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Papéis Avulsos de Zoologia

versión impresa ISSN 0031-1049versión On-line ISSN 1807-0205

Pap. Avulsos Zool. vol.59  São Paulo  2019  Epub 13-Jun-2019

http://dx.doi.org/10.11606/1807-0205/2019.59.26 

ARTICLE

What do we know about Neotropical trap-nesting bees? Synopsis about their nest biology and taxonomy

Camila Cristina Ferreira da Costa1  2 
http://orcid.org/0000-0003-1950-7525

Rodrigo Barbosa Gonçalves1  3 
http://orcid.org/0000-0001-5623-0938

1Universidade Federal do Paraná (UFPR), Departamento de Zoologia (DZOO). Curitiba, PR, Brasil.

Abstract

Cavity-nesting bees are enigmatic because they are difficult to observe in the wild, hence trap-nests (man-made cavities) provide the means by which these bees may be studied. Trap-nests is an efficient methodology to study these bees and are common worldwide. These traps have been used for a variety of reasons, including inventories, to examine pollen load, to study habitat disturbance, and bee conservation. However Neotropical trap-nesting bees’ taxonomy and biology are still poorly known and here we provide a review about these subjects. We searched for trap-nest bee studies in the Neotropical Region using Google Scholar and ISI Web of Science at any time in the past to December 2017. We found 109 independent studies, most of which were from Brazil (87 studies), followed by Argentina (10 studies), and other countries had fewer than five studies each. A total of 140 species, 24 genera, 10 tribes and three subfamilies were reported in trap-nests. Nest architecture was described for only 49 species. Taxonomy is only well-known for 14 genera, somewhat known for seven and is essentially unavailable for three genera. Construction material, closing plug and cell shape are similar among species in the same tribes and genera. Vestibular and intercalary cells, and the preliminary plug are variable, even at the specific level. Apinae is the most studied group with available data for all genera recorded in trap-nests. Colletinae is the least-studied group and nothing is known for their nesting biology. Megachilinae is intermediate, with some studies of taxonomy and nesting. We suggest that further trap-nest studies should provide more detailed information on nest architecture and construction materials, including explicit mention of structures that are absent. All Neotropical bees need more taxonomic studies, but some, such as Hylaeus and Megachile, require more attention since Hylaeus is essentially unknown and Megachile is very common on trap-nests.

Key-Words. Bee hotels; Diversity; Methodology; Nesting behavior; Systematics

INTRODUCTION

Bee nests ordinarily comprises brood cells and associated structures and are often in burrows in the soil, aboveground cavities or free-standing (Michener, 2007). Most bees and apoid wasps excavate underground nests and this form of nesting is primitive in the superfamily (Melo, 1999; Hedtke et al., 2013; Branstetter et al., 2017). While we do not yet have a phylogenetic reconstruction of substrate preference for all bee species, apparently aboveground nesting arose independently several times. Four of the seven bee main lineages have species that nest in cavities and there are some reversals to soil nesting (Almeida, 2008).

Aboveground substrates are variable and cavity-nesting bees are likely to be an artificial ecological grouping. The use of existing tunnels in deadwood is common and bees often excavate decomposing wood and soft pith in stems and galls for nests (Sheffield et al., 2011). Other examples of natural substrates include snail shells (Gess & Gess, 2008), rock surfaces (Eickwort, 1975) and man-made cavities, such as in brick walls (Santos et al., 2016), metal frames (Sheffield et al., 2011), farm tractor radiators (Sheffield, 2017) and door locks (RBG pers. obs.).

As a consequence of the wide variety of nesting substrates, artificial nesting substrates (trap-nests, nest-boxes, bee hotels) can be used to trap these cavity nesting bees and wasps (Krombein, 1967; MacIvor & Packer, 2015). These traps are often made of bundles of hollow stems, paper or cardboard tubes (Camillo et al., 1995; Araújo et al., 2016) and holes drilled in wood (Krombein, 1967; Buschini, 2006; see MacIvor, 2017 for a review). Characteristics of the entrance diameter, nest length, color and also placement of nests all influence bee selection and use of traps-nest (Krombein, 1967; MacIvor & Packer, 2015). Also, traps can be placed in aggregates of greater density to improve the likelihood of use. Studies tend to develop their own type of trap and so a wide variety of traps and their dispositions have been used, making comparisons of these studies very difficult.

As a consequence of the successful use of traps, studies are common worldwide, with over 1,300 results in Google (January 2018). Traps are used for many reasons, including to sample and monitor cavity nesting species and their predators (Araujo et al., 2017; Oliveira & Gonçalves, 2017), to compare habitats among different regions (Araújo et al., 2016), to examine altitudinal gradients (Perillo et al., 2017) and vertical stratification (Morato, 2001b; Stangler et al., 2015, 2016), to detect responses to fragmentation (Stangler et al., 2015, 2016; Rocha-Filho et al., 2017) and urbanization (Pereira-Peixoto et al., 2014), to promote pollination and pollinator conservation (MacIvor & Packer, 2015) and to study the nest biology and behavior of particular groups (Rocha-Filho & Garófalo, 2016a,b; Moure-Oliveira et al., 2017).

Despite of the large number of trap-nest studies, the Neotropical bee fauna taxonomy and diversity is still poorly known (Silveira et al., 2002). Here we summarize the available information on biology and taxonomy of trap-nesting bees in this region. A synopsis is important to provide direction for future studies because further coordinated efforts will be important to produce comparable data and robust advances in this research field.

MATERIAL AND METHODS

To summarize the trap-nesting studies, we searched using Google Scholar and ISI Web of Science through the end of 2017. We used the following search terms: (Ninhos armadilha OR Nidos trampa OR Trap-nest OR Trap-nest bees) AND (Neotropical OR countries names). We included all countries from Chile to Mexico as search terms. The literature cited along any retrieved study was also used to find additional references. The following criteria was used to select the studies for this work: (1) used trap-nesting methods (understood here as any artificial cavity that was built by the researcher in which bees nested); (2) a primary reference, revision studies were not included; and (3) published in a peer reviewed journal or as an academic thesis or dissertation (other gray literature such as abstracts and conference reports were not included).

