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Journal of Insect ConservationAn international journal devoted tothe conservation of insects and relatedinvertebrates ISSN 1366-638XVolume 18Number 6 J Insect Conserv (2014) 18:1193-1201DOI 10.1007/s10841-014-9730-9

Bee and wasp responses to a fragmentedlandscape in southern Brazil

Rodrigo B. Gonçalves, NicolleV. Sydney, Priscila S. Oliveira & NathieleO. Artmann

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ORIGINAL PAPER

Bee and wasp responses to a fragmented landscape in southernBrazil

Rodrigo B. Goncalves • Nicolle V. Sydney •

Priscila S. Oliveira • Nathiele O. Artmann

Received: 7 August 2014 / Accepted: 12 November 2014 / Published online: 16 November 2014

� Springer International Publishing Switzerland 2014

Abstract The available studies on Hymenoptera assem-

blages in fragmented landscapes have shown that these

insects are sensitive to fragmentation, besides some dif-

ferent conclusions which are possibly linked to different

landscape attributes and sampling designs. The present

objective is to determine the correlation among the

descriptors of bees and wasps assemblages with fragment

predictors (size, connectivity and edge effect) within a

fragmented landscape of Semidecidual Seasonal Forest

(Parana State, Brazil). For this purpose five forest frag-

ments, from three to 484 hectares, were sampled during a

year, summing up 480 samples of baited traps and 3,480 of

bowl traps. We have found that abundance of Apinae and

oligolectic bees increase and the richness of Augochlorini

bees decreases with increasing fragment size. Connectivity

has positively influenced bee richness and edge effect has

positively influenced the abundance of oligoletic bees.

Orchid bees also respond to the site predictors, especially

for the Eufriesea violacea, which abundance was positively

correlated with fragment size and connectivity, however

negatively with edge effect, and Eufriesea nigrita which

abundance was negatively correlated with fragment size,

but positively with edge effect. Composition of bees,

Crabronidae and Pompilidae wasps were influenced by

fragment size. Plebeia droryana and Tetrapedia diversipes

could be considered as indicators, according to their sen-

sitiveness to habitat predictors. Our results are congruent

with previous studies which found that bees are sensitive to

landscape fragmentation, we suggest that the group be used

in ecological indicator and monitoring studies.

Keywords Anthophila � Apoidea � Biodiversity loss �Conservation

Introduction

To detect the effects of habitat fragmentation on fauna and

flora it is necessary to find sensitive organisms (McGeoch

1998). In Hymenoptera, ants are the most common group

used as ecological indicators (e.g. Andersen et al. 2002),

but bees and wasps can also respond to habitat fragmen-

tation (e.g. Gibb and Hochuli 2002; Calvillo et al. 2010).

Unfortunately, the evaluation of wasps responses to habitat

loss is still incipient. Kremen et al. (1993) and Reyes-

Novelo et al. (2009) suggested that bees, among other

terrestrial arthropods, could be used as indicators since they

meet all the selection criteria of ecological indicators. It is

important to stress that the role of bees as the main poll-

inators of flowering plants in natural habitats (Kevan 1999)

reinforces the ecological relevance to use this group in

indication studies.

The available studies of bees assemblages on frag-

mented landscapes have shown that these insects are sen-

sitive to fragment variables. These studies show different

conclusions about the kind of association among bees and

fragment parameters, and these differences are possibly

linked to different conditions of landscape attributes and

sampling designs among studies. As examples of studies

Electronic supplementary material The online version of thisarticle (doi:10.1007/s10841-014-9730-9) contains supplementarymaterial, which is available to authorized users.

R. B. Goncalves (&) � P. S. Oliveira � N. O. Artmann

Setor Palotina, Universidade Federal do Parana, Palotina,

PR 85950-000, Brazil

e-mail: goncalvesrb@gmail.com

N. V. Sydney

Departamento de Zoologia, Universidade Federal do Parana,

Caixa Postal 19020, Curitiba, PR 81531-980, Brazil

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DOI 10.1007/s10841-014-9730-9

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carried out in Neotropical region, Aizen and Feinsinger

(1994), in Argentina, found that fragmentation affect native

bees negatively, and honey bees positively. Brosi et al.

(2007) studying fragments in Costa Rica, found effects of

forest variables on bee composition, but no influence on

bee diversity and abundance, while in Mexican fragments,

Calvillo et al. (2010) found that richness and diversity

increased with fragment size and connectivity.

