Research Article |
Corresponding author: Salvatore Bella ( salvatore.bella@crea.gov.it ) Academic editor: Michael Ohl
© 2021 Roberto Catania, Vittorio Nobile, Salvatore Bella.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Catania R, Nobile V, Bella S (2021) The species of Eucera Scopoli, subgenus Tetralonia Spinola from Sardinia (Italy) with new records and E. gennargentui sp. nov. (Hymenoptera, Apidae). Journal of Hymenoptera Research 88: 1-16. https://doi.org/10.3897/jhr.88.70819
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In this paper, an update of the species of the genus Eucera subgenus Tetralonia Spinola, 1838 from Sardinia is reported, based on data collection as well as on recent survey carried out at Gennargentu Massif. Seven species are recorded, four of which are newly added: Eucera fulvescens (Giraud, 1863), E. gennargentui sp. nov. Nobile, Catania & Bella, E. julliani (Pérez, 1879), and E. nana (Morawitz, 1873). The new species, Eucera (Tetralonia) gennargentui Nobile, Catania & Bella is described from the high altitude of Gennargentu Massif. Details on distributions, host plants, and other biological aspects are given for each species treated. The taxonomic comparison of the taxa belonging to the subgenus Tetralonia from Sardinia, including E. gennargentui sp. nov., are discussed taking into account both morphological and COI barcode sequences. An identification key to Eucera (Tetralonia) species from Sardinia is also provided.
Apidae, Eucera (Tetralonia), new taxon, Mediterranean bees, Sardinia
Belonging to the Eucerini tribe, Eucera Scopoli, 1770 is a genus of bees widespread in the world (
The subgenus Tetralonia includes different oligolectic species, some of them closely associated and specialised with plants of the Asteraceae family (
Eucera (Tetralonia) includes eleven species in Italy and some endemic subspecies of the main Italian islands, such as E. dentata amseli (Alfken, 1938) described from Sardinia and E. alticincta bindai (Nobile, 1993) described from Sicily (
To date, the knowledge on Sardinian bees is still limited, and only three species of Eucera (Tetralonia) are known: E. dentata amseli, E. graja (Eversmann, 1852) and E. malvae (Rossi, 1790) (
In this paper, we add a further four species of Eucera (Tetralonia) as new for Sardinia and describe a new endemic species E. gennargentui sp. nov. Nobile, Catania & Bella from Gennargentu Massif, based on both morphological and molecular data.
The material examined belongs partly to the collection of Vittorio Nobile and partly comes from field collecting efforts carried out by the two other authors in Sardinia during the year 2020.
Species identification was based on the works of
Observations in the field on Eucera gennargentui sp. nov. were made in the first week of August 2020 in the locality of Bruncu Spina, near the town of Fonni (40°01'48.0"N, 9°17'56.6"E), in the central area of Gennargentu Massif, at 1540 m a.s.l., characterized by several endemic high mountain species plants (
Gennargentu Massif is located near the centre of the island, almost directly at 40° N. Bruncu Spina, at 1829 m a.s.l., is the second highest mountain in Sardinia, after Punta La Marmora (1834 m a.s.l.), and is the northernmost summit of the main Gennargentu ridge.
In order to collect biological data on the new taxon, some specimens were marked using a dye specific to bees. The date of capture, general and Italian distribution, number of specimens observed, and the plants visited are reported for all species.
Each specimen was killed by freezing at -20 °C for use in DNA analysis and was dried and identified to species level after the observation of genital structures. The specimens were preserved in the collection of the authors, and in the collection of the Department of Agriculture, Food and Environment, sect. Applied Entomology, University of Catania (Di3A).
The specimens were studied with a stereomicroscope Leica EZ4HD, the photos taken with a Leica Application Suite vs. 4.13.
