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
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
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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´, Saõ Paulo and
1
Departamento de Cieˆncias Biolo´gicas, Universidade da Regiaõ 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 Saõ Paulo - USP, Rua do Mataõ
277, Cidade Universita´ria, Saõ 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
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
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

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

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.

Table 2. SimiIarity (Sørensen Index) among bee communities (Apidae) sampled in grasslands in
different areas of Brazil.
Author Localities Geographic coordinates
Altitude
(meters)
Sørensen
Ińdex
Martins, 1994 Lençois/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 Viamaõ/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.

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.

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

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

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.

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), Danuńcia
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 Gonçalves 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.
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