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Native and Invasive Ants Affect Floral Visits of Pollinating Honey Bees in Pumpkin Flowers (Cucurbita Maxima)

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Native and Invasive Ants Affect Floral Visits of Pollinating Honey Bees in Pumpkin Flowers (Cucurbita Maxima) www.nature.com/scientificreports OPEN Native and invasive ants afect foral visits of pollinating honey bees in pumpkin fowers (Cucurbita maxima) Anjana Pisharody Unni1,3, Sajad Hussain Mir1,2, T. P. Rajesh1, U. Prashanth Ballullaya1, Thomas Jose1 & Palatty Allesh Sinu1* Global pollinator decline is a major concern. Several factors—climate change, land-use change, the reduction of fowers, pesticide use, and invasive species—have been suggested as the reasons. Despite being a potential reason, the efect of ants on fowers received less attention. The consequences of ants being attracted to nectar sources in plants vary depending upon factors like the nectar source’s position, ants’ identity, and other mutualists interacting with the plants. We studied the interaction between fower-visiting ants and pollinators in Cucurbita maxima and compared the competition exerted by native and invasive ants on its pollinators to examine the hypothesis that the invasive ants exacerbate more interference competition to pollinators than the native ants. We assessed the pollinator’s choice, visitation rate, and time spent/visit on the fowers. Regardless of species and nativity, ants negatively infuenced all the pollinator visitation traits, such as visitation rate and duration spent on fowers. The invasive ants exerted a higher interference competition on the pollinators than the native ants did. Despite performing pollination in fowers with generalist pollination syndrome, ants can threaten plant-pollinator mutualism in specialist plants like monoecious plants. A better understanding of factors infuencing pollination will help in implementing better management practices. Humans brought together what continents isolated. One very conspicuous evidence of this claim rests in the rearranged biota. With the age of exploration, migration, and commerce, the previously unlikely event of organ- isms crossing the biogeographical and ecological barriers became typical1. Sometimes the introduced species could become a threat for native fora, fauna, ecosystems, and human welfare2. Despite causing a direct efect on biodiversity, the invasive species pose deleterious consequences to the community structure and ecosystem 3,4. One of the most successful taxa that invaded islands, mainland, and continents worldwide is ants5. Teir sociality and colony structure backing their success cause widespread damage in the introduced area 6. Tey are known to crash the populations of native ants, other invertebrates, reptiles, birds, and mammals in invaded sites6,7. Managing invasive ants has become a vital conservation tool8. Invasive ants participate and disrupt a range of plant-animal interactions as well 9,10. Although there are cases when invasive ant interactions contrib- ute to plant ftness as well11, the cost–beneft balance of such interactions are subtle and ofen result in negative repercussions12. It is widely believed that plants defend ants efectively on fowers either by producing ant deterrents in fowers or by distracting ants to extra-foral nectaries distributed on non-foral parts of plants13–15. Plants in over 100 families use extra-foral nectaries for defending ants on fowers 16. However, growing evidence shows that ants are also exploring fowers of a range of fowering plants, and giving diferential impacts to pollinators, pollina- tion, and plant reproduction17–26. Nevertheless, ants are mainly regarded as foral nectar thieves and disruptors of plant-pollinator mutualism19,20,27–31. Among ants, the invasive ants have been particularly demonstrated to have a disruptive efect on plant- pollinator mutualism20,23,24,29–33. Invasive ants, because aggressive and competent in locating carbohydrate-rich sources in a short period, can occupy more fowers in more numbers, which can signifcantly reduce diversity, frequency, and foraging time of legitimate pollinators on fowers12,34–36. While most of the nectar-thieving ants 1Central University of Kerala, Periya, Kerala 671316, India. 2Sher-E-Kashmir University of Agricultural Science and Technology of Kashmir, Wadura, Kashmir 193201, India. 3Present address: Max-Planck Institute for Chemical Ecology, Jena, Germany. *email: [email protected] Scientifc Reports | (2021) 11:4781 | https://doi.org/10.1038/s41598-021-83902-w 1 Vol.:(0123456789) www.nature.com/scientificreports/ primarily engaged in foraging foral nectar, a few also have attempted to prey upon pollinators18,20,27–29. Although some studies suggest that the invasive ants protect some plants against herbivores, it is likely that their aggres- siveness wards of some useful mutualists, too 29,35. Although a few studies examined the efect of invasive ants on pollinators, a comparative study between native and invasive ants has not been done yet 12. In this study, we have attempted to compare the efects of ants on pollinators and compare the competition exerted by non-native and native ants on the pollinators