Orchid bees (subtribe Euglossina) have been studied in

the fragmentation context, especially due the use of syn-

thetic chemical compounds to attract males for trap sam-

pling (Dodson et al. 1969; Campos et al. 1989) which

facilitates the sampling on forested areas of Neotropical

region. As examples of association of orchid bees and

fragment parameters, Brosi (2009) found that abundance of

euglossine bees was positively related to forest fragment

size in a significant manner, but negatively related to

fragment shape. The fragment size was also an important

predictor for orchid bees diversity (Knoll and Penatti

2012), composition and abundance (Ramalho et al. 2013).

Still, other predictors such as connectivity and edge effect

were related to richness of Euglossina by Storck-Tonon

et al. (2013).

Here we studied how bees assemblage change among

different fragments, specifically, we aim to determine the

correlation of abundance and richness of bees (Apidae) and

two families of wasps (Crabronidae and Pomilidae) with

fragment predictors (fragment size, connectivity, and edge

effect). Study sites are in southern Brazil, where no frag-

mentation studies using hymenopteran families as ecolog-

ical indicators were carried out. Also, we analyzed the

responses of bee taxonomical and functional ecological

groups in order to determine the possible effects in spe-

cialized groups.

Materials and methods

Study site

This study was conducted in an agricultural farm in the

western portion of Parana State (Brazil), around the UTM

coordinates -24.170248, -53.960579. Originally, the area

was entirely covered by Semidecidual Seasonal Forest, a

formation typical of the inland vegetation of the Brazilian

Atlantic Forest biome, but currently the area is almost

deforested to crops, a generalized condition in southern

Brazil. The main preserved area is a Private Reserve of

Natural Heritage with 484 hectares, but other fragments

with three to 46 hectares are scattered in the area. We

selected five forest fragments, including the Reserve,

which are listed in Table 1. The fragments are inserted

within a radius of 3 km which contains few unstudied

small fragments and riparian forests the matrix around all

of them was alternate soybean and corn crops. For each site

we calculated perimeter, size, edge effect (perimeter/size

ratio), and the fragment connectivity (C). C is a measure

based on both area and distance to the nearest neighbor

fragment, the value increases with decreasing fragment

isolation and greater connectivity, it was calculated with

C = Re-dij.Aj, where Aj is the size (ha) of the nearest

fragment and dij is the distance (km) to the study fragment

i (Hanski and Thomas 1994; Steffan-Dewenter 2003),

surrounded not studied areas were considered for C

calculation.

Specimen collection

Sampling was carried out between 9 A.M. and 3 P.M., from

August 2012 to July 2013, once a month, making up twelve

sampling days. For sampling method we opted to use

baited traps for orchid bees and bowl traps for bees and

wasps. Trap sets were arbitrarily installed on the border of

the fragments, and the number of traps in each study site

was proportional to fragment perimeter, using the relation

of one baited trap for each 500 m and one bowl for each

100 m. The the average number of individuals per sample

was used to the comparison among the studied fragments

for a better representation data of local populations. We

adopted the perimeter instead of fragment size to estimate

the number of traps due to inaccessibility to sites core area,

especially that from the larger fragment.

We used commercial plastic bowl traps, blue and yel-

low, with 14.5 cm of diameter at the upper surface, 10 of

diameter on mid portion, and six of height, filled one third

of its volume with a water and soap solution. The bowl

traps were placed on the ground, alternated by color and

spaced 10 m apart from each other. For bowl traps we

selected three Hymenoptera taxa, Apidae, Crabronidae and

Pompilidae, for identification and analysis. This choice was

based on the number of sampling individuals, since those

three families were collected among all fragments. Baited

traps (Campos et al. 1989) were made with commercial

500 ml plastic bottles, the 1–8 cineol scent was available at

the top, and the bottom was filled with 70 ml of ethanol

70 %. Two entrance platforms abraded with sandpaper

were attached to the lateral entrance. The bait traps were

placed in tree branches, about 10 m from each other and

about 1.5 m from the soil.

Bees and wasps were pinned, data based, separated in

morphospecies, and deposited at the Laboratorio de

Hymenoptera do Campus Palotina, Universidade Federal

do Parana (PAUP). The species of orchid bees (Euglossina)

were identified using Rebelo and Moure (1996). The higher

level bee classification follows Melo and Goncalves

(2005), where all bees are considered under Apidae and

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bees families sensu Michener (2007) are considered as

subfamilies, tribes remains unchanged.

Data analyses

Pearson correlations (a = 0.05), carried out with R pro-

gram (R Development Core Team 2014), were utilized to

explore the relationships among the assemblage descriptors

and site predictors (size, connectivity, and edge effect).

