A polyphagous, tropical insect herbivore shows strong seasonality in age-structure and longevity independent of temperature and host availability
1.Murphy, P. G. & Lugo, A. E. Ecology of tropical dry forest. Annu. Rev. Ecol. Syst. 17, 67–88 (1986).Article
Google Scholar
2.Kishimoto-Yamada, K. & Itioka, T. How much have we learned about seasonality in tropical insect abundance since Wolda (1988)?. Entomol. Sci. 18, 407–419. https://doi.org/10.1111/ens.12134 (2015).Article
Google Scholar
3.dos Santos, J. P. D., Iserhard, C. A., Carreira, J. Y. O. & Freitas, A. V. L. Monitoring fruit-feeding butterfly assemblages in two vertical strata in seasonal Atlantic Forest: Temporal species turnover is lower in the canopy. J. Trop. Ecol. 33, 345–355. https://doi.org/10.1017/s0266467417000323 (2017).Article
Google Scholar
4.Bonebrake, T. C., Ponisio, L. C., Boggs, C. L. & Ehrlich, P. R. More than just indicators: A review of tropical butterfly ecology and conservation. Biol. Conser. 143, 1831–1841 (2010).Article
Google Scholar
5.Molleman, F. Moving beyond phenology: New directions in the study of temporal dynamics of tropical insect communities. Curr. Sci. 114, 982 (2018).Article
Google Scholar
6.Frith, C. B. & Frith, D. W. Seasonality of insect abundance in an Australian upland tropical rainforest. Aust. J. Ecol. 10, 237–248 (1985).Article
Google Scholar
7.Braby, M. Seasonal-changes in relative abundance and spatial-distribution of Australian lowland tropical satyrine butterflies. Aust. J. Zool. 43, 209–229 (1995).Article
Google Scholar
8.Muniz, D. G., Freitas, A. V. & Oliveira, P. S. Phenological relationships of Eunica bechina (Lepidoptera: Nymphalidae) and its host plant, Caryocar brasiliense (Caryocaraceae), in a Neotropical savanna. Stud. Neotrop. Fauna Environ. 47, 111–118 (2012).Article
Google Scholar
9.Wolda, H. Insect seasonality: Why?. Annu. Rev. Ecol. Syst. 19, 1–18 (1988).Article
Google Scholar
10.Yonow, T. et al. Modelling the population dynamics of the Queensland fruit fly, Bactrocera (Dacus) tryoni: A cohort-based approach incorporating the effects of weather. Ecol. Model. 173, 9–30. https://doi.org/10.1016/s0304-3800(03)00306-5 (2004).Article
Google Scholar
11.Baker, R. et al. Bactrocera dorsalis pest report to support ranking of EU candidate priority pests. EFSA https://doi.org/10.5281/zenodo.2786921 (2019).12.Valtonen, A. et al. Tropical phenology: Bi-annual rhythms and interannual variation in an Afrotropical butterfly assemblage. Ecosphere https://doi.org/10.1890/es12-00338.1 (2013).Article
Google Scholar
13.Hernández, C. X. P. & Caballero, S. Z. Temporal variation in the diversity of Cantharidae (Coleoptera), in seven assemblages in tropical dry forest in Mexico. Trop. Conserv. Sci. 9, 439–464 (2016).Article
Google Scholar
14.Marchioro, C. A. & Foerster, L. A. Biotic factors are more important than abiotic factors in regulating the abundance of Plutella xylostella L., Southern Brazil. Rev. Bras. Entomol. 60, 328–333 (2016).Article
Google Scholar
15.Meats, A. The bioclimatic potential of the Queensland fruit fly, Dacus tryoni, Australia. Proc. Ecol. Soc. Aust. 11, 1–61 (1981).
Google Scholar
16.Sutherst, R. W. & Yonow, T. The geographical distribution of the Queensland fruit fly, Bactrocera (Dacus) tryoni, in relation to climate. Aust. J. Agric. Res. 49, 935–954 (1998).Article
Google Scholar
17.Choudhary, J. S. et al. Potential changes in number of generations of oriental fruit fly, Bactrocera Dorsalis (Diptera: Tephritidae) on mango in India in response to climate change scenarios. J. Agrometeorol. 19, 200–206 (2017).
Google Scholar
18.Clarke, A. R. Biology and Management of Bactrocera and Related Fruit Flies (CABI, 2019).Book
Google Scholar
19.Sakai, S. et al. Plant reproductive phenology over four years including an episode of general flowering in a lowland dipterocarp forest, Sarawak, Malaysia. Am. J. Bot. 86, 1414–1436 (1999).CAS
PubMed
Article
Google Scholar
20.Land, K. C., Yang, Y. & Zeng, Y. Mathematical demography. Handbook of Population 659–717 (Springer, 2005).21.Carey, J. R. & Roach, D. A. Biodemography: An Introduction to Concepts and Methods (Princeton University Press, 2020).MATH
Book
Google Scholar
22.Carey, J. R. Applied Demography for Biologists: With Special Emphasis on Insects (Oxford University Press, 1993).
