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Zootaxa 2892: 59–68 (2011) ISSN 1175-5326 (print edition)

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Copyright © 2011 · Magnolia Press
Article ZOOTAXA
ISSN 1175-5334 (online edition)

Euglossa marianae sp. n. (Hymenoptera: Apidae): a new orchid bee from the
Brazilian Atlantic Forest and the possible first documented local extinction of a
forest-dependent orchid bee

ANDRÉ NEMÉSIO
Instituto de Biologia, Universidade Federal de Uberlândia. Rua Ceará, S/N, Campus Umuarama, Uberlândia, MG. 38.400-902. Bra-
zil. E-mail: andre.nemesio@gmail.com

Abstract

The orchid bee faunas of Floresta Nacional do Rio Preto, Reserva Biológica Córrego Grande, and Reserva Biológica Córrego
do Veado, in the northernmost portion of the state of Espírito Santo, southeastern Brazil, were surveyed for orchid bees for the
first time. A total of 1,603 males belonging to 24 species were attracted to 16 different scent baits and actively collected with
insect nets during 100 hours from December, 2009, to February, 2010. One species of Euglossa, known as strongly dependent
on well preserved mature forests, once recorded at the region, was not found in this survey and may indicate the first docu-
mented local extinction of an orchid bee species. This species, which Atlantic Forest population has been treated as Euglossa
analis Westwood, 1840, is here considered a new species, Euglossa marianae sp. n.

Key words: Atlantic Forest, conservation, Euglossa analis, Euglossina, euglossine bees, extinction

Introduction

Field surveys of Neotropical orchid bees (Hymenoptera: Apidae: Euglossina) have gained in popularity through the
last decades (e.g. Pearson & Dressler 1985; Powell & Powell 1987; Roubik & Ackerman 1987; Becker et al. 1991;
Morato et al. 1992; Oliveira & Campos 1995; Rasmussen 2009). The Brazilian Atlantic Rain Forest domain was
the last of the big Neotropical forest biomes where orchid-bee fauna surveys started to be carried out (Rebêlo &
Garófalo 1991, 1997; Bezerra & Martins 2001; Tonhasca Jr. et al. 2002; Nemésio 2003, 2010b, 2011a; Sofia et al.
2004; Sofia & Suzuki 2004; Milet-Pinheiro & Schlindwein 2005; Darrault et al. 2006; Nemésio & Silveira 2006a,
b, 2007, 2010; Silveira et al. 2011). Contrary to the still mostly continuous forested areas in the Amazon Basin, the
Atlantic Forest is now highly scattered in thousands of fragments (Ribeiro et al. 2009), only a few of them being
larger than 10,000 ha. The combination of a fragmented biome with species highly dependent on forested areas –
some of them presenting apparently restricted geographic distributions – may represent a threat to many orchid
bees, as recently warned (Nemésio 2009, 2010a). Authors of the two most recently described orchid bee species
from this biome, for example, treated both species as potentially threatened and considered the loss of suitable
habitat as the main reason (Nemésio 2010a, Faria Jr. & Melo 2011). Faria Jr. & Melo (2011: 38) went still further
and mentioned that they hope the description of Eufriesea pyrrhopyga Faria Jr. & Melo, 2011 “does not represent a
description of an already extinct species”.
The state of Espírito Santo, southeastern Brazil, once held one of the most impressive forest cover of the Atlan-
tic Forest, but most of this forest was completely wiped out during the 20th century, with only a handful of forest
patches remaining (Dean 1995; Galindo-Leal & Câmara 2003). Only two of these forest fragments (Reserva Natu-
ral Vale, 22,000 ha; Reserva Biológica de Sooretama, 24,000 ha) are larger than 20,000 ha, but both are connected,
forming a 46,000-ha area, whereas the remaining forested areas in Espírito Santo are very small, rarely exceeding
3,000 ha (Ribeiro et al. 2009). Astonishingly, despite of many collections carried out in Espírito Santo and even
several species of orchid bees having Espírito Santo as their type localities, there is no published data on the
orchid-bee fauna of the state, except for Silveira et al. (2002) and Nemésio (2009: 17), the latter mostly based on
the unpublished study by Bonilla-Gómez (1999).

Accepted by C. Rasmussen: 19 May 2011; published: 26 May 2011 59


One of the most emblematic forest-dependent orchid-bee species of the Atlantic Forest is the bee until now
considered as Euglossa analis Westwood, 1840 (e.g. Tonhasca Jr. et al. 2002; Silveira et al. 2002; Nemésio & Sil-
veira 2006a; Nemésio 2009, 2010b). As pointed out by Nemésio (2010b), this species has only been recorded from
large forest fragments, the smallest area where this species was ever reported being a 2,700-ha area in the state of
Alagoas, northeastern Brazil.
Robert L. Dressler collected orchid bees in the Atlantic Forest in 1968, especially in the states of Bahia and
Espírito Santo, but his data were never published. Nevertheless, recently the original field notes from 1964 to 1978
by Dressler were made available by Dr. M. Whitten at ftp://ftp.flmnh.ufl.edu/Public/Dressler/. On page 80 of these
field notes there is the record (entry 1270) of twenty-one Eg. analis males collected in the vicinity of Conceição da
Barra, northern Espírito Santo, 16 of them attracted to cineole and the remaining five captured at skatole from the
9th to the 15th of November, 1968 (eight of these specimens deposited at Moure Collection in Curitiba – see the 109th
page of Dressler’s notes). As the largest forest fragments left in Conceição da Barra presently do not exceed 3,000
ha, it provided an opportunity to test the hypothesis that Eg. analis is a forest-dependent species that would not sur-
vive for long in small areas without access to deep interior of forest (Tonhasca Jr. et al. 2002; Nemésio & Silveira
2006a; Nemésio 2009, 2010b). Most of the original vegetation in northern Espírito Santo was completely wiped
out during the 1960’s and 1970’s.
The main goals of this study were: (i) to inventory the orchid-bee faunas of three forest preserves at the north-
ern portion of the state of Espírito Santo and (ii) to search for Euglossa analis in an area where it had been previ-
ously collected some 40 years ago, but subjected to strong anthropogenic pressures during the last decades.