The choice of parametric statistics was made after consider

the normality using the Shapiro–Wilk test, all variables

were log transformed. For assemblage descriptors we cal-

culated the mean sampled abundance (ma) and the mean

sampled richness (mr) of taxon or life form by trap and

study site. For mean sampled abundance we summed the

sampled number of individuals with each trap and then

divided by the total number of traps installed in the frag-

ment. For species, we summed the sampled number of

species with each trap unit and divided by the total number

of traps installed in the fragment. The classification of

ecological functional groups for bee species followed

Martins et al. (2013). A non metric dimensional scale

(NMDS) using Bray–Curtis similarity index was calculated

for bee data set in order to access the composition, which is

considered here as the first axis of NMDS. We also cal-

culated Shannon diversity index, probability of inter-spe-

cific encounter (an evenness measure), and the Dominance

index (Gotelli and Entsminger 2005), all using a rarefied

dataset.

Results

Bowl traps

The 3,480 bowl traps sampled 1,472 individuals and 97

species of Apidae, 358 individuals and 36 species of

Crabronidae, and 154 individuals and 37 species of

Pompilidae (Supplementary material). Mean sampled

abundance by sampling unit of bees was 0.74 and mean

sampled richness was 0.14, while for Crabronidae they

were 0.20 and 0.05 and for Pompilidae, 0.08 and 0.04,

respectively. The sampled bees belong to four subfamiles:

Andreninae, Apinae, Halictinae, and Megachilinae, with

Halictinae as the most abundant and rich group. All bees

were native except honey bee (Apis mellifera Linnaeus,

1758) sampled in three fragments. The most common bee

life forms were solitary, soil nester and polylectic.

Table 2 resumes the correlation of family level

descriptors and fragment predictors. No Pearson correla-

tion was significant for Shannon diversity index, proba-

bility of interspecific encounter so we opted not to show

these data. The NMDS axis 1 of all families assemblages

was correlated with fragment size and with edge effect.

Both wasp families have similar abundance and richness

among the study sites and they do not show significant

correlations with site predictors, but for bees, abundance

and richness vary among fragments and a correlation

between richness and connectivity was found (Table 2;

Fig. 1).

Moreover were found significant correlations among bee

taxonomical and functional groups and site predictors

(Tables 3, 4). The fragment size had a positive correlation

with Apinae (Fig. 2) and oligolectic bees abundance

(Fig. 3), but a negative correlation with Augochlorini

Table 1 Study fragments with

respective perimeter, size,

connectivity, edge effect and

number of baited and bowl traps

utilized

Perimeter (km) Size (ha) Connectivity Edge effect Baited traps Bowl traps

Fragment 1 11.08 484 19,476 0.44 264 1,320

Fragment 2 3.03 45.36 82,381 0.08 84 816

Fragment 3 1.97 23.89 19,554 0.13 72 768

Fragment 4 1.61 13.83 95,913 0.09 36 384

Fragment 5 0.69 3.27 116,851 0.05 24 192

Table 2 Pearson correlation of Hymenoptera families abundance,

richness and composition with fragment size, edge effect, and

connectivity

Apidae Crabronidae Pompilidae

Abundance

Size 0.28 0.86 0.27

Edge effect 0.23 0.72 0.2

Connectivity 0.7 0.77 0.07

Richness

Size 0.1 0.14 0.24

Edge effect 0.16 0.25 0.33

Connectivity 0.01* (?) 0.12 0.6

Composition

Size 0.04* (?) 0.00* (?) 0.04* (?)

Edge effect 0.04* (?) 0.00* (?) 0.05

Connectivity 0.13 0.13 0.2

* p \ 0.05. (?) positive correlation

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(Halictinae) richness (Fig. 4). Examining the the correla-

tion of this predictor at species level, only Plebeia dror-

yana (Friese, 1900), and Tetrapedia diversipes Klug, 1810

showed significant positive results (p 0.002 and 0.0003

respectively). For connectivity, positive correlations were

found with richness of solitary (Fig. 5), ground nesters

(Fig. 6) and both trophic specialization bee functional

groups (Figs. 7, 8). The edge effect was correlated with

composition and negatively correlated with oligolectic bees

(Fig. 9). No effects of predictors on the richness of clep-

toparasite bees were detected, but analyzing two species,

Leiopodus trochantericus (Ducke, 1907) (three individu-

als), and Pseudepeolus carinatus (Roig-Alsina, 2003) (one

individual) were sampled only in the larger fragment, while

the third cleptoparasite species, L. lacertinus (Smith, 1854)

(one individual) was sampled in a medium size fragment.

