Bombus terrestris terrestris (Linnaeus, 1758) and hybrids with the endemic Bombus xanthopus spotted on Capraia Island (Tuscan Archipelago, Italy): some conservation management implications.
Bumblebees
Bumblebees mass-migration
Conservation
Distribution range
Hybrid
Recolonization
Journal
Die Naturwissenschaften
ISSN: 1432-1904
Titre abrégé: Naturwissenschaften
Pays: Germany
ID NLM: 0400767
Informations de publication
Date de publication:
12 Apr 2023
12 Apr 2023
Historique:
received:
13
12
2022
accepted:
31
03
2023
revised:
24
03
2023
medline:
14
4
2023
entrez:
12
4
2023
pubmed:
13
4
2023
Statut:
epublish
Résumé
Expansion of wild and managed allochthonous species leads to potential negative consequences for the endemic wildlife, such as resource competition, pathogens spread, hybridization and native species replacements. On Capraia Island, the last sighting of Bombus terrestris terrestris dates back to 1917. All subsequent surveys carried out on the island only reported the presence of B. xanthopus and B. pascuorum melleofacies with B. t. terrestris apparently no longer existing in the area. In 2021 B. t. terrestris was again detected on the island raising two main hypotheses: (i) B. t. terrestris has always been present with a low population density, such as not to be detected in previous investigations, or (ii) its presence is the result of a more recent recolonization. The recolonization event may be promoted by either intentional or unintentional introduction or it may be the result of a natural migration from the mainland or surrounding islands. Hybridization between B. t. terrestris × B. xanthopus on Capraia Island has been also ascertained by the detection of hybrid queens, workers and males. These new finding provides insight on the distribution range of B. t. terrestris in the Tuscan Archipelago and raise concern on the conservation of the endemic B. xanthopus population.
Identifiants
pubmed: 37043047
doi: 10.1007/s00114-023-01843-y
pii: 10.1007/s00114-023-01843-y
pmc: PMC10097771
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
14Subventions
Organisme : Tuscan Archipelago National Park
ID : na
Informations de copyright
© 2023. The Author(s).
Références
Beekman M (1998) The bumblebee life cycle. Overwintering and colony growth of Bombus terrestris. PhD thesis, Universiteit van Amsterdam
Beekman M, Van Stratum P (2000) Does the diapause experience of bumblebee queens Bombus terrestris affect colony characteristics? Ecol Entomol 25(1):1–6
doi: 10.1046/j.1365-2311.2000.00235.x
Buttermore RE (1997) Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in southern Tasmania. Aust. J Entomol 36(3):251–254
Chandler D, Cooper E, Prince G (2019) Are there risks to wild European bumble bees from using commercial stocks of domesticated Bombus terrestris for crop pollination? J Apicul Res 58(5):665–681. https://doi.org/10.1080/00218839.2019.1637238
doi: 10.1080/00218839.2019.1637238
Chittka L, Ings TC, Raine NE (2004) Chance and adaptation in the evolution of island bumblebee behaviour. Popul Ecol 46(3):243–251
doi: 10.1007/s10144-004-0180-1
Cilia G, Flaminio S, Zavatta L, Ranalli R, Quaranta M, Bortolotti L, Nanetti A (2022) Occurrence of honey bee (Apis mellifera L.) pathogens in wild pollinators in Northern Italy. Front Cell Infect Microbiol 12:907489. https://doi.org/10.3389/fcimb.2022.907489
doi: 10.3389/fcimb.2022.907489
pubmed: 35846743
pmcid: 9280159
Cini A, Benetello F, Bonifacino M, Salvati V, Monterastelli E, Pasquali L, Sistri G, Dani FR, Dapporto L (2022) Simple and informative: applying a basic Anthophila monitoring scheme in a simplified insular ecosystem. Bull Insectology 75(1):83–95
Dafni A, Kevan P, Gross CL, Goka K (2010) Bombus terrestris, pollinator, invasive and pest: an assessment of problems associated with its widespread introductions for commercial purposes. Appl Entomol Zool 45(1):101–113
doi: 10.1303/aez.2010.101
Dafni A, Shmida A (1996) The possible ecological implications of the invasion of Bombus terrestris (L.) (Apidae) at Mt. Carmel, Israel. In: Matheson A, Buchmann SL, O’Toole CH, Westrich P, Williams IH (eds) The conservation of bees. Academic, London, pp 183–200
De Jonghe R (1986) Crossing experiments with Bombus terrestris terrestris (Linneus, 1758) and Bombus terrestris xanthopus Kriechbaumer 1870 and some notes on diapause and nosemose (Hymenoptera: Apoidea). Phegea 14:19–23
Fanfani A, Groppali R (1979) La fauna di Montecristo - Arcipelago Toscano. (Studi sulla Riserva Naturale dell'Isola di Montecristo). Ist Entomol Univ Pavia 9:1–52
Felicioli A (2021) Relazione finale delle attività svolte nell’ambito del Progetto “Studio degli insetti impollinatori e sull’agricoltura tradizionale presso le isole di Capraia e Giglio”. Technical Report.
