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Revista Brasileira de Entomologia

Print version ISSN 0085-5626On-line version ISSN 1806-9665

Rev. Bras. entomol. vol.60 no.4 São Paulo Oct./Dec. 2016

http://dx.doi.org/10.1016/j.rbe.2016.06.001 

BIOLOGY, ECOLOGY AND DIVERSITY

Bees as hosts of mutillid wasps in the Neotropical region (Hymenoptera, Apidae, Mutillidae)

David R. Luz a   *  

George C. Waldren b  

Gabriel A.R. Melo a  

aUniversidade Federal do Paraná, Departamento de Zoologia, Curitiba, PR, Brazil

bUtah State University, Department of Biology, Logan, United States

ABSTRACT

A review of bee species used as hosts of mutillid wasps in the Neotropical region is presented. Three new confirmed host records are provided for the mutillid species Hoplomutilla biplagiata Mickel, 1939, Pappognatha limes Mickel, 1939, and Tallium aracati Casal, 1962. Two potential host records are provided for Euspinolia rufula Mickel, 1938 and Lophomutilla inca Fritz and Pagliano, 1993. Additionally, Mutilla hoplitiformis Strand, 1909, is transferred to the genus Darditilla. Correlations between host nesting habits and female mutillid morphology are discussed. Lastly, all known confirmed and potential host records in the Neotropical region are compiled.

Keywords: Apidae; Host records; Mutillidae; Parasitoids

Introduction

Mutillid wasps (Hymenoptera, Mutillidae), also known as velvet ants, comprise a diverse group of solitary aculeate wasps with over 4200 described species worldwide (Lelej and Brothers, 2008). They occur on all continents except Antarctica, and are most diverse in tropical regions (Brothers, 1975). In the Neotropical region, there are about 1400 described species in two subfamilies, Mutillinae and Sphaeropthalminae (Nonveiller, 1990). A remarkable feature of mutillids is their extreme sexual dimorphism, wherein females are always wingless and males are almost always fully winged and capable of flight.

Most mutillids are solitary parasitoids of solitary hosts (Brothers et al., 2000). The larvae are always ectoparasitoids of host stages which are enclosed in some sort of protective package (i.e. cell, cocoon, puparium, ootheca) and which are not actively feeding (Brothers, 1989). The known host spectrum includes several species of Diptera (e.g. Brothers, 1971 and Amini et al., 2014), Coleoptera (Péringuey, 1898 and Sergeev and Lelej, 2011), Lepidoptera (Seyrig, 1936), and Blattodea (Mickel, 1974), but velvet ants mainly parasitize other aculeate Hymenoptera, especially bees (the family Apidae sensuMelo and Gonçalves, 2005). Despite the size of the family, knowledge of mutillid biology is scanty. The hosts for only 2-3% of velvet ants are known (Brothers, 1989), and complete life history for only a few species has been recorded (e.g. Brothers, 1972 and Brothers, 1978).

Apidae is one of the most diverse families of Hymenoptera, with more than 17,000 bee species in seven subfamilies (Michener, 2007). They occur in virtually all terrestrial habitats and they play a key role in ecosystem function as major pollinators of flowering plants (Waser and Ollerton, 2006). The Neotropical fauna encompasses over 5000 described species (Moure et al., 2007) in five subfamilies: Andreninae, Apinae, Colletinae, Halictinae, and Megachilinae (Melo and Gonçalves, 2005).

The vast majority of bees are solitary ground-nesting or twig-nesting species that provision their larvae with a mixture of pollen and nectar (Michener, 2007). Because of their nesting habits and diversity, bees are known as a major host for mutillid wasps (Brothers, 1989).

Here we present a review of mutillid wasps and their host bees in the Neotropical region based on published records as well as some new findings. A compilation of host records is provided in Table 1.

Table 1 Known bee host records for mutillid wasps in the Neotropical region. 

