nearby states (Moure et al., 2012). In the genus Pseudagapostemon, the subgenus Brasilagapostemon includes species with restricted distribution in southeast and south of Brazil, extending down to Parana´, the state neighboring SC on the north (Moure and Sakagami, 1984). The type locality of the species, Pseudagapostemon (Brasilagapostemon) fluminensis, is Itatiaia, in Rio de Janeiro, one of the places with a higher altitude in the southern region of Brazil; it includes the Agulhas Negras Park, the first protected area of the country, specially created for the purpose of preserving wildlife and flora of higher altitudes. This species is typically associated with high grasslands and could be a focal point for conservation purposes. In family Megachilidae, the genus Megachile is represented worldwide and is extremely rich in species; many of them, however, are rare. For the species Megachile (Austromegachile) trigonaspis Schrottky, 1913, the previously documented distribu- tion points to Santa Catarina as the southern limit of the species. In the Xylocopinae (non corbiculate Apidae), the species Ceratina (Crewella) cyanicollis had previously only been indicated for the State of Sa˜o Paulo (Moure et al., 2012). In summary, these findings extend or complement the geographical distribution of a number of bee species, providing evidence for some of them of a pattern of scattered dispersion, which can likely be attributed to the refuging and isolating effect of altitude. Bee Abundance In terms of abundance of individuals, Halictidae and Apidae were the more prevalent taxa during visits to plants. In southern Brazil, generally speaking, Halictidae is the group that presents the greatest diversity of species and Apidae the greatest abundance of individuals, and these two groups constitute the predominant apifauna (Mouga, 2009). It should also be remembered that the adverse weather conditions (fog, strong winds, low temperatures) of the highlands are not the best conditions for apifauna in general (Michener, 2007) and this may contribute to the small population numbers of the native bee species found in this study. The sequence of decreasing abundance is quite similar between the groups in this study, suggesting that the number of individuals is a reflection of the number of VOLUME 85, ISSUE 4 303
    • species, with the exception of the high numbers of individuals of Apis mellifera. This species with high abundance of individuals per colony is very active synecologically. It is an exotic species but is highly adaptable and has developed, in general, inter- specific competitive relationships. This competition can, according to the quantita- tive characteristics of the population, promote a depletion of resources, food and shelter (Zanella, 1999). The effect probably becomes more pronounced in environmental conditions already adverse for the native species. Authors such as Schwartz-Filho and Laroca (1999), point out that the frequency intensity of Apis mellifera can mask the real structure of a bee community. One must also remember that the biogeographical origin of this species is the temperate region. Similarity of Apifauna to that of Other High Grasslands The lack of surveys conducted in high grasslands in the southern part of the country, required making comparisons with the nearest similar habitats in other parts of Brazil. Similarity values obtained by the calculation of the Sørensen Index were not very high but still offered the possibility of some comparisons. Greater similarity occurred with two closer places (MG, RJ); this may reflect either a true likeness of apifaunas for this type of environment or, to the contrary, a relative nonspecificity. Faria (1994) noticed that most species of the bee fauna she found in a rocky environment were of tropical origin, with broad distribution, and not directly associated with those surroundings and concluded that the relations between the fauna and flora in rocky fields are largely generalist, with wide adaptive interactions in the different areas. This could explain, in part, the shortage of Apidae relatively to the abundance of resources in this kind of ecosystem. In any event, the analysis of the obtained values of SI are of interest for comparisons. According to Moldenke (1975) and Heithaus (1979), nearby environments with different vegetation types contain quite different bee faunas while plant communities geographically distant but physiognomically similar, can sustain more similar melissofaunas. Biogeography and Conservation Klein (1978) conducted a phytogeographic synthesis on the original botanic diversity of Santa Catarina, characterizing the primary vegetation remaining since the beginning of agricultural and livestock development. Examination of the map of his study reveals an archipelago-like framework for the grasslands (Fig. 4). The conformation of the SC highlands phytogeography to an archipelago suggests the applicability of the concepts of island biogeography (MacArthur, 1972). The structure of the community, under this type of distribution, is particularly affected because, for many species, the possibility of expanding and looking for resources is limited. According to Freitas and Sazima (2006), the shaping of the highlands in insula may have favored plant species able to quickly occupy new habitats, including those that do not depend on a few highly specialized pollinators, which would lead to a composition of botanic species that are widely visited by bee taxa in small numbers. The food resources on mountain tops, depending on the altitude restrictions that regard to the transition of environments, possibly act in an analogous way to what takes place in inselbergs (Porembski et al., 1998). Generally speaking, as a pattern, the fauna of the islands presents lower diversity. Zanella et al. (1998), reporting 304 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