Material and Methods

Study sites. This study was conducted at three Atlantic Forest preserves in the state of Espírito Santo (Fig. 1), all
belonging to the federal government of Brazil: Floresta Nacional do Rio Preto (FLONA Rio Preto, 18°24’S -
39°50’W, ca. 2,830 ha, municipality of Conceição da Barra), Reserva Biológica Córrego Grande (REBIO Córrego

FIGURE 1. Map showing the location of the three areas sampled in this study (yellow circles), the type locality of Euglossa
marianae sp. n. (green circle), and the known areas where this species has been recorded (red circles) (see text for details).

60 · Zootaxa 2892 © 2011 Magnolia Press NEMÉSIO


Grande, 18°16’S - 39°49’W, ca. 1,504 ha, municipality of Conceição da Barra) and Reserva Biológica Córrego do
Veado (REBIO Córrego do Veado, 18°22’S - 40°10’W, ca. 1,850 ha, municipality of Pinheiros) from December,
2009, to February, 2010, during the summer in Brazil, when orchid bees are most active (e.g. Martins & Souza
2005). The original vegetation at the north of Espírito Santo is essentially dense Atlantic Rain Forest (Veloso et al.
1984), but most part of the region was severely deforested for timber exploitation and only scattered forest frag-
ments remain. All three preserves suffered the action of intense fires at the end of the 1980’s.
Sampling. One site was sampled at REBIO Córrego Grande and two sites were sampled at both FLONA Rio
Preto and REBIO Córrego do Veado. This difference in sampling is due to (i) the most prominent heterogeneity
within both FLONA Rio Preto and REBIO Córrego do Veado, the areas most severely affected by the fires in the
1980’s; (ii) the larger areas of these latter areas and, (iii) especially because sampling at the single site at REBIO
Córrego Grande recorded the largest number of orchid bees of all the sampled sites in these areas (see Table 1);
since this is the smallest area, sampling another site would require the possible killing of many more bees, what
seemed not to be reasonable since the amount of bees collected (more than 500 specimens) was high enough to
make any needed inferences. Twenty hours of active sampling with insect nets were performed in each of the
selected sites in the preserves, totaling 100 hours: (i) FLONA Rio Preto, site-1 (18°21’28”S, 39°51’18”W, ca. 18 m
a.s.l., an area not affected by the fires in the 1980’s) was sampled on the 25th, 26th and 28th of December, 2009, from
07:00h to 14:00h (except on the 28th of December, from 07:00h to 13:00h); (ii) FLONA Rio Preto, site-2
(18°23’16”S, 39°51’09”W, ca. 40 m a.s.l., an area severely affected by the fires in the 1980’s) was sampled on the
24th, 27th and 29th of December, 2009, from 07:00h to 15:00h (except on the 24th of December, from 11:00h to
16:00h); (iii) REBIO Córrego Grande (18°15’37”S, 39°49’06”W, ca. 52 m a.s.l., an area severely not by fires) was
sampled from the 2nd to the 4th of February, 2010, from 07:00h to 15:00h (except on the 4th of February, from 07:00h
to 12:00h); (iv) REBIO Córrego do Veado, site-1 (18°22’05”S, 40°08’23”W, ca. 120 m a.s.l., an area affected by
the fires in the 1980’s) was sampled on the 5th, 8th and 9th of February, 2010, from 07:00h to 15:00h (except on the
5th of February, from 07:00h to 11:00h); (v) REBIO Córrego do Veado, site-2 (18°22’05”S, 40°08’23”W, ca. 120 m
a.s.l., an area affected by the fires in the 1980’s) was sampled on the 6th, 7th and 10th of February, 2010, from 07:00h
to 13:00h (except on the 7th of February, from 07:00h to 15:00h). At each site, 16 scent baits were placed ca. 2.0
meters apart from each other at about 1.5 m above the ground. These baits were made of cotton waddings soaked
with one of the following substances, known or believed to be attractive to orchid bees: benzyl acetate, benzyl alco-
hol, r-carvone, 1,8-cineole, p-cresol acetate, dimethoxybenzene, eugenol, β-ionone, methyl benzoate, methyl
trans-cinnamate, heneicosane, methyl salicylate, skatole, tricosane, p-tolyl acetate and vanillin. Baits with cineole,
the most volatile compound, were recharged every hour. Bees arriving on the baits during the sampling period were
collected with insect nets and killed with ethyl acetate. They were labeled as belonging to the project “Euglossina
da Hileia Baiana” and were deposited at the Entomological Collection of ‘Universidade Federal de Minas Gerais’
(UFMG), where they were numbered from 17375-49603 to 17606-50315 (specimens from FLONA Rio Preto), and
from 18036-51844 to 18323-52827 (specimens from REBIO Córrego Grande and REBIO Córrego do Veado).
Taxonomy. Taxonomy follows Nemésio (2009, 2010b, 2011a). General morphological terminology for bees
follows Roig-Alsina & Michener (1993) and Michener (2007). Specific morphological terminology for orchid bees
follows Nemésio (2009: 10, 12).
Type repositories. All material examined during this study is currently deposited at the Entomological Collec-
tion of the ‘Universidade Federal de Minas Gerais’ (UFMG).