Google Scholar
23.Carey, J. R. Insect biodemography. Annu. Rev. Entomol. 46, 79–110 (2001).CAS
PubMed
Article
Google Scholar
24.Southwood, T. R. E. Ecological Methods: With Particular Reference to the Study of Insect Populations. xviii + 391 (Methuen, London, 1966).25.Udevitz, M. S. & Ballachey, B. E. Estimating survival rates with age-structure data. J. Wildl. Manag. 62, 779–792 (1998).Article
Google Scholar
26.Müller, H. G. et al. Demographic window to aging in the wild: constructing life tables and estimating survival functions from marked individuals of unknown age. Aging Cell 3, 125–131 (2004).PubMed
PubMed Central
Article
CAS
Google Scholar
27.Zajitschek, F., Zajitschek, S. & Bonduriansky, R. Senescence in wild insects: Key questions and challenges. Funct. Ecol. 34, 26–37 (2020).Article
Google Scholar
28.Carey, J. R. et al. Age structure changes and extraordinary lifespan in wild medfly populations. Aging Cell 7, 426–437. https://doi.org/10.1111/j.1474-9726.2008.00390.x (2008).CAS
Article
PubMed
PubMed Central
Google Scholar
29.Rao, A. S. S. & Carey, J. R. Generalization of Carey’s equality and a theorem on stationary population. J. Math. Biol. 71, 583–594 (2015).MathSciNet
MATH
Article
Google Scholar
30.Carey, J. R. Biodemography of the Mediterranean fruit fly: Aging, longevity and adaptation in the wild. Exp. Gerontol. 46, 404–411. https://doi.org/10.1016/j.exger.2010.09.009 (2011).Article
PubMed
Google Scholar
31.Muller, H. G., Wang, J. L., Yu, W., Delaigle, A. & Carey, J. R. Survival and aging in the wild via residual demography. Theor. Popul. Biol. 72, 513–522. https://doi.org/10.1016/j.tpb.2007.07.003 (2007).Article
PubMed
PubMed Central
MATH
Google Scholar
32.Vaupel, J. Life lived and left: Carey’s equality. Demogr Res 20, 7–10. https://doi.org/10.4054/DemRes.2009.20.3 (2009).Article
Google Scholar
33.Carey, J. R., Papadopoulos, N. T., Papanastasiou, S., Diamantidis, A. & Nakas, C. T. Estimating changes in mean population age using the death distributions of live-captured medflies. Ecol. Entomol. 37, 359–369. https://doi.org/10.1111/j.1365-2311.2012.01372.x (2012).Article
Google Scholar
34.Papadopoulos, N. T. et al. Seasonality of post-capture longevity in a medically-important mosquito (Culex pipiens). Front. Ecol. Evol https://doi.org/10.3389/fevo.2016.00063 (2016).Article
Google Scholar
35.Behrman, E. L., Watson, S. S., O’Brien, K. R., Heschel, M. S. & Schmidt, P. S. Seasonal variation in life history traits in two Drosophila species. J Evol Biol 28, 1691–1704. https://doi.org/10.1111/jeb.12690 (2015).CAS
Article
PubMed
PubMed Central
Google Scholar
36.Drew, R. A. The tropical fruit flies (Diptera: Tephritidae: Dacinae) of the Australasian and Oceanian regions. Mem. Queensland Museum 26, 1 (1989).
