Temperature during pupal development affects hoverfly developmental time, adult life span, and wing length
Status PubMed-not-MEDLINE Language English Country Great Britain, England Media electronic-ecollection
Document type Journal Article
PubMed
37881229
PubMed Central
PMC10597744
DOI
10.1002/ece3.10516
PII: ECE310516
Knihovny.cz E-resources
- Keywords
- Diptera, Eristalis tenax, Syrphidae, body size, locomotor activity, morphometrics, phenotypic plasticity, rearing temperature, thermal performance,
- Publication type
- Journal Article MeSH
Hoverflies (Diptera, Syrphidae) are cosmopolitan, generalist flower visitors and among the most important pollinators after bees and bumblebees. The dronefly Eristalis tenax can be found in temperate and continental climates across the globe, often synanthropically. Eristalis tenax pupae of different generations and different climate zones are thus exposed to vastly different temperatures. In many insects, the ambient temperature during the pupal stage affects development, adult size, and survival; however, the effect of developmental temperature on these traits in hoverflies is comparatively poorly understood. We here reared E. tenax pupae at different temperatures, from 10°C to 25°C, and quantified the effect on adult hoverflies. We found that pupal rearing at 17°C appeared to be optimal, with high eclosion rates, longer wings, and increased adult longevity. Rearing temperatures above or below this optimum led to decreased eclosion rates, wing size, and adult survival. Similar thermal dependence has been observed in other insects. We found that rearing temperature had no significant effect on locomotor activity, coloration or weight, despite evidence of strong sexual dimorphism for each of these traits. Our findings are important as hoverflies are key pollinators, and understanding the effects of developmental temperature could potentially be useful for horticulture.
Department of Medical Cell Biology Uppsala University Uppsala Sweden
Department of Zoology Faculty of Science Charles University Praha 2 Czech Republic
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Angilletta, M. J., Jr. (2009). Thermal adaptation: A theoretical and empirical synthesis. Oxford University Press.
Angilletta, M. J. , Niewiarowski, P. H. , & Navas, C. A. (2002). The evolution of thermal physiology in ectotherms. Journal of Thermal Biology, 27, 249–268.
Arambourou, H. , Sanmartín‐Villar, I. , & Stoks, R. (2017). Wing shape‐mediated carry‐over effects of a heat wave during the larval stage on post‐metamorphic locomotor ability. Oecologia, 184, 279–291. PubMed
Atkins, E. L. J. (1948). Mimicry between the drone‐fly, Eristalis tenax (L.), and the honeybee, Apis mellifera L., its significance in ancient mythology and present‐day thought. Annals of the Entomological Society of America, 41, 387–392.
Atkinson, D. (1994). In Begon M. & Fitter A. H. (Eds.), Temperature and organism size – A biological law for ectotherms? Advances in ecological research (pp. 1–58). Academic Press.
Bahrndorff, S. , Gertsen, S. , Pertoldi, C. , & Kristensen, T. N. (2016). Investigating thermal acclimation effects before and after a cold shock in Drosophila melanogaster using behavioural assays. Biological Journal of the Linnean Society, 117, 241–251.
Berrigan, D. , & Partridge, L. (1997). Influence of temperature and activity on the metabolic rate of adult Drosophila melanogaster . Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology, 118, 1301–1307. PubMed
Bortolini, S. , Macavei, L. I. , Saadoun, J. H. , Foca, G. , Ulrici, A. , Bernini, F. , Malferrari, D. , Setti, L. , Ronga, D. , & Maistrello, L. (2020). Hermetia illucens (L.) larvae as chicken manure management tool for circular economy. Journal of Cleaner Production, 262, 121289.