Results

One thousand, six hundred and three orchid-bee males belonging to 24 species were collected in the three pre-
serves. The single site at REBIO Córrego Grande presented the highest abundance (more than 25 specimens col-
lected per hour) and number of species (20) of orchid bees. The abundance ranged from eight or nine specimens
collected per hour at sites affected by the fires in the 1980’s (site 1 at FLONA Rio Preto and site 2 at REBIO Cór-
rego do Veado) to around 25 specimens collected per hour at sites with best preserved vegetation not affected by
fires (site 2 at FLONA Rio Preto and the single site at REBIO Córrego Grande) (Table 1). When preserves are com-
pared, REBIO Córrego Grande presented the highest number of species (20), followed by FLONA Rio Preto (19)
and REBIO Córrego do Veado (17). Abundance was also lowest at REBIO Córrego do Veado, even at the site not

EUGLOSSA MARIANAE SP. N. (HYMENOPTERA: APIDAE) Zootaxa 2892 © 2011 Magnolia Press · 61
affected by fires (Table 1). The three species of Euglossa (Glossura) occurring in northern Espírito Santo and
southern Bahia – Euglossa ignita Smith, 1874, Eg. imperialis Cockerell, 1922, and Eg. roubiki Nemésio, 2009 –
were collected in all sites except those at REBIO Córrego do Veado, where only three specimens of Eg. ignita were
collected (Table 1). The most common species at each preserve was also different: Euglossa imperialis was the
dominant species at FLONA Rio Preto, although almost all specimens of this species were collected at site 2, the
best preserved one (at site 1, Eulaema marcii Nemésio, 2009 was the dominant species); Euglossa carolina Nemé-
sio, 2009 was the dominant species at REBIO Córrego Grande; and Eulaema nigrita Lepeletier, 1841 was the dom-
inant species at both sites at REBIO Córrego do Veado, albeit Euglossa augaspis Dressler, 1982b was almost as
common as El. nigrita at site 1, the best preserved one (Table 1).
The species until now treated as Euglossa analis, formerly known to occur in Conceição da Barra (see Intro-
duction and Discussion) was not recorded in any of the preserves sampled in this study. It is here described as a
new species. It shares many morphological characters with the Amazonian population of Eg. analis, but both can
be morphologically distinguished.

TABLE 1. List of species and number of specimens collected at three forest preserves at northern state of Espírito Santo. FRP
= Floresta Nacional do Rio Preto. RCG = Reserva Biológica do Córrego Grande. RCV = Reserva Biológica do Córrego do
Veado. Numbers after the acronyms of the Forest preserves indicate the sampling sites (see Material and Methods).

Species FRP 1 FRP 2 RCG RCV 1 RCV 2 Total


Eufriesea surinamensis (L., 1758) 03 01 00 00 00 04
Euglossa aratingae Nemésio, 2009 00 00 02 01 00 03
Eg. augaspis Dressler, 1982b 09 20 22 48 14 113
Eg. avicula Dressler, 1982c 00 01 00 00 00 01
Eg. carolina Nemésio, 2009 27 59 145 29 34 294
Eg. cognata Moure, 1970 00 00 03 00 00 03
Eg. crassipunctata Moure, 1968 10 63 38 32 17 160
Eg. despecta Moure, 1970 05 52 40 20 07 124
Eg. hemichlora Cockerell, 1917 00 01 00 00 00 01
Eg. heterosticta Moure, 1968 00 01 05 01 00 07
Eg. ignita Smith, 1874 02 22 45 03 00 72
Eg. imperialis Cockerell, 1922 02 102 28 00 00 132
Eg. leucotricha Rebêlo & Moure, 1996 00 00 00 00 01 01
Eg. milenae Bembé, 2007 00 00 36 08 12 56
Eg. mixta Friese, 1899 02 14 29 00 00 45
Eg. pleosticta Dressler, 1982c 02 02 08 17 02 31
Eg. roubiki Nemésio, 2009 03 66 45 00 00 114
Eg. securigera Dressler, 1982c 00 00 10 00 01 11
Eulaema atleticana Nemésio, 2009 00 03 05 03 10 21
El. marcii Nemésio, 2009 49 28 18 34 36 165
El. nigrita Lepeletier, 1841 44 38 07 49 41 179
El. niveofasciata (Friese, 1899) 00 05 11 07 06 29
Exaerete frontalis (Guérin, 1844) 00 02 02 01 00 05
Ex. smaragdina (Guérin, 1844) 02 10 04 08 08 32
Total 160 490 503 261 189 1,603

62 · Zootaxa 2892 © 2011 Magnolia Press NEMÉSIO


Euglossa (Euglossa) marianae Nemésio, sp. n.