Google Scholar
37.Dominiak, B. C. Components of a systems approach for the management of Queensland fruit fly Bactrocera tryoni (Froggatt) in a post dimethoate fenthion era. Crop prot. 116, 56–67 (2019).Article
Google Scholar
38.Boulter, S. L., Kitching, R. L. & Howlett, B. G. Family, visitors and the weather: patterns of flowering in tropical rain forests of northern Australia. J. Ecol. 94, 369–382. https://doi.org/10.1111/j.1365-2745.2005.01084.x (2006).Article
Google Scholar
39.Dominiak, B. C. & Mapson, R. Revised distribution of Bactrocera tryoni in eastern Australia and effect on possible incursions of Mediterranean fruit fly: Development of Australia’s eastern trading block. J. Econ. Entomol. 110, 2459–2465 (2017).PubMed
Article
PubMed Central
Google Scholar
40.Bateman, M. Adaptations to temperature in geographic races of the Queensland fruit fly Dacus (Strumenta) tryoni. Aust. J. Zool. 15, 1141–1161 (1967).Article
Google Scholar
41.Bateman, M. Determinants of abundance in a population of the Queensland fruit fly. In: Southwood, T.R.E. (ed.) Insect abundance 119–131 (Blackwell Scientific Publications, London, 1968).42.Drew, R., Zalucki, M. & Hooper, G. Ecological studies of eastern Australian fruit flies (Diptera: Tephritidae) in their endemic habitat. Oecologia 64, 267–272 (1984).ADS
CAS
PubMed
Article
Google Scholar
43.Muthuthantri, S., Maelzer, D., Zalucki, M. P. & Clarke, A. R. The seasonal phenology of Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) in Queensland. Aust. J. Entomol. 49, 221–233. https://doi.org/10.1111/j.1440-6055.2010.00759.x (2010).Article
Google Scholar
44.Lloyd, A. C. et al. Area-wide management of fruit flies (Diptera: Tephritidae) in the Central Burnett district of Queensland. Aust. J. Crop Prot. 29, 462–469. https://doi.org/10.1016/j.cropro.2009.11.003 (2010).CAS
Article
Google Scholar
45.Pritchard, G. The ecology of a natural population of Queensland fruit fly, Dacus tryoni III. The maturation of female flies in relation to temperature. Aust. J. Zool. 18, 77–89 (1970).Article
Google Scholar
46.Clarke, A. R., Merkel, K., Hulthen, A. D. & Schwarzmueller, F. Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) overwintering: an overview. Aust. Entomol. 58, 3–8. https://doi.org/10.1111/aen.12369 (2019).Article
Google Scholar
47.Merkel, K. et al. Temperature effects on “overwintering” phenology of a polyphagous, tropical fruit fly (Tephritidae) at the subtropical/temperate interface. J. Appl. Entomol. 143, 754–765 (2019).CAS
Article
Google Scholar
48.Raghu, S., Clarke, A. R., Drew, R. A. & Hulsman, K. Impact of habitat modification on the distribution and abundance of fruit flies (Diptera: Tephritidae) in Southeast Queensland. Popul. Ecol. 42, 153–160 (2000).Article
Google Scholar
49.Novotny, V., Clarke, A. R., Drew, R. A., Balagawi, S. & Clifford, B. Host specialization and species richness of fruit flies (Diptera: Tephritidae) in a New Guinea rain forest. J. Trop. Ecol. 21, 67–77 (2005).Article
Google Scholar
50.Fletcher, B. Temperature-regulated changes in the ovaries of overwintering females of the Queensland Fruit Fly, Dacus tryoni. Aust. J. Zool. 23, 91–102 (1975).Article
Google Scholar
51.Meats, A. & Fay, H. The effect of acclimation on mating frequency and mating competitiveness in the Queensland fruit fly, Dacus tryoni, in optimal and cool mating regimes. Physiol. Entomol. 1, 207–212 (1976).Article
Google Scholar
52.Balagawi, S. Comparative ecology of Bactrocera Cucumis (French) and Bactrocera Tryoni (Froggatt) (Diptera: Tephritidae)—Understanding the life history consequences of host selection and oviposition behavior. Unpublished Thesis, Griffith University (2006).53.Lee, K. P. et al. Lifespan and reproduction in Drosophila: New insights from nutritional geometry. Proc. Natl. Acad. Sci. 105, 2498–2503 (2008).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
54.Carey, J. R., Liedo, P., Müller, H.-G., Wang, J.-L. & Vaupel, J. W. Dual modes of aging in Mediterranean fruit fly females. Science 281, 996–998 (1998).ADS
CAS
PubMed
Article
PubMed Central
Google Scholar
55.Fanson, B. G. & Taylor, P. W. Protein: carbohydrate ratios explain life span patterns found in Queensland fruit fly on diets varying in yeast: Sugar ratios. Age 34, 1361–1368 (2012).CAS
PubMed
Article
Google Scholar
56.McElderry, R. M. Seasonal life history trade-offs in two leafwing butterflies: Delaying reproductive development increases life expectancy. J. Insect Physiol. 87, 30–34 (2016).CAS
PubMed
Article
Google Scholar
57.Werfel, J., Ingber, D. E. & Bar-Yam, Y. Theory and associated phenomenology for intrinsic mortality arising from natural selection. PLoS ONE 12, e0173677 (2017).PubMed
PubMed Central
Article
CAS
Google Scholar
58.Kozeretska, I. A., Serga, S. V., Koliada, A. K. & Vaiserman, A. M. Epigenetic regulation of longevity in insects. Adv. Insect Physiol. 53, 87–114 (2017).Article
Google Scholar
59.Meats, A. Critical periods for developmental acclimation to cold in the Queensland fruit fly. Dacus tryoni. J. Insect Physiol. 29, 943–946 (1983).Article
Google Scholar
60.Kumaran, N. et al. Plant-mediated female transcriptomic changes post-mating in a tephritid fruit fly, Bactrocera tryoni. Genome Biol. Evol. 10, 94–107 (2018).CAS
PubMed
Article
Google Scholar
61.Dominiak, B. C., Sundaralingam, S., Jiang, L., Jessup, A. & Barchia, I. Production levels and life history traits of mass reared Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) during 1999/2002 in Australia. Plant Prot. Q. 23, 131–135 (2008).
