Australian horticulture relies heavily on the introduced managed honey bee, Apis mellifera Linnaeus 1758 (Hymenoptera: Apidae), to pollinate crops. Given the risks associated with reliance upon a single species, it would be prudent to identify other taxa that could be managed to provide crop pollination services. We reviewed the literature relating to the distribution, efficiency and management potential of a number of flies (Diptera) known to visit pollinator-dependent crops in Australia and worldwide. Applying this information, we identified the taxa most suitable to play a greater role as managed pollinators in Australian crops. Of the taxa reviewed, flower visitation by representatives from the dipteran families Calliphoridae, Rhiniidae and Syrphidae was frequently reported in the literature. While data available are limited, there was clear evidence of pollination by these flies in a range of crops. A review of fly morphology, foraging behaviour and physiology revealed considerable potential for their development as managed pollinators, either alone or to augment honey bee services. Considering existing pollination evidence, along with the distribution, morphology, behaviour and life history traits of introduced and endemic species, 11 calliphorid, two rhiniid and seven syrphid species were identified as candidates with high potential for use in Australian managed pollination services. Research directions for the comprehensive assessment of the pollination abilities of the identified taxa to facilitate their development as a pollination service are described. This triage approach to identifying species with high potential to become significant managed pollinators at local or regional levels is clearly widely applicable to other countries and taxa.
BackgroundObligate pollination mutualisms (OPMs) are specialized interactions in which female pollinators transport pollen between the male and female flowers of a single plant species and then lay eggs into those same flowers. The pollinator offspring hatch and feed upon some or all of the developing ovules pollinated by their mothers. Strong trait matching between plants and their pollinators in OPMs is expected to result in reciprocal partner specificity i.e., a single pollinator species using a single plant species and vice versa, and strict co-speciation. These issues have been studied extensively in figs and fig wasps, but little in the more recently discovered co-diversification of Epicephala moths and their Phyllanthaceae hosts. OPMs involving Epicephala moths are believed occur in approximately 500 species of Phyllanthaceae, making it the second largest OPM group after the Ficus radiation (> 750 species). In this study, we used a mixture of DNA barcoding, genital morphology and behavioral observations to determine the number of Epicephala moth species inhabiting the fruits of Breynia oblongifolia, their geographic distribution, pollinating behavior and phylogenetic relationships.ResultsWe found that B. oblongifolia hosts two species of pollinator that co-occurred at all study sites, violating the assumption of reciprocal specificity. Male and female genital morphologies both differed considerably between the two moth species. In particular, females differed in the shape of their ovipositors, eggs and oviposition sites. Phylogenetic analyses indicated that the two Epicephala spp. on B. oblongifolia likely co-exist due to a host switch. In addition, we discovered that Breynia fruits are also often inhabited by a third moth, an undescribed species of Herpystis, which is a non-pollinating seed parasite.ConclusionsOur study reveals new complexity in interactions between Phyllantheae and Epicephala pollinators and highlights that host switching, co-speciation and non-pollinating seed parasites can shape species interactions in OPMs. Our finding that co-occurring Epicephala species have contrasting oviposition modes parallels other studies and suggests that such traits are important in Epicephala species coexistence.Electronic supplementary materialThe online version of this article (10.1186/s12862-018-1314-y) contains supplementary material, which is available to authorized users.
1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.
1. Hover flies (Syrphidae: Diptera) are a cosmopolitan group of insects that provide important ecosystem services including pollination and pest control. The seasonal migration of hover flies is probably best known in Europe, but it remains unstudied in many other parts of the world.2. Australia is believed to be home to around 160 hover fly species, some of which are common in urban and agricultural environments. The current evidence for hover fly migration in Australia is scarce and anecdotal, yet migration may be critical to the success of pollination and the biological control of aphids.3. In this study, species occurrence records from an online biodiversity database (Atlas of Living Australia) were used to look for evidence of migratory behaviours in all Australian hover flies with more than 200 occurrence records.4. Four of the 10 species displayed seasonal changes in their distribution consistent with migration, including Australia's two most abundant species: Melangyna viridiceps and Simosyrphus grandicornis. This work is an important first step in understanding the prevalence of migration in Australian hover flies. However, confirmation of our findings requires additional evidence to rule out other plausible explanations for the observed patterns.5. Based on changes in summer and winter latitudinal distribution, it is estimated that some Australian hover flies may make annual migrations of 400–1800 km.6. This work suggests that the management of beneficial insects requires consideration of factors at both local and continental scales, as landscape use changes may have an impact on ecosystem services delivered hundreds of kilometres away.