Diagnosis. This species is clearly assigned to the subgenus Euglossa (Euglossa) Latreille, 1802 due to its small
size, short extended tongue, rhomboid metatibia, small and widely separated tufts on S2. It is also easily included
within Euglossa analis group due to the throughout dark blue to violet coloration, except in the last three terga,
which are green or reddish depending on the species. In Euglossa marianae sp. n. the three last terga are bright
green (Figure 2C). Nevertheless, it can be distinguished from Euglossa analis, its most closely related species, by
the shape of the anterior mesotibial tuft (see Fig. 2E–F). In Euglossa analis, the anterior tuft is divided in two lobes,
the inferior one much larger than the superior lobe (see Fig. 2F and also this character in the holotype, illustrated in
Nemésio 2009: 103). In Euglossa marianae sp. n. the two lobes are approximately the same size, the superior lobe
slightly pointed (Fig. 2E). The other species in Euglossa analis group occurring in the Atlantic Forest domain pres-
ent the last three terga reddish colored and cannot be confused with E. marianae sp. n. It can be also differentiated
from the Amazonian Euglossa retroviridis Dressler, 1982a, the only other species in the group which also have the
last three terga green-colored, by the shape of mesotibial tufts (see drawings in Dressler, 1982a) and by having only
two teeth in the mandible (E. retroviridis males have three teeth).
Description (Male, Fig. 2)
Color and vestiture. Clypeus violet, rest of head dark blue to violet (Fig. 2B); mesosoma dark blue to violet
(Fig. 2A); T1–T4 solid violet, T5–T7 bright green (Fig. 2A, C). Wings pale brown. Pubescence very sparse,
predominantly fulvous hairs on metasoma and antennal sockets, black and fulvous hairs on mesosoma, black hairs
especially on scutum (compared to predominantly fulvous hairs in Eg. analis). Ivory paraocular markings well
developed, not reaching malar area; anterior surface of antennal scape black.
Head. Width 4.7 mm; interorbital distance at level of antennal sockets 2.7 mm; maximum interorbital distance
3.0 mm; scape 1.1 mm; eye length 2.9 mm.
Body. Body length ca. 11.0 mm; anterior wing ca. 8.9 mm; tongue in repose reaching hindcoxa; scutellum 2.8
mm wide and 1.3 mm long; abdominal width 4.5 mm.
Legs. Foretibia and forebasitarsus fringed with medium-sized, dense, fulvous hairs; velvet area occupying all
the ventral side of mesotibia, posterior mesotibial tuft small, oblong; anterior mesotibial tuft deeply notched, with
two lobes of approximately the same size (in Eg. analis the inferior lobe much larger than the superior lobe – see
Fig. 2F), upper lobe slightly pointed (Fig. 2E); metatibia oblong-rhomboid, inflated, post-glandular area fringed
with medium-sized hairs (Fig. 2D).
Metasoma. Punctation on discal base of T1 sparse, with large circular punctures; on distal part of T1 and T2-
T4 dense, comprised of small circular punctures; on T5-T7 dense, with large circular punctures. S2 with small,
widely separated tufts.
Etymology. The specific epithet honors Mariana Abrahão Assunção, student of Biological Sciences at the Uni-
versidade Federal de Uberlândia, Minas Gerais.
Type locality. Holotype collected at Parque Estadual do Rio Doce (19º43’S - 42º34’W; 200 m a.s.l.), in the
municipality of Marliéria, state of Minas Gerais, southeastern Brazil.
Attractive baits. Specimens of this species have been collected at cineole and skatole baits, some with orchid
pollinaria of Coryanthes attached (Dressler’s field notes).
Female. Unknown.
Type material: HOLOTYPE – male, with the following data: “Euglossini do PERD, Pq. E. Rio Doce, 3858-
11096” and “Brasil, Marliéria, MG, 04/07/1999, A. Nemésio” and “Euglossa (Euglossa) marianae Nemésio, sp. n.,
HOLOTYPUS” (UFMG). PARATYPES – 30 males, with the same label data: “Brasil, MG, Marliéria, Pq. E. Rio
Doce, Junho/1999, A. Nemésio leg.” (UFMG – to be distributed to other institutions).

Discussion

The strategy of intensive sampling over a few days during the rainy season has been demonstrated to be very useful
(Nemésio 2010b, 2011), and the number of specimens collected in this study supports this view. As pointed out by
Nemésio (2010b), twenty hours of sampling during the season when orchid bees are most abundant provides simi-
lar results to one year of monthly samplings of three to four hours each sampling (e.g. Rebêlo & Garófalo 1991,
1997; Santos & Sofia 2002; Nemésio & Silveira 2007, 2010), with the advantage of reducing costs of field trips.

EUGLOSSA MARIANAE SP. N. (HYMENOPTERA: APIDAE) Zootaxa 2892 © 2011 Magnolia Press · 63
FIGURE 2. Holotype Euglossa marianae sp. n. A: dorsal view. B: frontal view of face. C: last three terga. D: metatibia. E:
mesotibia. F: mesotibia of one specimen of Euglossa analis from Parque Nacional da Serra do Divisor, state of Acre, Brazilian
Amazon (specimen number 12417-36556, deposited at UFMG).

The species collected at the region are mostly the same as those recorded by Bonilla-Gómez (1999) (consider-
ing the taxonomic review provided by Nemésio 2009) for a 22,000 ha forest remnant in Linhares, some 100 km
southwards from Conceição da Barra.
Except for the highly seasonal Eufriesea Cockerell, 1908 species, which due to the sampling method used here
are more difficult to be recorded (discussed by Nemésio 2010b, 2011), the only outstanding absence in this study is
Euglossa marianae sp. n., which represented 17% of the orchid-bee community at Reserva Natural Vale (Bonilla-
Gómez 1999 as Eg. analis). Although this species is considered as highly sensitive and extremely dependent on