Google Scholar
62.Fanson, B., Sundaralingam, S., Jiang, L., Dominiak, B. & D’arcy, G. A review of 16 years of quality control parameters at a mass-rearing facility producing Queensland fruit fly, Bactrocera tryoni. Entomol. Exp. Appl. 151, 152–159 (2014).Article
Google Scholar
63.Papadopoulos, N., Katsoyannos, B., Carey, J. & Kouloussis, N. Seasonal and annual occurrence of the Mediterranean fruit fly (Diptera: Tephritidae) in northern Greece. Ann. Entomol. Soc. Am. 94, 41–50 (2001).Article
Google Scholar
64.Brakefield, P. M. & Reitsma, N. Phenotypic plasticity, seasonal climate and the population biology of Bicyclus butterflies (Satyridae) in Malawi. Ecol. Entomol. 16, 291–303 (1991).Article
Google Scholar
65.Molleman, F., Zwaan, B., Brakefield, P. & Carey, J. Extraordinary long life spans in fruit-feeding butterflies can provide window on evolution of life span and aging. Exp. Gerontol. 42, 472–482 (2007).CAS
PubMed
PubMed Central
Article
Google Scholar
66.Denlinger, D. L. Dormancy in tropical insects. Ann. Rev. Entomol 31, 239–264 (1986).CAS
Article
Google Scholar
67.Canzano, A. A., Jones, R. E. & Seymour, J. E. Diapause termination in two species of tropical butterfly, Euploea core (Cramer) and Euploea sylvester (Fabricius) (Lepidoptera: Nymphalidae). Aust. J. Entomol 42, 352–356 (2003).Article
Google Scholar
68.Lankinen, P. & Forsman, P. Independence of genetic geographical variation between photoperiodic diapause, circadian eclosion rhythm, and Thr-Gly repeat region of the period gene in Drosophila littoralis. J. Biol. Rhythms 21, 3–12 (2006).CAS
PubMed
Article
PubMed Central
Google Scholar
69.Kouloussis, N. A. et al. Seasonal trends in Ceratitis capitata reproductive potential derived from live-caught females in Greece. Entomol. Exp. Appl. 140, 181–188. https://doi.org/10.1111/j.1570-7458.2011.01154.x (2011).Article
PubMed
PubMed Central
Google Scholar
70.Kouloussis, N. A. et al. Life table assay of field-caught Mediterranean fruit flies, Ceratitis capitata, reveals age bias. Entomol. Exp. Appl. 132, 172–181. https://doi.org/10.1111/j.1570-7458.2009.00879.x (2009).Article
PubMed
PubMed Central
Google Scholar
71.Tasnin, M. S., Silva, R., Merkel, K. & Clarke, A. R. Response of male Queensland fruit fly (Diptera: Tephritidae) to host fruit odors. J. Econ. Entomol. 113, 1888–1893 (2020).PubMed
Article
Google Scholar
72.Clarke, A. R., Powell, K. S., Weldon, C. W. & Taylor, P. W. The ecology of Bactrocera tryoni (Diptera: Tephritidae): What do we know to assist pest management?. Ann. Appl. Biol. 158, 26–54 (2011).Article
Google Scholar
73.Chinajariyawong, A., Drew, R., Meats, A., Balagawi, S. & Vijaysegaran, S. Multiple mating by females of two Bactrocera species (Diptera: Tephritidae: Dacinae). Bull. entomol. research 100, 325 (2010).CAS
Article
Google Scholar
74.Pike, N. & Meats, A. Potential for mating between Bactrocera tryoni (Froggatt) and Bactrocera neohumeralis (hardy) (Diptera: Tephritidae). Aust. J. Entomol. 41, 70–74 (2002).Article
Google Scholar
75.Tasnin, M. S., Merkel, K. & Clarke, A. R. Effects of advanced age on olfactory response of male and female Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). J. Insect Physiol. 122, 104024 (2020).CAS
PubMed
Article
Google Scholar
76.Perez-Staples, D., Prabhu, V. & Taylor, P. W. Post-teneral protein feeding enhances sexual performance of Queensland fruit flies. Physiol. Entomol. 32, 225–232 (2007).Article
Google Scholar More