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Evolution of the Suctorial Proboscis in Pollen Wasps (Masarinae, Vespidae)

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Evolution of the Suctorial Proboscis in Pollen Wasps (Masarinae, Vespidae) Arthropod Structure & Development 31 (2002) 103–120 www.elsevier.com/locate/asd Evolution of the suctorial proboscis in pollen wasps (Masarinae, Vespidae) Harald W. Krenna,*, Volker Maussb, John Planta aInstitut fu¨r Zoologie, Universita¨t Wien, Althanstraße 14, A-1090, Vienna, Austria bStaatliches Museum fu¨r Naturkunde, Abt. Entomologie, Rosenstein 1, D-70191 Stuttgart, Germany Received 7 May 2002; accepted 17 July 2002 Abstract The morphology and functional anatomy of the mouthparts of pollen wasps (Masarinae, Hymenoptera) are examined by dissection, light microscopy and scanning electron microscopy, supplemented by field observations of flower visiting behavior. This paper focuses on the evolution of the long suctorial proboscis in pollen wasps, which is formed by the glossa, in context with nectar feeding from narrow and deep corolla of flowers. Morphological innovations are described for flower visiting insects, in particular for Masarinae, that are crucial for the production of a long proboscis such as the formation of a closed, air-tight food tube, specializations in the apical intake region, modification of the basal articulation of the glossa, and novel means of retraction, extension and storage of the elongated parts. A cladistic analysis provides a framework to reconstruct the general pathways of proboscis evolution in pollen wasps. The elongation of the proboscis in context with nectar and pollen feeding is discussed for aculeate Hymenoptera. q 2002 Elsevier Science Ltd. All rights reserved. Keywords: Mouthparts; Flower visiting; Functional anatomy; Morphological innovation; Evolution; Cladistics; Hymenoptera 1. Introduction Some have very long proboscides; however, in contrast to bees, the proboscis is formed only by the glossa and, in Evolution of elongate suctorial mouthparts have some species, it is looped back into the prementum when in occurred separately in several lineages of Hymenoptera in repose (Bradley, 1922; Schremmer, 1961; Richards, 1962; association with uptake of floral nectar. They can be found, Osten, 1982; Carpenter, 1996/1997; Gess, 1998). The for example, in various ‘symphytans’ (Jervis and Vilhelmsen, traditional classification of the Masarinae, dating back to 2000), parasitoid Apocrita (Jervis, 1998), sphecids (Ulrich, Saussure (1854), was based on the misunderstanding that Paragia 1924), Scoliidae, Sapygidae, Tiphiidae (Osten, 1982, 1991) the glossa of one group (based on ) cannot be retracted at all and the glossa of the other group (based on and in many bees (Michener, 1944, 2000). In Vespidae, Masaris ) can be retracted into the prementum. Carpenter’s despite the fact that the adults of both sexes obtain at least (1996/1997) study of the Paragiina clarified the morpho- some nourishment from floral nectar (Kugler, 1970; Proctor logical misunderstanding and demonstrated that the glossa et al., 1996), a very long elongate suctorial proboscis is not in all groups is retractable. The separation of the Masarinae common, except in Eumeninae (Osten, 1982) and Masarinae. into two main lineages, the Paragiina and Masarina, The Masarinae, or pollen wasps, are unique among the however, was upheld in that study by other features. vespids for their bee-like habits of provisioning each larval Currently the Masarinae contains 14 genera with about 300 brood cell with pollen and nectar. Female pollen wasps use species (Carpenter 1982, 2001) and is divided into the their mouthparts to gather pollen and nectar from flowers Gayellini and Masarini. The latter tribe consists of and for nest construction (Gess and Gess, 1992; Gess, Paragiina (Australian region only), Masarina (widespread 1996, 2001; Mauss, 1996, 2000; Mauss and Mu¨ller, 2000). except Australia) and Priscomasarina, which was estab- lished to accommodate a newly discovered species from * þ þ Corresponding author. Tel.: 43-1-4277-54497; fax: 43-1-4277- Namibia (Gess, 1998, Fig. 1). 