Baited traps

The 480 baited traps sampled 311 individuals and six

species of orchid bees (Supplementary material), the mean

sampled abundance by traps was 0.65 and mean sampled

Fig. 1–9 Scatter plots correlating assemblages’ parameters and

fragment predictors. 1 Apidae richness and connectivity. 2 Apinae

abundance and fragment size. 3 Oligolectic bees abundance and

fragment size. 4 Augochlorini richness and fragment size. 5 Solitary

bees richness and connectivity. 6 Ground nester bees richness and

connectivity. 7 Oligolectic bees richness and connectivity. 8 Richness

of polylectic bees and connectivity. 9 Oligolectic bees abundance and

edge effect

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richness 0.09. The mean abundance was very similar

among the sampling sites and no significant correlation was

found between this descriptor and any site predictor, but for

richness a positive correlation was found with edge effect

and connectivity (Table 3, Figs. 10, 11). Analyzing the

orchid bee species, Eufriesea violacea (Blanchard, 1840)

and Eulaema nigrita (Lepeletier, 1841) showed different

patterns of mean abundance, E. violacea was positively

correlated to fragment size (Fig. 12) and negatively cor-

related with edge effect (Fig. 13) and connectivity, while

E. nigrita was negatively correlated with size and posi-

tively correlated with edge effect (Figs. 14, 15). No sig-

nificant correlation was found for other Euglossina species.

Discussion

Fragmentation is a process (Wilcove et al. 1986) and the

most used measure of fragmented landscape is the frag-

ment size, which is frequently positively associated with

biodiversity (Fahrig 2003). However, many other fragment

parameters, such as edge effect, connectivity, isolation and

shape can measure the configuration of these forest patches

(McGarigal and Cushman 2002). Here we selected three

measures, but two of them, fragment size and edge effect,

showed to be negatively correlated to each other

(p = 0.002) explaining the similar correlations with

assemblage descriptors. The association of both metrics is

logic, since fragment size is used to calculate edge effect.

The sampling methodology of the present study was

designed with two guidelines. First, to provide a great

number of samples, maximizing the data explanatory

power, we opted to use traps that are easy to replicate than

alternative active sampling methods such as hand-netting,

in spite of the possibility that traps could give a poor

representation of bee community when compared with

active sampling (Campbell and Hanula 2007). Second, we

aimed to make a proportional sampling effort along the

study sites, so we used a number of traps proportional to

the sites perimeter. Usually, bees assemblage studies apply

an unequal effort to different fragment sizes, leaving the

larger fragments less sampled than the smaller ones when

the same number of samples is taken.

Here bowl traps sampled a great number of individuals

and species of target families, and baited traps sampled a

richness and abundance comparable to other studies in the

same region (see Goncalves et al. 2014), all groups showed

correlations to fragment predictors, results interpreted as

meaningful. For the three families tested here, the com-

position was correlated with fragment size and edge effect,

and bee richness was positively correlated with connec-

tivity. The lack of correlation of wasp abundance and

Table 3 Pearson correlation of

bee taxonomical groups

abundance and richness with

fragment size, edge effect, and

connectivity

* p \ 0.05. (?) positive

correlation; (-) negative

correlation

Andreninae Apinae Augochlorini Halictini Euglossina E. nigrita E. violacea

Abundance

Size 0.22 0.04* (?) 0.45 0.07 0.74 0.03* (-) 0.05 (?)

Edge effect 0.31 0.06 0.57 0.21 0.59 0.04* (?) 0.03* (-)

Connectivity 0.97 0.46 0.49 0.58 0.55 0.34 0.04* (-)

Richness

Size 0.11 0.25 0.05* (-) 0.7 0.06

Edge effect 0.29 0.63 0.19 0.98 0.02* (?)

Connectivity 0.26 0.92 0.26 0.43 0.04* (?)

Table 4 Pearson correlation of

bee functional groups

abundance and richness with

fragment size, edge effect, and

connectivity

* p \ 0.05. (?) positive

correlation; (-) negative

correlation

Nesting behavior Nesting habit Trophic specialization

Solitary Eusocial Cleptoparasite Cavity Ground Oligolectic

Abundance

Size 0.3 0.38 0.21 0.11 0.39 0.04* (?)

Edge effect 0.26 0.34 0.39 0.08 0.35 0.01* (?)