Mutillidae Host bee Subfamily Parasitism References
Sphaeropthalminae
Anomophotopsis
A. quinteroi Cambra, 2006 Paroxystoglossa transversa Moure, 1943 Halictinae Confirmed Rocha-Filho and Melo (2011: 2825)
Atillum
A. albicomum Mickel, 1943 Caupolicana sp. Colletinae Potential Fritz (1998: 445)
A. charoneum Mickel, 1943 Caupolicana sp. Colletinae Potential Fritz (1998: 445)
A. sumptuosum (Gerstaecker, 1874)1 ? Apinae? Potential Lynch Arribálzaga (1878: 178)2
A. venatrix Mickel, 1943 Caupolicana sp. Colletinae Potential Fritz (1998: 445)
Calomutilla
C. temporalis (Gerstaecker, 1874)3 Pseudaugochlora graminea (Fabricius, 1804) Halictinae Confirmed Ihering (1904: 466)4
Darditilla
D. hoplitiformis (Strand, 1909) comb. nov.5 Ptilothrix plumata Smith, 1853 Apinae Potential Friese (1908: 51)6, Strand (1909: 233)
Dasymutilla
D. aequatorialis (André, 1906)7 Melitoma sp. Apinae Confirmed André (1906: 167)8
D. araneoides (Smith, 1862) Centris (Centris) flavofasciata Friese, 1899 Apinae Potential Vinson et al. (1987: 260)
D. blattoserica (Kohl, 1882) Melitoma sp. Apinae Confirmed Manley and Pitts (2007: 32)
D. canina (Smith, 1855) Melitoma marginella (Cresson, 1872) Apinae Confirmed Linsley et al. (1980: 22)
D. jaliscoManley, 2003 Diadasia knabiana Cockerell, 1917 Apinae Confirmed Manley (2003: 682)
D. mirabilisManley and Pitts, 2007 Centris sp. Apinae Confirmed Manley and Pitts (2007: 69)
Dasymutilla sp. Centris (Centris) aethiocesta Snelling, 1984 Apinae Confirmed Vinson et al. (1987: 260)9
Dasymutilla sp. Centris (Centris) flavofasciata Friese, 1899 Apinae Potential Vinson et al. (1987: 260)
Dimorphomutilla
D. formosaMickel, 193810 Corynura (Corynura) chilensis (Spinola, 1851) Halictinae Potential Janvier (1933)11
D. lunulata (Spinola, 1851)12 Alloscirtetica tristrigata (Spinola, 1851) Apinae Potential Janvier (1933)13
Euspinolia
E. albicomaMickel, 1938 Anthophora (Mystacanthophora) incerta Spinola, 1851 Apinae Confirmed Mickel (1938: 66)14
E. rufulaMickel, 1938 Melitoma sp. Apinae Potential This study
Hoplocrates
H. specularis (Gerstaecker, 1874) Monoeca haemorrhoidalis (Smith, 1854) Apinae Potential Rocha-Filho and Melo (2011: 2825)
Hoplognathoca
H. costarricensis Suárez, 1962 Thygater sp. Apinae Potential Roubik (1989: 235)
Hoplomutilla
H. biplagiata Mickel, 1939 Centris (Paracentris) burgdorfi Friese, 1900 Apinae Confirmed This study
H. conspecta Mickel, 1939 Eulaema (Eulaema) meriana (Olivier, 1789) Apinae Potential Cameron and Ramírez (2001: 154)
H. myops myops (Burmeister, 1854) Epicharis (Xanthepicharis) bicolor Smith, 1854 Apinae Potential Rocha-Filho et al. (2008: 237)
H. opima Mickel, 1939 Centris (Melacentris) rufosuffusa Cockerell, 1935 Apinae Confirmed Callan (1977: 131)
H. spinosa (Swederus, 1787) Eulaema (Apeulaema) nigrita Lepeletier, 1841 Apinae Confirmed Quintero and Cambra (2001: 300)
H. triumphans Mickel, 1939 Eufriesea sp. Apinae Confirmed Lenko (1964: 200)15
H. xanthocerata (Smith, 1862) Eulaema (Eulaema) meriana (Olivier, 1789) Apinae Confirmed Roubik (1990: 151)
Hoplomutilla sp. Centris (Ptilotopus) derasa Lepeletier, 1841 Apinae Potential Vesey-Fitzgerald (1939: 109)
Hoplomutilla? sp. Eulaema (Eulaema) terminata Smith, 1874 Apinae Potential Bennett (1972: 120), Yanega (1994: 465)
Lophomutilla
L. corupa Casal, 1968 Dialictus seabrai (Moure, 1956) Halictinae Potential Bergamaschi et al. (2010: 2604)
L. halicta (Mickel, 1973) Augochlorella comis (Vachal, 1911)16 Halictinae Confirmed Eickwort and Eickwort (1973: 13), Mickel (1973: 3)
L. inca Fritz and Pagliano, 1993 Neocorynura sp. Halictinae Potential This study
Lophomutilla sp. Neocorynura muiscae Smith-Pardo and Gonzalez, 2006 Halictinae Potential Gonzalez and Engel (2004: 68), V.H. Gonzalez, pers. comm.
Lophostigma
L. cincta (du Buysson, 1892) Megalopta genalis Meade-Waldo, 1916 Halictinae Confirmed Cambra et al. (2005: 232)
L. cincta (du Buysson, 1892) Megalopta amoena (Spinola, 1853) Halictinae Confirmed Cambra et al. (2005: 232)17
Lynchiatilla
L. parana Cambra, 2012 Paroxystoglossa spiloptera Moure, 1960 Halictinae Potential Bergamaschi et al. (2012: 63)
Pappognatha
P. limes Mickel, 1939 Euglossa (Glossura) ignita Smith, 1874 Apinae Confirmed This study
P. myrmiciformis (Cameron, 1897) Euglossa (Glossurella) dodsoni Moure, 1965 Apinae Confirmed Dodson (1966: 619), Yanega (1994: 465)
P. panamensisQuintero and Cambra, 2005 Euglossa (Euglossa) hemichlora Cockerell, 1917 Apinae Confirmed Cambra et al. (2015: 6)
P. panamensisQuintero and Cambra, 2005 Euglossa (Glossura) imperialis Cockerell, 1922 Apinae Confirmed Cambra et al. (2015: 6)
P. patruelis (André, 1898) Euglossa sp. Apinae Confirmed Quintero and Cambra (2005: 196), this study
P. speciosa Mickel, 1939 Euglossa (Glossuropoda) intersecta Latreille, 1817 Apinae Confirmed Dodson (1966: 625)18, Yanega (1994: 465)
Pseudomethoca
P. hesperusBrothers, 1982 Halictus (Pachyceble) hesperus Smith, 1862 Halictinae Potential Brothers (1982: 209), Brooks and Roubik (1983: 278)
P. pumila (Burmeister, 1854) Dialictus seabrai (Moure, 1956) Halictinae Potential Bergamaschi et al. (2011: 59)
P. ravula (Cameron, 1894) Xenoglossa fulva Smith, 1854 Apinae Potential Linsley et al. (1955: 137)
P. spixi (Diller, 1989)19 Monoeca haemorrhoidalis (Smith, 1854) Apinae Potential Rocha-Filho and Melo (2011: 2825)
P. spixi (Diller, 1989)20 Monoeca xanthopyga Harter-Marques, Cunha and Moure, 2001 Apinae Confirmed Cunha and Blochtein, 2003 and Cunha, 2004
P. willeiMickel, 1969 Dialictus umbripennis (Ellis, 1913) Halictinae Confirmed Mickel (1969: 526), Wille and Orozco (1970: 215)21
P. willeiMickel, 1969 Halictus (Pachyceble) hesperus Smith, 1862 Halictinae Potential Brothers (1982: 211)22, Brooks and Roubik (1983: 278)
Pseudomethoca sp. Dialictus figueresi (Wcislo, 1990) Halictinae Confirmed Cambra (1997: 123)23
Pseudomethoca sp. Augochlora (Oxystoglossella) nominata Michener, 1954 Halictinae Potential Brothers et al. (2000: 210)
Pseudomethoca sp.24 Augochloropsis iris (Schrottky, 1902) Halictinae Confirmed Coelho (2002: 185)
Reedomutilla
R. heraldica (Saussure, 1867)25 Melissoptila dama (Vachal, 1904) Apinae Potential Jörgensen (1912b: 274)26
Sphaeropthalma
S. (Photopsis) gayi Mickel, 193727 Neofidelia profuga Moure and Michener, 1955 Megachilinae Confirmed Rozen (1973: 10)
S. (Photopsis) jacala Schuster, 1958 Centris (Hemisiella) nitida Smith, 1874 Apinae Confirmed Pitts and Parker (2005: 62)
Tallium
T. aracati Casal, 1962 Centris (Paracentris) burgdorfi Friese, 1900 Apinae Confirmed This study
Traumatomutilla
Traumatomutilla sp. Diadasina distincta (Holmberg, 1903)28 Apinae Confirmed Jörgensen (1912a: 158)
Mutillinae
Timulla
T. intermissaMickel, 1938 Exomalopsis (Exomalopsis) fulvofasciata Smith, 1879 Apinae Potential Aranda and Graciolli (2013: 2)
T. terminalis (Gerstaecker, 1874) Exomalopsis (Exomalopsis) fulvofasciata Smith, 1879 Apinae Potential Aranda and Graciolli (2013: 2)