Total DNA was extracted from one posterior leg using the NucleoSpin Tissue Kit (Macherey-Nagel, Germany) following the manufacturer’s instructions. Subsequently, the enzymatic amplification took place using primers LCO1490F and HC02198R (
The sequences were aligned with seven COI sequences of Eucera (Tetralonia) available in GenBank, and we also included two sequences of Habropoda tarsata (Spinola, 1838) (accession numbers MN919536, MN919537) as an outgroup (Table
Species | Accession number | Country |
---|---|---|
Eucera alticincta alticincta | MNHNL005-20 | Luxembourg |
Eucera alticincta bindai | MZ437367 | Italy, Sicily |
Eucera dentata | FBAPD711-11 | Germany |
Eucera fulvescens | ABEE208-17 | Austria |
Eucera gennargentui sp. nov. | MZ437082 | Italy, Sardinia |
Eucera graja | MG251108 | - |
Eucera malvae | FBAPC604-11 | Germany |
Eucera nana | ABEE206-17 | Austria |
Eucera salicariae | FBAPC749-11 | Croatia |
Habropoda tarsata | MN919536 | Italy, Sicily |
Habropoda tarsata | MN919537 | Italy, Sicily |
Di3A Department of Agriculture, Food and Environment, Catania, Italy;
RC Roberto Catania, Catania, Italy;
SB Salvatore Bella, Catania, Italy;
VN Vittorio Nobile, Ragusa, Italy.
Genus Eucera Scopoli, 1770
Tetraloniella dentata amseli Alfken, 1938, Mem. Soc. Entomol. It., 16: 97–114.
• 1 ♀; Italy Sardinia, Iglesias, San Pietro (Cagliari province); 12.VII.1976.
Sardinia and Corsica.
Tetralonia fulvescens Giraud, 1863, Verh. zool.-bot. Ges. Wien, 13: 42–43.
• 1 ♀; Italy Sardinia, Busachi (Oristano province); 10.VI.1975; coll. C. Meloni – D. Sechi.
South Europe, North Africa, West and Central Asia (
This species is discontinuously present in the Italian peninsula and Sicily.
10 ♀, 1 ♂: Holotype: • 1 ♀; Italy, Sardinia, Fonni (Nuoro province), Gennargentu Massif, Bruncu Spina, 1540 m a.s.l.; 6–8.VIII.2020; S. Bella and R. Catania leg.; Di3A. Paratypes: • 9 ♀, 1 ♂; paratypes identical data to previous; Di3A, RC, VN, SB.
Female (Fig.
Male (Figs
The new species Eucera gennargentui, is similar to E. alticincta (Lepeletier, 1841), including the nominate subspecies and E. alticincta bindai.
In the female of E. gennargentui, the long fringes of the sternites are yellow-gold, whereas in the closest related species E. alticincta alticincta, they are white; the scopa is yellow-rust in the new species, whitish externally and brown internally in E. alticincta alticincta.
In the male of the new species, the long silky hairs of the mesosoma are whitish, while they are brownish-yellow in E. alticincta alticincta. Genitalia of E. gennargentui is very similar to that of E. alticincta alticincta, however, in the gonostylus the inward-facing triangular protuberance, that in E. alticincta is located in the middle part, in the new species is placed slightly over half of the gonostylus, slightly closer to the apex. Further differences can be noted in the morphology of the hidden sterna, especially for the medial and lateral processes in S7, and for apical lobes and apicomedian ventral process in S8.
In both sexes of the new species, the integument and wings are considerably darker than E. alticincta alticincta, and the body length of both sexes of E. gennargentui is greater than that of the related species.
Further morphological and bio-ecological comparisons between E. alticincta alticincta, E. alticincta bindai, and E. gennargentui are reported in Tables
Morphological comparison between Eucera gennargentui sp. nov. and the closest related taxa.