Carter, A. W. , & Sheldon, K. S. (2020). Life stages differ in plasticity to temperature fluctuations and uniquely contribute to adult phenotype in Onthophagus taurus dung beetles. The Journal of Experimental Biology, 223, jeb227884. PubMed
Cook, D. F. , Voss, S. C. , Finch, J. T. D. , Rader, R. C. , Cook, J. M. , & Spurr, C. J. (2020). The role of flies as pollinators of horticultural crops: An Australian case study with worldwide relevance. Insects, 11, 341. PubMed PMC
Dolley, W. L., Jr. , & Golden, L. H. (1947). The effect of sex and age on the temperature at which reversal in reaction to light in Eristalis tenax occurs. The Biological Bulletin, 92, 178–186. PubMed
Dolley, W. L., Jr. , & White, J. D. (1951). The effect of illuminance on the reversal temperature in the drone fly, Eristalis tenax . The Biological Bulletin, 100, 84–89. PubMed
Doyle, T. , Hawkes, W. L. S. , Massy, R. , Powney, G. D. , Menz, M. H. M. , & Wotton, K. R. (2020). Pollination by hoverflies in the Anthropocene. Proceedings of the Royal Society of London B, 287, 20200508. PubMed PMC
Ezeakacha, N. F. , & Yee, D. A. (2019). The role of temperature in affecting carry‐over effects and larval competition in the globally invasive mosquito Aedes albopictus . Parasites & Vectors, 12, 123. PubMed PMC
Forsman, A. (2011). Rethinking the thermal melanism hypothesis: Rearing temperature and coloration in pygmy grasshoppers. Evolutionary Ecology, 25, 1247–1257.
Francuski, L. , Djurakic, M. , Ludoski, J. , Hurtado, P. , Perez‐Banon, C. , Stahls, G. , Rojo, S. , & Milankov, V. (2014). Shift in phenotypic variation coupled with rapid loss of genetic diversity in captive populations of Eristalis tenax (Diptera: Syrphidae): Consequences for rearing and potential commercial use. Journal of Economic Entomology, 107, 821–832. PubMed
Francuski, L. , Djurakic, M. , Ludoski, J. , & Milankov, V. (2013). Landscape genetics and spatial pattern of phenotypic variation of Eristalis tenax across Europe. Journal of Zoological Systematics and Evolutionary Research, 51, 227–238.
Francuski, L. , Matić, I. , Ludoški, J. , & Milankov, V. (2011). Temporal patterns of genetic and phenotypic variation in the epidemiologically important drone fly, Eristalis tenax . Medical and Veterinary Entomology, 25, 135–147. PubMed
Garibaldi, L. A. , Steffan‐Dewenter, I. , Winfree, R. , Aizen, M. A. , Bommarco, R. , Cunningham, S. A. , Kremen, C. , Carvalheiro, L. G. , Harder, L. D. , Afik, O. , Bartomeus, I. , Benjamin, F. , Boreux, V. , Cariveau, D. , Chacoff, N. P. , Dudenhoffer, J. H. , Freitas, B. M. , Ghazoul, J. , Greenleaf, S. , … Klein, A. M. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608–1611. PubMed
Gilbert, F. S. (1984). Thermoregulation and the structure of swarms in Syrphus ribesii (Syrphidae). Oikos, 42, 249–255.
Gilbert, F. S. (1985). Diurnal activity patterns in hoverfies (Diptera, Syphidae). Ecological Entomology, 10, 385–392.
Gladis, T. (1994). Establishment and utilization of a mass rearing of Eristalis tenax (Diptera, Syrphidae) in the Gatersleben genebank. Insecta, 1, 287–294.
Gladis, T. (1997). Bees versus flies? Rearing methods and effectiveness of pollinators in crop germplasm regeneration (pp. 235–238). International Society for Horticultural Science (ISHS).
Hart, A. J. , Bale, J. S. , & Fenlon, J. S. (1997). Developmental threshold, day‐degree requirements and voltinism of the aphid predator Episyrphus balteatus (Diptera: Syrphidae). The Annals of Applied Biology, 130, 427–437.
Heal, J. (1979). Colour patterns of Syrphidae: 1. Genetic variation in the dronefly Eristalis tenax . Heredity, 42, 223–236.
Heal, J. R. (1989). Variation and seasonal changes in hoverfly species: Interactions between temperature, age and genotype. Biological Journal of the Linnean Society, 36, 251–269.
Hochachka, P. W. , & Somero, G. N. (2002). Biochemical adaptation: Mechanism and process in physiological evolution. Oxford University Press.
Holloway, G. J. (1993). Phenotypic variation in colour pattern and seasonal plasticity in Eristalis hoverflies (Diptera: Syrphidae). Ecological Entomology, 18, 209–217.
Howlett, B. , & Gee, M. (2019). The potential management of the drone fly (Eristalis tenax) as a crop pollinator in New Zealand. New Zealand Plant Protection, 72, 221–230.
