A scientific note on Bombus (Psithyrus) insularis invasions of bumblebee nests and honeybee hives in the western USA

HAL Id: hal-01234751

https://hal.archives-ouvertes.fr/hal-01234751

Submitted on 27 Nov 2015

HAL is a multi-disciplinary open access

archive for the deposit and dissemination of

sci-entific research documents, whether they are

pub-lished or not. The documents may come from

teaching and research institutions in France or

abroad, or from public or private research centers.

L’archive ouverte pluridisciplinaire HAL, est

destinée au dépôt et à la diffusion de documents

scientifiques de niveau recherche, publiés ou non,

émanant des établissements d’enseignement et de

recherche français ou étrangers, des laboratoires

publics ou privés.

A scientific note on Bombus (Psithyrus) insularis

invasions of bumblebee nests and honeybee hives in the

western USA

James Strange, Abby Baur, Jonathan Koch

To cite this version:

A scientific note on

Bombus (Psithyrus) insularis invasions of bumblebee

nests and honeybee hives in the western USA

James P. STRANGE1,Abby BAUR1,2,Jonathan B. KOCH1,3

1

USDA-ARS Pollinating Insects Research Unit, Utah State University, BNR Room 261, Logan, UT 84322, USA

2

Department of Environment and Society, Utah State University, Logan, UT 84322, USA

3

Department of Biology, Utah State University, Logan, UT 84322, USA Received 11 July 2013– Revised 22 November 2013 – Accepted 9 January 2014

social parasites / inquilines /Apis mellifera / bumblebees

Bumblebees (Bombus) in the subgenus Psithyrus are obligate social parasites that usurp the nests of other bumblebees in order to reproduce. Usurpation occurs after nest establishment by the host species when, upon entry to the nest, the invading Psithyrus kills or suppresses the host queen and dominates host workers to rear her offspring, but considerable behavioral variation occurs in host–parasite interac-tions among members of the genus (Fisher 1988). While many Psithyrus species are known to parasitize a number of species, few of the relationships are well understood. Of the six North American Psithyrus species, most have been recorded from the nests of several host species, and it is reasonable to assume that each host species reacts differently to an invasion.

In addition to usurping bumblebee nests, Plath (1927) noted that females of Psithyrus laboriosus (=Bombus citrinus (Smith)) would attempt to invade honeybee hives (Apis mellifera L.). This was noted as a “dead end,” usually resulting in the death of the invading bee. Subsequently, records of several Bombus species attempting to enter honeybee hives

were made by Morse and Gary (1961), but of these records, only 1 of the 28 bumblebees found in 25 honeybee colonies was a social parasite (B. citrinus). The authors attributed these nest invasions to re-source robbing and not nest usurpation. Here, we report Bombus insularis (Smith) invading the nest of two bumblebee species in the subgenus Pyrobombus, Bombus huntii Greene, and Bombus bifarius Cresson, and attempted invasions of honeybee hives at four apiaries by B. insularis.

During the summer of 2012, numerous female B. insularis were observed near bumblebee nest boxes and honeybee hives in Utah, USA. Although obser-vations from previous years were not quantified, it is uncommon to see dead B. insularis around honeybee hives; for example in 2013 at apiary 1, we found no B. insularis at three colonies during weekly inspec-tion. The exception was in 2007 when several dead B. insularis were observed at hive entrances at apiary 1. That year, a B. insularis was observed entering a honeybee hive and was forced out within a minute. When the invader exited the hive, it had several honeybee workers attacking her, by biting her legs and tegulae; however, the parasite managed to escape and fly away. The number of invasions in 2012 by B. insularis provided an opportunity to study aspects of nest usurpation and hive invasion. We collected dead B. insularis from the ground in front of honeybee hives at four apiary sites from 12 June to 12 August (Table I). Apiary 1 was inspected weekly for dead Psithyrus in front of the hives, and apiaries 2–4 were

Electronic supplementary material The online version of this article (doi:10.1007/s13592-014-0271-8) contains supplementary material, which is available to authorized users.

Corresponding author: J.P. Strange, James.Strange@ars.usda.gov Manuscript editor: James Nieh

Apidologie (2014) 45:554–556

_{Scientific note}

visited one time each in mid-July. We also observed female B. insularis invading nests of B. huntii and B. bifarius placed in the field at the Logan Bee Lab Gardens (BLG) and apiary 1 (TableI).

A total of 47 female B. insularis and one female B. huntii were found dead in front of honeybee hives at four apiaries. The average number of dead B. insularis was 2.9 per hive across all apiaries (range, 0.7–6 per hive). Microscopic inspection of the dead B. insularis showed some cuticular damage to the dead bees, most notably extensive removal of setae. Of the 47 B. insularis that were found dead in front of honeybee colonies, only two were found to have sting remnants in the cuticle, both found in the thin cuticle between abdominal sterna, indicating that the sting may not be effective in killing these invaders. Perhaps, the honeybees kill these larger and well-armored parasites through balling behavior (Papachristoforou et al. 2007); however, the cause of death is uncertain.

In June 2012, we deployed nests of B. bifarius, B. huntii, and Bombus occidentalis Greene that had been reared from locally sourced queen bumblebees in two-chambered wooden nest boxes (Plowright and Jay 1966). Nests had between 15 and 30 workers when deployed. Three nests were placed in the BLG on 19 June, while nests of B. huntii and B. occidentalis were placed in apiary 1 on 30 June. After observing parasites investigating the nests, we made approximately weekly observations during the summer to understand the dynamics of B. insularis invasion.

