Our results indicate that temperature might affect the frequency of bee visits to avocado flowers, with higher frequencies being related to higher temperatures in the Mediterranean region of Chile. Surprisingly, the frequency of bees in avocado flowers is not simply affected by the amount of open flowers. Accordingly, other intrinsic characteristics of the avocado flower or aspects related to the bees’ own sensitivity to cold weather could be more important variables affecting the visits. In fact, the temperature has been related to many physiological and morphological functions of the avocado flower. For example, avocado flowers are sensitive to cool temperatures, which can affect the temporal separation of male and female stages [40]. When air temperatures are below 20 °C, some overlapping of receptive stigmas and anther dehiscence occurs, which may lead to some pollination within an individual tree [33,34,35, 41]. Colder temperature also affects pollen tube growth, with 25 °C being the optimum temperature [34, 41, 42]. On the other hand, bees prefer to visit parts of the tree warmer and more exposed to sunlight, where also there is a greater number of flowers, and avoiding the shaded and colder parts [31]. Therefore, we assumed that the frequency of bees in avocado flowers is not directly affected by the amount of open flowers, but due to other morphological and physiological characteristics of the avocado flower or of the bees sensitive to the cold weather.
Apis mellifera is the only pollinator managed for commercial proposes in Chile. Indeed, the European honeybee plays a leading role in avocado pollination [8, 21]. Nonetheless, avocado flowers were also visited by the local bee community in Chile, some of which were frequent flower visitors (see also [30, 31]). However, there is no evidence supporting these native bees have specialized interactions with avocado crops. Contrariwise, these bees are considered polylectic, generalists visitors that collect pollen from both related and unrelated plant species, including natives and cultivated [43,43,44,45,47]. Therefore, it is likely that the floral visitors of avocado are shared with local native and cultivated vegetation. Consequently, the richness and abundance of bees that visit the avocado flowers are subject to the taxonomic composition, phenological fluctuations and floral morphophysiology of surrounding flowering plants, similarly to what occurs with honeybee [3, 15, 24,25,26].
Furthermore, honeybees and native bees were found to be equally fast at handling avocado flowers. Honeybees and the two most frequent native bees (Colletes cyanescens and Cadeguala occidentalis) fed on nectar and pollen in avocado flowers, however, visiting bees searched more for nectar than pollen. Many studies have suggested that nectar-feeding bees achieve more efficient pollination of avocado because they actively move between both male- and female-stage flowers, while pollen-gathering bees visit male-stage flowers more frequently [8, 21, 24, 30, 32];). Therefore, based on foraging behaviour, native species and honeybees can be equally probable pollinators of avocado plants.
However, there are few studies clarifying the role of native bee species in relation to exotic species in avocado pollination (e.g. [3, 30,31,32]). These studies consider honeybees and some native bees (not all) potentially efficient pollinators of this crop. However, other studies argue that the honeybees are the most frequent flower visitors (representing until 92.9% of all visits), usually carry avocado pollen on their body, and generally deposit intraspecific pollen in the stigmas [8, 48]. Because of that, honeybees are considered the most efficient pollinators. However, there are many more studies focusing only on the pollination effectiveness of honeybees than those that also include other local visitors. Therefore, it is still unclear whether native bees can function as supplementary or alternative pollinators when honeybee frequency reduces in flowers.
Moreover, particularities involving avocado pollination impose requirements to pollination studies. Avocado plants are characterized as having low fruit set, with values worldwide varying from 1 to 200 fruit per 100,000 flowers [10, 20, 21, 49]. Fruit set for the “Hass” cultivar in Chile can reach as low as 0.01%, or one fruit per 10,000 flowers [49]. Besides, the temporal separation of the sexes in flowers [12] requires additional attention by researchers, including cross-pollination treatments between plants in male and female stages. Due to this, pollination experiments (e.g., breeding system and fruit set, pollen flow, pollination effectiveness) on avocado require employing a huge amount of flowers to achieve a satisfactory number of samples and replicates. Despite these challenges, studies of pollination efficiency could reveal the role of Chilean native bees, in relation to exotics, in pollinating avocado flowers.