Data for nesting behavior, other biological details at higher taxonomic levels and the number of species in the world follow Michener (2007). The number of Neotropical species follows the online version of Moure’s Bee Catalogue (Moure et al., 2013). Nesting behaviors of species and genera were gathered from the original studies. Terminology for nest architecture follows Krombein (1967) as illustrated in Fig. 1. Trap-nest biology knowledge is considered “available” when there is at least one published description with details on the architecture using the trap-nest methodology, and “unavailable” in the absence of this information. Species identification was taken from the original studies and, if necessary, revised following Moure’s Bee Catalogue (Moure et al., 2013). We adopt the single-family classification for bees following Melo & Gonçalves (2005). Identification at morphospecies (“spp.”) was also included in Table S1 but not counted in Table 1 except for the genera only recorded for undetermined species. We opted to include all records of primary references except for a single morphospecies of Neofidelia (Veddeler et al., 2010). This refers to soil nesting species that are probably incorrectly identified. Taxonomy for each genus was evaluated at the species level and was considered “sufficient” when published taxonomical revision with identification keys is available, “moderate” when species are relatively well known and partial (regional or subgeneric) revisions are available, but much of the identification relies on taxonomists, and “insufficient” otherwise. Identification resources were gathered from Michener (2007), Moure et al. (2013) and published studies as described above. For the distributions of genera we followed Moure et al. (2013) and for species we used information from the original trap-nest studies (Table S1). States or provinces are informed of Argentina, Brazil and Mexico.

Figure 1 A generalized bee trap-nest architecture. At the left is the first cell made. The dark grey indicates food objects for the larvae (white). On the right is the last cell built with presence of a vestibular cell being variable. 

Table 1 A summary of trap-nesting bee genera from the Neotropical region. Notes: ¹morphospecies are excluded for most genera; ²only recorded as morphospecies; ³available for nest description of at least one species; ⁴sufficient for taxa with published taxonomical revision, moderate for taxa only identified by taxonomists, insufficient when no revision is available. 

Taxon Number of recorded species¹ Trap-nest description³ Taxonomic knowledge⁴
Apinae
Centridini
Centris 14 Available Moderate
Euglossini
Eufriesea 8 Available Sufficient
Euglossa 14 Available Moderate
Tetrapediini
Tetrapedia 7 Available Insufficient
Xylocopini
Xylocopa 6 Available Moderate
Colletinae
Colletini
Colletes 1 Unavailable Insufficient
Rhynchocolletes Available Sufficient
Hylaeini
Hylaeus 1 Unavailable Insufficient
Megachilinae
Anthidiini
Anthidium 4 Available Sufficient
Anthidulum Unavailable Sufficient
Anthodioctes 5 Available Sufficient
Carloticola 1 Available Sufficient
Ctenanthidium 1 Available Sufficient
Dicranthidium 3 Unavailable Sufficient
Duckeanthidium 1 Available Moderate
Epanthidium 5 Available Sufficient
Hypanthidium 1 Unavailable Moderate
Loyolanthidium Unavailable Moderate
Nananthidium 1 Unavailable Sufficient
Saranthidium 2 Unavailable Sufficient
Lithurgini
Microthurge 1 Unavailable Sufficient
Trichothurgus 1 Available Sufficient
Megachilini
Megachile 33 Available Insufficient
Osmiini
Heriades Unavailable Moderate

RESULTS

Our literature search resulted in a total of 109 independent studies, 87 from Brazil followed by Argentina (10), Costa Rica (5), Ecuador (2), Colombia (2), Mexico (1), Jamaica (1) and Trinidad and Tobago (1) (Table S1 summarizes trap-nesting bee literature). These studies comprised 140 species, 24 genera, 10 tribes and three subfamilies of trap-nesting bees in the Neotropical region. Nest architecture was described for 49 species and another 65 species were reported without descriptions (Tables 1 and 2). Fourteen genera had sufficient taxonomic descriptions, seven moderate and three insufficient.

Table 2 A summary on nest architecture of trap-nesting bee genera from Neotropical region. Data was summarized through the end of 2017. (?) There is not information or is dubious; (P) present, (O) occasional, (A) absent. The genera without published information about nest architecture we did not list in table. 

Taxon Material Entrance diameter (mm) Cell arrangement Number of brood cells Brood cells shape Vestibular cells Closing plug Empty space Preliminary plug Intercallary cells
Anthidium trichomes, plants parts, detritus 5-11 linear 1-19 ? ? P ? ? ?
Anthodioctes resin, mud, wood chips 5-11 linear 2-11 ? O P O O O
Carloticola resin, clay, sand 6-10 ? 3-6 ? P ? ? P ?
Centris oil, wood chips or sand 4.8-14 linear or irregular 1-16 cylindrical or oval O P P ? O
Ctenanthidium resin 4 linear ? ? ? P P ? ?
Duckeanthidium resin, saliva 11-13 ? 1-3 ? ? ? ? ? ?
Epanthidium resin, mud, sand ? linear 2-9 ? O ? ? ? ?
Eufriesea resin, wood chips 15-25 linear or irregular 2-4 oval O ? A A A
Euglossa resin 11-22 linear or cluster 2-14 oval ? P P A A
Megachile leaves, petals, mud rocks 6-27 linear 1-16 cylindrical O ? ? O ?
Tetrapedia oil, soil, sand 3-12 linear 1-9 ? P P P P ?
Trichothurgus wood chips, pollen 8-11 ? no partition ? ? A ? ? ?
Xylocopa wood particles 12-23 linear 1-6 barrel ? A ? ? ?

APINAE. Although this group lacks a phylogenetic consensus (Cardinal et al., 2010; Hedtke et al., 2013; Martins et al., 2014; Bossert et al., 2019), wood nesting arose from soil nesting at least seven times following those topologies. All tribes of wood cavity nesting bees except the Tapinotaspidini were sampled using trap-nests, and Centridini, Euglossini and Tetrapediini were often found in these Neotropical studies.

Centridini. Traditionally the tribe comprised Centris and Epicharis (Bossert et al., 2019), but it can be paraphyletic (e.g.,Martins & Melo, 2016). Centris included 251 species (Michener, 2007), mostly Neotropical (224 species) (Moure et al., 2013), use floral oils mixed with other material for nest construction and protection (Vinson et al., 1996). Nesting in existing cavities arose two times in this tribe in C. (Xanthemisia) and the clade C. (Hemisiella) + C. (Heterocentris) (Martins & Melo, 2016) and according with Moure et al. (2013) they comprise 35 described species. Only C. (Hemisiella) and C. (Heterocentris) were reported using trap nests (Vinson et al., 2010; Vélez et al., 2017). These subgenera use different material for nest construction; for example, Heterocentris use wood chips and Hemisiella use sand (Vinson et al., 2010). Otherwise, nest characteristics are similar among these subgenera (Table 2).