Connectivity 0.74 0.81 0.37 0.39 0.86 0.23

Richness

Size 0.09 0.21 0.23 0.14 0.08 0.06

Edge effect 0.15 0.27 0.32 0.25 0.12 0.1

Connectivity 0.01* (?) 0.13 0.52 0.06 0.01* (?) 0.03* (?)

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richness and bee abundance with area predictors does not

indicate that the diversity is the same among fragments,

however it means that abundance and richness are pro-

portional to fragment relative size, so even small fragments

can support bees assemblages.

Differently from bees, the response of wasps to fragment

measures are not so well documented, possibly due to

relatively fewer attempts or difficulties on sampling

designs. The main problem for the use of Crabronidae and

Pompilidae in indication in the Neotropical region is the

difficulty of species identification due to few generic

revisions and identification keys for Brazil (Melo et al.

2012). However, wasps are predators or parasitoids, being

one to two trophic levels higher than bees (Schuepp et al.

2011), they have varied functional groupings, pointing to a

great biological relevance of wasps on fragmentation

studies. Previous studies show that fragment isolation has

influence upon wasps assemblages on trap nesting studies

(Schuepp et al. 2011; Coudrain et al. 2013), and that

fragment size can have positive or negative effects (Santos

et al. 2014), but under our scale and sampling effort only

composition was affected.

The association of fragment size with diversity of bees

was described in literature, as examples, the positive effect

of fragment size on bee richness was found by Aizen and

Feinsinger (1994), Alfert et al. (2001), Steffan-Dewenter

(2003), and Calvillo et al. (2010). More than examining the

richness alone, inferences on composition give us a more

accurate outlook on the effects of fragment size. Studies

have found effects of fragment size directly in composition

(Aizen and Feinsinger 1994, this study) and on bee taxo-

nomical of functional groups (Calvillo et al. 2010, this

study). We have found effect of fragment size on abun-

dance of Apinae and on abundance of oligolectic bees, but

interestingly most Apinae are no oligolectic. Most of the

oligolectic bees sampled in our study are within Apinae

and the correlation with fragment size agrees with the

general tendency mentioned by Williams et al. (2010); for

whom specialized groups are more sensitive than generalist

ones. The oligolectic bees abundance was also negatively

correlated with edge effect, and two species, Anthenoides

meridionalis (Schrottky, 1906) and T. diversipes had a

remarkable higher abundance in the larger site (lower edge

effect) than in the remaining sampling sites. T. diversipes

very common and abundant in Brazilian forests, a good

candidate to a monitoring program.

Augochlorini not followed the the expected notion that

richness could increase with fragment size. Winfree et al.

Fig. 2–15 Scatter plots correlating assemblages’ parameters and

fragment predictors. 10 Euglossina richness and edge effect. 11

Euglossina richness and connectivity. 12 E. violacea abundance and

fragment size. 13 E. violacea abundance and edge effect. 14 E. nigrita

abundance and area. 15 E. nigrita abundance and edge effect

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(2007), explaining the finding that bee richness is posi-

tively related to land use, pointed out that richness may be

maximized at an intermediate level of human disturbance,

due to a higher occupation of different species than in

undisturbed landscapes. Augochlorini is a common ele-

ment in southern Neotropics, in terms of richness and

abundance, especially in open vegetational areas (Goncal-

ves and Melo 2005). Moreover, the group has generalist

life form, considered as polylectic, with variable nesting

behavior and habits (Michener 2007), and the great plas-

ticity of sweat bees can explain why the group is com-

monly sampled in degraded areas including forest edges,

pastures, and secondary vegetation. Therefore augochlorine

bees can be considered with great importance in disturbed

areas.

For fragment connectivity, Calvillo et al. (2010) did not

find effect on assemblage descriptors, arguing that the

distance among their fragments exceed the dispersal ability

of bees, but here we have found positive correlation of

connectivity and Apidae richness (Fig. 1), as well as with

the richness of both categories of trophic specialization

(Figs. 1, 8), clearly a reflection of Apidae overall pattern.

Solitary bees and ground nester bees also were positively

associated with connectivity (Figs. 5, 6), and those func-

tional groups correspond to most bees, 98 and 80 %

respectively, in the present study. As pointed out by Stef-

fan-Dewenter (2003) the dispersal abilities of bees and the

distance among fragments should be analyzed together.