    • research on islands, found lesser richness of bee species there than on the nearby mainland. According to Mocochinski and Scheer (2008), the current orographic character- istics of the high grasslands recreate weather conditions like those prevalent in past times, thus providing a refuge for wildlife from southernmost or Laurasic sources in the times of advancing tropicalization that began in the Quaternary (Brown and Ab’ Saber, 1979). Thus the faunal composition present today in this environment may represent a picture of the community structure in the Pleistocene in this region of Brazil. On the other hand, the resemblances of the found apifauna to similar compositions from distant but analogous environments suggest possible Andean connections to the flora and fauna of South America (Simpson, 1979). In addition, it is known that changes occurred under the depression of montane climatic zones which provided biotic exchanges between neighboring peaks that were previously isolated (Safford, 2007). Reitz (1965) had already noticed that the high grassland of Iquererim Hill (the former name of Quiriri) provided Santa Catarina with many features that originated in the high peaks of the Serra do Mar and Serra da Mantiqueira (mountain formations from neighboring northern states). Interestingly, Porembski et al. (1998) mention the possibility of close parallels between the inselbergs and the grasslands. In most cases, the highlands areas are less impacted by human influences than lower altitude areas. Reasons for this include difficulty of access, inhospitable environment, and adverse abiotic conditions, which make economic use difficult (Martinelli, 1996). There remain the few areas that are probably still in a state of floristic composition very similar to the environments that existed before the advent of colonization by man (Safford, 1999a). On the other hand, the apifauna maintains Fig. 4. Areas with high grasslands in Santa Catarina State (adapted from Klein, 1978). The circle represents the study site. VOLUME 85, ISSUE 4 305
    • close and peculiar links with the flora that penetrates, providing a bioindicator of diversity and conservation (Reyes-Novelo et al., 2009). The study of the composition of apifauna may thus provide aid in characterizing pristine environments. In discussing the state of conservation of the bee species in Brazil, Silveira et al. (2002) report the depleted status of populations of several native species, previously reported as abundant, caused by anthropogenic impact on the environment. The grasslands in Brazil have suffered from many problems: invasive weeds, tourism, grazing, fire to pastures, and pine plantations, among others caused by human interference. In the case of bees, added to all these is the pressure of the effort required to interact with large numbers of highly competitive invasive species (Apis mellifera). Human influence on the Morro do Iquererim dates back 270 years (Reitz, 1965). In biological terms, this period of environmental change is relatively short, and there is the possibility of a community structure of bees remaining close to that of its pristine time (Ab’ Saber, 1996). As highlands constitute ecosystems that offer frugal resources, their biotic communities are in a fragile balance. These findings reinforce the need for greater understanding and protection of these environments. Acknowledgments Thanks to the Dean of Research and Post-Graduate Studies of UNIVILLE for scholarship support. To the experts, Padre Jesus S. Moure (in memoriam), Danu´ncia Urban, Gabriel A. R. Melo, Fernando A. Silveira, Clemens Schlindwein, Fernando C. V. Zanella, Isabel Alves dos Santos, Beatriz W. T. Coelho, Favı´zia Freitas de Oliveira, Rodrigo Gonc¸alves and Antonio Aguiar, for their assistance in taxonomic identification of the bees. To the Herbarium Joinvillea of the UNIVILLE, to the Botanical Museum of the city of Curitiba and to the expert Leandro Freitas, specialist at the National Museum of Rio de Janeiro, for their assistance in botanical identification. To everyone who contributed to this work. Literature Cited Ab’Saber, A. N. 1996. Paleoclimas quaterna´rios e pre´-histo´ria da Ame´rica Tropical. II. Revista Brasileira de Biologia 50:821–831. Almeida, F. F. M., de, and C. D. Carneiro. 1998. Origem e evoluc¸a˜o da Serra do Mar. Revista Brasileira de Geocieˆncias 28:135–150. Alves-dos-Santos, I. 1999. Abelhas e plantas melı´feras da mata atlaˆntica, restinga e dunas do litoral norte do estado do Rio Grande do Sul, Brasil. Revista Brasileira de Entomologia 43:191–223. Araujo, V. A., Y. Antonini, and A. P. A. Araujo. 2006. Diversity of bees and their floral resources at altitudinal areas in the southern Espinhac¸o Range, Minas Gerais, Brazil. Neotropical Entomology 35:30–40. Behling, H., and M. Lichte. 1997. Evidence of dry and cold climatic conditions at glacial times in tropical southeastern Brazil. Quaternary Research 48:348–358. Brown, K. S., Jr., and A. N. Ab’Saber. 1979. Ice-age forest refuges and evolution in the Neotropics: correlation of paleoclimatological, geomorphological and pedological data with modern biolocal endemisms. Paleoclimas 5:1–30. Doumenge, C., D. Gilmour, M. R. Perez, and J. Blockhus. 1995. Tropical montane cloud forests: conservation status and management issues. In L. S. Hamilton, J. O. Juvik, and F. N. Scatena (eds.). Tropical Montane Cloud Forests, pp. 24–37. Springer Verlag, New York. 407 pp. Faria, G. M. 1994. A flora e fauna apı´cola de um ecossistema de campo rupestre, Serra do Cipo´, MG, Brasil. Ph.D. Dissertation, UNESP University; Rio Claro, Sa˜o Paulo. x + 239 pp. 306 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY
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