Ireland, S. , & Turner, B. (2006). The effects of larval crowding and food type on the size and development of the blowfly, Calliphora vomitoria . Forensic Science International, 159, 175–181. PubMed
Jarlan, A. , De Oliveira, D. , & Gingras, J. (1997). Pollination by Eristalis tenax (Diptera: Syrphidae) and seed set of greenhouse sweet pepper. Journal of Economic Entomology, 90, 1646–1649.
Jauker, F. , Bondarenko, B. , Becker, H. C. , & Steffan‐Dewenter, I. (2012). Pollination efficiency of wild bees and hoverflies provided to oilseed rape. Agricultural and Forest Entomology, 14, 81–87.
Jauker, F. , Diekotter, T. , Schwarzbach, F. , & Wolters, V. (2009). Pollinator dispersal in an agricultural matrix: Opposing responses of wild bees and hoverflies to landscape structure and distance from main habitat. Landscape Ecology, 24, 547–555.
Kendall, D. A. , & Stradling, D. J. (1972). Some observations on over wintering of the drone fly Eristalis tenax Syrphidae. Entomologiste, 105, 229–230.
Khelifa, R. , Blanckenhorn, W. U. , Roy, J. , Rohner, P. T. , & Mahdjoub, H. (2019). Usefulness and limitations of thermal performance curves in predicting ectotherm development under climatic variability. The Journal of Animal Ecology, 88, 1901–1912. PubMed
Kingsolver, J. G. , Arthur Woods, H. , Buckley, L. B. , Potter, K. A. , MacLean, H. J. , & Higgins, J. K. (2011). Complex life cycles and the responses of insects to climate change. Integrative and Comparative Biology, 51, 719–732. PubMed
Klecka, J. , Hadrava, J. , Biella, P. , & Akter, A. (2018). Flower visitation by hoverflies (Diptera: Syrphidae) in a temperate plant‐pollinator network. PeerJ, 6, e6025. PubMed PMC
Kuntz, S. G. , & Eisen, M. B. (2014). Drosophila embryogenesis scales uniformly across temperature in developmentally diverse species. PLoS Genetics, 10, e1004293. PubMed PMC
Li, L. T. , Wang, Y. Q. , Ma, J. F. , Liu, L. , Hao, Y. T. , Dong, C. , Gan, Y. J. , Dong, Z. P. , & Wang, Q. Y. (2013). The effects of temperature on the development of the moth Athetis lepigone, and a prediction of field occurrence. Journal of Insect Science, 13, 103–113. PubMed PMC
Menz, M. H. M. , Brown, B. V. , & Wotton, K. R. (2019). Quantification of migrant hoverfly movements (Diptera: Syrphidae) on the west coast of North America. Royal Society Open Science, 6, 190153. PubMed PMC
Morales, G. E. , & Wolff, M. (2010). Insects associated with the composting process of solid urban waste separated at the source. Revista Brasileira de Entomologia, 54, 645–653.
Nicholas, S. , Thyselius, M. , Holden, M. , & Nordström, K. (2018). Rearing and long‐term maintenance of Eristalis tenax hoverflies for research studies. Journal of Visualized Experiments, 135, e57711. PubMed PMC
Nordström, K. , Dahlbom, J. , Pragadheesh, V. S. , Ghosh, S. , Olsson, A. , Dyakova, O. , Suresh, S. K. , & Olsson, S. B. (2017). In situ modeling of multimodal floral cues attracting wild pollinators across environments. Proceedings of the National Academy of Sciences of the United States of America, 114, 13218–13223. PubMed PMC
Osburn, R. C. (1915). Studies in Syrphidæ‐IV. Species of Eristalis new to America, with notes on others. Journal of the New York Entomological Society, 23, 139–145.
Osten‐Sacken, C. R. (1886). Some new facts concerning Eristalis tenax . The Entomologist's Monthly Magazine, 23, 97–99.
Ottenheim, M. , & Volmer, A. (1999). Wing length plasticity in Eristalis arbustorum (Diptera: Syrphidae). Netherlands Journal of Zoology, 49, 15–27.
Ottenheim, M. M. (2000). Annual and diurnal rhythms of Eristalis species (Diptera: Syrphidae). Proceedings of the Section Experimental and Applied Entomology, 11, 169–174.
Ottenheim, M. M. , & Holloway, G. J. (1995). The effect of diet and light and larval and pupal development of laboratory‐reared Eristalis arbustorum (Diptera: Syprhidae). Netherlands Journal of Zoology, 45, 305–314.
