Abstract
Hoverflies can play an important role in aphid biological control. Adult hoverflies depend on pollen and nectar to survive. Therefore the placement of flower resources in agroecosystems is a common method to enhance the populations of these insects. When foraging, hoverflies rely on visual cues to select flowers. We studied the preference of Sphaerophoria rueppelli (Wiedemann) (Diptera: Syrphidae) adults for several flower traits and examined whether mating influenced foraging behavior. We observed that these insects were greatly attracted to bouquets of 12 flat circle-shaped flowers (half white and half yellow). Furthermore, yellow flowers elicited landing more than other colors, regardless of the type of bouquet. With respect to the effect of mating on posterior foraging behavior, virgin individuals showed more movement than gravid ones. Our results shed light on the behavior of adult hoverflies and can be used to improve habitat management practices that seek to promote biological control.
Similar content being viewed by others
References
Almohamad R, Verheggen FJ, Haubruge E (2009) Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review. Biotechnol Agron Soc 13:467–481
Ambrosino MD, Luna JM, Jepson PC, Wratten SD (2006) Relative frequencies of visits to selected insectary plants by predatory hoverflies (Diptera: Syrphidae), other beneficial insects, and herbivores. Environ Entomol 35:394–400
Blaauw BR, Isaacs R (2014) Larger patches of diverse floral resources increase insect pollinator density, diversity, and their pollination of native wild flowers. Basic Appl Ecol 15:701–711
Branquart E, Hemptinne JL (2000a) Development of ovaries, allometry of reproductive traits and fecundity of Episyrphus balteatus (Diptera: Syrphidae). Eur J Entomol 97:165–170
Branquart E, Hemptinne JL (2000b) Selectivity in the exploitation of floral resources by hoverflies (Diptera: Syrphinae). Ecography 23:732–742
Chandler AE (1968) Some factors influencing occurrence and site of oviposition by aphidophagous Syrphidae (Diptera). Ann Appl Biol 61:435–446
Conner JK, Rush S (1996) Effects of flower size and number on pollinator visitation to wild radish, Raphanus raphanistrum. Oecologia 105:509–516
Day RL, Hickman JM, Sprague RI, Wratten SD (2015) Predatory hoverflies increase oviposition in response to colour stimuli offering no reward: implications for biological control. Basic Appl Ecol 16:544–552
Dinkel T, Lunau K (2001) How drone flies (Eristalis tenax L., Syrphidae: Diptera) use floral guides to locate food sources. J Insect Physiol 47:1111–1118
Gilbert FS (1981) Foraging ecology of hoverflies—morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecol Entomol 6:245–262
Gilbert F (1993) Hoverflies. In: Naturalists’ handbooks 5, 2nd edn. Richmond Publishing Co., Slough, Berkshire
Golding YC, Sullivan MS, Sutherland JP (1999) Visits to manipulated flowers by Episyrphus balteatus (Diptera: Syrphidae): partitioning the signals of petals and anthers. J Insect Behav 12:39–45
Gong Y-B, Huang S-Q (2009) Floral symmetry: pollinator-mediated stabilizing selection on flower size in bilateral species. Proc R Soc Lond B 276:4013–4020
Gurr GM, Wratten SD, Landis DA, You MS (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109
Haenke S, Scheid B, Schaefer M, Tscharntke T, Thies C (2009) Increasing syrphid fly diversity and density in sown flower strips within simple vs. complex landscapes. J Appl Ecol 46:1106–1114
Haslett JR (1989a) Adult feeding by Holometabolous insects—pollen and nectar as complementary nutrient sources for Rhingia campestris (Diptera, Syrphidae). Oecologia 81:361–363
Haslett JR (1989b) Interpreting patterns of resource utilization—randomness and selectivity in pollen feeding by adult hoverflies. Oecologia 78:433–442
Hegland SJ, Boeke L (2006) Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol 31:532–538
Hickman JM, Wratten SD (1996) Use of Phacelia tanacetifolia strips to enhance biological control of aphids by hoverfly larvae in cereal fields. J Econ Entomol 89:832–840
Hickman JM, Lovei GL, Wratten SD (1995) Pollen feeding by adults of the hoverfly Melanostoma fasciatum (Diptera: Syrphidae). N Z J Zool 22:387–392
Hickman JM, Wratten SD, Jepson PC, Frampton CM (2001) Effect of hunger on yellow water trap catches of hoverfly (Diptera: Syrphidae) adults. Agric For Entomol 3:35–40
Hogg BN, Nelson EH, Mills NJ, Daane KM (2011) Floral resources enhance aphid suppression by a hoverfly. Entomol Exp Appl 141:138–144
Irvin NA, Wratten SD, Frampton CM, Bowie MH, Evans AM, Moar NT (1999) The phenology and pollen feeding of three hover fly (Diptera: Syrphidae) species in Canterbury, New Zealand. N Z J Zool 26:105–115
Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu Rev Entomol 45:175–201
Laubertie EA, Wratten SD, Sedcole JR (2006) The role of odour and visual cues in the pan-trap catching of hoverflies (Diptera: Syrphidae). Ann Appl Biol 148:173–178
Lunau K (1995) Notes on the colour of pollen. Plant Syst Evol 198:235–252
Lunau K, Maier EJ (1995) Innate color preferences of flower visitors. J Comp Physiol A 177:1–19
Lunau K, Wacht S (1994) Optical releasers of the innate proboscis extension in the hoverfly Eristalis tenax L. (Syrphidae: Diptera). J Comp Physiol A 174:575–579
Lunau K, An L, Donda M, Hohmann M, Sermon L, Stegmanns V (2018) Limitations of learning in the proboscis reflex of the flower visiting syrphid fly Eristalis tenax. PLoS ONE 13(3):e0194167
Macleod A (1999) Attraction and retention of Episyrphus balteatus DeGeer (Diptera: Syrphidae) at an arable field margin with rich and poor floral resources. Agric Ecosyst Environ 73:237–244
Maier CT (1978) Immature stages and biology of Mallota posticata (Fabricius) (Diptera: Syrphidae). Proc Entomol Soc Wash 80:424–440
Maier CT, Waldbauer GP (1979) Dual mate-seeking strategies in male syprhid flies (Diptera: Syrphidae). Ann Entomol Soc Am 72:54–61
Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186
Nordstrom K, Dahlbom J, Pragadheesh VS, Ghosh S, Olsson A, Dyakova O, Suresh SK, Olsson SB (2017) In situ modeling of multimodal floral cues attracting wild pollinators across environments. Proc Natl Acad Sci USA 114:13218–13223
Power EF, Jackson Z, Stout JC (2016) Organic farming and landscape factors affect abundance and richness of hoverflies (Diptera, Syrphidae) in grasslands. Insect Conserv Divers 9:244–253
Primante C, Dotterl S (2010) A syrphid fly uses olfactory cues to find a non-yellow flower. J Chem Ecol 36:1207–1210
Rojo S, Gilbert F, Marcos-García MA, Nieto J, Mier MP (2003) A world review of predatory hoverflies (Diptera, Syrphidae: Syrphinae) and their prey. CIBIO Ediciones, Alicante
Sadeghi H, Gilbert F (2000) Oviposition preferences of aphidophagous hoverflies. Ecol Entomol 25:91–100
Skirvin DJ, Kravar-Garde L, Reynolds K, Wright C, Mead A (2011) The effect of within-crop habitat manipulations on the conservation biological control of aphids in field-grown lettuce. Bull Entomol Res 101:623–631
Sutherland JP, Sullivan MS, Poppy GM (1999) The influence of floral character on the foraging behaviour of the hoverfly, Episyrphus balteatus. Entomol Exp Appl 93:157–164
Sutherland JP, Sullivan MS, Poppy GM (2001) Distribution and abundance of aphidophagous hoverflies (Diptera: Syrphidae) in wildflower patches and field margin habitats. Agric For Entomol 3:57–64
Tenhumberg B, Poehling HM (1995) Syrphids as natural enemies of cereal aphids in Germany—aspects of their biology and efficacy in different years and regions. Agric Ecosyst Environ 52:39–43
van Rijn PCJ, Wäckers FL (2016) Nectar accessibility determines fitness, flower choice and abundance of hoverflies that provide natural pest control. J Appl Ecol 53:925–933
van Rijn PCJ, Kooijman J, Wäckers FL (2006) The impact of floral resources on syrphid performance and cabbage aphid biological control. IOBC/WPRS Bull 29:149–152
Warzecha D, Diekoetter T, Wolters V, Jauker F (2018) Attractiveness of wildflower mixtures for wild bees and hoverflies depends on some key plant species. Insect Conserv Divers 11:32–41
White AJ, Wratten SD, Berry NA, Weigmann U (1995) Habitat manipulations to enhance biological control of brassica pests by hover flies (Diptera, Syrphidae). J Econ Entomol 88:1171–1176
Wratten SD, Bowie MH, Hickman JM, Evans AM, Sedcole JR, Tylianakis JM (2003) Field boundaries as barriers to movement of hover flies (Diptera: Syrphidae) in cultivated land. Oecologia 134:605–611
Wratten SD, Gillespie M, Decourtye A, Mader E, Desneux N (2012) Pollinator habitat enhancement: benefits to other ecosystem services. Agric Ecosyst Environ 159:112–122
Acknowledgements
We thank Ariadna Marmol and Quico Vila d’Abadal for their collaboration with data collection. Special thanks go to Francis Gilbert for his help differentiating between virgin and gravid females. This research was funded by Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (Spain), by means of the Project RTA 2013-00039-C03-00.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Patrick De Clercq.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rodríguez-Gasol, N., Avilla, J., Alegre, S. et al. Sphaerophoria rueppelli adults change their foraging behavior after mating but maintain the same preferences to flower traits. BioControl 64, 149–158 (2019). https://doi.org/10.1007/s10526-019-09928-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-019-09928-2