Centris nests entrance diameter varies from 4.8-14 mm (Drummont et al., 2008; Vinson et al., 2010; Carvalho et al., 2016; Vélez et al., 2017). Nests usually comprise linear brood cells (Drummont et al., 2008; Vinson et al., 2010; Carvalho et al., 2016; Vélez et al., 2017), with two rows of cells in Centris tarsata Smith, 1874 (Aguiar & Garófalo, 2004). Nests have from one to 16 circular to oval brood cells (Aguiar & Garófalo, 2004; Aguiar et al., 2006; Buschini & Wolff, 2006; Drummont et al., 2008; Vinson et al., 2010; Carvalho et al., 2016; Moure-Oliveira et al., 2017; Vélez et al., 2017). Vestibular and intercalary cells are occasionally found (Buschini & Wolff, 2006; Vinson et al., 2010; Vélez et al., 2017). A closing plug and an empty space in the distal end of the cell rows are common (Aguiar & Garófalo, 2004; Aguiar et al., 2006). The genus is mostly Neotropical with few species reaching North America (Moure et al., 2013). Subgenera of Centris may be identified by Silveira et al. (2002) and Michener (2007). Some C. (Hemisiella) and C. (Heterocentris) species may be identified by Thiele (2003) and Vivallo & Vélez (2016). Keys to Centris species from Central and North America and for species from Argentina are available Snelling (1984) and Roig-Alsina (2000), respectively.

Euglossini. Orchid bees are mostly Neotropical, comprising five genera: Aglae (1 Neotropical species), Eufriesea (67 Neotropical species), Euglossa (128 Neotropical species and 6 subgenera), Eulaema (33 Neotropical species and 2 subgenera), and Exaerete (8 Neotropical species). This tribe is unique in its elongate tongue and males collect orchid fragrances. Aglae and Exaerete are cleptoparasites of Eufriesea and Eulaema. Most species nest in existing cavities in which they do not build storage cells, unlike the other corbiculate bees (Michener, 2007). Taxonomy of the group is mostly based on males while females are identified by experts.

Eufriesea nests are built with wood chips and plant resins (Viana et al., 2001; Kamke et al., 2008). Entrance diameter varies from 15-25 mm (Viana et al., 2001; Kamke et al., 2008). Cell orientation may be horizontal as in Eufriesea mussitans, (Fabricius, 1787) (Viana et al., 2001) to irregular as in Eufriesea smaragdina (Perty, 1833) (Kamke et al., 2008). In the latter, cells are still built sequentially (Kamke et al., 2008). Usually 2-4 oval and smooth brood cells are built having internal divisions of resin, with occasional vestibular cells (Viana et al., 2001; Kamke et al., 2008). Eufriesea is distributed from Argentina to Mexico (Moure et al., 2013). Kimsey (1982) provided a key to the males.

Euglossa have nest architecture in the subgenera Euglossa s.s. and Glossura similar to Eufriesea, with brood cell divisions and closing plugs of resins only (Garófalo et al., 1998; Peruquetti, 1998; Augusto & Garófalo, 2004; Parra-H & Nates-Parra, 2009). Entrance diameters varied from 11-22 mm. Brood cells may be linear (vertical or horizontal) or clustered (Garófalo et al., 1998; Peruquetti, 1998; Augusto & Garófalo, 2004, 2009), and the usually oval cells vary from 4-14 per nest (Garófalo et al., 1998; Peruquetti, 1998; Augusto & Garófalo, 2004). Preliminary plugs were not mentioned, while a distal empty space is typical (Parra-H & Nates-Parra, 2009). Females may nest alone or with other, usually sister, females, and may reuse empty cells (Silva et al., 2016). If with others, a dominant female remains at the nest while others forage (Augusto & Garófalo, 2004, 2009, 2011; Freiria et al., 2017). Euglossa is found from Mexico to Argentina (Moure et al., 2013). Most subgenera can be identified using Silveira et al. (2002), while no complete revision of the genus is available. Males from São Paulo (Brazil) can be identified using keys provided by Rebêlo & Moure (1995), males and females of E. (Glossura) from Atlantic forest with Faria-Jr. & Melo (2007) and E. (Euglossa) in the E. analis group using Faria & Melo (2012).

Tetrapediini. Traditionally including two genera, the cleptoparasite Coelioxoides Cresson and Tetrapedia (Michener, 2007), recent phylogenetic hypotheses place Coelioxoides within the cleptoparasitic clade of Apinae (Cardinal et al., 2010; Hedtke et al., 2013). The Tetrapedia position in Apinae is uncertain, Martins et al. (2014) suggested that the genus is related to Ctenoplectrini, and Bossert et al. (2019) consider both as related with Xylocopini. In both genera include species that nest aboveground. Tetrapedia, comprising 28 species, is found from Mexico to Argentina (Moure et al., 2013). There is no available key for species identification. They collect floral oils and nest in existing cavities (Alves-dos-Santos et al., 2002). Cell partitions and closing plug are of soil or sand mixed with floral oils (Alves-dos-Santos et al., 2002; Camillo, 2005; Menezes et al., 2012; Rocha-Filho & Garófalo, 2016a). Entrance diameter varies between 3-12 mm (Alves-dos-Santos et al., 2002; Camillo, 2005; Menezes et al., 2012; Rocha-Filho & Garófalo, 2016a). Cells are linear and horizontal (Alves-dos-Santos et al., 2002; Camillo, 2005; Menezes et al., 2012; Rocha-Filho & Garófalo, 2016a), or linear and vertical (Camillo, 2005). Brood cells vary from 1-9 (Alves-dos-Santos et al., 2002; Camillo, 2005; Menezes et al., 2012; Rocha-Filho & Garófalo, 2016a). Vestibular cells, preliminary plugs and distal empty spaces are present (Rocha-Filho & Garófalo, 2016a).

Xylocopini. Among the most speciose lineages of aboveground nesting bees, most nest in cavities, with one reversal to ground-nesting in X. (Proxylocopa) (Leys et al., 2002). The tribe has four lineages, of which only Allodapina is not Neotropical (Michener, 2007). Ceratina, with 199 species, has never been reported in trap-nests. Also, Manuelia (3 species) in Argentina and Chile has not been reported in trap-nests (see Daly et al., 1987; Flores-Prado et al., 2008 for detailed biology). Xylocopa (111 species) in the Neotropical region (Moure et al., 2013) includes trap-nesting only in the subgenus Neoxylocopa (Table 1, Table S1). Phylogenetic relationships among these four lineages vary by study, yet Allodapina and Ceratinina are consistently considered to be sister groups (Flores-Prado et al., 2008; Cardinal et al., 2010; Martins et al., 2014).