Unidentified genera
Mutillidae sp. Alepidosceles filitarsis (Vachal, 1904)29 Apinae Confirmed Jörgensen (1909: 64)
Mutillidae sp. Alloscirtetica tristrigata (Spinola, 1851)30 Apinae Potential Ruiz (1940: 309)
Mutillidae sp. Chalepogenus caeruleus (Friese, 1906)31 Apinae Confirmed Janvier (1926: 240)
Mutillidae sp. Exomalopsis sp. Apinae Potential Ruiz (1940: 322)
Mutillidae sp. Augochlora (Oxystoglossella) morrae Strand, 1910 Halictinae Confimed Michener and Lange (1958: 491)

1Cited as Mutilla sumptuosa.

2Eucera sp.

3Ephuta temperalis [sic].

4Augochlora gramminea [sic].

5Mutilla hoplitiformis.

6Mutilla sp.

7Ephuta aequatorialis.

8Entechnia taurea.

9Centris aethectera [sic].

10Neomotilla attenuata [corrected by Quintero and Cambra, 2001].

11Halictus chloris.

12Mutilla lunulata.

13Tetralonia tristrigata.

14Podalirius incertus.

15Euplusia sp.

16Augochlorella edentata [ Eickwort and Eickwort (1973) reared the mutillid and Mickel (1973) described as Paramutilla halicta].

17Megalopta ecuadoria.

18Euglossa brullei.

19Pseudomethoca melanocephala.

20Traumatomutilla sp. [a misidentification, corrected by Bartholomay et al. (2015a)].

21Lasioglossum (Dialictus) umbripenne.

22Pseudomethoca transversa.

23Lasioglossum (Dialictus) figueresi.

24Sphinctopsis sp.

25Reedia Claraziana [sic].

26Epimelissodes dama.

27Photopsis gayi.

28Ancyloscelis distinca.

29Ancyloscelis nigriceps Friese, 1906.

30Tetralonia tristrigata.

31Exomalopsis caerulea.

Material and methods

Data on host associations were compiled from literature records and, in a few cases, from specimens deposited in the entomological collections of the Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, Paraná, Brazil (DZUP) and Utah State University, Logan, Utah, USA (EMUS). The names of the mutillids and the bees were updated according to Nonveiller (1990) and Moure et al. (2007), respectively.

Parasitism was classified into two categories: (A) confirmed, when the mutillid was reared from host bee cells; and (B) potential, when the mutillid was observed entering or attempting to enter the bee nest, or found within the bee nest, or walking on nest entrances and surroundings, or when potential host cells found inside the bee nest contained mutillid cocoons or empty brownish papery cocoons, presumed to belong to mutillids. We do not consider as a valid potential host record some cases in literature in which a mutillid was only observed in the vicinity of nesting sites of bees.

Results

A summary of all potential and confirmed known records of bees as hosts of mutillid wasps in the Neotropical region is presented in Table 1. Data on confirmed parasitism are available for 29 species in 12 genera, only in the subfamily Sphaeropthalminae, and involve a total of 34 cases of parasitism of bees, including three cases where the mutillids were not identified (Table 1). Their host bees belong to the subfamilies Apinae (24 cases), Halictinae (nine cases) and Megachilinae (one case). The mutillid genera with the most records as a parasitoid are Dasymutilla Ashmead, with six species, Hoplomutilla Ashmead and Pappognatha Mickel, both with five species, and Pseudomethoca Ashmead, with four species. Orchid bees (Apinae, Euglossini) are the group of bees with the most records as hosts of mutillid wasps, with nine cases. Further, Euglossa Latreille is the genus of bees with the most records as hosts of Mutillidae, with six cases (see Table 1).

Three new confirmed host records, as well as two potential host records, are presented here, with voucher specimens deposited at DZUP and EMUS collections. Hoplomutilla biplagiata Mickel, 1939 and Tallium aracati Casal, 1962 emerged from the nests of Centris (Paracentris) burgdorfi Friese, 1900 (bee specimens are deposited in the Museu de Zoologia da Universidade de São Paulo (MZSP) collection and in DZUP) in Natal, Rio Grande do Norte, Brazil (DZUP), and the third record was made based on a specimen of Pappognatha limes Mickel, 1939 bearing a label on the pin indicating that Euglossa (Glossura) ignita Smith, 1874 was its host in Iquitos, Peru (DZUP). Additionally, a potential host record is based on a pinned female specimen of Lophomutilla inca Fritz and Pagliano, 1993, which bears a label noting that it was taken from a nest of Neocorynura sp. in Tunja, Colombia (EMUS). Lastly, an additional potential host record is based on two pinned female specimens of Euspinolia rufula Mickel, 1938 collected near Sayán, Peru (EMUS); one specimen bears a label stating, "dead in nests of Melitoma", while the second specimen bears a label stating, "in nest of Melitoma".

