Abstract
Besides the wind, insects are the main pollinating agents and many of them are hymenopterans. However, among the 20,000 species of bees (Superfamily Apoidea), only a very restricted group has been domesticated for commercial crop pollination, including social and solitary species. The honey bee Apis mellifera L. has been the first domesticated pollinator species, anyway, many cultivated crops benefit largely from the activity of other pollinators, especially when honey bees cannot provide a sufficient pollination service. This occurrence is particularly frequent in crops blooming in early spring or in crops with flowers not enough attractive to honey bees, i.e. because of low nectar and pollen production or for particular flower shapes.
In addition to these ecological aspects, which are the result of a long history of coevolution between insects and flowers, modern agriculture and the well-known difficulties that honey bees are suffering of, create new concern that a general decline in the native pollinator populations will have unavoidable consequences on crop production due to insufficient pollination service. The most striking contradiction of the “industrial” extensive monocultures is that on one side they put in forth the need of enormous number of pollinators to satisfy the vast number of flowers contemporarily ready to be pollinated; on the other side, they cancel from the agroecosystem uncultivated meadows, edges and forests, which serve as refuge and conservation areas. The immediate repercussion on pollinating insects is the lack of continuity in blooms: on large areas, flowers are extremely abundant during the short blooming period of the main crops and nearly almost absent in the remaining part of their reproductive season (what is called “green desert”). In addition, very often a dramatic reduction of adequate nesting sites and materials may strongly limit the reproductive success, while, up today, the knowledge about the acute and chronic effects of pesticides on native bees is still insufficient.
Bettina Maccagnani – Scientific advisor for the Automobili Lamborghini project “Environmental Biomonitoring with Honey Bees: Science and Education”
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1 Working Mothers: This Makes the Difference
What makes the difference between solitary and social bees? Every female makes her own nest, and has her own brood to rear without the assistance from other females. This means that each female collects pollen, and the need of nectar is limited to the amount required to get enough energy for individual activities plus little amounts used to mix up the pollen for the brood (Ladurner et al. 1999). This biological trait has the direct consequence that solitary bees can profit also from flowers that are not particularly rich in nectar or in its sugar concentration, while they are much more interested in the pollen rewards offered by the flowers (Nepi et al. 2005).
The pollen collecting organs of the solitary bees can be very different from the well-known structures honey bees have on the hind legs, which build up a compact pollen mass around a spine, mixing a little nectar to the pollen in order to fix it (Fig. 1a-b). In Antophoridae bees, for example, the hind legs are covered by dense and long hairs which allows them to collect huge amounts of pollen (Fig. 2a and Fig. 3a-d). Megachilidae bees collect pollen through series of special hairs in the ventral part of the abdomen Fig. 3a-b; in (Fig. 1b, Fig. 3a-b); in other species hairs are distributed both in the legs and in the ventral parts of the abdomen and of the thorax. The most important difference with the pollen mass produced by honey bees and bumble bees is that the pollen remains dusty, and easily can detach from the body of the bee when passing from one flower to another. This morphological aspects plus the behavioural trait of landing on the reproductive organs in the central part of the flower (Fig. 5a-b) are present in many solitary bee species, which bring the collected pollen directly in contact with the stigmas. This increase the pollinating efficiency compared with the performance of the nectar foraging honeybees, which very often land on the petals, unless they are contemporarily collecting pollen and nectar, or in case of flower shapes that oblige them to land in the central part of the flower to reach the nectar (Fig. 6a-b) (Fig. 4).
Being a solitary bee species does not mean to be territorial: on the contrary, many species show gregarious nesting habits. In fact, if the site offers optimal nesting conditions, hundreds of nests of solitary bees can be established in a very restricted area. The nesting habits of solitary bee species can be very different, but three main groups can be described: species that dig nests in the soil (Fig. 7), species that nest in pre-existing cavities (Fig. 8a-b), mainly in the stem of plants or in cavities excavated by other insects (or in old house walls, in the modern age), species that excavate their nests in the wood (Fig. 9).
2 Which Bee for Which Crop
Many studies have been run in recent years to find out which pollinator features are to be considered to determine which pollinator species could be candidate for improving the pollination service of a certain crop (Cane 1997; Thomson 2001; Kevan and Phillips 2001; Cane and Tepedino 2001; Bosch and Kemp 2002; James and Pitts-Singer 2008). These features consider the ecological link between plant and insect, the synchronism between foraging activity and blooming period, between flower attractiveness and exploitation modalities put into effect by the insect (McGregor 1976; Buchmann 1983; Free 1993; Benedek and Nyeki 1996; Goodell and Thomson 1998; Javorek et al. 2002) (Table 1).