64 · Zootaxa 2892 © 2011 Magnolia Press NEMÉSIO


well-preserved large forest fragments, it must be stressed that it is relatively common where it does occur. For
example, at Parque Estadual do Rio Doce (PERD), a 36,000 ha forested area in the state of Minas Gerais, it repre-
sented around 50% of the orchid-bee community, reaching up to 70% at sites inside the forest fragment (Nemésio
& Silveira 2006a). It also represented 5% of the orchid-bee community at Parque Estadual do Desengano in the
state of Rio de Janeiro (Tonhasca Jr. et al. 2002). On the other hand, it was not recorded at a 1,000 ha forested area
in the municipality of Caratinga, only ca. 50 km distant from PERD, in Minas Gerais (Nemésio 2003), suggesting
the population of PERD is completely isolated from other populations. This species was also commonly collected
at Parque Nacional do Monte Pascoal (southern Bahia), but no specimens were collected during more than 100
hours of sampling in five nearby fragments ranging from 1 to 300 ha situated quite close (10 to 30 km away) to the
large (> 10,000 ha) Parque Nacional do Monte Pascoal (Nemésio, unpub. data). The same happens in the region of
Una (southern Bahia), where the species is commonly caught at the Reserva Biológica de Una (>18,000 ha), but
absent from the smaller areas around it (Nemésio, unpub. data).
I could find Euglossa marianae sp. n. in only thirteen areas in the Atlantic Forest (Fig. 1) (from north to
south): (i) Estação Ecológica de Murici, state of Alagoas, ca. 6,000 ha (split in two larger fragments and several
smaller ones) (Nemésio 2010b); (ii) Reserva Biológica Michelin, municipality of Igrapiúna, state of Bahia, ca.
(3,000 ha, but connected to other large fragments covering a total area >10,000 ha) (unpub. data); (iii) Parque
Estadual da Serra do Conduru, Uruçuca, Bahia, ca. 10,000 ha (Nemésio 2011); (iv) Reserva Biológica de Una,
Una, Bahia, ca. 18,500 ha (unpub. data); (v) RPPN Estação Veracel, Santa Cruz Cabrália, Bahia, ca. 6,000 ha
(unpub. data); (vi) Parque Nacional do Pau Brasil, Porto Seguro, Bahia, ca. 10,000 ha (unpub. data); (vii) Parque
Nacional do Monte Pascoal, Porto Seguro, Bahia, ca. 12,000 ha (unpub. data); (viii) Parque Nacional do Descobri-
mento, Prado, Bahia, ca. 22,500 ha (unpub. data); (ix) Reserva Natural Vale, Linhares, Espírito Santo, ca. 22,000
ha (Bonilla-Gómez 1999); (x) Reserva Biológica de Sooretama, Sooretama, Espírito Santo, ca. 24,000 ha (unpub.
data); (xi) PERD, Marliéria, Minas Gerais, ca. 36,000 ha (Nemésio & Silveira 2006a); (xii) Parque Estadual do
Desengano, Campos dos Goytacazes, Rio de Janeiro, ca. 22,500 ha (Tonhasca Jr. et al. 2002); and (xiii) Parque
Nacional da Serra do Mar, São Sebastião, São Paulo, ca. 47,500 ha (Nemésio 2009). Only two of these areas (Esta-
ção Ecológica Murici and RPPN Estação Veracel) are smaller than 10,000 ha. Although Reserva Biológica
Michelin is smaller than 10,000, the forest patch where Euglossa marianae sp. n. was collected (unpub. data) is
connected to a forest remnant larger than 10,000 ha. In only two of the above forest patches the specimens were not
collected by myself (Parque Estadual do Desengano and Parque Nacional da Serra do Mar), but specimens from
both areas are currently deposited at UFMG. As can be seen in Fig. 1, the original geographic distribution of this
species was very large, and it should have been one of the most common and widespread orchid-bee species of the
entire biome. Nowadays, however, it is restricted to the areas shown in Fig. 1 and, probably, some other unsampled
areas to date, such as Reserva Biológica Augusto Ruschi, in Santa Teresa, Espírito Santo [in fact, there are some
specimens collected in this area deposited at Museu Nacional (Rio de Janeiro) and UFMG, but these are old speci-
mens and I know of no recent collections in this area to confirm the species still persists there].
R. L. Dressler collected 361 orchid bees attracted to bait scents in Conceição da Barra, 21 (6%) of them being
identified as the former Eg. analis. It is roughly the same percentage found by Tonhasca Jr. and colleagues (2002)
at Parque Estadual do Desengano. Forty years later, no specimen was recorded, even during the season when this
species was most abundant at the nearby Parque Nacional do Monte Pascoal (north of Conceição da Barra) and
Reserva Biológica de Sooretama (south of Conceição da Barra) (Nemésio, unpub. data). This seems to corroborate
the hypothesis by Nemésio & Silveira (2007a: 189) that orchid bee populations of some species in small fragments
may represent the last survivors of species condemned to extinction. Since orchid-bee inventories using bait scents
to attract males is a recent methodology, there are no previous data to compare to current ones to estimate whether
populations are actually declining. This is, thus, the first indication that an orchid bee species may have declined to
local extinction. The sampling of more than 1,600 specimens, 1,150 of them in the two preserves close to the coast,
cannot be considered low sampling. In fact, in no study carried out in the Atlantic Forest to date such a large num-
ber of specimens had been collected, except that performed by Tonhasca Jr. and colleagues (2002).
During previous years, I hesitated to separate Euglossa analis into two species (one representing the Amazo-
nian population, the other one representing the Atlantic Forest population), for the reasons explained in Nemésio
(2009: 13). Nevertheless, the data gathered in the last two years (Nemésio 2010b, 2011, and this work), convinced
me that it is urgent to consider the Atlantic Forest population as a species under threat and only its recognition as a
distinct species, with a name, will make it eligible to be considered in any Brazilian official program for preserva-