Strand (1909) described Mutilla hoplitiformis from San Bernardino, Paraguay based on a single female that was found inside the nest of the bee Ptilothrix plumata Smith, 1853 (here considered as a potential host). This species has not been treated since its description ( Strand, 1909) and was still in the genus Mutilla Linnaeus until this paper ( Nonveiller, 1990). The type of M. hoplitiformis is deposited in the Museum für Naturkunde, Berlin, Germany (ZMB), and was examined by DRL. Based on its granulate pygidium (see Luz and Williams, 2014), it is clear that this species belong to the genus Darditilla Casal. Therefore, it is hereby transferred to Darditilla, in the new combination Darditilla hoplitiformis ( Strand, 1909) comb. nov.

Discussion

Based on the available data, Apidae appear to be the primary hosts for mutillid wasps in the Neotropical region. Nevertheless, there are several cases of other hymenopterans as confirmed hosts of Mutillidae in the neotropics, such as apoid wasps of the families Crabronidae (e.g. Quintero and Cambra, 2001 and Bartholomay et al., 2015b) and Sphecidae (e.g. Morato, 1994 and Fritz, 1998), and spider wasps of the family Pompilidae (e.g. Zanette et al., 2004).

In the Neotropical region, the cases of confirmed parasitism of bees by mutillid wasps occur only in the subfamily Sphaeropthalminae. The other subfamily of Mutillidae present in the neotropics, Mutillinae, has been implicated only as a potential parasite of one bee species (Aranda and Graciolli, 2013; see Table 1). Otherwise, it is known to parasitize members of the families Crabronidae (e.g. Callan, 1942 and Quintero and Cambra, 1996b) and Pompilidae (e.g. Zanette et al., 2004 and Loyola and Martins, 2006).

The degree of host specificity remains poorly known in Mutillidae. Some species seem to be more situation-specific rather than host-specific, and this could be a general characteristic of the entire family (Brothers, 1989). Despite this situation, Krombein (1972), Quintero and Cambra (1996a), and Williams et al. (2011) have revealed a link between female morphology and host preference in Mutillidae. According to Quintero and Cambra (1996a, referencing Naumann, 1991), species with a well-defined pygidial plate bound by lateral carinae in the female typically parasitize ground-nesting hosts, while females with an undefined pygidium parasitize arboreal or twig-nesting hosts. A well-developed pygidial plate is also found in females of bee species nesting in the ground, while those nesting in other substrates have a vestigial plate or lack it entirely (Michener, 2007). Bees use the pygidial plate to smooth out the walls of their underground brood cells and to pack soil when closing the lateral tunnels (Batra, 1984). Brothers (1972) noted that females of the mutillid Pseudomethoca frigida (Smith, 1855), after ovipositing on an immature ground-nesting sweat bee, Dialictus zephyrus (Smith, 1853), used their [defined] pygidium to tamp down soil particles used to seal the host cell.

Additionally, according to Krombein (1972) and Williams et al. (2011), mutillid species that parasitize ground-nesting hosts usually have a well-developed foretarsal rake on the external margin of the foretarsus, and the mid- and hindtarsi have apical spines on the outer margin that are longer than the spines on the inner margin. Conversely, mutillid species that parasitize arboreal or twig-nesting hosts lack a foretarsal rake, and the apical spines on the inner and outer margins of the mid- and hindtarsi are similar in length. Unlike bees, which do not have well-developed tarsal rakes, mutillid females probably behave like other aculeate wasps that build underground nests and use their tarsal rakes to push the soil backwards under the body when excavating the ground in search of host brood cells to parasitize.

Although the available host information is sparse, there seems to be a non-random association between some genera of Mutillidae and some genera of Apidae that they parasitize; further, female mutillid morphology and nesting habits of the host appear to be correlated. We discuss some known cases below.

Dasymutilla Ashmead is a genus of mutillid wasps with over 200 described species that are distributed throughout North America, Central America, and northern South America ( Pilgrim et al., 2009). Females of this genus have a well-defined pygidial plate and foretarsal rake, and six different species are known to parasitize ground-nesting bees of the subfamily Apinae in the neotropics (see Table 1). This evidence corroborates the assertions made by Krombein (1972), Quintero and Cambra (1996a), and Williams et al. (2011). In addition to parasitizing ground-nesting Centris bees, four species of Dasymutilla are known to parasitize Emphorini bees of the genera Melitoma Lepeletier and Serville and Diadasia Patton in the neotropics. Nests of emphorine bees are shallow and often built in aggregations in banks or in flat ground; the nest entrances are frequently surrounded by mud turrets ( Michener, 2007). Species of Dasymutilla are known to parasitize numerous ground-nesting bee genera in the Nearctic region, including species of Melitoma and Diadasia ( Bartholomay et al., 2015a).

Hoplomutilla Ashmead is a Neotropical genus with more than 90 described species ( Mickel, 1939a and Schuster, 1951) that includes some of the largest species of mutillid wasps in the neotropics. Females usually have a well-defined pygidium and are known to parasitize large apine oil-collecting bees of the tribes Centridini (Centris Fabricius) and Epicharitini (Epicharis Klug), as well as large orchid bees (the genera Eufriesea Cockerell and Eulaema Lepeletier in the tribe Euglossini). Most species of Centridini and all Epicharitini bees build underground nests in banks or in flat ground ( Michener, 2007), while orchid bees of the genera Eufriesea and Eulaema construct their nests in cavities in banks, tree trunks, logs, etc. ( Dressler, 1982 and Michener, 2007). Surprisingly, female morphology (i.e. form of foretarsus and pygidium, outlined above) is indicative of host preference for only some members of Hoplomutilla, such as H. biplagiata Mickel, 1939 parasitizing the ground-nesting Centris (Paracentris) burgdorfi Friese, 1900 (this study) and H. xanthocerata (Smith, 1862) parasitizing Eulaema (Eulaema) meriana (Olivier, 1789) in a rotten log 1.5 m above the ground (Roubik, 1990). Mutillid females in the former case have well developed pygidium and foretarsal rake, while in the latter case the females have an undefined pygidium and lack a foretarsal rake, a pattern consistent with the nesting habits of their bee hosts. On the other hand, there are two unusual records, one confirmed and one potential, involving Hoplomutilla species with a foretarsal rake and defined pygidium parasitizing the orchid bee genera Eufriesea and Eulaema, which nest above-ground ( Cameron and Ramírez, 2001 and Quintero and Cambra, 2001; see Table 1). These latter records are noteworthy considering the otherwise consistent relationship between morphology and host choice for the other records reviewed in this study.