Xylocopa nests comprise fine wood particles that the bees excavate (Marchi & Melo, 2010; Pereira & Garófalo, 2010; Lucia et al., 2017) and cell partitions are of wood particles mixed with saliva (Pereira & Garófalo, 2010; Lucia et al., 2017). Females of Xylocopa and Ceratina remove nest partitions and the allodapines lack cell partitions (Michener, 2007). Entrance diameter varies from 12-23 mm (Marchi & Melo, 2010) with 1-6 brood cells (Marchi & Melo, 2010; Pereira & Garófalo, 2010). Brood cells are barrel-shaped (Pereira & Garófalo, 2010), as in species of Manuelia (Flores-Prado et al., 2008). Cells are aligned (Marchi & Melo, 2010; Pereira & Garófalo, 2010). Females may reuse nests and nest cooperatively with sisters (Camillo & Garófalo, 1989). Guarding behavior, recognition and tolerance of nest males are found too in all xylocopines (Flores-Prado et al., 2010). Xylocopa is distributed in all Neotropical region. Subgenera are identified following Silveira et al. (2002) and Michener (2007). Species from São Paulo (Brazil) are identified following the key in Marchi & Alves-dos-Santos (2013).

COLLETINAE. Known for polyester brood-cell lining, wood nesting probably arose once in the subfamily along with multiple reversals to soil nesting (Almeida, 2008). Of the Neotropical aboveground nesting lineages, only Xeromelissini was not sampled with trap-nests. Nesting behavior in this subfamily was revised by Almeida (2008).

Colletini. This tribe comprises three Neotropical genera, Hemicotelles (2 species), Rhynchocolletes (12 species) and Xanthocotelles (11 species) plus the cosmopolitan Colletes (330 species, 108 Neotropical species) (Michener, 2007). The nesting substrates of Hemicotelles and Xanthocotelles are unknown (Michener, 2007). One species of Rhynchocolletes was recently sampled with trap-nests (Diniz, 2010). Colletes was sampled only once with trap-nests in Neotropical region. Most species nests in soil, some in stem pith or existing cavities (Almeida, 2008). Soil nesting Colletes have linear cells and they lack basitibial and pygidial plates, for this the cavity nesting behavior may be primitive (Almeida, 2008). Otherwise, trap-nest biology in Neotropical species is unknown. Ferrari & Silveira (2015) provided a key to species of Colletini of Minas Gerais (Brazil) and Ferrari (2017) for Colletes of Chile.

Hylaeini. Hylaeus comprises 624 species worldwide of which 111 are Neotropical (Michener, 2007). They nest in existing cavities in a variety of substrates, including wood, pith, rock and soil (Michener, 2007; Almeida, 2008). Nothing is known of the Neotropical species and no identification key is available.

MEGACHILINAE. Most lineages of this subfamily include species that nest above ground, except near root lineages (Gonzalez et al., 2012). Nests may be in the soil, in burrows in the wood, in plant stems, in other cavities, or may be free-standing constructs. Materials used to construct their nest are variable (petals and leaves, resin, nectar, saliva, others). The tribes Anthidiini, Megachilini and Osmiini have been observed carrying material for nesting (Michener, 2007) and all these tribes, along with the Lithurgini, used trap-nests in the Neotropical region.

Anthidiini. This tribe comprises 677 species worldwide and 339 Neotropical species, with 38 (Moure et al., 2013) genera in the neotropics. See Martins et al. (2015) for a list of Danuncia Urban’ publications that include comparative notes and keys to the species. Anthiidines nest in existing cavities or build exposed nests, while few species excavate soil nests (Michener, 2007). Nests comprise a wide variety of materials, including resin, leaf and flower pieces, plant fibers and pebbles (Michener, 2007). A total of 26 species and 12 genera were reported using trap-nests (Tables 1 and S1). Nest architecture is known for: Anthidium (50 Neotropical species), Anthodioctes (43 species), Carloticola (2 Neotropical species) Ctenanthidium (4 species), Duckeanthidium (4 species), Epanthidium (23 species), while nothing is known for half of the genera: Anthidulum (7 species), Dicranthidium (8 species), Hypanthidium (20 species), Loyolanthidium (8 Neotropical species), Nananthidium (13 species) and Saranthidium (10 species) (Moure et al., 2013, Table 1, Table S1).

Anthidium nests partitions and plugs include plant trichomes and other material such as fruits, seeds, leaves, small rocks, wood chips and detritus (Vitale et al., 2017). Entrance diameter varies from 5-11 mm (Vitale et al., 2017). Brood cells are linear, except for Anthidium vigintipunctatum Friese, 1908, which cells were perpendicular or oblique. Brood cells vary from 1-19 (Vitale et al., 2017). The genus occurs from Argentina to Mexico (Moure et al., 2013). Gonzalez & Griswold (2013) provided a key to species.

Anthodioctes cells and closing plug are made with resins, sometimes mixed with mud or wood chips (Morato, 2001a; Alves-dos-Santos, 2004; Camarotti-de-Lima & Martins, 2005). Entrance diameter ranges from 5-11 mm (Morato, 2001a; Camarotti-de-Lima & Martins, 2005). The 2-11 brood cells are linear, some with vestibules and preliminary plugs (Morato, 2001a; Alves-dos-Santos, 2004; Camarotti-de-Lima & Martins, 2005). Anthodioctes megachiloides Holmberg 1903 nests sometimes have intercalary cells and distal empty space (Alves-dos-Santos, 2004). The genus occurs from Mexico to Argentina (Moure et al., 2013). Identification of its species is possible following Urban (1999, 2002, 2003, 2004).

Carloticola nests and cells partitions are of clay or sand mixed with resin (Mello, 2014). Entrance diameter varies from 6-10 mm and nests have 3-6 brood cells. Vestibular cells are filled with flower buds (Asteraceae or Malpighiaceae) and a preliminary plug is present (Mello, 2014). The genus occurs in Argentina, Brazil and Paraguay (Moure et al., 2013). Identification follows Moure & Urban (1990).

Ctenanthidium, a single nest of Ctenanthidium bifasciatumUrban, 1993 was described by Alvarez et al. (2015). Resin covered the inner walls, brood cells and partitions. The entrance was 4.0 mm in diameter. The nest had three serial brood cells between an empty space in the distal end of the nest and a closing plug. The genus is found in Argentina, Bolivia, Brazil and Uruguay (Moure et al., 2013). Identification follows Urban (1991).