of Cucurbita maxima—a monoecious globally-important, pollination-defcient crop plant. To understand the efects of ants on pollinators, we took three attributes of pollinators and observed how these were afected by fower-visiting ants (hereafer, foral ants). Tey were the pollinators’ choice to visit or not to visit the fowers, the frequency of pollinators’ visits (visitation rate), and the time the pollinators spent inside the fowers. We expected the visitation rate and visit duration of pollinators to be negatively afected by ants’ presence. Since invasive ants are known for displacing biodiversity and interrupting species interactions, we hypothesize that the invasive ants exert more pressure on plant-pollinator interaction than the native ants do. We considered the ant’s ability to occupy the maximum number of fowers and maximize the number of individu- als occupying a single fower as the parameters for assessing ants’ exploitation competition on pollinators. Our expectation for this was that the fowers occupied by invasive ants in the population are higher than the fowers occupied by native ants. Since the plant in our study is monoecious, we also asked whether the ant-pollinator interaction was afected by fower sex. Material and methods Study site. Our study was conducted at Kasaragod, the northernmost district of Kerala state in the peninsu- lar India. Te district is located at 12.5° N 75.0° E with an average elevation of 19 m above sea level. Te highest and lowest temperature is 37 °C and 17 °C respectively. Te district enjoys a tropical and sub-tropical climate, with winter (January and February), hot summer (March–May), and two rotations of Monsoon, the Southwest Monsoon (June–September) and Northeast Monsoon (October to November), giving an average annual rainfall of approx. 2000 mm. Te district exhibits a topographic division into three, the lowland bordering the sea, the mainlands, and the forest highlands on the eastern side. Te coastal strips are sandy, the lowland has red fer- ruginous loam with a mixture of clay and sandy soil, and the highland region is laterite. Te study took place in seven independent farmer-managed vegetable gardens in Kasaragod. Tese sites stood 3–10 km apart. Te farmers of these sites cultivate rice paddy as their main crop, sowing in June to August and harvesting in November to January months of the year. From November to April, they cultivate vegetables belong to Amaranthaceae, Cucurbitaceae, Malvaceae, Solanaceae, and Fabaceae families as smallholdings (approximately one-acre land). Study system. We took pumpkin (Cucurbita maxima) as our study system. It is a monoecious plant with separate staminate (male) and pistillate (female) fowers. Both fowers are borne on diferent nodes with a dis- proportionately high number of staminate fowers per feld37. Te staminate and pistillate fowers are large, showy yellow with abundant foral nectar—the pistillate fowers producing a slightly higher quantity of quality nectar38. We harvested nectar from pre-caged staminate (N = 14; 2 per site) and pistillate fowers (N = 14; 2 per site) soon afer anthesis using Drummond micro-capillary tubes (10 μL) and estimated the sugar concentration using a hand-held refractometer. A large ovary at the fower base and three stigma lobes inside the fower distinguishes the pistillate fower from the staminate fower. Te staminate fower has its anthers united into a single long flament of about 10 cm. Te pollen grains are large and sticky; thus, pollination is dependent on the animal pollinator. Flower longevity is one day. Te fower opened between 0630 and 0700 h and remained open for about 6 h. Native honey bee, Apis cerana, is the primary pollinator of C. maxima in our study area37. Farmers raised plants from the seeds collected from their previous years, with "Ambili" being the predominant variety in feld populations. Four to six seeds were sowed in a pit of about 60 cm diameter and 30–45 cm depth, mixing it with neem cake and cow dung. Te feld is irrigated daily morning using the traditional pot method or water hose 38. Sampling method. Our study’s observations were carried out from 28th December 2018 to 15th February 2019, at the peak season of pumpkin fowering. During the study days (44 days), the data on ant visits and pol- linator visits were collected from 0700 to 0800 h. We counted a total of 1664 fowers from all seven sites together to record the number of pistillate and staminate fowers. From this, we studied the pollinator and ant activity on 348 randomly chosen fowers (206 ant-occupied fowers (93 staminate and 113 pistillate fowers) and 142 ant-unoccupied fowers (33 pistillate and 109 staminate fowers)) belong to 102 plants (14.57 ± 21 plants/site). To observe pollinator and ant activity, we spent 15 min per fower during the early hours of the anthesis and pollinators’ peak activity (0700–0800 h). We observed the fowers in which ants were present and the fowers in which ants were absent in the felds. During this observation window, we assessed the visitation rate, the dura- tion of the visit, and pollinators’ hovering activity. We observed the visitation rate as the number of times the pollinator entered the fower.
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