Within 4 h of placing nests in the BLG on 19 June, B. insularis were observed investigating the nest boxes for an entrance. Because one B. huntii nest was queenless when deployed, we captured one of the searching B. insularis on 20 June and introduced her into the nest. She harassed approximately 35 workers and males in the nest by biting and pushing the workers around the nest, but only one worker was killed in the melee. Six days after the nests were deployed, on 25 June, there were two dead B. insularis in the nest box and one live B. insularis. It is unknown if the remaining bee was the original invader. The B. huntii nest was then abandoned by the inquiline for several days and reinvaded by a B. insularis on 2 July 2012. All the B. insularis we observed harassed workers and then appeared to be incubating brood in the nests within a few hours of invasion, a pattern that repeated in all the Bombus colonies, as shown in the animation (Online Resource).

Although the queenless nest of B. huntii was invaded with little loss of life, a queen right nest at apiary 1 had a different outcome. The first B. insularis invasion occurred two days after the nest was placed, on 2 July. Workers had been marked with colored tags before the nest was deployed, and all the tagged bees either abandoned the nest or were dead within a week. The B. huntii queen and two B. insularis were also found dead in the nest within 7 days. However, newly emerging B. huntii workers stayed in the nest and adopted the remaining B. insularis invader as queen. This nest was subsequent-ly invaded by two additional B. insularis, resulting in the death of the young, unmarked workers of B. huntii, resulting in no workforce for any B. insularis to exploit. Thus, by the end of August, the nest had produced no B. insularis offspring. In all, at least five B. insularis attempted to invade the B. huntii nest.

The B. bifarius nest in the BLG met a similar fate to the queen right B. huntii nests. The first B. insularis invasion occurred before 25 June when a parasite was seen in the nest. There were two dead workers and five live workers in the nest, but the original queen and most of her workers were no longer there, apparently having abandoned it. The next day, a second B. insularis was seen invading the nest, and the encounter was video recorded. The two females fought, but the second invader then retreated, leaving the nest to the first. By 27 June, the nest was empty but for a single B. bifarius worker. Eleven days later, on 8 July, a single B. bifarius worker and a B. insularis were observed in the nest, but the B. insularis died that night having not reproduced. Table I. Apidae hosts ofB. insularis at five locations

in northern Utah.

Site Hosts Coordinates Apiary 1 B. huntii 41°44.72′N

111 49.74′W B. occidentalisa

A. mellifera–four colonies

Apiary 2 A. mellifera–four colonies 41°45.76′N 111°47.97′W Apiary 3 A. mellifera–six colonies 41°45.73′N

111°47.76′W Apiary 4 A. mellifera–two colonies 41°41.16′N

111°50.08′W Bee lab B. bifarius 41°45.45′N

111° 48.69′W B. huntii

B. occidentalisa

a_{No invasion attempts were recorded on these nests}

Considering the volatile history of the usurpation by B. insularis in our observations, it is unknown if the B. insularis female observed on 26 June is the same individual that died on 8 July.

Neither B. occidentalis nest deployed in apiary 1 nor BLG was observed to have an attempted invasion. Twice we observed B. insularis females flying around a B. occidentalis nest for several minutes; however, the parasite did not enter the nest nor was there any evidence of an attempted invasion, such as a dead B. insularis outside the nests.

The number of B. insularis appearing in the summer of 2012 suggests that this species has the potential for population outbreaks which are not uncommon for social Hymenoptera (Akre and Reed

1981). Perhaps the high population densities leading to multiple invasions are a negative feedback that keeps the parasite population in check if repeated invasions impact the species ability to produce offspring. Alternatively, it may be that B. huntii and B. bifarius are suboptimal hosts in comparison to the other 12 bumblebee species in northern Utah, but this is unclear.

The cause of incursions into honeybee colonies is also perplexing. Were these events, as Morse and Gary (1961) suggest, simple attempts to rob hive resources, or are high population densities of B. insularis driving it to attempt usurpation of novel species? Questions of host preference and the cause of honeybee hive invasion remain to be determined. Finally, considering so many bumblebee workers die during invasions, thus reducing the pollination service that a colony can provide, is there a management strategy to limit the number of bumblebee colony invasions in outbreak years? Initial attempts to modify

bumblebee nest entrances by reducing the size of the opening seemed to reduce invasions, yet a controlled study was not conducted. Much needs to be learned about the ecology, behavior, and management of these social parasites.

Note scientifique sur les invasions de Bombus (Psithyrus) insularis dans les nids de bourdons et les ruches d’abeilles dans l’ouest des Etats-Unis

Eine wissenschaftliche Notiz über das Eindringen von Bombus (Psithyrus) insularis in Hummelnester und Honigbienenvölker im Westen der Vereinigten Staaten von Amerika

REFERENCES

Akre, R.D., Reed, H. (1981) Population cycles of yellow jackets (Hymenoptera: Vespinae) in the Pacific Northwest. Environ. Entomol. 10(3), 267_–274

Fisher, R.M. (1988) Observations on the behaviours of three European cuckoo bumble bee species (Psithyrus). Insectes Soc. 35(4), 341–354

Morse, R.A., Gary, N.E. (1961) Insect invaders of the honeybee colony. Bee World 42, 179–181

Papachristoforou, A., Rortais, A., Zafeiridou, G., Theophilidis, G., Garnery, L., et al. (2007) Smothered to death: hornets asphyxiated by honeybees. Curr. Biol. 17(18), 795–796 Plath, O.E. (1927) Psithyrus laboriosus, an unwelcome guest in

the hives of Apis mellifera. Bull. Brooklyn Entomol. Soc. 22, 121–125

Plowright, R.C., Jay, S.C. (1966) Rearing bumblebee colonies in captivity. J. Apic. Res. 5, 155–165