Duckeanthidium cells are made with glandular substance and plant resins (Thiele, 2002). Entrance diameter varies from 11-13 mm. Nests have 1-3 brood cells, 15-45 mm from the preliminary plug. Partitions and closing plug were extremely hard, with a resin-like material in the closing plug. The genus occurs from Costa Rica to Brazil (Moure et al., 2013). Comparative notes about taxonomy of the species can be found in Michener (2002) and Urban (2004).

Epanthidium nests are of resin mixed with mud or sand (Gomes, 2016) with 2-9 linear brood cells, occasionally with vestibules. The genus occurs from Mexico to Argentina (Moure et al., 2013) and information to identify its species can be found in Urban (1992, 2006, 2011).

Lithurgini. This tribe comprises two South American genera, Microthurge (4 species) and Trichothurgus (14 species) plus two genera with Neotropical species, Lithurgopsis (5 Neotropical species) and Lithurgus (1 Neotropical species), these species nest in dead, dry, decomposing wood, making nests without cell linings and often without partitions (Michener, 2007; Moure et al., 2013). Microthurge corumbae (Cockerell, 1901) can reuse nests made by one or more females in which guarding occurs (Garófalo et al., 1992). Trichothurgus laticeps (Friese, 1906) build nests with wood particles and pollen (Vitale & Vázquez, 2017). Entrance diameter varying from 8-11 mm and nests are without a closing plug and most are without cell partitions. Females excavate wood with mandibles (Vitale & Vázquez, 2017). Trichothurgus occurs in Argentina, Chile and Peru (Moure et al., 2013), and an identification key is provided by Michener (1983).

Megachilini. This tribe has two Neotropical genera: Megachile and the cleptoparasite Coelioxys. Megachile comprises 1,093 species, of which 431 are Neotropical (Michener, 2007; Moure et al., 2013), with 32 Neotropical subgenera. Nests are built, often with petals and leaves, in existing cavities in soil, wood, and man-made objects, while some may be free-standing construction (Michener, 2007). Seventeen subgenera and 33 species were studied using trap-nests. Megachile builds with leaves, petals, soil, mud and pebbles (Torretta & Durante, 2011; Torretta et al., 2012, 2014, Marques & Gaglianone, 2013; Sabino & Antonini, 2017). Entrance diameter varies from 6-27 mm (Torretta & Durante, 2011; Torretta et al., 2012, 2014; Marques & Gaglianone, 2013; Sabino & Antonini, 2017). One to 16 brood cells tend to be cylindrical and linear (Teixeira et al., 2011; Cardoso & Silveira, 2012; Marques & Gaglianone, 2013; Rocha-Filho & Garófalo, 2016b; Sabino & Antonini, 2017). Preliminary plugs and vestibular cells are uncommon (Torretta & Durante, 2011; Teixeira et al., 2011; Cardoso & Silveira, 2012; Torretta et al., 2012, 2014; Marques & Gaglianone, 2013; Rocha-Filho & Garófalo, 2016b; Sabino & Antonini, 2017). Two species were observed sharing the same nest (Cardoso & Silveira, 2012). Megachile occurs from Mexico to Argentina (Moure et al., 2013). The Megachile subgenera can be identified following Michener (2007) and Silveira et al. (2002). A key to the Neotropical species is not available.

Osmiini. Twenty genera are recognized in this tribe, four of which are found in Mexico and Central America (Ashmeadiella, Atoposmia, Heriades and Osmia;Michener, 2007). Osmiini nest in the soil and in existing cavities (Rozen et al., 2010; Rozen-Jr. & Praz, 2016), using a variety of materials, including petals, mud, pebbles and resins (Praz et al., 2008). Osmiini from the New World tend to nest aboveground more than those from the Old World (Praz et al., 2008), however, the group lacks phylogenetic consensus which is necessary for a proper reconstruction of nesting behavior (Praz et al., 2008; Gonzalez et al., 2012). One Heriades morphospecies was reported in trap-nests in the Neotropical region without nest information (Roubik & Villanueva-Gutiérrez, 2009). An identification subgenera’s key is provided by Michener (2007).

DISCUSSION

We reviewed 109 trap-nesting studies in the Neotropical region that included information for 140 species and 24 genera. Garófalo et al. (2004) listed 57 species for Brazil while we report 90 Brazilian species demonstrating rapid advancement in the study of this group of bees. Some of them are studied more often than others. The Apinae are the most studied, with data for all genera sampled in trap-nests. Conversely, trap-nesting Colletinae have not been reported, and the taxonomy of this subfamily has received little attention (see below). Megachilinae are intermediate, with many nests of the Anthidiini being properly described. Their taxonomy is relatively well-understood (Table 1).

We found that most studies were from Brazil and they were restricted to about half of the states, mostly southeastern (Freitas et al., 2009). The other Neotropical countries continue to be very poorly studied. Argentina, Ecuador and Colombia have several studies and may be considered to have quite understanding of their trap-nesting bees biodiversity. In Central America, Costa Rica is better sampled (e.g.,Coville & Coville, 1980; Thiele, 2005; Vinson et al., 2010), followed by Panama.

The details of nest architecture are similar to most of the taxa with respect to construction material, closing plug and cell shape (Table 2), while other structures may vary among lineages and intraspecifically. For example, entrance diameter is correlated with female body size ensuring the fit of brood cells (Krombein, 1967; MacIvor, 2017). Diameter of trap-nests also seems to be due to female choice, in part, and varies widely among studies (Coville, 1982; MacIvor, 2017). The number of brood cells is also variable and associated with resource availability, sex ratio of progeny and of course, nest length (Coville, 1982; Morato & Martins, 2006). Vestibular and intercalary cells and the preliminary plug also vary widely among trap-nesting bees (Table 2). Vestibular cells vary from occasional to common (Krombein, 1967; Asís et al., 2007), and while they have been suggested to be a defense against parasites (Krombein, 1967; Coville & Coville, 1980), their true purpose has not been experimentally tested (Asís et al., 2007). Also, vestibular cells often remain unmentioned in studies and so their presence or absence in those studies is unclear. As an important nest feature, we recommend that presence and absence of the vestibular cells always be clearly stated. Intercalary cells and the preliminary plug are seldom observed, they may be used in the defense against parasites or to change the conformation of the inner end of the boring, respectively (Krombein, 1967; O’Neill, 2001).

Taxonomic information was sufficient for only 14 genera, more than half of which are in the Anthidiini. This well-known tribe was studied extensively by Urban (see bibliography in Martins et al., 2015). Essentially all the remaining groups are poorly studied taxonomically (Table 1). Relatively well known genera include Centris, and Xylocopa, whose species can often be identified by specialists, but comprehensive keys are not yet available. Hylaeus and Megachile remain poorly studied with many unnamed species (Moure et al., 2013). Tetrapedia is also poorly studied but not so diverse as Hylaeus and Megachile (Moure et al., 2013).