Ottenheim, M. M. , Volmer, A. D. , & Holloway, G. J. (1996). The genetics of phenotypic plasticity in adult abdominal colour pattern of Eristalis arbustorum (Diptera: Syrphidae). Heredity, 77, 493–499.
Paaijmans, K. P. , Heinig, R. L. , Seliga, R. A. , Blanford, J. I. , Blanford, S. , Murdock, C. C. , & Thomas, M. B. (2013). Temperature variation makes ectotherms more sensitive to climate change. Global Change Biology, 19, 2373–2380. PubMed PMC
Pallarés, S. , Verberk, W. C. E. P. , & Bilton, D. T. (2021). Plasticity of thermal performance curves in a narrow range endemic water beetle. Journal of Thermal Biology, 102, 103113. PubMed
Rader, R. , Cunningham, S. A. , Howlett, B. G. , & Inouye, D. W. (2020). Non‐bee insects as visitors and pollinators of crops: Biology, ecology, and management. Annual Review of Entomology, 65, 391–407. PubMed
RC Team . (2022). R: A language and environment for statistical computing. R Foundation for Statistical Computing.
Rebolledo, A. P. , Sgrò, C. M. , & Monro, K. (2021). Thermal performance curves are shaped by prior thermal environment in early life. Frontiers in Physiology, 12, 738338. PubMed PMC
Roffeis, M. , Muys, B. , Almeida, J. , Mathijs, E. , Achten, W. M. J. , Pastor, B. , Velásquez, Y. , Martinez‐Sanchez, A. I. , & Rojo, S. (2015). Pig manure treatment with housefly (Musca domestica) rearing – An environmental life cycle assessment. Journal of Insects as Food and Feed, 1, 195–214.
Sánchez‐Bayo, F. , & Wyckhuys, K. A. G. (2019). Worldwide decline of the entomofauna: A review of its drivers. Biological Conservation, 232, 8–27.
Schneider, C. A. , Rasband, W. S. , & Eliceiri, K. W. (2012). NIH image to ImageJ: 25 years of image analysis. Nature Methods, 9, 671–675. PubMed PMC
Schou, T. M. , Faurby, S. , Kjaersgaard, A. , Pertoldi, C. , Loeschcke, V. , Hald, B. , & Bahrndorff, S. (2013). Temperature and population density effects on locomotor activity of Musca domestica (Diptera: Muscidae). Environmental Entomology, 42, 1322–1328. PubMed
Sekar, S. (2012). A meta‐analysis of the traits affecting dispersal ability in butterflies: Can wingspan be used as a proxy? The Journal of Animal Ecology, 81, 174–184. PubMed
Sengupta, J. , Naskar, A. , Maity, A. , Hazra, S. , Mukhopadhyay, E. , Banerjee, D. , & Ghosh, S. (2016). An updated distributional account of indian hover flies (Insecta: Diptera: Syrphidae). Journal of Entomology and Zoology Studies, 4, 381–396.
Speight, M. C. D. (2017). Species accounts of European Syrphidae, 2017. Syrph the net, the database of European Syrphidae (Diptera) (p. 294). Syrph the Net Publications.
Speight, M. C. D. , Good, J. A. , & Castella, E. (2002). Predicting the changes in farm syrphid faunas that could be caused by changes in farm management regimes (Diptera, Syrphidae). Volucella, 6, 125–137.
Stavert, J. R. , Pattemore, D. E. , Bartomeus, I. , Gaskett, A. C. , & Beggs, J. R. (2018). Exotic flies maintain pollination services as native pollinators decline with agricultural expansion. Journal of Applied Ecology, 55, 1737–1746.
Thyselius, M. , & Nordström, K. (2016). Hoverfly locomotor activity is resilient to external influence and intrinsic factors. Journal of Comparative Physiology, 202, 45–54. PubMed PMC
Van Der Have, T. M. (2002). A proximate model for thermal tolerance in ectotherms. Oikos, 98, 141–155.
Wotton, K. R. , Gao, B. , Menz, M. H. M. , Morris, R. K. A. , Ball, S. G. , Lim, K. S. , Reynolds, D. R. , Hu, G. , & Chapman, J. W. (2019). Mass seasonal migrations of hoverflies provide extensive pollination and crop protection services. Current Biology, 29, 2167–2173. PubMed
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10.5061/dryad.2z34tmpr1