The most remarkable and specific case of association between mutillid wasps and bees appears to occur between the genera Pappognatha Mickel and orchid bees of the genus Euglossa Latreille. Pappognatha is a Neotropical mutillid genus with 15 described species ( Quintero and Cambra, 2005) that possess a unique characteristic for the New World mutillids, wherein both sexes have the mandibles clothed with dense, short setae (Mickel, 1939b). Females have an undefined pygidium and do not possess a foretarsal rake. In addition to these morphological traits, Pappognatha is the only known mutillid genus that has an arboreal habit as a general characteristic ( Yanega, 1994). Their unique confirmed hosts are orchid bees of the genus Euglossa, with six reported cases, including the new one presented here. Many species of Euglossa build aerial resin nests ( Dressler, 1982 and Michener, 2007), which suggests host-specificity for Pappognatha species. On the other hand, species of Pappognatha are also able to parasitize non-aerial nests of Euglossa built in cavities close to the ground surface, as observed for P. patruelis by GARM (unpubl. obs.; reported by Quintero and Cambra (2005) from specimen label data). A female of P. patruelis was found inside a nest of an unidentified species of Euglossa built in a small cavity of a rotten log lying in the ground of a forest site in Minas Gerais, Brazil. The mutillid female was inside the cavity with her head near the entrance orifice in the resin wall made by the Euglossa female. The female and the brood cells were collected, but no adults emerged from the nest in the following weeks. Upon dissection of the nest, two dead mutillid imagoes (one female and one male) were found within their respective cells, as well as additional dead mutillid pupae. No immatures of the host bee were present, indicating that all cells had been successfully parasitized by the Pappognatha female. Based on this single observation, the behavior of the female Pappognatha suggested that she was guarding the parasitized host nest. Regarding the peculiar mandibles of Pappognatha, their dense cover of pubescence might be an adaptation to prevent resin from sticking to them as they chew through the host cell walls.

According to Brothers (1989), fewer than 4% of mutillid species have any biological traits studied. More than 25 years since Brothers' observation, most aspects of the biology of Mutillidae remain unclear and have been little studied. Detailed studies on host-parasitoid relations and behavior of mutillid wasps are still lacking and virtually missing worldwide.

Acknowledgments

We thank William Sabino (Universidade de São Paulo) for kindly donating the specimens from Natal, RN, Brazil to the DZUP collection; and V.H. Gonzalez for providing unpublished information on host records. DRL also want to thank Frank Koch and Michael Ohl for their hospitality during his stay at the Museum für Naturkunde (Berlin, Germany). DRL and GARM thank CNPq for financial support.

References

Amini, A., Lelej, A.S., Sadeghi, H., Karimi, J., 2014. First record of the velvet ants (Hymenoptera: Mutillidae) reared from puparia of the ber fruit fly Carpomya vesuviana Costa (Diptera: Tephritidae) in Iran. Zootaxa 3861, 585-590. [ Links ]

André, E., 1906. Nouvelles espèces de Mutillides d'Amérique (Hym.). Z. Hymen. Dipt. 6, 33-48, 65-80, 161-169. [ Links ]

Aranda, R., Graciolli, G., 2013. First report of Exomalopsis fulvofasciata (Hymenoptera: Anthophoridae) as host of two Timulla species (Hymenoptera: Mutillidae). Biota Neotrop. 13, 382-384. [ Links ]

Bartholomay, P.R., Williams, K.A., Waldren, G.C., de Oliveira, M.L., 2015a. Correc- tions on the biology of Traumatomutilla André, 1901 (Hymenoptera: Mutillidae). Zootaxa 3920, 198-200. [ Links ]

Bartholomay, P.R., Williams, K.A., Luz, D.R., Morato, E.F., 2015b. Frigitilla gen. nov., a new genus of Amazonian Mutillidae (Hymenoptera). Zootaxa 3957, 49-58. [ Links ]

Batra, S.W.T., 1984. Solitary bees. Sci. Am. 250, 120-127. [ Links ]

Bennett, F.D., 1972. Observations on Exaerete spp. and their hosts Eulaema termi- nata and Euplusia surinamensis (Hymen., Apidae, Euglossinae) in Trinidad. J. N. Y. Entomol. Soc. 80, 118-124. [ Links ]

Bergamaschi, A.C.B., Cambra, R., Melo, G.A.R., 2010. Male description and host record for Lophomutilla corupa Casal, 1968 (Hymenoptera: Mutillidae), with behavioural notes on mating behaviour and host nest attacks. J. Nat. Hist. 44, 2597-2607. [ Links ]

Bergamaschi, A.C.B., Cambra, R.A., Melo, G.A.R., 2011. New combinations, sex asso- ciation, behavioural notes and potential host record for two Neotropical species of Pseudomethoca Ashmead, 1896 (Hymenoptera: Mutillidae). Zootaxa 3062, 55-63. [ Links ]

Bergamaschi, A.C.B., Cambra, R.A., Brothers, D.J., Melo, G.A.R., 2012. Lynchiatilla Casal, 1963 (Hymenoptera: Mutillidae): a new species from Brazil associated with Paroxystoglossa spiloptera Moure (Hymenoptera: Apidae: Halictinae), and notes on other species. Zootaxa 3548, 55-64. [ Links ]

Brooks, R.W., Roubik, D.W., 1983. A halictine bee with distinct castes: Halictus hespe- rus (Hymenoptera, Halictidae) and its bionomics in central Panama. Sociobiology 7, 263-282. [ Links ]

