Twenty New Records of Bees (Hymenoptera, Apoidea) for Sardinia (Italy)

Simple Summary Recently, several studies have highlighted the global decline of pollinators. This has increased concern for the long-term sustainability of plant biodiversity, food production, human nutrition, and human well-being. In Europe, approximately 40% of bee species are threatened in some countries. The Mediterranean Basin is one of the richest areas of diversity of wild bees. Sardinia, the second largest island in the basin, has a flora and fauna with many endemic taxa. Until recently, a number of 316 species of bees was reported on the island. However, the identification of the bee fauna of Sardinia still remains incomplete compared to other islands of the Mediterranean Basin, such as Sicily, Malta, Cyprus, and the Balearic Islands. It is very important to know and protect the potentially rich bee biodiversity of Sardinia, considering that the different factors that now threaten wild pollinators in Europe could lead to its impairment. This paper reports 20 new records of bee species from Sardinia based on observations made in different coastal and mountain ecosystems of the island. These findings contribute to the knowledge of the systematics and distribution of the Sardinian bee fauna. Abstract In Sardinia, the second largest Mediterranean island, 316 species of bees are known. Here, for the first time, the following 20 taxa are reported: Colletes cunicularius (Linnaeus, 1761), and C. eous Morice, 1904 (Colletidae); Andrena humilis Imhoff, 1832, A. granulosa Pérez, 1902, A. cineraria (Linnaeus, 1758), A. pallitarsis Pérez, 1903, A. rugulosa Stöckhert, 1935, A. savignyi Spinola, 1838, and A. tenuistriata Pérez, 1895 (Andrenidae); Sphecodes reticulatus Thomson, 1870 (Halictidae); Lithurgus tibialis Morawitz, 1875, Chelostoma emarginatum (Nylander, 1856), Dioxys cinctus (Jurine, 1807), Coelioxys caudatus Spinola, 1838, C. obtusus Pérez, 1884, and Megachile ericetorum (Lepeletier, 1841) (Megachilidae); and Nomada melathoracica Imhoff, 1834, N. pulchra Arnold, 1888, Eucera proxima Morawitz, 1875 and Tetralonia malvae (Rossi, 1790) (Apidae). N. pulchra is reported for the first time in Italy.