The degree of effective contact between the pollinating insect and the reproductive organs of the flower depends on these modalities, and also on the ratio between the size of the insect and the size of the flower (Figs. 10; 11a-b). The relative values of pollinators to crops depend on how much pollen they remove from anthers as well as how much they deposit on stigmas. According to Goodell and Thomson (1998) in a comparison on apple pollination efficacy, Apis workers and Bombus queens differ in both pollen deposition and removal because they frequently adopt different foraging behaviors. Nectar-collecting Apis removed fewer pollen grains from the anthers of cv Delicious than did nectar- and pollen-collecting Bombus. As these differences are part of the complex reproductive strategy of entomophilous flowered plants, they are applicable to all the other crop/pollinator species comparisons (Kendall 1973; Kendall and Solomon 1973; Harder and Thomson 1989; Harder and Wilson 1998; Thomson and Thomson 1999).
Many studies have been published on the potential pollinating efficiency of native solitary bees on several crops (Willians 2002; Shuler et al. 2005; Klein et al. 2007) which undoubtedly and essentially contribute to maintain an unwavering background ecosystem service of crop pollination. The populations of wild bees can be very abundant if sufficiently large conservation areas are preserved (Kremen et al. 2004; Potts et al. 2010; Abrol 2011).
In some cases, effective and manageable native solitary bees were identified. For example, in US, the squash bee Peponapis pruinosa Say is a very effective pollinator of Cucurbita pepo (Tepedino 1981; Artz and Nault 2011), while the southeastern blueberry bee, Habropoda laboriosa (Fabricius) can very well compensate for inadequate honey bee pollination the rabbiteye blueberry, Vaccinium ashei; on this crop, a new adaptable pollinator Osmia ribifloris Cockerell was successfully reared and used in captivity (Sampson and Cane 2000). Despite the high number of crop-pollinator interactions studied with the aim of highlighting how effective pollinators can maximize crop yield, only few native bee species are commercially available. This discrepancy is due to some limiting factors, related to the possibility to develop a mass reared populations of pollinators: the number of reproductive cycles completed by the insect in one year, the duration of the diapause, the adaptability to artificial nesting sites, the gregariousness degree during nesting (Kevan and Phillips 2001; Cane and Tepedino 2001; Cane 2008). On the basis of these criteria, several authors give indications on how to re-establish a numerically adequate population of the pollinating insect in the cultivated area (Bosch and Kemp 2001; Kevan and Phillips 2001).
Up today among the few reared solitary bee species present in North America, the alfalfa leaf-cutter bee Megachile rotundata Fabricius (Pitts-Singer and Cane 2011), the blue orchard bee Osmia lignaria Say and the alkali bee Nomia melanderi Cockerell (Cane 2008) are commercially available on the large scale, or can be reared by the growers themselves. Osmia cornifrons (Radzowski) has been managed in Japan for apple pollination since the 1940s (McKinney and Park 2012), and is used also in Korea and China (Da-Yong and Long-Shi 2007; Lee et al. 2008); it was introduced into the United States for pollination in 1977. In Australia, a promising study on tomatoes pollination in greenhouses has been performed by rearing the blue banded bee, Amegilla chlorocyanea Cockerell on artificial substrates in captivity (Hoogendorn et al. 2007) (www.beaware.org.au; http://www.aussiebee.com.au). In Europe, O. rufa L. (syn. O. bicornis) and O. cornuta Latreille are reared and used for orchard pollination and seed productions (Pinzauti et al. 1997; Ladurner et al. 2002; Maccagnani et al. 2003a, b; Krunic et al. 2005; Gruber et al. 2011).
3 Solitary Bees: A Focus on Osmia sp.
The genus Osmia Panzer (Hymenoptera Megachilidae) comprises 300 species (Michener 2000). Among those already commercially available as crop pollinators, O. cornuta, O. rufa and O. cornifrons are Palearctic species; O. cornuta (Fig. 12) occurs in Central and Southern Europe, Turkey and Northern Africa; O. rufa (Fig. 13) shows a more Northern distribution, while O. cornifrons (Fig. 14) is native from Japan. O. lignaria (Fig. 15), with different subspecies, is a Nearctic species, widely distributed in the U.S., where also O. cornuta has been introduced in the late eighties for almond and apple pollination, and is now established (Torchio and Asensio 1985; Vicens and Bosch 2000).
Osmia species show gregarious nesting behavior and build their nests in pre-existing cavities (Fig. 16), where the female produces a linear series of cells divided by mud walls (Tasei 1973; Peters 1977) (Fig. 17).This is why they are called generically “mason bees”; in each pedotrophic cell, one egg is laid on a nectar-pollen based mixture (Nepi et al. 2005) which the five larval instars will grow on.