Fijen TP (2021) Mass-migrating bumblebees: an overlooked phenomenon with potential far-reaching implications for bumblebee conservation. J Appl Ecol 58(2):274–280
doi: 10.1111/1365-2664.13768
Generani M, Pagliano G, Scaramozzino P, Strumia E (1998) Nuovi Imenotteri dell’Isola di Montecristo. Frustula Entomol 21:75–83
Generani M, Pagliano G, Scaramozzino P, Strumia F (2001) Gli Imenotteri delle isole di Capraia, Giglio, Gorgona, Pianosa e Montecristo (Arcipelago Toscano). Frustula Entomol 24(37):51–74
Ghisbain G, Gérard M, Wood TJ, Hines HM, Michez D (2021) Expanding insect pollinators in the Anthropocene. Biol Rev 96(6):2755–2770
pubmed: 34288353
doi: 10.1111/brv.12777
Goulson D (2003) Bumblebees: their behaviour and ecology. Oxford University Press, USA
Hingston AB, McQuillan PB (1998) Nectar robbing in Epacris impressa (Epacridaceae) by the recently introduced bumblebee Bombus terrestris (Apidae) in Tasmania. Vic Nat 115(4):116–119
Inari N, Nagamitsu T, Kenta T, Goka K, Hiura T (2005) Spatial and temporal pattern of introduced Bombus terrestris abundance in Hokkaido, Japan, and its potential impact on native bumblebees. Popul Ecol 47:77–82
doi: 10.1007/s10144-004-0205-9
Ings TC, Ings NL, Chittka L, Rasmont P (2010) A failed invasion? Commercially introduced pollinators in Southern France. Apidologie 41(1):1–13
doi: 10.1051/apido/2009044
Ings TC, Schikora J, Chittka L (2005) Bumblebees, humble pollinators or assiduous invaders? A population comparison of foraging performance in Bombus terrestris. Oecologia 144(3):508–516
pubmed: 15891827
doi: 10.1007/s00442-005-0081-9
Intoppa F, Piazza MG, Bolchi Serini G, Cornalba M (2009) I bombi. Guida al riconoscimento delle specie italiane. CRA - Unita di Ricerca di Apicoltura e Bachicoltura, Bologna
Intoppa F, Piazza MG, D'Albore GR (1995) Catalogo bibliografico delle specie di Bombidae (Hymenoptera Apoidea) segnalate per l'Italia. Supplement Apicult 10
Kanbe Y, Okada I, Yoneda M, Goka K, Tsuchida K (2008) Interspecific mating of the introduced bumblebee Bombus terrestris and the native Japanese bumblebee Bombus hypocrita sapporoensis results in inviable hybrids. Naturwissenschaften 95:1003–1008
pubmed: 18594790
doi: 10.1007/s00114-008-0415-7
Kondo NI, Yamanaka D, Kanbe Y, Kunitake YK, Yoneda M, Tsuchida K, Goka K (2009) Reproductive disturbance of Japanese bumblebees by the introduced European bumblebee Bombus terrestris. Naturwissenschaften 96:467–475
pubmed: 19089400
doi: 10.1007/s00114-008-0495-4
Krüger E (1954) Phänoanalytische Studien an einigen Arten der Untergattung Terrestribombus O. Vogt (Hymenoptera Bombidae). Teil Tijdschr Entomol 97:263–298
Lecocq T, Brasero N, De Meulemeester T, Michez D, Dellicour S, Lhomme P, De Jonghe R, Valterovà I, Urbanovà K, Rasmont P (2015) An integrative taxonomic approach to assess the status of Corsican bumblebees: implications for conservation. Anim Conserv 18(3):236–248