Taxonomical impediment is an important issue in many insect studies (Oliveira et al., 2011; Begum et al., 2011; Jordaens et al., 2013), including in trap-nesting bee studies Araujo et al., 2017; Matos et al., 2016; Iantas et al., 2017). Reliable identification is necessary when using bees as ecological indicators (Tscharntke et al., 1998) even if morphospecies can be used in some diversity metrics and analyses (Magurran, 2004; Tylianakis et al., 2007; Pereira-Peixoto et al., 2014; Araújo et al., 2016; Iantas et al., 2017). Studies of phylogenetic and beta diversity, temporal and spatial distribution patterns and nesting behaviors are all hampered by problems with species identification (Faith, 1992; Magurran, 2004; Mittelbach et al., 2007; Faith, 2015).

CONCLUSIONS

Herein we summarized biological and taxonomic knowledge of trap-nest bees in the Neotropical region. Priorities for future research must be settled to fill the more important gaps. For example, researchers should clearly provide details of nest architecture, including clear statements about the presence and absence of structures that can be considered as characters. We propose that researchers provide details of building material, entrance diameter (if oval, diameter along both axes), cell arrangement, number and shapes of brood cells, presence/absence of vestibular and intercalary cells, preliminary and closing plugs and the back empty space. Some of Neotropical trap-nesting groups require further taxonomical work, but especially Hylaeus and Megachile seeing of the absence of modern taxonomic studies. Megachile has an additional requirement since its high abundance in trap-nests studies.

ACKNOWLEDGMENTS

Camila C.F. Costa is funded by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and Rodrigo B. Gonçalves by CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico). We thank Carlos Garófalo, Gabriel Melo and John Lattke for comments on a previous version of the manuscript. Special thanks to Anderson Lepeco for the nest drawing. James J. Roper, reviewed the English and provided additional suggestions.

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Published with the financial support of the Committee of "Programa de Apoio às Publicações Científicas Periódicas da USP" (SIBi-USP)

Appendices

Table S1 A summary of trap nesting bee species from Neotropical region. Data was summarized through the end of 2017. (Available) It is when there is at least one published description with details on the architecture using trap-nest methodology; (unavailable) is when information is absence. Abbreviations follow: Argentina: BA = Buenos Aires, LP = La Pampa and MZ = Mendoza. Brazil: AC = Acre, AM = Amazonas, BA = Bahia, CE = Ceará, MA = Maranhão, MG = Minas Gerais, PB = Paraíba, PE = Pernambuco, PR = Paraná, RJ = Rio de Janeiro, RN = Rio Grande do Norte, SC = Santa Catarina and SP = São Paulo. Mexico: QR = Quintana Roo. 

