Ants, though sometimes help in pollinating flowers of some species28–31 have a complex interaction with the plants14. This interaction has a narrow cost-benefit border15. Invasive ants are particularly known to give an exploitative competition and predation pressure on foraging legitimate pollinators (see Sinu et al.18 and references therein). They predate on pollinators18 and decrease the chances of pollinator visit by exhausting the floral rewards32. There are quite a handful of studies exploring the impacts of invasive ants on pollinators. However, a comparison of invasive and native ants concerning their interaction with floral visitors are scarce15.
In this study, we attempted to explore the effects of ants on pollinators, as well as to compare these effects in cases of invasive and native ants. The study found that ants regardless of the nativity gave a competitive pressure for honeybees in pumpkin flowers. Both the visitation rate and the duration they spent foraging floral resources was significantly low in ant-infested flowers. Although the bees tend to spend more time on native-ant occupied flowers, when the number of ants is high, they avoid such flowers.
With its showy flowers with a reasonable amount of floral rewards in the form of both pollen and nectar, pumpkin (Cucurbita maxima) is a noteworthy lure for both ants and bees. We found that ants occupied more than 75% of the flowers during the early hours of anthesis in different fields. The ratio of staminate flowers to pistillate flowers counted in our study agrees that the number of staminate flowers is mostly higher in a field25,33,34. As the nectar amount varies between the staminate and pistillate flowers, this might be a major determinant of ant infestation of flowers. This is a possible justification of why a larger margin of pistillate flowers was found to be occupied by ants than staminate flowers.
Ants generally repel pollinators by its aggressive nature35. Sometimes, the pollinator might choose not to enter a flower due to the presence of ants18. The scent of ants negatively influences the choice of pollinator’s entry into flower21. In our study, we found that the pollinator entry was significantly lower in the case of ant-occupied flowers. We also observed several cases of hovering, wherein the bee hovered around the flower or landed on petals but flew off. The bees in such cases avoided contact with ants and did not touch the reproductive structures of the flower. This may be a huge loss for the plant as pollination is likely to be directly affected. The pollination frequency was also significantly lowered in case of ant-occupied flowers18. Some studies suggest that the pollinator might frequently reposition in ant-occupied flower, and have more pollen deposited on them, which might increase the seed set15. Although there were cases of predation attack by yellow crazy ants previously18, we found the native ant, Diacamma sp. was opportunistically predating upon honey bees in the present study. The duration of each visit was also significantly higher in the case of an antless flower. This is an indication of direct interference competition that ants offer to the pollinators. The duration of the visit was significantly lower in the case of Solenopsis geminata and Tetramorium sp. The presence of sting could be a possible defence to drive off pollinators. Although there were other ants with a sting, only these two stinged ants occupied a considerable number of flowers to draw a possible conclusion.
There are several cases of ant-pollinated plants. In the Western Ghats, ants were recently reported as a pollinator of Syzigium occidentale plant inflorescence29. In the Atlantic rainforest system, ants have been found to be a major pollinator of aggregated inflorescence28. Though there is a possibility that ants might pollinate pumpkin, it will have to be tested through a seed set experiment to be certain. During our observation, we did find some amount of pollen sticking onto the ants. However, as most of the characters of pumpkin flower did not resonate with the characters of ant pollinated flowers18,36, ants might not play a major role in the pollination of pumpkin flowers. Additionally, exposing flower to ant secretions seems to deter viability. When subjected to ant secretions, the pollen vitality, the germination rate and the length of pollen tubes significantly reduced37. While they feed nectar, ants sometimes damage the base of pistil affecting the seed set38. Although ant-visited or pollinated flowers are not rare in tropics29,39 they are mostly bisexual and have either generalist pollination syndrome or have no bee pollinators on them. Pumpkin is a major floral resource for specialist bees including honey bees, bumblebees, and squash bees, which perform cross-pollination in their monoecious flowers. Because they are monoecious, the visitors should travel from staminate to pistillate flowers for effecting pollination. It is very unlikely that the ants switch visits between staminate and pistillate flowers in pumpkin fields as staminate flowers are abundant and pistillate flowers are not necessarily to be closer to staminate flowers. Although not investigated on all the nine species of ants in this study, Sinu et al. (2017)18 found that none of the A. gracilipes visited flowers sets fruits.
The efficiency with which ants used up resources determined the exploitation competition offered by ants to the pollinators. The main parameters of the ants that we used to measure this were the number of individuals that occupy a single flower and the number of flowers occupied by a single species of ant. S. geminata was found with the highest number of individuals per single flower. This mass recruitment, although not particularly common in S. geminata is a key character of invasive ants23. Similarly, invasive ants, in general, had a higher number of individuals recruited to a single flower compared to the native ants. The black crazy ant, P. longicornis occupied the highest number of flowers. This implies that they are highly efficient in locating resources. P. longicornis has a complicated modular recruitment system as well as polydymous nesting23,40. This minimises the distance between the nest and food resource and increases their foraging efficiency. The other globally-important invasive species colonized in pumpkin flowers, A. gracilipes, is also known to make supercolonies and exploit resources quickly41. Thus, invasive ants exerted a higher exploitation competition on pollinators than native ants. Both the visitation frequency and the duration of visit decreased with the increasing number of ants; thus, a higher number of invasive ants indirectly influenced the pollinator attributes. The interference competition offered by invasive and native ants seemed to be similar. The visitation frequency and the duration spent by the pollinators are affected by the attack and aggression of ants on pollinator directly. These were considered key attributes for comparing the interference competition. In our studies, there was no considerable difference in these characters irrespective of which ant (invasive or native, or any of the nine species) occupied the flower. The choice of the pollinator entry was not affected by whether the flower was occupied by an invasive or native ant. Bees did not particularly show any discretion between the scents of an invasive ant occupied and native ant occupied flower.
Our studies further confirmed the negative effect of ants on pollinators of pumpkin18. We found that ants negatively influenced most crucial visitation characters of the pollinators. However, concluding from this is quite complicated as the interactions between ants, plants, other herbivores, and pollinators are quite complex14. Unlike many of the previous studies, we compared the competition offered by invasive ants and native ants on the pollinators. The exploitation competition is largely offered by invasive ants owing to their supercolonies and high population size. However, the interference competition can be offered by any native and invasive ants which can show aggressive and predatory behaviour to pollinators. But it is not possible to draw a fine border between these two competitions. Information on the effects of invasive ants on pollinators will help in implementing better pollination management practices in agricultural lands15,42.