E. alticincta alticincta | E. alticincta bindai | E. gennargentui sp. nov. |
---|---|---|
Female | ||
1) slim overall appearance | 1) compact and robust overall appearance | 1) slim overall appearance |
2) mesosoma with sparse punctation | 2) mesosoma with dense punctation | 2) mesosoma with denser punctation |
3) metasoma ovoidal | 3) metasoma subspherical | 3) metasoma ovoidal |
4) 3° and 4° metasomal tergites with white, broad, median tomentose band, slightly narrowing in the middle | 4) 3° and 4° metasomal tergites with white, broad, median tomentose band, deeply narrowing in the middle | 4) 3° and 4° metasomal tergites with white, broad, median tomentose band, deeply narrowing in the middle |
5) white long fringes on the metasomal sternites | 5) white long fringes on the metasomal sternites | 5) yellow-gold long fringes on the metasomal sternites |
6) scopa whitish externally and brownish internally | 6) scopa whitish externally and yellowish internally | 6) yellow-rust scopa |
7) pigidial plate normally thinned | 7) less thinned pigidial plate | 7) pigidial plate normally thinned |
8) body length = 7 mm | 8) body length = 8 mm | 8) body length = 9–10 mm |
Male | ||
1) compact overall appearance | 1) less compact overall appearance | 1) less compact overall appearance |
2) brownish-yellow long silky mesosomal setae | 2) brownish-yellow long silky mesosomal setae | 2) whitish long silky mesosomal setae |
3) metasomal ovoidal (longer than wide) | 3) metasomal subspherical (as long as wide) | 3) metasomal ovoidal (longer than wide) |
4) 3° and 4° metasomal tergites with white, broad, median tomentose band, slightly narrowing in the middle | 4) 3° and 4° metasomal tergites with white, broad, median tomentose band, deeply narrowing in the middle | 4) 3° and 4° metasomal tergites with white, broad, median tomentose band, deeply narrowing in the middle |
5) 1° – 4° metasomal sternites distally with fringe of dense, bristly, short and protruding light ivory setae (more developed those on the 2° and 3°) | 5) 1° – 4° metasomal sternites without fringe | 5) 3° – 5° metasomal sternites distally with fringe of short and protruding yellow setae |
6) normal pigidial plate | 6) less wide pigidial plate | 6) normal pigidial plate |
7) body length = 8 mm | 7) body length = 7 mm | 7) body length = 9 mm |
Geographic and bio-ecological comparison between Eucera gennargentui sp. nov. and the closest related taxa.
E. alticincta alticincta | E. alticincta bindai | E. gennargentui sp. nov. |
---|---|---|
Distribution | ||
Widespread in Europe, North Africa, and western Asia ( |
Sicily (Nobile, 1987; 1993), Nebrodi Mts (Messina province), northern slope of Mt Etna (RC, pers. observ.), and Syracuse province | Central Sardinia, Gennargentu Massif |
Host plants | ||
oligolectic on Inula and Pulicaria (Tkalcu, 1979; Müller, 2008) | observed on Pulicaria (RC, pers. observ.) | oligolectic on Carlina, Helichrysum, and Tanacetum |
Environments | ||
Temperate and Mediterranean | Mediterranean and Mediterranean mountains (100 – 1350 m a.s.l.) | Mediterranean high mountains (1540 m a.s.l.) |
Phenology (generation and months) | ||
probably univoltine; VII-VIII | probably univoltine; VIII-IX | probably univoltine; VIII |
We named the new species after Gennargentu Massif, where the specimens were found.
Sardinia (Italy).
Specimens of the new taxon were observed on Carlina macrocephala subsp. macrocephala, Tanacetum audibertii (Req.) DC. (Sardo-Corsican endemisms), and Helichrysum saxatile subsp. saxatile (Sardinian endemism) (Asteraceae) (Fig.
A total of 22 specimens (half captured and half marked) were observed in the sampling site: 20 females and 2 males. Specimens of E. gennargentui were observed in activity in a restricted area of about 300 m2, from 10:30 to 15:00; in particular, the females visited the flowers from 10:30 to 14:30, and the two males were observed from 13:30 to 15:00 on Carlina macrocephala subsp. macrocephala. The female specimens visited the same flowers at intervals of about ten minutes, with a preference for the flowers of Carlina macrocephala subsp. macrocephala.