doi: 10.1111/acv.12164
Masi L (1933) Raccolte entomologiche nell'isola di Capraia fatte da C. Mancini e E. Capra (1927-1931). III. Hymenoptera Aculeata, vol 11. Memorie della Società Entomologica italiana, Genova, pp 181–205
Matsumura C, Nakajima M, Yokoyama J, Washitani I (2004) High reproductive ability of an alien bumblebee invader, Bombus terrestris L., in the Hidaka region of southern Hokkaido, Japan. Japanese. J Conserv Ecol 9(1):93–101
Mikkola K (1978) Spring migrations of wasps and bumble bees on the southern coast of Finland (Hymenoptera, Vespidae and Apidae). Ann Zool Fenn 44:10–26
Ministero dell’Ambiente e della Tutela del Territorio e del Mare (2019) Direttiva agli enti parco nazionali e alle aree marine protette per l’indirizzo delle attività dirette alla conservazione della biodiversità. Prot. 0023838/UDCM of 12/10/2019
Nagamitsu T, Yamagishi H, Kenta T, Inari N, Kato E (2009) Competitive effects of the exotic Bombus terrestris on native bumble bees revealed by a field removal experiment. Popul Ecol 52(1):123–136
doi: 10.1007/s10144-009-0151-7
Pawlikowski T, Sparks TH, Olszewski P, Pawlikowski K, Rutkowski L, Jakubowski R (2020) Rising temperatures advance the main flight period of Bombus bumblebees in agricultural landscapes of the Central European Plain. Apidologie 51:652–663
doi: 10.1007/s13592-020-00750-9
Potts S, Dauber J, Hochkirch A, Oteman B, Roy D, Ahnre K, Biesmeijer K, Breeze T, Carvell C, Ferreira C, Fitzpatrick Ú, Isaac N, Kuussaari M, Ljubomirov T, Maes J, Ngo H, Pardo A, Polce C, Quaranta M, Settele J, Sorg M, Stefanescu C, Vujic A (2020) Proposal for an EU pollinator monitoring scheme, EUR 30416 EN, Publications Office of the European Union, Luxembourg, ISBN 978-92-76-23859-1, doi:10.2760/881843, JRC122225
Quaranta M, Felicioli A (2012) First report of Bombus terrestris xanthopus Kriechbaumer on the Italian peninsula (Hymenoptera: Apidae). Ann Soc Entomol Fr 48(3-4):343–346
doi: 10.1080/00379271.2012.10697783
Rasmont P (1985) Bombus terrestris (L.) (Hymenoptera, Apidae) dans le Massif des Maures (France, Var), une génération d’hiver. Bull Ann Soc R Belge Entomol 120:359–363
Rasmont P, Adamski A (1995) Les bourdons de la Corse (Hymenoptera, Apoidea, Bombinae). Notes Fauniques Gembloux 31:3–87
Rasmont P, Coppée A, Michez D, De Meulemeester T (2008) An overview of the Bombus terrestris (L. 1758) subspecies (Hymenoptera: Apidae). Ann Soc Entomol Fr 44(2):243–250
doi: 10.1080/00379271.2008.10697559
Rasmont P, Ghisbain G, Terzo M (2021) Bumblebees of Europe and neighbouring regions. Nap Editions
Rasmont P, Quaranta M (1997) I Bombi dell’Arcipelago Toscano. Boll Soc Entomol Ital 129:31–38
Rasmont P, Scholl A, De Jonghe R, Obrecht E, Adamski A (1986) Identité et variabilité des mâles de bourdons du genre Bombus Latreille sensu stricto en Europe occidentale et centrale (Hymenoptera, Apidae, Bombinae). Rev Suisse Zool 93(3):661–682