Taxon Distribution records (States or provinces from Argentina, Brazil and Mexico are indicated under parenthesis) References for records Trap nest description References for nest descriptions
APINAE
Centridini
Centris (Hemisiella) crassipes Smith, 1874 Jamaica (1) Available (1)
Centris (Hemisiella) dichrootricha (Moure, 1945) Brazil (AC, AM, MA) (2)-(4) Available (4)
Centris (Hemisiella) facialis Mocsáry, 1899 Colombia (5) Unavailable
Centris (Hemisiella) merrillae Cockerell, 1919 Brazil (AC), Trinidad and Tobago (3),(6) Available (6)
Centris (Hemisiella) nitida Smith, 1874 Brazil (AM), Costa Rica (7)-(9) Available (8), (9)
Centris (Hemisiella) tarsata Smith, 1874 Argentina (BA); Brazil (BA, CE, MA, MG, PB, PE, PR, RJ, RN, SC, SP) (10)-(42) Available (33). (43), (44)
Centris (Hemisiella) trigonoides Lepeletier, 1841 Brazil (AM, MG, RN); Costa Rica; Colombia (2),(5),(8),(16),(21) Available (8),(9),(45)
Centris (Hemisiella) vittata Lepeletier, 1841 Brazil (MA, MG, SP); Costa Rica (3), (7), (8), (15), (19), (26), (28), (36), (46), (47) Available (8). (9). (47). (48)
Centris (Hemisiella) sp. Brazil (AC) (3) -
Centris (Heterocentris) adunca Moure, 2003 Brazil (AC) (3) Unavailable
Centris (Heterocentris) analis (Fabricius, 1804) Brazil (AC, AM, BA, MG, PB, PE, PR, RJ, SP); Costa Rica; Colombia; Mexico (QR) (2), (3), (5), (7), (8), (12), (13), (15), (22), (24), (25). (27), (28), (32), (36) (38)-(40), (42), (46), (49)-(55) Available (8), (54)
Centris (Heterocentris) bicornuta Mocsáry, 1899 Brazil (AM, MA); Costa Rica (2), (7), (8), (19), (46) Available (8), (9)
Centris (Heterocentris) difformis Smith, 1854 Costa Rica (46) Unavailable
Centris (Heterocentris) labrosa Friese, 1899 Brazil (SP); Costa Rica (25), (36), (46), (50) Unavailable
Centris (Heterocentris) terminata Smith, 1874 Brazil (AC, AM, BA, MA, MG, PB) (2), (3), (12), (14), (18), (19), (22), (27), (56), (57) Available (58)
Centris (Heterocentris) spp. Brazil (AC, CE, MG, RJ) (3), (14), (18), (27) -
Centris spp. Brazil (SP); Ecuador (25), (59), (60) -
Euglossini
Eufriesea auriceps (Friese, 1899) Brazil (SP) (25), (36) Unavailable
Eufriesea mussitans (Fabricius, 1787) Brazil (BA) (35) Unavailable
Eufriesea purpurata (Mocsáry, 1896) Brazil (AM) (2) Unavailable
Eufriesea smaragdina (Perty, 1833) Brazil (SC) (61) Available (62)
Eufriesea surinamensis (Linnaeus, 1758) Brazil (SP) (25) Unavailable
Eufriesea theresiae (Mocsáry, 1908) Brazil (AM) (2) Unavailable
Eufriesea violacea (Blanchard, 1840) Brazil (MG, SC, SP) (15), (37), (63) Available (63)
Eufriesea violascens (Mocsáry, 1898) Brazil (SP) (36) Unavailable
Eufriesea sp. Brazil (MG) (26) -
Euglossa (Euglossa) amazonica Dressler, 1982 Brazil (CE) (18) Unavailable
Euglossa (Euglossa) anodorhynchi Nemésio, 2006 Brazil (SP) (30), (64) Unavailable
Euglossa (Euglossa) avicula Dressler, 1982 Brazil (AC, MG) (3), (65) Unavailable
Euglossa (Euglossa) cordata (Linnaeus, 1758) Brazil (BA, MA, MG, RN, SP) (17), (21), (32), (35), (36), (39), (65)-(67) Available 68)
Euglossa (Euglossa) fimbriata Moure, 1968 Brazil (SP) (69) Unavailable
Euglossa (Euglossa) gaianii Dressler, 1982 Brazil (AM, MA) (2), (17), (67) Unavailable
Euglossa (Euglossa) hemichlora Cockerell, 1917 Colombia (70) Available (70)
Euglossa (Euglossa) melanotricha Moure, 1967 Brazil (MG, SP) (12), (36), (65) Unavailable
Euglossa (Euglossa) modestior Dressler, 1982 Brazil (AC) (3) Unavailable
Euglossa (Euglossa) pleosticta Dressler, 1982 Brazil (CE, SP) (15), (18), (36) Unavailable
Euglossa (Euglossa) townsendi Cockerell, 1904 Brazil (CE, MG, SP) (16), (19), (25), (26), (38), (36), (65), (66) Available (71)
Euglossa (Euglossa) truncata Rebêlo & Moure, 1996 Brazil (SP) (36), (66) Unavailable
Euglossa (Euglossa) variabilis Friese, 1899 Ecuador (59) Unavailable
Euglossa (Glossura) annectans Dressler, 1982 Brazil (SC, SP) (61), (72), (73) Available (73)
Euglossa spp. Brazil (BA, MA) (35), (74) -
Tetrapediini
Tetrapedia amplitarsis Friese, 1899 Brazil (SP) (36) Available (75)
Tetrapedia curvitarsis Friese, 1899 Brazil (BA, MG, SP) (15), (25), (28), (36), (39), (75) Available (75)
Tetrapedia diversipes Klug, 1810 Brazil (BA, CE, MG, PB, PE, RJ, SP) (15), (22), (24), (25), (27), (28), (32), (36), (38), (42), (75), (76) Available (75), (77), (78)
Tetrapedia garofaloi Moure, 1999 Brazil (SP) (36), (75) Available (75)
Tetrapedia maura Cresson, 1878 Costa Rica (46), (50) Unavailable
Tetrapedia ornata (Spinola, 1853) Brazil (AM) (2) Unavailable
Tetrapedia rugulosa Friese, 1899 Brazil (MG, SP) (25), (28), (36), (75) Unavailable
Tetrapedia spp. Argentina (BA); Brazil (AC, MG, PE, SP); Ecuador (3), (12), (14)-(16), (29), (36), (40), (41), (60) -
Xylocopini
Xylocopa (Neoxylocopa) augusti Lepeletier, 1841 Argentina (BA); Brazil (PR) (34), (79) Available (79)
Xylocopa (Neoxylocopa) frontalis (Olivier, 1789) Brazil (BA, MG, SP) (28), (35), (39), (80)-(82) Available (82), (83)
Xylocopa (Neoxylocopa) grisescens Lepeletier, 1841 Brazil (BA, MG, SP) (28), (35), (39), (80)-(82) Available (82)
Xylocopa (Neoxylocopa) suspecta Moure & Camargo, 1988 Brazil (MA, MG) (28), (74), (80) Unavailable
Xylocopa (Schoenherria) subcyanea Pérez, 1901 Brazil (BA, MG) (23), (35) Unavailable
Xylocopa (Schoenherria) varians Smith, 1874 Costa Rica (46) Unavailable
Xylocopa sp. Brazil (MG) (29) -
Colletinae
Colletini
Colletes rufipes Smith, 1879 Brazil (SP) (25) Unavailable
Colletes spp. Brazil (PE, PR) (24), (34) -
Rhynchocolletes sp. Brazil (PR) (34) Available (34)
Hylaeini
Hylaeus transversus (Vachal, 1909) Brazil (SP) (15) Unavailable
Hylaeus spp. Brazil (PB, RN, PR, SC, SP); Costa Rica (11), (21), (22), (37), (38), (50), (84) -
Megachilinae
Anthidiini
Anthidium andinum Jörgensen, 1912 Argentina (MZ) (85) Available (85)
Anthidium decaspilum Moure, 1957 Argentina (MZ) (85) Available (85)
Anthidium rubripes Friese, 1908 Argentina (MZ) (85) Available (85)
Anthidium vigintipunctatum Friese, 1908 Argentina (LP, MZ) (41), (85), (86) Available (85)
Anthidium spp. Costa Rica, Ecuador (7), (59) -
Anthidulum sp. Brazil (SP) (36) Unavailable
Anthodioctes claudii Urban, 1999 Brazil (PR) (34) Unavailable