For pollinating insects that visit just a single flowering species, the co-occurrence of flowers and insects in time is likely to have critical implications for both plant and pollinator. Insects often utilise diapause to persist through periods in which resources are unavailable, timing their re-emergence by responding to the same environmental cues as their host plants. The obligate pollination mutualisms (OPMs) between Epicephala moths (Gracillariidae) and their leaf flower host plants are some of the most specialised interactions between plants and insects. However, to date there have been very few studies of Epicephala moth lifecycles and none of how they synchronise their activity with the flowering of their host plants. Breynia oblongifolia (Phyllanthaceae) is known to be exclusively pollinated by two highly specific species of Epicephala moth (Gracillariidae). We surveyed populations of both the host plant and its pollinators over multiple years to determine their annual phenology and then modelled the climatic factors that drive their activity. Using our newly gained knowledge of moth and host plant phenology, we then looked for evidence of diapause at both the egg and pre-pupal stages. Our phenology surveys showed that although female flowers were present throughout the entire year, the abundance of flowers and fruits was highly variable between sites and strongly associated with local rainfall and photoperiod. Fruit abundance, but not flower abundance, was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant flowers and emerge as fruits mature. Searches of overwintering flowers confirmed this, with many containing evidence of pollen and diapausing pollinators. We also observed the behaviour of adult Epicephala prior to pupation and found that ~10% of the Autumn emerging Epicephala enter diapause, eclosing to adulthood after 38-56 weeks. The remaining 90% of autumn emerging adults pupate directly with no diapause, suggesting a bet hedging strategy for adult emergence. As such, Epicephala moths appear to utilise diapause at multiple stages in their lifecycle, and possibly bet hedging, in order to deal with variable flowering phenology and climatic unpredictability.
Plants with a small number of specific pollinators may be vulnerable to fluctuations in the availability of those pollinators, which could limit plant reproductive success and even result in extinction. Plants can develop mechanisms to mitigate this risk, such as apomixis. Reproductive assurance mechanisms have been largely ignored in obligate pollination mutualisms (OPMs), that are some of the most specialised of plant-pollinator interactions. Furthermore, although OPMs are often referred to as obligate, this is rarely tested. We performed a flower-bagging experiment to test if the unisexual flowers of Breynia oblongifolia could set fruit in the absence of its highly specialised seed-eating moth pollinators. Surprisingly, many bagged female flowers developed fruits, suggesting apomixis. We therefore conducted a second series of experiments in which we 1) added or excluded pollinators from caged plants; and 2) surveyed a wild population for apomictic reproduction using mother-offspring genotyping. In the absence of pollinators, no fruits developed. In addition, we detected no genetic evidence for apomixis when comparing between mothers and their offspring or between adults in a wild population. We explain the production of fruits in bagged branches by our discovery that B. oblongifolia can retain pollinated female flowers over the winter period. These flowers develop to fruits in the spring in the absence of male flowers or pollinators. Our study thus shows that B. oblongifolia is unable to produce fruit in the absence of its specialist moth pollinators. Thus, the highly specific interaction between plant and pollinators appears to be truly obligate.
Background For specialised pollinators, the synchrony of plant and pollinator life history is critical to the persistence of pollinator populations. This is even more critical in nursery pollination, where pollinators are obligately dependant on female host plant flowers for oviposition sites. Epicephala moths (Gracillariidae) form highly specialised nursery pollination mutualisms with Phyllanthaceae plants. Several hundred Phyllanthaceae are estimated to be exclusively pollinated by highly specific Epicephala moths, making these mutualisms an outstanding example of plant–insect coevolution. However, there have been no studies of how Epicephala moths synchronise their activity with host plant flowering or persist through periods when flowers are absent. Such knowledge is critical to understanding the ecology and evolutionary stability of these mutualisms. We surveyed multiple populations of both Breynia oblongifolia (Phyllanthaceae) and it’s Epicephala pollinators for over two years to determine their phenology and modelled the environmental factors that underpin their interactions. Results The abundance of flowers and fruits was highly variable and strongly linked to local rainfall and photoperiod. Unlike male flowers and fruits, female flowers were present throughout the entire year, including winter. Fruit abundance was a significant predictor of adult Epicephala activity, suggesting that eggs or early instar larvae diapause within dormant female flowers and emerge as fruits mature. Searches of overwintering female flowers confirmed that many contained pollen and diapausing pollinators. We also observed diapause in Epicephala prior to pupation, finding that 12% (9/78) of larvae emerging from fruits in the autumn entered an extended diapause for 38–48 weeks. The remaining autumn emerging larvae pupated directly without diapause, suggesting a possible bet-hedging strategy. Conclusions Epicephala appear to use diapause at multiple stages in their lifecycle to survive variable host plant phenology. Furthermore, moth abundance was predicted by the same environmental variables as male flowers, suggesting that moths track flowering through temperature. These adaptations may thereby mitigate against unpredictability in the timing of fruiting and flowering because of variable rainfall. It remains to be seen how widespread egg diapause and pre-pupal diapause may be within Epicephala moths, and, furthermore, to what degree these traits may have facilitated the evolution of these highly diverse mutualisms.
Pollinator communities are composed of diverse groups of insects, with radically different life histories and resource needs. Blow flies are known to visit a variety of economically important crop plants. Larval blow flies develop by feeding on decaying animals. Some fruit growers are known to place carrion on farms during the flowering season to attract adult blow flies (Calliphoridae). However, the efficacy of these “stink stations” has not been tested. We conducted a series of experiments to determine: 1) if stink stations promote the abundance of blow flies in mango orchards (Mangifera indica L.), 2) if any increases in the abundance of flies acts to promote pollination and fruit set in Australian mango orchards. Farms with stink stations had approximately three times more flies than control farms. However, the increased abundance of blow flies did not result in increased fruit set. Although stink stations increased the abundance of blow flies, we found no evidence that their use improves mango yield. This may be due to pollination saturation by a highly abundant native hover fly, Mesembrius bengalensis (Syrphidae), during our study. We hypothesize that stink stations may only be beneficial in years or regions where other pollinators are less abundant.
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