Concerning the relationship with the plant food source exploited, Osmia species are oligolectic or polylectic, and for many of them the timing of the life cycle is related to the flowering of the Rosaceae botanical family (Márquez et al. 1994), whose pollen is highly preferred in comparison to others (Tasei 1973; Márquez et al. 1994; Maccagnani et al. 2003a, b). Their efficiency as pollinators, which has been compared to that one of honey bees by many authors (Bosch 1994; Monzon et al. 2004; Maccagnani et al. 2003a, b) is due to several eco-ethological traits. The most noticeable trait is that their foraging activity is mainly oriented to collect pollen, and in this aspect Osmia species are substantially different from honeybees. In fact, the flower visit performed by honeybees in search of nectar implies a limited contact with the reproductive parts of the flowers, as foragers land very often on petals than elongate the proboscis towards the nectaries, at the base of the stamens (Barth 1985; Free 1993, Fig. 9). Instead, mason bees are “top-foragers” and collect the pollen with their ventral abdominal sets of hairs, using either the forelegs or the abdomen to scratch the anthers, according to the flower morphology (Tasei 1973). Direct observations of O. cornuta foraging on apple flowers showed that all visits are performed landing on the flower reproductive organs to collect pollen from the anthers, contemporarily feeding a small amount of nectar, which is possible thanks to a much longer tongue with respect to honey bees (personal observations). The dimensions, the kind of approach to the flower and the efficiency of the ventral scopa allow Osmia species to collect the pollen with quick and effective movements, ensuring, at the same time, very fast flower handling and high pollinating efficiency, thus reaching also 100% flower pollination (Bosch and Blas 1994; Maeta 1978; Vicens and Bosch 2000). In fact, the number of pollen granules transferred to the stigma by mason bees is much higher with respect to the honeybees, which transport the collected pollen with the hindlegs, a modality that prevent any direct contact between the collected granules and the reproductive flower organs (Harder and Wilson 1998). Pinzauti (2001) demonstrated in Osmia that the pollen germination potential is conserved until the deposition of the mass in the larval cell. In fact, only in this moment the female adds to the discharged pollen little drop of stomodeal content, composed by nectar with the addition of glandular secretions that, someway, reduces the pollen viability (Nepi et al. 2005).
Osmia species have been assessed for crop pollination in different countries, both in open field on fruit trees like almond, apricot and apple (Bosch 1994; Bosch and Blas 1994; Krunic et al. 1995; Pinzauti et al. 1997) and in confined environments (Ladurner et al. 2002; Felicioli and Pinzauti 2008). Excellent results were obtained using O. cornuta for pear pollination (Maccagnani et al. 2003a, b, 2007; Monzon et al. 2004). Vicens and Bosch (2000) found that this species is a more efficient pollinator on almond and apple flowers than A. mellifera, because of its higher rate of stigma contact. Mason bees move from tree to tree more readily than honey bees, are less prone to orient along rows, thus enhancing cross pollination. Moreover, O. cornuta can adapt to a number of artificial nesting materials: another important aspect for the development of a pollinator management system (Krunic et al. 1995; Bosch 1995; Bosch and Kemp 2002).
4 Osmia cornuta
Osmia cornuta is an obligate monovoltine species distributed in the South-Central Europe and in Northern Africa, and is a highly gregrarious nesting species.
Females emerge from cocoons in March (some variations depend on the latitude), and the nesting period is concluded within 1 month. In natural environments, nests are constructed in broken giant cane stems (Arundo donax L.), but females easily accept many different substrates if dimensions are appropriated (8–10 mm diameter). Visual stimula are very important for the females to orient their choice during the search for a suitable place to nest. Osmia cornuta showes no difference in visual perception and colour discrimination ability when compared to honey bees (Menzel et al. 1988). Thus, every dark point visible from the distance is explored. In its lifetime, the female lays around 30 eggs, producing, on average, one cell per day (Tasei 1973; Krunic et al. 2005). The pollen is collected and transported on the abdomen, thanks to a ventral hairy structure named scopa (Fig. 8). Upon return to her nest from a foraging flight, the female compacts the pollen discharged during the previous flight by using the head and the frontlegs, and while doing this, she deposits drops of stomodeal content on the pollen mass. Then, she turns back within the nest and discharges the new pollen load. When the diameter is too small, the female gets out, turn back at the nest entrance, and reach the provision walking backwards.