Brothers, D.J., 1971. The genera of Mutillidae (Hymenoptera) parasitic of tsetse flies (Glossina, Diptera). J. Entomol. Soc. S. Afr. 34, 101-102. [ Links ]

Brothers, D.J., 1972. Biology and immature stages of Pseudomethoca f. frigida, with notes on other species (Hymenoptera: Mutillidae). Univ. Kans. Sci. Bull. 50, 1-38. [ Links ]

Brothers, D.J., 1975. Phylogeny and classification of the aculeate Hymenoptera, with special reference to Mutillidae. Univ. Kans. Sci. Bull. 50, 483-648. [ Links ]

Brothers, D.J., 1978. Biology and immature stages of Myrmosula parvula (Hymenoptera: Mutillidae). J. Kans. Entomol. Soc. 51, 698-710. [ Links ]

Brothers, D.J., 1982. Two new species of Mutillidae associated with Halictus hesperus (Halictidae) in Panama (Hymenoptera). Sociobiology 7, 205-212. [ Links ]

Brothers, D.J., 1989. Alternative life -history styles of mutillid wasps (Insecta, Hymenoptera). In: Bruton, M.N. (Ed.), Alternative Life -History Styles of Animals. Kluwer Academic Publishers, Dordrecht, Netherlands, pp. 279-291. [ Links ]

Brothers, D.J., Tschuch, G., Burger, F., 2000. Associations of mutillid wasps (Hymenoptera, Mutillidae) with eusocial insects. Insectes Soc. 47, 201-211. [ Links ]

Callan, E.M., 1942. A note on Timulla (Timulla) eriphyla Mickel (Hym., Mutillidae), a parasite of Tachysphex blatticidus F.X. Williams (Hym., Larridae), from Trinidad, B.W.I. Proc. R. Entomol. Soc. Lond. Ser. A Gen. Entomol. 17, 18. [ Links ]

Callan, E.M., 1977. Observations on Centris rufosuffusa Cockerell (Hymenoptera: Anthophoridae) and its parasites. J. Nat. Hist. 11, 127-135. [ Links ]

Cambra, R.A., 1997. Comparacion de la diversidad en la Sphaeropthalminae (Hymenoptera: Mutillidae) de Costa Rica y Panamá, con notas sobre biología. Scientia 12, 115-128. [ Links ]

Cambra, R.A., Gonzalez, V.H., Wcislo, W.T., 2005. Description of the male, host associations, and new distribution records for Lophostigma cincta (du Buysson) (Hymenoptera: Mutillidae). Proc. Entomol. Soc. Wash. 107, 229-234. [ Links ]

Cambra, R.A., Roubik, D.W., Quintero, D.A., 2015. Hospederos de Pappognatha pana- mensis Quintero & Cambra, 2005 (Hymenoptera: Mutillidae) y su primer registro de distribuición para Costa Rica. Bol. Mus. Entomol. Univ. Valle 16, 5-7. [ Links ]

Cameron, S.A., Ramírez, S., 2001. Nest architecture and nesting ecology of orchid bee Eulaema meriana (Hymenoptera: Apidae: Euglossini). J. Kans. Entomol. Soc. 74, 142-165. [ Links ]

Coelho, B.W.T., 2002. The biology of the primitively eusocial Augochloropsis iris (Schrottky, 1902) (Hymenoptera, Halictidae). Insectes Soc. 49, 181-190. [ Links ]

Cunha, R., 2004. Monoeca xanthopyga (Hymenoptera, Apoidea, Tapinotaspidini), primeiro registro de hospedeiro para parasitóide do gênero Traumatomutilla (Hymenoptera: Mutillidae) na Serra Geral do Rio Grande do Sul. Acta Sci. 6, 35-40. [ Links ]

Cunha, R., Blochtein, B., 2003. Bionomia de Monoeca xanthopyga Harter-Marques, Cunha & Moure (Hymenoptera, Apidae, Tapinotaspidini) no Planalto das Araucárias, Rio Grande do Sul, Brasil. Rev. Bras. Zool. 20, 107-113. [ Links ]

Dodson, C.H., 1966. Ethology of some bees of the tribe Euglossini (Hymenoptera: Apidae). J. Kans. Entomol. Soc. 39, 607-629. [ Links ]

Dressler, R.L., 1982. Biology of the orchid bees (Euglossini). Annu. Rev. Ecol. Syst. 13, 373-394. [ Links ]

Eickwort, G.C., Eickwort, K.R., 1973. Aspects of the biology of Costa Rican halictine bees, V. Augochlorella edentata (Hymenoptera: Halictidae). J. Kans. Entomol. Soc. 46, 3-16. [ Links ]

Friese, H., 1908. Die Apidae (Blumenwespen) von Argentina nach den Reisenergeb- nissen der Herren A. C. Jensen-Haarup und P. Jörgensen in den Jahren 1904-1907. Flora og Fauna, Silkeborg. [ Links ]

Fritz, M.A., 1998. Mutillidae. In: Morrone, J.J., Coscarón, S. (Eds.), Biodiversidad de artrópodos argentinos, una perspectiva biotaxonómica. Ediciones Sur, La Plata, Argentina, pp. 445-451. [ Links ]

Gonzalez, V.H., Engel, M.S., 2004. The tropical Andean bee fauna (Insecta: Hymenoptera: Apoidea), with examples from Colombia. Entomol. Abh 62, 65-75. [ Links ]

Ihering, R., 1904. Biologia das abelhas solitarias do Brazil. Rev. Mus. Paul. 6, 461-481. [ Links ]

Janvier, H., 1926. Recherches biologiques sur les Hyménoptères du Chili (Mellifères). Ann. Sci. Nat. Zool. Biol. Anim. (Ser. 10) 9, 113-268. [ Links ]

Janvier, H., 1933. Étude biologique de quelques hyménoptères du Chili. Ann. Sci. Nat. Zool. Biol. Anim. (Ser. 10) 16, 209-356. [ Links ]

Jörgensen, P., 1909. Beobachtungen über blumenbesuch, biologie, verbreitung usw. der bienen von Mendoza. (Hym.). Teil I. Dtsch. entomol. Z.1909. Heft 1, 53-65. [ Links ]