Anthodioctes lunatus (Smith, 1854) Brazil (AC, PE) (3), (24) Available (87)
Anthodioctes manauara Urban, 1999 Brazil (AM) (88) Unavailable
Anthodioctes megachiloides Holmberg, 1903 Brazil (MG, SP) (15), (25), (29), (30), (38) Available (89)
Anthodioctes moratoi Urban, 1999 Brazil (AM) (2) Available (88)
Anthodioctes spp. Brazil (AC, BA, SP), Mexico (QR) (3), (36), (39), (49) -
Carloticola paraguayensis (Schrottky, 1908) Brazil (RJ, SP) (36), (90) Available (90)
Ctenanthidium bifasciatum Urban, 1993 Argentina (BA) (91) Available (91)
Dicranthidium arenarium (Ducke, 1907) Brazil (BA, PB, PE, RN) (21), (22), (24), (39) Unavailable
Dicranthidium luciae Urban, 1993 Brazil (BA) (39) Unavailable
Dicranthidium seabrai Urban, 2002 Brazil (SP) (92) Unavailable
Dicrantidium spp. Brazil (MA, PE) (17), (40) -
Duckeanthidium thielei Michener, 2002 Costa Rica (46), (50) Available (93)
Duckeanthidium sp. Brazil (AM) (2) Unavailable
Epanthidium autumnale (Schrottky, 1909) Brazil (PR, SC) (11) Unavailable
Epanthidium erythrocephalum (Schrottky, 1902) Brazil (SP) (36) Unavailable
Epanthidium maculatum Urban, 1995 Brazil (MG) (26), (28) Unavailable
Epanthidium nectarinioides (Schrottky, 1902) Brazil (PR, SC, SP) (11), (34), (36) Unavailable
Epanthidium tigrinum (Schrottky, 1905) Brazil (CE, MG, PB, PE, RN, SP) (15), (16), (19), (21), (22), (24), (26), (32), (36), (92), (94) Available (94)
Epanthidium spp. Brazil (BA, MG, SP) (12), (36), (39) -
Hypanthidium maranhense Urban, 1998 Brazil (MA, PE) (24), (27) Unavailable
Loyolanthidium sp. Mexico (QR) (49) Unavailable
Nananthidium gualanense (Cockerell, 1912) Costa Rica (50) Unavailable
Saranthidium marginatum Moure & Urban, 1994 Brazil (SP) (25) Unavailable
Saranthidium musciforme (Schrottky, 1902) Brazil (SP) (36), (92) Unavailable
Lithurgini
Microthurge corumbae (Cockerell, 1901) Brazil (SP) (95) Unavailable
Trichothurgus laticeps (Friese, 1906) Argentina (MZ) (96) Available (96)
Megachilini
Megachile (Acentron) sp. Argentina (BA) (41) Unavailable
Megachile (Austromegachile) facialis Vachal, 1909 Brazil (SP, MG) (15), (23), (29) Unavailable
Megachile (Austromegachile) fiebrigi Schrottky, 1908 Brazil (PR) (13), (34) Unavailable
Megachile (Austromegachile) orbiculata Mitchell, 1930 Brazil (AC, AM) (2), (3) Unavailable
Megachile (Austromegachile) sejuncta Cockerell, 1927 Brazil (MA) (74) Unavailable
Megachile (Austromegachile) susurrans Haliday, 1836 Brazil (PR) (13) Unavailable
Megachile (Austromegachile) trigonaspis Schrottky, 1913 Brazil (PR) (97) Unavailable
Megachile (Austromegachile) spp. Argentina (BA), Brazil (AC, CE, MG, PR) (3), (14), (18), (41), (97) -
Megachile (Callomegachile) rufipennis (Fabricius, 1793) Jamaica (1) Available (1)
Megachile (Chrysosarus) catamarcensis Schrottky, 1908 Argentina (LP) (41), (86), (98) Available (98)
Megachile (Chrysosarus) guaranitica Schrottky, 1908 Brazil (PR, SP) (13), (15), (36) Available (99)
Megachile (Chrysosarus) jenseni Friese, 1906 Argentina (BA) (41) Unavailable
Megachile (Chrysosarus) pseudanthidioides Moure, 1943 Brazil (SC) (100) Available (100)
Megachile (Chrysosarus) ruficornis Smith, 1853 Brazil (AC) (3) Unavailable
Megachile (Chrysosarus) spp. Argentina (BA), Brazil (AC, BA, CE, MG, PB, PE, PR, RN, SC, SP) (3), (11), (14), (21), (22), (24), (30), (37), (39), (41) -
Megachile (Dasymegachile) sp. Brazil (PR) (34) Unavailable
Megachile (Eutricharaea) concinna Smith, 1879 Argentina (BA), Jamaica (1), (101) Available (1), (101)
Megachile (Grafella) sp. Brazil (SC) (61) -
Megachile (Melanosarus) brasiliensis Dalla Torre, 1896 Brazil (PR) (34) Unavailable
Megachile (Melanosarus) nigripennis Spinola, 1841 Brazil (RJ) (102) Available (102)
Megachile (Melanosarus) spp. Brazil (MG, SC) (12), (61) -
Megachile (Moureapis) benigna Mitchell, 1930 Brazil (MG, RJ) (103), (104) Available (104), (105)
Megachile (Moureapis) maculata Smith, 1853 Brazil (MG, PR) (14), (97), (104), (106) Available (104), (106)
Megachile (Moureapis) pleuralis Vachal, 1909 Brazil (PR, SC) (11) Unavailable
Megachile (Moureapis) spp. Brazil (AC, CE, MG, PR) (3), (14), (19), (34), (97), (107) -
Megachile (Neochelynia) brethesi Schrottky, 1909 Brazil (MA, MG) (32), (74) Unavailable
Megachile (Neochelynia) paulista (Schrottky, 1920) Brazil (AC) (3) Unavailable
Megachile (Pseudocentron) curvipes Smith, 1853 Brazil (AC, MA, SP) (3), (15), (74) Unavailable
Megachile (Pseudocentron) gomphrenoides Vachal, 1909 Argentina (BA) (41), (108) Available (108)
Megachile (Pseudocentron) inscita Mitchell, 1930 Brazil (BA) (39) Unavailable
Megachile (Pseudocentron) nudiventris Smith, 1853 Brazil (SC) (61) Unavailable
Megachile (Pseudocentron) spp. Argentina (BA); Brazil (AC, MG, PE, RN, SP) (3), (21), (24), (25), (29), (32), (38), (41) -
Megachile (Pseudomegachile) lanata (Fabricius, 1775) Jamaica (1) Available (1)
Megachile (Ptilosarus) bertonii Schrottky, 1908 Brazil (MG) (29) Unavailable
Megachile (Ptilosarus) leucostomella Cockerell, 1927 Brazil (AC) (3) Unavailable
Megachile (Ptilosarus) spp. Brazil (AC, SP) (3), (30) -
Megachile (Ptilosaroides) neoxanthoptera Cockerell, 1933 Brazil (SP) (25), (36) Unavailable
Megachile (Rhyssomegachile) sp. Brazil (AM) (2) Unavailable
Megachile (Sayapis) cylindrica Friese, 1906 Brazil (MG, PB, PE) (24), (32) Available (24)
Megachile (Sayapis) mendozana Cockerell, 1907 Argentina (BA) (109) Available (109)
Megachile (Sayapis) planula Vachal, 1909 Brazil (SP) (15) Unavailable
Megachile (Sayapis) zaptlana Cresson, 1878 Jamaica, Mexico (QR) (1), (49) Available (1)
Megachile (Sayapis) spp. Brazil (CE, PB, RN) (19), (21), (22), (57) -
Megachile (Tylomegachile) orba Schrottky, 1913 Brazil (AC) (3) Unavailable
Megachile spp. Brazil (AM, BA, MA, MG, PR, SP); Costa Rica; Ecuador (2) (7), (12), (17), (25), (26), (36), (50), (59), (60), (74), (107) -
Osmiini
Heriades spp. Mexico (QR) (49) -

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Recibido: 29 de Agosto de 2018; Aprobado: 15 de Abril de 2019

2E-mail: ccfdacosta@gmail.com (corresponding author)

3E-mail: goncalvesrb@gmail.com

Edited by: Kelli dos Santos Ramos

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