The foraging range of bees are variable, from 0.1 to about

13 km, and strongly dependent of body size (Greenleaf

et al. 2007), with smaller bees being more strongly affected

by isolation than large ones (Williams et al. 2010). Gath-

mann and Tscharntke (2002) claimed that for small solitary

bees the local habitat structure appears to be of more

importance than the large-scale landscape structure,

therefore, in the scale of the present study, connectivity

plays an important role, allowing that bees explore

resources of different fragment patches.

The other functional classes did not show any correla-

tion, possibly for the few numbers of sampled species. For

eusocial bees, Brosi et al. (2007) showed that stingless bees

are positively related to fragment size, especially due to

forest cover, and Aizen and Feinsinger (1994) found that

fragmentation affect native bees negatively, but honey bees

positively. Here no statistical correlation was found for

honey bees, stingless bees or eusocial group, but P. dror-

yana abundance was positively correlated with fragment

size, being another candidate to ecological indication. The

cleptoparasite bees were considered as potential indicator

taxa for assessing bee communities (Sheffield et al. 2013).

In the cases of fragmentation studies, some studies such as

Alfert et al. (2001) and Calvillo et al. (2010) found effects

of fragment size on the richness of cleptoparasite bees,

indicating the sensibility of this group in some conditions.

However, in the present study no statistical effect was

found, probably due to low sampled richness and abun-

dance of the group, an indication of rarity as pointed out by

Sheffield et al. (2013).

In Neotropics, orchid bees are the most studied bee

group on fragmentation studies. Here Orchid bee richness

increases with less edge effect and more connectivity but

no relation with fragment was found. Storck-Tonon et al.

(2013), studying the response of Amazonian assemblage,

also found that edge effect and connectivity were an ade-

quate predictor of Euglossina richness. The connectivity as

argued by the authors (Storck-Tonon et al. 2013) is

important due to the high foraging range of orchid bees

(Wikelski et al. 2010), which is superior to the distance

among the studied fragments. Previous studies show

associations of fragment size and abundance (Brosi 2009),

composition, (Ramalho et al. 2009), and diversity (Peru-

quetti et al. 1999, Nemesio and Silveira 2010), but here we

have only found effects on the abundance of two particular

species, E. nigrita and E. violacea.

Several studies considered the E. nigrita, a widely dis-

tributed species in Neotropical, as indicator of habitat

perturbation (e.g. Peruquetti et al. 1999; Bezerra and

Martins 2001; Tonhasca et al. 2002; Nemesio and Silveira

2006; Aguiar and Gaglianone 2008; Knoll and Penatti

2012; Storck-Tonon et al. 2013;) and our results corrobo-

rate these studies, once E. nigrita was negatively correlated

with fragment size, but positively with edge effect. On the

other hand, E. violacea can be considered as indicator of

habitat quality since it is positively correlated with size, but

negatively with edge effect. Some studies have considered

this species as ecological indicator of conservation in forest

habitats. For instance, Sofia and Suzuki (2004), studying

forest fragments in Londrina, Parana State, found the

sensitiveness of this species to size reduction and, in the

same region, Giangarelli et al. (2009), studying nine frag-

ments from 10 to 580 ha, found a positive correlation of E.

violacea and fragment size, advocating for the use of this

species as ecological indicator. A similar pattern was

recently found by Knoll and Penatti (2012) in five frag-

ments in Sao Paulo State. E. violacea has a distribution in

Atlantic forest (Nemesio and Silveira 2007), being extre-

mely common in southern Brazil during the spring season

(Goncalves et al. 2014), when the species can be used as

ecological indicator in habitat fragmentation and monitor-

ing studies, as summarized above.

As showed by Reyes-Novelo et al. (2009), bees fit the

criteria of bioindicators selection of habitat fragmentation.

Most of the criteria are implicit to the group biology or rely

on the state of the group knowledge, such as environmental

relevance, geographical and habitat range, economic

potential and easiness of sampling. But the response to

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habitat change parameters can be directly tested and our

results reinforce the sensibility of bees to forest fragmen-

tation and the group as a whole, as well as its subgroups or

selected species, as E. violacea, E. nigrita, P. droryana,

and T. diversipes should be considered in conservation

programs.

Acknowledgments The authors are grateful to Ruford Small Grants

Foundation for financial support. We also thank Instituto Chico

Mendes de Conservacao da Biodiversidade (license number 12195-1)

and Ivan Riedi for permission to access the study the area. Special

thanks to Marilia Favalesso, Mariele Camargo, Vanessa Scherer, and

Vinicius Berno for helping with sampling and processing the mate-

rial; to Gabriel Melo for helping with species identification; and to

Fernando Medeiros for proofreading.

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