9544. E-mail addresses: [email protected] (H.W. Krenn), volker. The evolution of an elongate proboscis occurred at least [email protected] (V. Mauss). twice in the Masarinae. Elongation of the proximal part of 1467-8039/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S1467-8039(02)00025-7 104 H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 braunsi Schulthess, Celonites peliostomi Gess and Quarti- nioides sp. (classification after Carpenter (2001),who regards Quartinioides as a subgenus of Quartinia ). Fresh specimens were fixed in 70% ethanol or Duboscq- Brasil solution (Romeis, 1989). Whole mount preparations of the mouthparts were made from dissected heads. They were soaked in diluted lactic acid at 40–50 8C for 1–2 days, washed in distilled water, and embedded in polyvinyl lactophenol without dehydration on glass slides. The preparations were covered with glass slips and dried at 50 8C. Serial semithin-section technique was used to examine mouthpart anatomy with light microscopy and to recon- struct the possible functional mechanisms of glossal move- ments. The isolated heads were dehydrated with acidified DMP (2,2-dimethoxypropane) and acetone, then embedded Fig. 1. Dendrogram showing hypothesized phylogeny of Masarinae, in ERL-4206 epoxy resin under vacuum impregnation. combined from Carpenter (1982, 1989, 1993, 1996) and Gess (1998). Taxa in bold type are investigated in this study. Semithin sections were cut using diamond knives. They were stained with a mixture of 1% azure II and 1% the glossa or of the distal part thus defines two lineages, the methylene blue in an aqueous 1% borax solution for subtribe Masarina and Metaparagia (Paragiina) (Carpenter, approximately 1 min at 80 8C. Series of sagittal semithin 1996/1997). As a relatively small group of flower visiting sections were prepared for all the above listed species of Hymenoptera, the Masarinae offer the possibility to Masarinae. Preparations were made of P. decipiens and C. examine the pathways of mouthpart evolution in the context hispanicus individuals with retracted and extended probos- of nectar feeding. We focus on a comparative functional cides. The mechanism of glossal movements was studied in anatomy of the glossa in Masarini since in some genera it is thawed specimens of freeze-killed C. hispanicus and in relatively short yet retractable while in others it is extremely freshly collected C. lusitanicus, C. hispanicus and C. long. We delineate several morphological innovations fonscolombei. which are important for the formation and functioning of For viewing in the scanning electron microscope (SEM), a suctorial proboscis, in addition to discussing further fixed samples of P. decipiens, C. hispanicus, C. peliostomi evolutionary aspects of the proboscis in Hymenoptera. and Quartinioides sp. were dehydrated in ethanol and submerged in hexamethyldisilazane prior to air drying (Bock, 1987). A graphite adhesive tape was used to mount 2. Material and methods them on SEM viewing stubs. The samples were sputter- coated with gold and viewed in a Jeol JSM-35 CF SEM. 2.1. Field observation Flower visiting behavior and water uptake were observed 3. Results in Ceramius fonscolombei Latreille, C. hispanicus Dusmet, C. lusitanicus Klug in Spain (Arago´n, Province Teruel: Barranco de Zorita, 19–26 June 1998; north of Almohaja, 3.1. Flower visiting behavior 16–18 June 1998; east of Los Iban˜ez, 7–12 June 2000; Rambla de Rio Seco, west of Valdecebro, 9–16 June 2000) The behavioral pattern exhibited by Ceramius on flowers and in C. tuberculifer Saussure in France (Alpes-de-Haute- differed according to the shape of the flower and whether Provence: Peyresq 19–28 July 1994; Montagne de Boules pollen or nectar was collected. On flowers with exposed 26–29 July 1994) in part with the aid of close-up binoculars anthers [Helianthemum spec. (Cistaceae) (C. lusitanicus and and documented by macro-photography (scale 1:1). C. hispanicus ); Reseda spec. (Resedaceae) (C. fonscolom- bei )] females primarily harvested pollen directly (Fig. 2), 2.2. Morphology their mandibles clasped and nibbled the anthers; their maxillae were visibly active during ingestion of the The mouthparts of females were examined using light loosened pollen. The proboscis was never extended. Pollen microscopy in Priscomasaris namibiensis Gess (Priscoma- uptake at zygomorphic flowers with hidden anthers (Lotus sarina), Paragia decipiens Shuckard (Paragiina), Ceramius corniculatus L. (Fabaceae) (C. hispanicus ); Dorycnium hispanicus and C. fonscolombei which are considered to be hirsutum (L.) Ser. (Fabaceae) (C. lusitanicus ); Teucrium basal representatives of Masarina, and several higher montanum L. (Lamiaceae) (C. tuberculifer )) was indirect; Masarina, i.e. Masarina familiaris Richards, Jugurtia pollen was brushed from the anthers or from parts of the H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 105 Figs. 2 and 3. Fig. 2: Ceramius lusitanicus female collecting pollen with mandibles and maxillae at a flower of Helianthemum organifolium (Lam.) Pers. Fig. 3: C. hispanicus female imbibing water from moist soil with extended glossa (arrow). body and brought between the mouthparts by movements of their heads above the main body axis (Fig. 3). When the forelegs, the distal parts of which form pollen brushes. imbibing water the outer surface of the glossa appears to be Although nectar uptake is difficult to verify, it can be covered with adherent water which resulted in shiny supposed to occur at several zygomorphic flowers with a reflections. deep tubular corolla (Marrubium supinum
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