doi: 10.5962/bhl.part.79505
Razzauti A (1917) Contributi alla conoscenza faunistica delle isole toscane. I. Isola di Capraia. Atti Soc Tosc Sci Nat Pisa Mem 31:196–224
Ricciardelli d’Albore G (1986) Bombus Latr. e Psithyrus Lep. in Umbria. Redia 69:171–256
Russo L (2016) Positive and negative impacts of non-native bee species around the world. Insects 7(4):69. https://doi.org/10.3390/insects7040069
doi: 10.3390/insects7040069
pubmed: 27916802
pmcid: 5198217
Ruz L (2002) Bee pollinators introduced to Chile: a review. In: Kevan P, Fonseca IVL (eds) Pollinating Bees - The Conservation Link Between Agriculture and Nature. Ministry of Environment, Brasília, pp 155–167
Semmens TD, Turner E, Buttermore R (1993) Bombus terrestris (L.) (Hymenoptera: Apidae) now established in Tasmania. J Aust Entomol Soc 32(4):346
doi: 10.1111/j.1440-6055.1993.tb00598.x
Tsuchida K, Kondo NI, Inoue MN, Goka K (2010) Reproductive disturbance risks to indigenous Japanese bumblebees from introduced Bombus terrestris. Appl Entomol Zool 45(1):49–58
doi: 10.1303/aez.2010.49
Tsuchida K, Yamaguchi A, Kanbe Y, Goka K (2019) Reproductive interference in an introduced bumblebee: polyandry may mitigate negative reproductive impact. Insects 10:59. https://doi.org/10.3390/insects10020059
doi: 10.3390/insects10020059
pubmed: 30813290
pmcid: 6409605
van den Eijnde J, de Ruijter A (2000) Bumblebees from the Canary Islands: mating experiments with Bombus terrestris L. from the Netherlands. In Sommeijer MJ, Meeuwsen FJAJ (eds.) Proceedings of the Section Experimental and Applied Entomology of the Netherlands Entomological Society 11:159-161
Velthuis HH, Van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37(4):421–451
doi: 10.1051/apido:2006019
Williams PH (2021) Not just cryptic, but a barcode bush: PTP re-analysis of global data for the bumblebee subgenus Bombus s. str. supports additional species (Apidae, genus Bombus). J Nat Hist 55(5-6):271–282
doi: 10.1080/00222933.2021.1900444
Winter K, Adams L, Thorp R, Inouye D, Day L, Ascher J, Buchmann S (2006) Importation of non-native bumble bees into North America: potential consequences of using Bombus terrestris and other non-native bumble bees for greenhouse crop pollination in Canada, Mexico, and the United States. North American Pollinator Protection Campaign (NAPPC)
Yoneda M, Furuta H, Tsuchida K, Okabe K, Goka K (2008) Commercial colonies of Bombus terrestris (Hymenoptera: Apidae) are reservoirs of the tracheal mite Locustacarus buchneri (Acari: Podapolipidae). Appl Entomol Zool 43(1):73–76
doi: 10.1303/aez.2008.73
Yoon HJ, Kim SY, Lee KY, Lee SB, Park IG, Kim I (2009) Interspecific hybridization of the bumblebees Bombus ignitus and B. terrestris. Int J Indust Entomol 18(1):41–48