Jörgensen, P., 1912a. Revision der Apiden der Provinz Mendoza, Republica Argentina (Hym.). Zool. Jahrb. Abt. Sys. Geogr. Biol. Tiere 32, 89-162, 643-644. [ Links ]

Jörgensen, P., 1912b. Los crisídidos y los himenópteros aculeatos de la Provincia de Mendoza. An. Mus. Nac. Hist. Nat. Buenos Aires 22, 267-338. [ Links ]

Krombein, K.V., 1972. Monograph of the Madagascan Mutillidae (Hymenoptera). Part I: Myrmillini, Mutillini and Smicromyrmini. Ann. Mus. R. Afr. Cent. Sér. Octavo Sci. Zool. 199, 1-61. [ Links ]

Lelej, A.S., Brothers, D.J., 2008. The genus-group names of Mutillidae (Hymenoptera) and their type species, with a new genus, new name, new synonymies, new combinations and lectotypifications. Zootaxa 1889, 1-79. [ Links ]

Lenko, K., 1964. Hoplomutilla triumphans Mickel, 1939 (Hymenoptera, Mutillidae) como parasito de abelhas do gênero Euplusia (Hymenoptera, Apoidea). Pap. Avulsos Dep. Zool. Sec. Agric. 16, 199-205. [ Links ]

Linsley, E.G., MacSwain, J.W., Smith, R.F., 1955. Biological observations on Xenoglossa fulva Smith with some generalizations on biological characters of other eucerine bees. Bull. South. Calif. Acad. Sci. 54, 128-141. [ Links ]

Linsley, E.G., MacSwain, J.W., Michener, C.D., 1980. Nesting biology and associates of Melitoma (Hymenoptera, Anthophoridae). Univ. Calif. Publ. Entomol. 90, 1-45. [ Links ]

Loyola, R.D., Martins, R.P., 2006. Trap-nest occupation by solitary wasps and bees (Hymenoptera: Aculeata) in a forest urban remanent. Neotrop. Entomol. 35, 41-48. [ Links ]

Luz, D.R., Williams, K.A., 2014. The first sexual associations in the genus Darditilla Casal, 1965 (Hymenoptera, Mutillidae). Zookeys 454, 41-68. [ Links ]

Lynch Arribálzaga, F., 1878. Ensayo sobre los Mutílidos del Partido del Baradero (Provincia de Buenos Aires). El Naturalista Argentino. Rev. Hist. Nat. 1, 129-136, 172-187, 201-214. [ Links ]

Manley, D.G., 2003. Dasymutilla jalisco, a new species of velvet ant (Hymenoptera: Mutillidae) plus synonymy for Dasymutilla canina (Smith). Proc. Entomol. Soc. Wash. 105, 679-684. [ Links ]

Manley, D.G., Pitts, J.P., 2007. Tropical and subtropical velvet ants of the genus Dasymutilla Ashmead (Hymenoptera: Mutillidae) with descriptions of 45 new species. Zootaxa 1487, 1-128. [ Links ]

Melo, G.A.R., Gonçalves, R.B., 2005. Higher -level bee classifications (Hymenoptera, Apoidea, Apidae sensu lato). Rev. Bras. Zool. 22, 153-159. [ Links ]

Michener, C.D., 2007. The Bees of the World, 2nd ed. The Johns Hopkins University Press, Baltimore. [ Links ]

Michener, C.D., Lange, R.B., 1958. Observations on the behavior of Brasilian halictid bees, III. Univ. Kans. Sci. Bull. 39, 473-505. [ Links ]

Mickel, C.E., 1938. A synopsis of the neotropical mutillid genus Euspinolia Ashmead (Hym.). Rev. Entomol. Rio J. 9, 53-74. [ Links ]

Mickel, C.E., 1939a. A monograph of the Neotropical mutillid genus Hoplomu- tilla Ashmead (Hymenoptera: Mutillidae). Rev. Entomol. Rio J. 10 (337-403), 641-717. [ Links ]

Mickel, C.E., 1939b. Monograph of a new neotropical mutillid genus, Pappognatha (Hymenoptera: Mutillidae). Ann. Entomol. Soc. Am. 32, 329-343. [ Links ]

Mickel, C.E., 1969. Pseudomethoca willei n. sp. reared from cells of the bee Lasioglos- sum (Dialictus) umbripenne (Ellis) (Hymenoptera: Mutillidae; Apoidea). J. Kans. Entomol. Soc. 42, 524-526. [ Links ]

Mickel, C.E., 1973. Paramutilla halicta n. genus, n. species, a parasite of the halictine bee Augochlorella edentata (Hymenoptera: Mutillidae). J. Kans. Entomol. Soc. 46, 1-3. [ Links ]

Mickel, C.E., 1974. Mutillidae miscellanea: taxonomy and distribution. Ann. Entomol. Soc. Am. 67, 461-471. [ Links ]

Morato, E.F., 1994. Xystromutilla asperiventris André, 1905 (Mutillidae) reared from sphecid wasps in trap-nests, Manaus, Amazonas, Brazil. Sphecos 28, 13-14. [ Links ]

Moure, J.S., Urban, D., Melo, G.A.R., 2007. Catalogue of Bees (Hymenoptera, Apoidea) in the Neotropical Region. Sociedade Brasileira de Entomologia, Curitiba. [ Links ]

Naumann, I.D., 1991. Hymenoptera (wasps, bees, ants, sawflies). In: Naumann, I.D., et al. (Eds.), The Insects of Australia, vol. 2. Cornell University Press, Ithaca, pp. 916-1000. [ Links ]

Nonveiller, G., 1990. Catalogue of the Mutillidae, Myrmosidae and Bradynobaenidae of the Neotropical Region including Mexico (Insecta, Hymenoptera). Hymenopterorum Catalogus (Nova Editio), vol. 18. SPB Academic Publishing, Den Haag. [ Links ]

