Gabriela Chavarría.
First Neotropical mutualistic associations in bumblebee nests (Hymenoptera: Apidae).
Psyche 101(1-2):113-118, 1994.

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FIRST NEOTROPICAL MUTUALISTIC ASSOCIATIONS IN BUMBLEBEE NESTS (HYMENOPTERA: APIDAE)
Museum of Comparative Zoology
Harvard University
Cambridge, MA 02 138
Ectosymbionts of bumblebee nests of Bombus ephippiatus are recorded for first time from the American Tropics. An overview of this interaction is provided.
"The insect colony and its immediate environment can be thought of as an island which symbiotic organisms are continu- ously attempting to colonize"
E.O. Wilson, 1971
Much is known about the enemies and inquilines which, directly or indirectly, affect the existence of the bumblebees (Alford, 1975). Many occur in nests as either accidental visitors or harmless scavengers, some may be beneficial, but several are either parasites of adult bees or they damage the brood or the comb. A large num- ber act either as social parasites as in the case of Psithyrus Le- peletier (Hymenoptera: Apidae) (Sladen, 19 15; Frison, 191 6, 1921 ; Plath, 1922a), or as parasites of the adults, larvae and pupae as in the case of the conopid flies Physocephala sagittaria (Say) (Packard, 1865; Meijere, 1904; Frison, 19 18), Spherularia bombi Dufour (Rkaumur, 1742; Leuckart, 1887), Brachycoma sarcophag- ina (Townsend)(Davidson, 1894; Sladen, 1912; Plath, 1922b), Mel- litobia sp. (Prison, 1926), Parasitus sp. (Oudemans, 1902; Banks, 1919; Richards, 1976; Richards and Richards, 1976), or as insect enemies of the bumblebee comb, like the pyralid moths Vitula edmandsii (Packard) (Franklin, 191 2-13; Prison, 191 8) and Plodia Manuscript received 17 April 1994.
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Pu&e 101:113-118 11994) hItp/@ychr rnlcluborgY101/101-113 html



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114 Psyche [VOI. 101
interpunctella Hiibner (Davidson, 1894), or as scatophagus associ- ates and occasional lodgers. A number of insects act as scavengers within the bumblebee nest. Among the most interesting of these is the beetle Antherophagus Latreille (Coleoptera: Cryptophagidae). Many European and American investigators record the capture of Antherophagus (pollens F., silaceus Herbst and nigricornis F.) in the nests of bumblebees. As Carus and Gerstaecker (1863) stated of Antherophagus: "The species live on flowers, attach themselves to bumble-bees and permit the latter to transport them to their nests, probably for the purpose of oviposition." In fact several authors (Gorham, 1869; Perris, 1869-70; Bugnion, 1869-70; Seid- litz, 1869-70) described seeing the larvae of these beetles in the nests of bumblebees.
Several observations have been made comparing the European and American beetle species and have found that both species are similar in habits. The adults of Antherophagus gain admittance to the nests of bumblebees often if not always by attaching them- selves to the proboscis of bumblebees while the bees are feeding at the flowers. They are then carried back to the nests and upon releasing their hold fall onto the comb and eventually reproduce in the debris of the nest, particularly at the bottom of the comb. Packard (1864) said that these beetles have a certain attraction for sweet flowers and that they visit the nests of the bees for the pur- pose of consuming the honey stored there, but Packard (1873) inferred that the beetles probably feed upon the wax and pollen. However, it seems that the views of various other authors are unan- imous concerning the feeding habits of the larva. Perris (1875) says that the larvae of Antherophagus probably play the same role in the bumblebee nests as do Cryptophagus in the nests of wasps, "they live on the feces of the inhabitants and that they are, prop- erly speaking, merely scavengers" and that seems to be the most realistic explanation.
MATERIAL AND METHODS
During a field trip to Cerro de la Muerte, Costa Rica in July, 1993 and January, 1994, while collecting bumblebee nests for stud- ies on nesting behavior, the author collected four nests of Bombus ephippiatus Say. The bumblebee nests were collected at Cerro de la Muerte in the Talamanca Cordillera in Costa Rica. Some other