EUGLOSSA MARIANAE SP. N. (HYMENOPTERA: APIDAE) Zootaxa 2892 © 2011 Magnolia Press · 65
tion of threatened species. The morphological characters presented here are enough to distinguish both populations.
Nevertheless, some ecological considerations should also be made. As pointed out above, although restricted to and
isolated in the largest forest remnants, populations of Euglossa marianae sp. n. are not particularly small in most of
these remnants. On the other hand, the Amazonian Euglossa analis is never collected in high numbers in Amazo-
nian inventories (e.g. Morato et al. 1992; Oliveira & Campos 1995; Nemésio & Morato 2004, 2006; Storck-Tonon
et al. 2009).
The last point addressed by Nemésio (2009: 13), however, remains. Isolation between the Amazon and the
Atlantic forests is here argued to split both populations into two species. Nonetheless, the Atlantic Forest “popula-
tions” are also isolated from each other and gene flow is most probably interrupted due to isolation. Thus, would it
be reasonable to consider all the Atlantic Forest populations as belonging to only one species? This is not a simple
question, since, as pointed out before (Nemésio 2009: 13), these populations may actually become distinctive but,
most probably, as seen in the present study, most of them, especially those in the smaller areas, as in Alagoas, seem
to become extinct.
Nemésio (2009) performed the first attempt to assess the conservation status of each orchid bee species occur-
ring in the Atlantic Forest using the criteria established by IUCN (IUCN 2001). Nevertheless, data were scarce for
most species and accurate assumptions could not be safely made. Euglossa marianae sp. n. (as Eg. analis) was
then considered to be Near Threatened (Nemésio 2009: 102). Current data do not support that Eg. marianae sp. n.
should be considered as Vulnerable (the first risk category according to IUCN criteria), since it is known from more
than 10 locations and there is no throughout study showing the declining rates of its populations. Nevertheless, the
data presented here strongly suggest that its populations are declining. More important, if Eg. marianae sp. n. can-
not be considered under immediate threat when considered globally, at least some of its populations could clearly
be considered as such if considered regionally. Conservation measures in Brazil are taken both by the federal gov-
ernment and by the governments of the states. Thus, when considered at the state level, at least four populations of
Eg. marianae sp. n. can be considered as threatened: in the states of Alagoas, Minas Gerais, Rio de Janeiro and São
Paulo Eg. marianae sp. n. is only found in one forest fragment. In all these states, the species should be considered
as Endangered [IUCN (2001) criteria: EN B1 ab(ii,iii)], but in Alagoas (very small area) and in São Paulo (only
one known specimen), it should be considered as Critically Endangered [IUCN (2001) criteria: CR B1 ab(ii,iii)].
Conservation action must be immediately taken and field studies are also urgently necessary to estimate the declin-
ing rates of Eg. marianae sp. n. populations.

Acknowledgments

The Brazilian government, through the environmental departments IBAMA and ICMBio, provided the collecting
permits (#19136-1, 19136-2, 19976-1) which allowed me to survey the orchid-bee fauna of FLONA Rio Preto,
REBIO Córrego Grande, and REBIO Córrego do Veado. I also thank Alberto F. Klotz (FLONA Rio Preto), Lígia
M. Coser (REBIO Córrego Grande), and José Maria A. Poubel (REBIO Córrego do Veado), who were very helpful
during my field research. Prof. Dr. Marcelo O. Gonzaga, from the Universidade Federal de Uberlândia, helped me
with the photographs of the holotype Euglossa marianae sp. n. (using equipment provided by the project INCT/
HYMPAR/SUDESTE) depicted as Figure 2. Dr. Claus Rasmussen, as the Zootaxa Editor for Apoidea, and two
anonymous referees made valuable comments on the first draft of this manuscript.

References

Becker, P., Moure, J.S. & Peralta, F.J.A. (1991) More about euglossine bees in Amazonian Forest fragments. Biotropica, 23,
586–591.
Bembé, B. (2007) Revision der Euglossa cordata-Gruppe und Untersuchungen zur Funktionsmorphologie und Faunistik der
Euglossini (Hymenoptera, Apidae). Entomofauna, Supplement, 14, 1–146.
Bezerra, C.P. & Martins, C.F. (2001) Diversidade de Euglossinae (Hymenoptera, Apidae) em dois fragmentos de Mata Atlânti-
ca localizados na região urbana de João Pessoa, Paraíba, Brasil. Revista Brasileira de Zoologia, 18, 823–835.
Bonilla-Gómez, M.A. (1999) Caracterização da Estrutura Espaço-temporal da Comunidade de Abelhas Euglossinas
(Hymenoptera, Apidae) na Hiléia Bahiana. Unpublished Ph. D. Dissertation. Universidade Estadual de Campinas, Campi-
nas, Brazil, xii + 153pp.

