Pollination Efficiency of Managed Bee Species (Apis mellifera and Bombus pauloensis) in Highbush Blueberry (Vaccinium corymbosum) Productivity

Bees are some of the most important insect pollinators. The evaluation of how different bee species select and use certain resources within their environment is important to understand fundamental ecological processes in agroecosystems (Gill et al. 2016; Campbell et al. 2018). In intensive agricultural areas, it has been documented that several species of wild bees are threatened and declining (Garibaldi et al. 2013; Cariveau & Winfree 2015). At the same time, the abundance of populations of managed honey bees (mostly Apis mellifera) decreases to provide services in crops with high dependence on entomophilic pollination (Agüero et al. 2018; Requier et al. 2018). Understanding how bees use the resources provided by crops of massive flowering is essential to develop meaningful agricultural management plans that both sustain bee populations and maximize the potential pollination service they may provide to farmers (Pasquet et al. 2008).

Vaccinium is a large genus of plants with many cultivated species. Blueberry (Vaccinium corymbosum L.) is a very important crop in Argentina, with more than 2700 ha cultivated. This intensive agricultural practice reduces the heterogeneity of habitats; it helps to create a large mass of homogeneous flowers and, consequently, rapidly changes the composition and diversity of pollinators (Steffan-Dewenter et al. 2005; Chacoff & Aizen 2006; Tylianakis et al. 2008).

Although some cultivars of blueberry are autogamous, cross-pollination is generally the rule. The bell-shaped pendant form of the flower discourages self-pollination via wind or gravity. Bee pollination is essential for a maximum blueberry production (Chiasson & Argall 1996) and honey bee, A. mellifera L., is the most widespread for blueberry pollination (Free 1993) as the introduction of honey bees’ hives in orchard significantly increases the production (Aras et al. 1996; Basualdo et al. 2007). On the other hand, bumblebees probably coevolved with similar-type vegetation (Heinrich 2004) and a reciprocal adaptation has made bumblebees ideal pollinators of blueberry (Desjardins & De Oliveira 2006). The bumblebee's behavioral characteristic is buzz pollination, which induces anther dehiscence, and consequently, the release of a large amount of pollen (Goulson 2010; De Luca & Vallejo-Marín 2013), and their foraging capacity in a wide range of ambient temperature (Goulson et al. 2010), makes it an effective blueberry pollinator (Buchmann 1983). Several papers have demonstrated the pollinating effectiveness of Bombus spp.; most of them are from cold temperate climate (Tuell et al. 2008; Stephen et al. 2009), but utilization of the neotropical species, Bombus pauloensis, for blueberry pollination has not been documented. Methods for rearing of this native species from South America have been developed and the use of B. pauloensis commercial colonies has been evaluated in Argentina for blueberry (Basualdo et al. 2013), strawberry, kiwi, and tomato pollination (Basualdo & Rodríguez 2009).

Recent studies have demonstrated that wild pollinators enhance fruit setting of crops, where managed pollinators such as honey bees or bumblebees are being used (Garibaldi et al. 2013; Milfont et al. 2013; Breeze et al. 2014). The contribution of wild pollinators would be valuable for blueberry pollination because plants bloom at the end of winter with low temperatures.

The objective of this work is to assess the effect of pollination carried out by B. pauloensis and A. mellifera on fruit formation and physicochemical characteristics that determine the quality of the V. corymbosum ‘Emerald’ fruit. In this context, we tested the prediction that pollinator assemblages with more species benefit V. corymbosum ‘Emerald’ production and the quality of fruit. We also elucidated the relationship between the frequency of visits (FVs) of each pollinator individually and the production, weight, seed number, and the internal quality of berries.

Our work evaluated an important aspect of blueberry production – influence of different types of pollination on fruit set and quality. This study highlights the issue of a necessity to introduce specific pollinators on blueberry plantations.

The results show that V. corymbosum ‘Emerald’ is highly dependent on entomophilous pollination for optimal production and producing high-quality fruits. Similar results were reported for the cultivars ‘Northland’ and ‘Patriot’ (MacKenzie 1997), where both honey bees and bumblebees could provide adequate pollination service. Fruit setting did not increase at open pollination with wild insect visitation. This result disagrees with the data obtained by Garibaldi et al. (2013), who concluded that fruit setting could be maximized by wild pollinators in crops such as blueberry and almond, which are stocked with high densities of honey bee colonies. In the pollination mediated by A. mellifera, the highest number of fruits was set, which agrees with the results of Sampson and Cane (2000) and Javorek et al. (2002), who reported high fruit production of rabbiteye and lowbush blueberry due to pollination by honey bees. These results can be attributed to the high FVs of honey bees (0.05 visits per flower per 5 min) in caged plots, grown in conditions with no competing flowers of other plant species and wild insects.

Although we did not quantify the pollen deposition in different treatments, we considered the number of seeds as an indirect estimator of reproductive success (Dafni 1992). The number of seeds and, consequently, reproductive success was the highest on open pollination plots, where there was a stronger influence of honey bee visitation (89%) and a lower proportion of wild pollinators. The combined action of pollinators improved pollen deposition on the stigmas, this agrees with the data reported for other crops (Garibaldi et al. 2013, 2017). Despite the fact that the FVs on open pollinated plants was much lower than those made by honey bees under cages, the seed production was ~27% higher, evidencing a synergistic interaction between honey bees and wild pollinators. Bumblebees are considered the most efficient pollinators of blueberry due to the fact that they generate buzz pollination, through which the pollen is released. This non-Apis population carries a high amount of pollen in its body (De Luca & Vallejo-Marín 2013) and could enhance pollen deposition on the stigmas. Even though the stocking rate of bumblebees used in our cage resulted in adequate fruit setting, colonies with more individuals could even improve the productivity.

Berries pollinated in open system had more seeds, lower soluble solids, and consequently, higher water content resulting in better firmness, that is a component of a good fruit quality. Apparently, the relationship between seed setting and water content of fruit is regulated by gibberellins; therefore, both adequate pollination and nutrition are very important for the quality of fruit (Cano-Medrano & Darnell 1997).

This is the first report of the useful service of B. pauloensis in blueberry pollination. The use of native bees is relevant, since in some South American countries such as Chile, exotic bumblebee species such as Bombus ruderatus and Bombus terrestris were imported for commercial pollination; consequently, these species invaded Argentina, producing a considerable ecological impact on native bees (Morales 2007). Therefore, the incorporation of this native species would be an advantage, avoiding the use of invasive species and, furthermore, improving the productivity of V. corymbosum crops. Finally, we conclude that in the conditions of our trial, pollinator assemblages benefit some aspects of quality, but not the productivity of blueberries. Additional research is needed to understand interspecific behavioral relationships, such as competence or synergy, between A. mellifera and B. pauloensis in blueberry cultivation before incorporating them into blueberry production systems as an agent that provides an ecosystem service.