To know better the flights period of E. gennargentui, further surveys in the same site were conducted during mid-July 2021, however no specimens were found. This confirms the relationship between the new species and its main host plant, in fact Carlina macrocephala subsp. macrocephala was at the beginning of its flowering.
Macrocera graja Eversmann, 1852, Bull. soc. natural. Moscou. 25: 124.
South and Central Europe, and West Asia (Banaszak & Ortiz-Sànchez 1993).
This species is discontinuously present in the Italian peninsula, Sardinia and Sicily.
Macrocera julliani Pérez, 1879, Act. Soc. Linn., 33: 150.
• 1 ♀; Italy Sardinia, Assemini (Cagliari province); 3.IX.1990; L. Fancello leg. • 1 ♂; Sardinia, Rio Flumini Mannu (Cagliari province), 2.VII.1992; C. Meloni leg.; on Ammi visnaga (L.) Lam. (Apiaceae).
Turanic-South-European (
This species is discontinuously present in the Italian peninsula, and Sicily.
Apis malvae Rossi 1790, Fauna Etrusca II, p. 107.
• 1 ♀, 1 ♂; Italy Sardinia, Capoterra, Rio S. Lucia (Cagliari province); 4.VI.1985; C. Meloni leg.
Widespread in Europe, Eastern Mediterranean (Cyprus) and Western Asia (Turkey).
This species is discontinuously present in the Italian peninsula, and Sicily.
Tetralonia nana Morawitz, 1873, Horae soc. entom. Ross. X, p. 144.
• 1 ♀; Italy Sardinia, Teulada, Tuerru (South Sardinia province); 16.VII.1973; • 3 ♂♂; Sardinia, Rio Flumini Mannu (Cagliari province); 2.VII.1992; C. Meloni leg.; on Ammi visnaga (L.) Lam. (Apiaceae).
Widespread in Europe, and Western Asia (Turkey).
This species is known in the regions of
.New record for Sardinia.
Female:
1 | Clypeus more or less yellow | 2 |
– | Clypeus black | 5 |
2 | Antennae ventrally dark brown. 10,5–11,5 mm | E. dentata amseli |
– | Antennae ventrally light red, except for the scape and 1–2 flagellar articles that are black | 3 |
3 | Scopa dark brown externally and even darker internally. 12–14 mm | E. graja |
– | Different colour of the scopa, smaller body size | 4 |
4 | Scopa whitish externally and brown internally. 8–9 mm | E. julliani |
– | Scopa uniformly rusty-yellow. 9–10 mm | E. gennargentui sp. nov. |
5 | Orange scopa. 11–12 mm | E. fulvescens |
– | White or whitish scopa | 6 |
6 | Scopa with long, sparse, thin, and white setae. 8 mm | E. nana |
– | Scopa with long, sparse and whitish setae. 11–13 mm | E. malvae |
Male: | ||
1 | Antennae ventrally more or less dark brown | 2 |
– | Antennae ventrally light red except for the scape black | 5 |
2 | Labrum and clypeus yellow | 3 |
– | Labrum and the lower part of the clypeus yellow. 11–13 mm | E. malvae |
3 | T6 laterally with short and stocky teeth, one on each side, facing backwards. 8 mm | E. nana |
– | More tergites with teeth, larger body size | 4 |
4 | In addition to clypeus and labrum, the base of the mandibles is yellow, T 5–6 with short and stocky teeth. 10 mm | E. dentata amseli |
– | Mandibles black, T5–7 with slightly longer and sharper teeth. 11–12 mm | E. fulvescens |
5 | Clypeus, labrum, supraclypeal space and mandible yellow. 11–13 mm | E. graja |
– | Mandibles and supraclypeal space black | 6 |
6 | In the genital capsule the apex of the gonostylus facing inwards are almost straight. 9–10 mm | E. julliani |
– | In the genital capsule the apex of the gonostylus are remarkably arched. 9 mm | E. gennargentui sp. nov. |
High-quality DNA sequences were obtained for the two specimens analysed, one sequence of E. gennargentui sp. nov. from Sardinia (GenBank accession number MZ437082) and one of E. alticincta bindai from Sicily (1 ♀; Italy, Sicily, Mount Etna, Gurrida Lake, 25.VIII.2020 RC leg., det., and coll.) (GeneBank accession number MZ437367). Both COI sequences obtained from the samples were used as queries in BOLD-IDS tools, and the system returned a match (sequence of E. gennargentui: 97.88%; sequence of E. alticincta bindai: 98.77%) with a sequence of E. alticincta present in GenBank.