Introduction
One of the major hotspots for plant and animal diversity in Europe and the world is the Mediterranean Basin, which is characterized by a high incidence of endemic entities (species or subspecies) [1] and is one of the richest areas of diversity of wild bees (Hymenoptera, Apoidea) [2][3][4]. Recently, several reviews have highlighted the global decline of insects [5,6] including pollinators [7][8][9]. This has increased concern for the long-term sustainability of plant biodiversity, food production, human nutrition, and human well-being. The International Union for Conservation of Nature and Natural Resources (IUCN) European Red List for bees shows that 37% of bee species suffer from declining populations. Approximately 9% of all bees and 26% of bumblebees are classified as threatened, whereas 57% of bee species could not be assessed because of insufficient data [3]. In some cases, national Red Lists in Europe indicate that approximately up to 40% of bee species are threatened [9].
Probably the most important role of bees for humans is the pollination of wild plants with respect to the pollination of crops. Because most plant species are pollinated by insects, especially bees, the conservation of many habitats depends on their preservation. This is particularly important for wild species, many of which are pollen specialists on certain kinds of flowers, often with a strong preference for a given species. Hence, it is important to investigate wild bees in a certain region, in order to prevent their reduction due to the destruction of natural habitats or food competition with honey bees, especially when hive density is high.
In the Mediterranean Basin, Sardinia is the second largest island after Sicily, with a surface of 24,089 km 2 . Sardinia shows unique flora and fauna characteristics related to paleogeographic connections with other Mediterranean cross-border regions [10]. It is located between 38 • 51 52 and 41 • 15 42 N latitude and between 8 • 8 and 9 • 50 E longitude, in the centre of the Western Mediterranean, neighbouring Corsica, about 300 km from the Ligurian and Provence coasts, 200 km from the Latium and Tunisian coasts, and 300 km from Sicily and the Balearic Islands [10,11]. The flora and fauna of the island are characterized by the presence of many peculiar species, with some endemic taxa shared with Corsica or other regions, including several species with a very restricted range. For example, the Sardinian Maghrebine, Sardinian Corsican, or Western Mediterranean areas have species such as Anthophora nigrovittata Dours, 1869, Bombus ruderatus sardiniensis Tournier, 1890, B. terrestris sassaricus Tournier, 1890, Epeolus compar Alfken, 1938, Panurgus corsicus Warncke, 1972, and Tetraloniella dentata amseli Alfken, 1938. Several authors have studied Sardinian bees and other Hymenoptera Aculeata in the last century [12][13][14][15][16][17][18][19], and others have studied the ecological aspects of Apis mellifera L. and other pollinators [20,21]. To date, 316 species of bees are reported in Sardinia [22].
In the last decade, numerous studies on bees have been conducted in different islands of the Mediterranean Basin, such as Sicily [23][24][25][26][27][28], Malta [29,30], Cyprus [31], and the Balearic Islands [32]. However, the bee fauna of Sardinia still remains incomplete. Apart from some reports, such as Lasioglossum zonulum (Smith, 1848), Sphecodes ferruginatus von Hagens, 1882, and Nomada corcyraea Schmiedecknecht, 1882 [23,24], Osmia spinulosa (Kirby, 1802), and a newly described species, Hoplitis occidentalis Müller, 2012 [33,34], there is a lack of studies on the systematics, distribution, population trends, and ecology of bees in Sardinia [3,35]. It is very important to know and protect the potentially rich bee biodiversity of Sardinia before the different factors that now threaten wild pollinators in Europe could lead to its impairment. This paper, in which 20 new records of bees are reported for Sardinia, following observations made in different coastal and mountain ecosystems, represents a first attempt to collect more information about bee biodiversity on the island.

Materials and Methods
Sardinia is included in the Mediterranean biogeographical region and is, therefore, only marginally composed of habitats characteristic of the continental region and, even less so, of the Alpine region. Some habitats of the island are indicated as priority in Natura 2000. Coordinates of the sampling sites as well as the location, mapping, and European classification of the habitats studied are shown in Figures 1 and 2. The sampling sites represent various natural and anthropized habitats located in the main districts (i.e., Cagliari, Nuoro, Oristano, and Sassari) of the island. As an example, two sites representing a typical semi-natural area and a semi-intensive farming system of northern Sardinia, the area studied the most in this survey, are shown in Figure 3.
classification of the habitats studied are shown in Figures 1 and 2. The sampling sites represent various natural and anthropized habitats located in the main districts (i.e., Cagliari, Nuoro, Oristano, and Sassari) of the island. As an example, two sites representing a typical semi-natural area and a semi-intensive farming system of northern Sardinia, the area studied the most in this survey, are shown in Figure 3.
The surveys were conducted during the last decade, specifically by one of the authors (P.N.), in 20 natural sites, characterized by diverse altitudes, from sea level to 516 m a.s.l., and by different climatic and vegetational conditions, as follows:   classification of the habitats studied are shown in Figures 1 and 2. The sampling sites represent various natural and anthropized habitats located in the main districts (i.e., Cagliari, Nuoro, Oristano, and Sassari) of the island. As an example, two sites representing a typical semi-natural area and a semi-intensive farming system of northern Sardinia, the area studied the most in this survey, are shown in Figure 3.
The surveys were conducted during the last decade, specifically by one of the authors (P.N.), in 20 natural sites, characterized by diverse altitudes, from sea level to 516 m a.s.l., and by different climatic and vegetational conditions, as follows:   [36,37] and sampling sites ( ) where the new Apoidea were recorded. Figure 2. Mapping of habitats present in Sardinia [36,37] and sampling sites ( classification of the habitats studied are shown in Figures 1 and 2. The sampling sites represent various natural and anthropized habitats located in the main districts (i.e., Cagliari, Nuoro, Oristano, and Sassari) of the island. As an example, two sites representing a typical semi-natural area and a semi-intensive farming system of northern Sardinia, the area studied the most in this survey, are shown in Figure 3.
The surveys were conducted during the last decade, specifically by one of the authors (P.N.), in 20 natural sites, characterized by diverse altitudes, from sea level to 516 m a.s.l., and by different climatic and vegetational conditions, as follows:     The surveys were conducted during the last decade, specifically by one of the authors (P.N.), in 20 natural sites, characterized by diverse altitudes, from sea level to 516 m a.s.l., and by different climatic and vegetational conditions, as follows: The distribution, locality and date of collection, number of specimens, visited plants, and collector are given for each bee species. Bees were collected mainly on flowers using a hand net. Sampling was carried out between 9:00 and 17:00. As reported in the text, some specimens came from previous samplings carried out during the second part of the 21th century. All specimens were prepared dry and identified through the observation of sexual structures.
Our specimens confirm the presence of the species on the island 78 years later.