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Chavarria
nests of other bumblebee species were collected in other areas and contained no ectosymbionts. Several bees were collected while fly- ing and while foraging; observations were made also on several flower patches, in order to find a possible phoretic organism. Bumblebee nests were dissected and all inquilines were placed in 80% ethanol and samples of the different inquilines were sent to Q.D. Wheeler and P. Fraissinet (Cornell University) for identifica- tion. Field collected adult bumblebees were pinned. Adults, larvae, and pupae of a number of species of different families of primarily Coleoptera and Diptera were found in all four nests (Table l), and a new species of Antherophagus (Wheeler and Fraissinet, pers. comm.) is reported for the first time. The study of bumblebee nests is at an early stage, therefore, not so many nests of Neotropical bumblebees have been studied in detail. Flies (Phoridae) were also found; this is not unusual because phorid flies have been reported as guests of many social insects, including bumblebees (Wilson, 197 1).
Of the bumblebees that were collected while flying or foraging (157 specimens), none had any inquilines except for mites. All bumblebee colonies were very active and were producing a lot of brood, and in two cases the colonies were producing queens. This activity in the nests, in conjunction with the presence of sev- eral inquilines, demonstrates that the inquilines are probably obli- gate ectosymbionts (Wilson, 1971) in some kind of relationship other than internal parasitism.
In 1982 Roubik and Wheeler mentioned Roubik's personal observation of a nest of B. atratus Franklin, kept in captivity at the Universidad Nacional de Colombia in Bogota, where beetles of the genus Antherophagus lived in the nest and left phoretically on for- aging bees; however aside from this report, such behavior has not been mentioned for the Neotropical bumblebees. More studies are needed, especially field work, in order to understand truly the behavior and other patterns of these beetles, including whether there is any specificity in relation to different bumblebee species. This type of study will contribute to a better understanding of the host relationships. Finally, the concept of an insect colony as a partially isolated ecosystem can be extended and



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Table 1. Insect ectosymbionts of Bombus ephippiatus nests. a\
NEST # 1 NEST # 2 NEST # 3
NEST # 4
COLEOPTERA
- adult Antherophagus n.sp.
(Cryptophagidae)
- larval Antherophagus n.sp.
- adult Loberopsyllus * n.sp.
Cryptophagidae
DIPTERA
- larval & pupal Phoridae
COLEOPTERA
- adult Antherophagus n.sp.
- larval Antherophagus n.sp.
- adult Gonicoelus sp.
(Biphyllidae)
- adult Ptomuphagus sp.
(Lei0didae:Cholevinae)
- adult Ptiliidae n.sp. ?
(blind, flightless)
- adult Ptiliidae normal sp.
- adult Amblyopinus
(S taphylinidae)
- pupal Staphylinidae
- larval Staphylinidae
DIPTERA
- larval or pupal Phoridae
- larval Scatopsidae
* Determined by R. Leschen, University of Kansas, Lawrence COLEOPTERA
- larval Antherophagus n.sp
- adult Tenebrionidae undet.
COLEOPTERA
- adult Antherophagus n.sp.
- larval Antherophagus nsp.
- larval ?Carabidae undet.
DIPTERA
DIPTERA
- larval & pupal Phoridae
- adult Brachycera undet.
HEMIPTERA
- adult Cydnidae
- adult Phoridae
- larval and pupal Phoridae
- adult Brachycera undet.




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Chavarria
this way we can gain a better understanding of biological aspects of the symbionts.
I would like to thank Quentin D. Wheeler and Peter Fraissinet (Cornell University) for identifying the material in the nests. I thank Adam Lazarus for assistance in the field. I would like to express my gratitude to the people at la Georgina and Villa Mills, Cerro de la Muerte Costa Rica for their hospitality and help in finding the nests. The field work in Costa Rica was supported by a post-course award from the Organization for Tropical Studies (OTS) and the Pew Charitable Trust, and the Graduate Student Council, Harvard University.
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118 Psyche [vo~. 101
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