Sequence divergences calculated using the p-distance model are reported in Table
p-distance and nucleotide divergences (expressed as percentages) of Eucera gennargentui sp. nov., E. alticincta bindai, and Eucera (Tetralonia) species with Habropoda tarsata used as the outgroup. Average distance: 12.25.
1 | Eucera gennargentui sp. nov. | ||||||||||
2 | Eucera alticincta bindai | 2.21 | |||||||||
3 | Eucera alticincta alticincta | 2.08 | 1.21 | ||||||||
4 | Eucera fulvescens | 4.09 | 3.55 | 3.41 | |||||||
5 | Eucera graja | 7.65 | 7.31 | 7.47 | 7.47 | ||||||
6 | Eucera dentata | 8.34 | 8.0 | 8.05 | 8.68 | 8.34 | |||||
7 | Eucera salicariae | 7.30 | 6.95 | 6.68 | 6.82 | 7.65 | 8.20 | ||||
8 | Eucera nana | 7.69 | 8.84 | 8.07 | 8.84 | 9.61 | 8.84 | 6.92 | |||
9 | Eucera malvae | 7.82 | 8.0 | 8.51 | 7.44 | 6.43 | 8.81 | 6.38 | 6.92 | ||
10 | Habropoda tarsata MN919536 | 22.61 | 23.29 | 24.73 | 24.92 | 23.29 | 23.96 | 23.05 | 24.61 | 23.05 | |
11 | Habropoda tarsata MN919537 | 22.61 | 23.29 | 24.06 | 24.24 | 22.76 | 23.44 | 22.36 | 24.61 | 22.51 | 0 |
In the current study, Eucera fulvescens, E. julliani, and E. nana are reported for the first time for Sardinia, and E. gennargentui sp. nov. is described from Gennargentu Massif.
This new species shows a larger body size and a darker appearance than the closest related taxa E. alticincta alticincta and E. alticincta bindai, and other different characters reported in this work. Furthermore, following our field observations, we ascertained how the new species was linked to three Sardo-Corsican and Sardinian endemic botanical species of the flora of Gennargentu Massif.
The barcode sequence of the new species Eucera gennargentui diverged from that of E. alticincta alticincta from 2.08% and from that of E. alticincta bindai by 2.21%.
In Europe, wild bees are threatened by habitat changes resulting from human activities, e.g., urban exspansion, agricultural practices, habitat destruction or changes, and climate changing (
In Italy, the availability of information on bees is particularly scarce, especially in southern and insular regions, so it is important to increase research to better understand the distribution and the population tendencies, especially for localised taxa.
More observations are necessary to understand the conservation status of this new species and of the other Eucera (Tetralonia) species present in Sardinia. However, the area of Gennargentu where Eucera gennargentui was found is rather restricted and subject to disturbing factors due to strong grazing regimes and reckless reforestation that inexorably damage the grasslands where the endemic host plants live. The frequency of numerous fires that devastate natural ecosystems and rural areas in Sardinia (
The present study greatly improves the Sardinian bee fauna, showing that this Mediterranean island will surely deserves further new acquisitions, in order to increase our knowledge of its still underestimated pollinator fauna.
We thank Pietro Niolu (Alghero, Italy) for guiding us in the territory of Gennargentu Massif, and Silvia Di Silvestro (CREA, Acireale, Italy) for helping us in the genetic investigations. We also wish to thank the two reviewers, whose detailed comments and suggestions helped improve this manuscript.