Discussion
Currently, 316 species of bees are known in Sardinia [22]. Data on bees are lacking for most of the central and southern areas of the island, whereas much more data are available for the northwestern area of Sardinia. This was thanks to the work carried out by the Department of Agricultural Sciences of the University of Sassari, especially from 1997 to 2010, when a survey on wild pollinators was conducted, jointly with eight other research teams in Italy, using a unique scheme for monitoring the bee fauna [18]. The increased knowledge of this group of insects is of primary importance for knowing the local populations of pollinators of wild and cultivated plants [18,56]. In this context, studies have focused on the role of pollinators in certain agroecosystems or crops, such as the pollinators of white clover (Trifolium repens L.) in northern Sardinia [57], where the primary role of the wild bees belonging to Andrena, Megachile, and Osmia genera was evidenced.
A study [58] on the pollinating insects of Hedysarum coronarium L. in northern Sardinia reported a total of 18 wild bee species, among which Eucera numida Lep. visited the crop most actively, followed by the endemic Bombus subspecies (B. ruderatus sardiniensis and B. terrestris sassaricus), Osmia bicornis L., and Megachile parietina Geoffroy. A survey of bee fauna in two different agroecosystems (semi-intensive vs. extensive) located in northern Sardinia (Nurra) [21] evidenced 28 species belonging to the Andrenidae, Halictidae, Megachilidae, and Apidae families in the semi-intensive agroecosystem compared to 31 species in the extensive agroecosystem, which showed the same families plus Colletidae. The results indicate that agriculture intensification did not lead to a significant decrease in species richness. However, the Sorensen's community index showed a medium similarity between the insect composition of the two landscapes. The effect of agricultural intensification was particularly evident on Collectidae, Andrenidae, and Halictidae species that usually use the soil as nesting sites. In fact, these families were more represented in the extensive site, probably thanks to the minimum tillage and the wider availability of uncultivated zones compared to the semi-intensive area. On the contrary, the semi-intensive landscape had a higher number of Megachilidae and Apidae species recorded, compared to the extensive one, probably because of the presence of forage legume crops.
Understanding the diversity of pollinators in an insular context and how it can be preserved is an important step for better understanding the biodiversity of this fauna at the global level. In fact, the latter certainly requires more efforts to collect observational and experimental data, to monitor the situation, and to conduct detailed surveys to determine pollinator diversity and the threats behind their decline. In particular, in the islands, the pollinator diversity is the result of a long and diffuse coevolution with floral diversity and nest conditions, which lead, thanks to isolation, to speciation processes with richness of endemism.

Data Availability Statement:
The data presented in this study are available on request from the corresponding author.