Péringuey, L., 1898 [1899]. Description of some new or little known South African Mutillidae in the collection of the South African Museum. Ann. S. Afr. Mus. 1, 33-94. [ Links ]

Pilgrim, E.M., Willians, K.A., Manley, D.G., Pitts, J.P., 2009. Addressing the Dasymutilla quadriguttata species-group and species -complex (Hymenoptera: Mutillidae): several distinct species or a single, morphologically variable species? J. Kans. Entomol. Soc. 82, 231-249. [ Links ]

Pitts, J.P., Parker, F.D., 2005. Description of the female, redescription of the male, and host associations of the Nearctic species Sphaeropthalma jacala Schuster (Hymenoptera: Mutillidae). Zootaxa 1011, 55-64. [ Links ]

Quintero, D., Cambra, R.A., 1996a. Horcomutilla Casal: description of previously unknown males, new distribution records, and comments on the genus (Hymenoptera: Mutillidae). J. Hymenopt. Res. 5, 53-63. [ Links ]

Quintero, D., Cambra, R.A., 1996b. Timulla centroamericana (Dalla Torre) (Hymenoptera: Mutillidae), a parasitoid of Liris (Hymenoptera: Sphecidae). Southwest. Entomol. 21, 205-207. [ Links ]

Quintero, D., Cambra, R.A., 2001. On the identity of Scaptopoda F. Lynch Arribálzaga, new taxonomic changes and new distribution records for Neotropical Mutilli- dae (Hymenoptera), with notes on their biology. Trans. Am. Entomol. Soc. 127, 291-304. [ Links ]

Quintero, D., Cambra, R.A., 2005. Pappognatha Mickel (Hymenoptera: Mutillidae: Sphaeropthalminae): new species, sex associations, hosts, and new distribution records. J. Hymenopt. Res. 14, 191-199. [ Links ]

Rocha-Filho, L.C., Melo, G.A.R., 2011. Nesting biology and behavioural ecology of the solitary bee Monoeca haemorrhoidalis (Smith) and its cleptoparasite Proto- siris gigas Melo (Hymenoptera: Apidae: Tapinotaspidini; Osirini) . J. Nat. Hist. 45, 2815-2840. [ Links ]

Rocha-Filho, L.C., Silva, C.I., Gaglianone, M.C., Augusto, S.C., 2008. Nesting behavior and natural enemies of Epicharis (Epicharis) bicolor Smith, 1854 (Hymenoptera Apidae). Trop. Zool. 21, 227-242. [ Links ]

Roubik, D.W., 1989. Ecology and Natural History of Tropical Bees. Cambridge Uni- versity Press, Cambridge. [ Links ]

Roubik, D.W., 1990. A mixed colony of Eulaema (Hymenoptera: Apidae), natural enemies, and limits to sociality. J. Kans. Entomol. Soc. 63, 150-157. [ Links ]

Rozen, J.G., 1973. Life history and immature stages of the bee Neofidelia (Hymenoptera, Fideliidae). Am. Mus. Novit. 2519, 1-14. [ Links ]

Ruiz, F., 1940. Apidologia Chilena. Rev. Chil. Entomol. 44, 281-377. [ Links ]

Schuster, R.M., 1951. Notes on Neotropical Mutillidae. V. Contributions to the genus Hoplomutilla Ashmead. Rev. Entomol. Rio J. 22, 315-328. [ Links ]

Sergeev, M.E., Lelej, A.S., 2011. On the parasitism of velvet ant Physetopoda halensis (Hymenoptera: Mutillidae) on the larva of leaf beetle Labidostomis hummeralis (Coleoptera, Chrysomelidae, Clytrinae) in South-East Ukraine. Vestnik Zool. 45, 144 (in Russian). [ Links ]

Seyrig, A., 1936. Un Mutillide parasite d'un Lépidoptère: Stenomutilla freyi. In: Livre Jubilaire de M. Eugène-Louis Bouvier, member de l'Institut, professor honoraire au Muséum. Firmin-Didot et Cie, Paris, France, pp. 313-316. [ Links ]

Strand, E., 1909. Beitrag zur Bienenfauna von Paraguay. (Hym.). Dtsch. Entomol. Z. 1909, 227-237. [ Links ]

Vesey-FitzGerald, D., 1939. Observations on bees (Hym.: Apoidea) in Trinidad, B.W.I. Proc. R. Entomol. Soc. Lond. Ser. A Gen. Entomol. 14, 107-110. [ Links ]

Vinson, S.B., Frankie, G.W., Coville, R.E., 1987. Nesting habits of Centris flavofasciata Friese (Hymenoptera: Apoidea: Anthophoridae) in Costa Rica. J. Kans. Entomol. Soc. 60, 249-263. [ Links ]

Waser, N.M., Ollerton, J., 2006. Plant-Pollinator Interactions: From Specialization to Generalization. University of Chicago Press, Chicago. [ Links ]

Wille, A., Orozco, E., 1970. The life cycle and behavior of the social bee Lasioglos- sum (Dialictus) umbripenne (Hymenoptera: Halictidae). Rev. Biol. Trop. 17, 199-245. [ Links ]

Williams, K.A., Brothers, D.J., Pitts, J.P., 2011. New species of Tobantilla Casal, 1965 and a new genus and species, Gogoltilla chichikovi gen. et sp. nov., from Argentina (Hymenoptera: Mutillidae). Zootaxa 3064, 41-68. [ Links ]

Yanega, D., 1994. Arboreal, ant -mimicking mutillid wasps, Pappognatha; parasites of Neotropical Euglossa (Hymenoptera: Mutillidae and Apidae). Biotropica 26, 465-468. [ Links ]

Zanette, L.R.S., Soares, L.A., Pimenta, H.C., Gonçalves, A.M., Martins, R.P., 2004. Nesting biology and sex ratios of Auplopus militaris (Lynch -Arribalzaga 1873) (Hymenoptera Pompilidae). Trop. Zool. 17, 145-154. [ Links ]

Received: April 28, 2016; Accepted: June 02, 2016

* Corresponding author. E-mail: drdaluz@gmail.com(D.R. Luz).

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