66 · Zootaxa 2892 © 2011 Magnolia Press NEMÉSIO


Cockerell, T.D.A. (1908) Notes on the bee-genus Exaerete. Psyche, 15, 41–42.
Cockerell, T.D.A. (1917) Some euglossine bees. Canadian Entomologist, 49, 144–146.
Cockerell, T.D.A. (1922) Bees in the collection of the United States Museum, IV. Proceedings of the U. S. National Museum,
60, 1–20.
Darrault, R.O., Medeiros, P.C.R., Locatelli, E., Lopes, A.V., Machado, I.C. & Schlindwein, C. (2006) Abelhas Euglossini. In:
Porto, K. C, Almeida-Cortez, J. S. & Tabarelli, M. (Eds), Diversidade biológica e conservação da Floresta Atlântica ao
norte do rio São Francisco. Ministério do Meio Ambiente, Brasília, pp. 239–253.
Dean, W. (1995) With Broadax and Firebrand—The Destruction of the Brasilian Atlantic Forest. University of California
Press, Berkeley.
Dressler, R.L. (1982a) New species of Euglossa II. (Hymenoptera: Apidae). Revista de Biologia Tropical, 30, 121–129.
Dressler, R.L. (1982b) New species of Euglossa III. The bursigera species group (Hymenoptera: Apidae). Revista de Biologia
Tropical, 30, 131–140.
Dressler, R.L. (1982c) New species of Euglossa IV. The cordata and purpurea species groups. Revista de Biologia Tropical, 30,
141–150.
Fabricius, J.C. (1787) Mantissa Insectorum sistens eorum species nuper detectas adjectis characteribus genericis, differentiis
specificis, emedationibus, ovservationibus. Vol. 1, Christi. Gottl. Proft, Copenhagen, xx + 348 pp.
Faria Jr., L.R.R. & Melo, G.A.R. (2011) A new species of Eufriesea Cockerell (Hymenoptera, Apidae, Euglossina) from north-
eastern Brazil. Revista Brasileira de Entomologia, 55(1), 35–39.
Friese, H. (1899) Monographie der Bienengattung Euglossa Latr. Természetrajzi Füzetek, 22, 117–172.
Galindo-Leal, C. & Câmara, I.G. (2003) Atlantic Forest hotspots status: an overview. In: Galindo-Leal, C. & Câmara, I.G.
(Eds), The Atlantic Forest of South America—biodiversity status, threats, and outlook. Island Press, Washington, pp. 3–
11.
Guérin-Menéville, F.E. (1844) Iconographie du règne animal de G. Cuvier, ou représentation d’après nature de l’une des espèc-
es les plus remarquables, et souvent non encore figurées, de chaque genre d’animaux. Avec un texte descriptif mis au cou-
rant de la science. Ouvrage pouvant servir d’atlas a tous les traités de zoologie. J. B. Baillière, Paris, Vol. 3 (Insectes), xvi
+ 576 pp.
IUCN. (2001) The IUCN Red List of Threatened Species. Categories and Criteria, version 3.1. Available at http://www.iuc-
nredlist.org/info/categories_criteria2001#critical [Accessed on February 20th, 2011].
Latreille, P.A. (1802) Historie Naturelle, Generale et Particuliere des Crustaces et des Insectes. 14 volumes. F. Dufart. Paris.
Lepeletier de Saint Fargeau, A.L.M. (1841) Histoire Naturelle des Insectes, Hyménoptères, Vol. 2. Librairie Encyclopédique de
Roret, Paris, 680 pp.
Linnaeus, C. (1758) Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteri-
bus, Differentiis, Synonymis, Locis. Editio decima, reformata. I. Laurentii Salvii, Holmiae, iv + 824 pp.
Martins, C.F. & Souza, A.K.P. (2005) Estratificação vertical de abelhas Euglossina (Hymenoptera, Apidae) em uma área de
Mata Atlântica, Paraíba, Brasil. Revista Brasileira de Zoologia, 22, 913–918.
Michener, C.D. (2007) The Bees of the World. Second Edition. Johns Hopkins University, Baltimore, 1016 pp.
Milet-Pinheiro, P. & Schlindwein, C. (2005) Do euglossine males (Apidae, Euglossini) leave tropical rainforest to collect fra-
grances in sugarcane monocultures? Revista Brasileira de Zoologia, 22, 853–858.
Mittermeier, R.A., Myers, N., Gil, P.R., Mittermeier, C.G. (1999) Hot spots: Earth’s Biologically Richest and Most Endangered
Terrestrial Ecoregions. CEMEX, Mexico, 430 pp.
Morato, E.F., Campos, L.A.O. & Moure, J.S. (1992) Abelhas Euglossini (Hymenoptera, Apidae) coletadas na Amazônia Cen-
tral. Revista Brasileira de Entomologia, 36, 767–771.
Moure, J.S. (1968) Espécies novas de Euglossa da América Central. Boletim da Universidade Federal do Paraná, Zoologia, 3,
13–64.
Moure, J.S. (1970) The species of euglossine bees of Central América belonging to the subgenus Euglossella. Anais da Aca-
demia Brasileira de Ciências, 42, 148–157.
Nemésio, A. (2003) Preliminary sampling of Euglossina (Hymenoptera: Apidae: Apini) of Reserva Particular do Patrimônio
Natural Feliciano Miguel Abdala, Caratinga, Minas Gerais state, Brazil. Lundiana, 4, 121–124.
Nemésio, A. (2007) Three new species of Euglossa Latreille (Hymenoptera: Apidae) from Brazil. Zootaxa, 1547, 21–31.
Nemésio, A. (2009) Orchid bees (Hymenoptera: Apidae) of the Brazilian Atlantic Forest. Zootaxa, 2041, 1–242.
Nemésio, A. (2010a) Eulaema (Apeulaema) felipei sp. n. (Hymenoptera: Apidae: Euglossina): a new forest-dependent orchid
bee found at the brink of extinction in northeastern Brazil. Zootaxa, 2424, 51–62.
Nemésio, A. (2010b) The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in northeastern Brazil, with new geo-
graphic records and an identification key to the known species of the Atlantic Forest of northeastern Brazil. Zootaxa, 2656,
55–66.
Nemésio, A. (2011) The orchid-bee fauna (Hymenoptera: Apidae) of a forest remnant in southern Bahia, Brazil, with new geo-
graphic records and an identification key to the known species of the area. Zootaxa, 2821, 47–54.
Nemésio, A. & Faria Jr., L.R.R. (2004) First assessment of orchid bee fauna (Hymenoptera: Apidae: Apini: Euglossina) of
Parque Estadual do Rio Preto, a cerrado area in southeastern Brazil. Lundiana, 5, 113–117.
Nemésio, A. & E.F. Morato (2004) Euglossina (Hymenoptera: Apidae: Apini) of the Humaitá Reserve, Acre state, Brazilian
Amazon, with comments on bait trap efficiency. Revista de Tecnologia e Ambiente, 10(2), 71–80.