Nepi et al. (2005) hypothesized that adding stomodeal regurgitation (plus glandular secretions?) to the pollen, to prepare the provision the larva will feed on, may serve to initiate germination or pseudo-germination. Pollen grains are probably the most difficult food from which nutrients can be obtained, because the pollen walls are among the hardiest structures in the biological world. Thus, pollen feeding animals have evolved different and complicated mechanisms to obtain the nutrients and the energy stored in the pollen cytoplasm (Roulston and Cane 2000; Nepi et al. 2005). The morphological and biochemical changes occurring in O. cornuta pollen provisions might be necessary for “activating” the pollen grains for the digestive process. Other active substances could play a role in the pollen digestion process in the solitary bee larvae, such as mother-derived secretions produced by the female and added to the provision (Ladurner et al. 1999; Heroin-Delauney 1966).
It is worthwhile to point out that solitary bee larvae feed directly on the mother provision, and this makes a big difference with respect to the social species like Bombus terrestris, in which adult workers contribute to larval nutrition pre-digesting the pollen (Ribeiro et al. 1999; Pereboom 2000), and A. mellifera, in which nurse bees feed the larvae with a glandular secretion after having themselves eaten and digested the pollen (Roulston and Cane 2000). The possible role of commensalistic microbial fauna of the larval cell in inducing biochemical changes in pollen-nectar provision remains to be investigated.
The energetic investment in the two sexes is quite different, as female cocoons weight, on average, around 0.4–0.5 g while male cocoons only 0.2 g (Bosch 1994; Maccagnani et al. 2007). As a result, a sex-dipendent dimorphism is considerably high in O. cornuta, and implies a much stronger foranging effort to produce female cell provisions than to produce males. Coherently, the female progeny originated from fertilized (diploid) eggs is produced at the beginning of the nesting period, when the mother female is at her maximum efficiency, while males are produced at the end, from unfertilized eggs. The pre-imaginal development lasts several weeks, and go through five moults, the first occurring within the egg. The first larva that can be observed feeding on cell provision is the second stage larva,; the following larval stages consume the provision in a few weeks. Than the fifth instar larva spin its cocoons, overpass the summer, and undergo the methamorphosis into adult before Autumn. Overwintering occurs as adult in the cocoon.
In the sister species O. lignaria, Sgolastra et al. (2011, 2012) found that adult eclosion follows the end of the summer diapause occurred during the prepupal stage; few weeks later, the adults lower their respiration rates (to ∼0.1 ml/g h) and undergo the winter diapause, that lasts until February–March, depending on the latitude. Winter diapause development in Osmia spp. occur in two phases. In the first phase, cold temperatures are required to increase the respiration response, which reaches a plateau in mid-winter. In the second phase, the respiration response follows an exponential increase, and when it has reached 0.45 ml/g/h the adult emerge promptly when exposed to 20°C, indicating diapause completion (Sgolastra et al. 2010).
In O. bicornis, a study by Wasielewski et al. (2013) found a complex dynamic of different energetic resources and enzymes that could explain the changes in the respiratory trends.
As each female can occupy simultaneously more cavities, and female eggs are layed at the beginning of the nesting period, female cocoons are generally found at the bottom of the cavity, while male cocoons occupy the front part of it. This behaviour has the biological significance of inducing a pronounced proterandry, resulting in the activation of males some days before females (likely related to the warmer temperatures in the front portion of the nesting tunnels, and to a higher oxigen diffusion, in comparison to the adults overwintering in the bottom portion), and to protect the female progeny (half of the male progeny, sex-ratio ff:mm 1:2) by rearing females in the most protected part of the nest.
In the perspective of the use of solitary bees to enhance pollination, it has to be considered the time needed for adult diapause termination in early spring. This duration depends on overwintering conditions and on early spring weather conditions, mainly the mean daily temperature.
If the release of O. cornuta populations occurs at the beginning of crop flowering, females might not be “ready” for an efficient pollination service before the end of the flowering period. Early flowering crops with short flowering periods would profit from a good landscape management with the introduction of ecological infrastructures with nectariferous/polliniferous botanical species can support the bee population prior and after the blooming period of the target crop, thus enhancing both crop pollination and bee reproduction (Maccagnani et al. 2007).
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Acknowledgements
We wish to thank Alessandra Montanari who made the drawing in Fig. 1, and Antonio Marzocchi for the pictures 1B-13 and 16–17.
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Maccagnani, B., Sgolastra, F. (2020). Solitary Bees As Pollinators. In: Smagghe, G., Boecking, O., Maccagnani, B., Mänd, M., Kevan, P. (eds) Entomovectoring for Precision Biocontrol and Enhanced Pollination of Crops. Springer, Cham. https://doi.org/10.1007/978-3-030-18917-4_4
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