EUGLOSSA MARIANAE SP. N. (HYMENOPTERA: APIDAE) Zootaxa 2892 © 2011 Magnolia Press · 67
Nemésio, A. & E.F. Morato (2006) The orchid-bee fauna (Hymenoptera: Apidae) of Acre state (northwestern Brazil) and a re-
evaluation of euglossine bait-trapping. Lundiana, 7(1), 59–64.
Nemésio, A. & Silveira, F.A. (2006a) Edge effects on the orchid-bee fauna (Hymenoptera: Apidae) at a large remnant of Atlan-
tic Forest in southeastern Brazil. Neotropical Entomology, 35, 313–323.
Nemésio, A. & Silveira, F.A. (2006b) First record of Eulaema helvola (Hymenoptera: Apidae: Euglossina) for the state of
Minas Gerais: biogeographic and taxonomic implications. Neotropical Entomology, 35, 418–420.
Nemésio, A. & Silveira, F.A. (2007) Orchid bee fauna (Hymenoptera: Apidae: Euglossina) of Atlantic Forest fragments inside
an urban area in southeastern Brazil. Neotropical Entomology, 36, 186–191.
Nemésio, A. & Silveira, F.A. (2010) Forest fragments with larger core areas better sustain diverse orchid bee faunas
(Hymenoptera: Apidae: Euglossina). Neotropical Entomology, 39, 555–561.
Oliveira, M.L. & Campos, L.A.O. (1995) Abundância, riqueza e diversidade de abelhas Euglossinae (Hymenoptera: Apidae)
em florestas contínuas de terra firme na Amazônia central, Brasil. Revista Brasileira de Zoologia, 12, 547–556.
Pearson, D.L. & Dressler, R.L. (1985) Two-year study of male orchid bee (Hymenoptera: Apidae: Euglossini) attraction to
chemical baits in lowland south-eastern Perú. Journal of Tropical Ecology, 1, 37–54.
Powell, A.H. & Powell, G.V.N. (1987) Population dynamics of male euglossine bees in Amazonian forest fragments. Biotro-
pica, 19, 176–179.
Rasmussen, C. (2009) Diversity and abundance of orchid bees (Hymenoptea: Apidae, Euglossini) in a tropical rainforest
succession. Neotropical Entomology, 38, 66–73.
Rebêlo, J.M.M. & Garófalo, C.A. (1991) Diversidade e sazonalidade de machos de Euglossini (Hymenoptera, Apidae) e prefer-
ência por iscas odores em um fragmento de floresta no sudeste do Brasil. Revista Brasileira de Biologia, 51, 787–799.
Rebêlo, J.M.M. & Garófalo, C.A. (1997) Comunidades de machos de Euglossinae (Hymenoptera, Apidae) em matas semi-
decíduas do nordeste do estado de São Paulo. Anais da Sociedade Entomológica do Brasil, 26, 243–256.
Rebêlo, J.M.M. & Moure, J.S. (1996) [1995] As espécies de Euglossa Latreille do nordeste de São Paulo (Apidae, Euglossi-
nae). Revista Brasileira de Zoologia, 12, 445–466.
Ribeiro, M.C., Metzger, J.P., Martensen, A.C., Ponzoni, F.J. & Hirota, M.M. (2009) The Brazilian Atlantic Forest: how much is
left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153.
Roig-Alsina, A. & Michener, C.D. (1993) Studies of the phylogeny and classification of long-tongued bees (Hymenoptera:
Apoidea). The University of Kansas Science Bulletin, 55, 123–173.
Roubik, D.W. & Ackerman, J.D. (1987) Long-term ecology of euglossine orchid-bees (Apidae: Euglossini) in Panama. Oecolo-
gia, 73, 321–333.
Sakagami, S.F., Laroca, S. & Moure, J.S. (1967) Two Brazilian apid nests worth recording in reference to comparative bee soci-
ology, with description of Euglossa melanotricha Moure. Annotationes Zoologicae Japonensis, 40, 45–54.
Santos, A.M. & Sofia, S.H. (2002) Horário de atividade de machos de Euglossinae (Hymenoptera, Apidae) em um fragmento
de floresta semidecídua no norte do estado do Paraná. Acta Scientiarum, 24, 375–381.
Silveira, F.A., Melo, G.A.R. & Almeida, E.A.B. (2002) Abelhas Brasileiras: sistemática e identificação. F. A. Silveira. Belo
Horizonte. 253 pp.
Silveira, G.D., Nascimento, A.M., Sofia, S. H. & Augusto, S.C. (2011) Diversity of the euglossine bee community
(Hymenoptera, Apidae) of an Atlantic Forest remnant in southeastern Brazil. Revista Brasileira de Entomologia, 55(1),
109–115.
Smith, F. (1874) A revision of the genera Epicharis, Centris, Eulema and Euglossa, belonging to the family Apidae, section
Scopulipedes. Annual Magazine of Natural History, 4, 440–446.
Sofia, S.H., Santos, A.M. & Silva, C.R.M. (2004) Euglossine bees (Hymenoptera, Apidae) in a remnant of Atlantic Forest in
Paraná state, Brazil. Iheringia, Série Zoologia, 94, 217–222.
Sofia, S.H. & Suzuki, K.M. (2004) Comunidades de machos de abelhas Euglossina (Hymenoptera: Apidae) em fragmentos flo-
restais no sul do Brasil. Neotropical Entomology, 33, 693–702.
Storck-Tonon, D., Morato, E.F. & Oliveira, M.L. (2009) Fauna de Euglossina (Hymenoptera: Apidae) da Amazônia Sul-Oci-
dental, Acre, Brasil. Acta Amazonica, 39, 693–706.
Tonhasca Jr., A., Blackmer, J.L. & Albuquerque, G.S. (2002) Abundance and diversity of euglossine bees in the fragmented
landscape of the Brazilian Atlantic Forest. Biotropica, 34, 416–422.
Veloso, H.P., Rangel Filho, A.L.R. & Lima, J.C.A. (1984) Caracterização de solos e avaliação dos principais sistemas de
manejo dos tabuleiros costeiros do Baixo Rio Doce e da região norte do Espírito Santo, e sua interpretação para uso agrí-
cola. Viçosa, UFV. 153p.
Westwood, J.O. (1840) Foreign Bees. In: Duncan, J. (Ed.) The Natural History of Bees, in W. Jardine (ed.) The Naturalist’s
Library. Lizars, Edinburgh, pp. 260–301.

68 · Zootaxa 2892 © 2011 Magnolia Press NEMÉSIO

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