Hostname: page-component-77c89778f8-9q27g Total loading time: 0 Render date: 2024-07-22T22:46:46.390Z Has data issue: false hasContentIssue false
  • English
  • Français

The effect of winter length on duration of dormancy and survival of specialized herbivorous Rhagoletis fruit flies from high elevation environments with acyclic climatic variability

Published online by Cambridge University Press:  19 September 2017

J. Rull ,
E. Tadeo ,
R. Lasa  and
M. Aluja
J. Rull*
Affiliation:
PROIMI Biotecnología-CONICET, LIEMEN-División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
E. Tadeo
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
R. Lasa
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
M. Aluja
Affiliation:
Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C., Xalapa, Veracruz 91070, México
*
*Author for correspondence: Tel: +54 381 434 4888 Fax: +54 381 434 4887 Email: pomonella@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Dormancy can be defined as a state of suppressed development allowing insects to cope with adverse conditions and plant phenology. Among specialized herbivorous insects exploiting seasonal resources, diapause frequently evolves as a strategy to adjust to predictable plant seasonal cycles. To cope with acyclic and unpredictable climatic events, it has been found for some insects that a proportion of the population undergoes prolonged dormancy. We compared the response of three species in the Rhagoletis cingulata species group exploiting plants differing in fruiting phenology from environments varying in frequency and timing of acyclic climatic catastrophic events (frost during flowering and fruit set) and varying also in the time of the onset of the rainy season. Small proportions (<2%) of Central and Northeastern Mexico R. cingulata and Rhagoletis turpiniae, and a few associated adult parasitoids, emerged without becoming dormant. Pupae exposed to 5°C for different periods of time (0–16 weeks) became dormant and emerged as adults in proportions <30%, compared with other studied species in the group from the USA (up to 80%). Large proportions (19–55%) of exposed pupae entered prolonged dormancy (>10 months), and large proportions of pupae died without emerging as adults. The number of days elapsed from the end of artificial winter and adult eclosion was longer for R. cingulata exploiting late fruiting Prunus serotina in Northeastern Mexico than for flies recovered from earlier fruiting plants in the central Altiplano. Rhagoletis turpiniae and northeastern R. cingulata pupae suffered high proportions of parasitism. Large proportions of R. cingulata from central Mexico engaging in prolonged dormancy may be explained by the fact that flowering and fruit set for its host, P. serotina var capuli, driven by the timing of maximum precipitation, matches a period of highest probability of frost often resulting in large areas with fruitless trees at unpredictable time intervals. As a consequence of differences in host plant fruiting phenology, central and northeastern Mexican R. cingulata were found to be allochronically isolated. Prolonged dormancy may have resulted in escape from parasitism.

Keywords

diapauseallochronic isolationhost plant phenologyTephritidaeprolonged dormancy
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 108 , Issue 4 , August 2018 , pp. 461 - 470
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

AliNiazee, M.T. (1975) Susceptibility of diapausing pupae of the western cherry fruit fly (Diptera: Tephritidae) and a parasite (Hymenoptera: Diapriidae) to subfreezing temperatures. Environmental Entomology 4, 1011–1013.Google Scholar
Aluja, M., Guillén, L., Rull, J., Höhn, H., Frey, J., Graf, B. & Samietz, J. (2011) Is the alpine divide becoming more permeable to biological invasions? – insights on the invasion and establishment of the walnut husk Fly, Rhagoletis completa (Diptera: Tephritidae) in Switzerland. Bulletin of Entomological Research 101, 451–465.CrossRefGoogle ScholarPubMed
Baerwald, R.J. & Boush, M.G. (1967) Selection of a nondiapausing race of apple maggot. Journal of Economic Entomology 60, 682–684.CrossRefGoogle Scholar
Baker, C.R.B. & Miller, G.W. (1978) The effect of temperature on the post-diapause development of four geographical populations of the European fruit fly (Rhagoletis cerasi). Entomologia Experimentalis et Applicata 23, 1–13.Google Scholar
Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K., Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, J., Hartley, S., Hefin Jones, T., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002). Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology 8, 1–16.CrossRefGoogle Scholar
Berlocher, S.H. (2000) Radiation and divergence in the Rhagoletis pomonella species group: inferences from allozymes. Evolution 54, 543–557.Google Scholar
Boller, E.F. & Bush, G.L. (1974) Evidence for genetic variation in populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera: Tephritidae) based on physiological parameters and hybridization experiments. Entomologia Experimentalis et Applicata, 17, 279–293.Google Scholar
Boller, E.F. & Prokopy, R.J. (1976) Bionomics and management of Rhagoletis. Annual Review of Entomology 21, 223–246.Google Scholar
Boyce, A.M. (1931) The diapause phenomenon, in insects, with special reference to Rhagoletis completa cress.(Diptera: Trypetidæ). Journal of Economic Entomology 24, 1018–1024.CrossRefGoogle Scholar
Bush, G.L. (1966). The taxonomy, cytology, and evolution of the genus Rhagoletis in North America (Diptera, Tephritidae). Bulletin of the Museum of Comparative Zoology 134, 431–562.Google Scholar
Brown, R.D. (1978) Gamma irradiation of the western cherry fruit fly for the sterile male control technique. PhD Thesis, Oregon State University, 240p.Google Scholar
Brown, R.D. & AliNiazee, M.T. (1977) Synchronization of adult emergence of the western cherry fruit fly in the laboratory. Annals of the Entomological Society of America 70, 678–680.CrossRefGoogle Scholar
Dambroski, H.R. & Feder, J.L. (2007) Host plant and latitude-related diapause variation in Rhagoletis pomonella: a test for multifaceted life history adaptation on different stages of diapause development. Journal of Evolutionary Biology 20, 2101–2112.Google Scholar
Dean, R.W. (1973). Bionomics of the Apple Maggot in Eastern. New York, Cornell University. Volume 3, 64p.Google Scholar
Donaldson-Matasci, M.C., Bergstrom, C.T. & Lachmann, M. (2013) When unreliable cues are good enough. The American Naturalist 182, 313–327.CrossRefGoogle ScholarPubMed
Dowell, R.V. & Penrose, R.L. (2012) Distribution and phenology of Rhagoletis fausta (Osten Sacken 1877) and Rhagoletis indifferens curren 1932 (Diptera: Tephritidae) in California. The Pan-Pacific Entomologist 88, 130–150.CrossRefGoogle Scholar
Feder, J.L. & Filchak, K.E. (1999) It's about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. pp. 211–225 in Proceedings of the 10th International Symposium on Insect-Plant Relationships. The Netherlands, Springer.CrossRefGoogle Scholar
Feder, J.L., Hunt, T.A. & Bush, G.L. (1993) The effects of climate, host plant phenology and host fidelity on the genetics of apple and hawthorn infesting races of Rhagoletis pomonella. Entomologia Experimentalis et Applicata 69, 117–135.Google Scholar
Feder, J.L., Berlocher, S.H., Roethele, J.B., Dambroski, H., Smith, J.J., Perry, W.L., Garvrilovic, V., Filchak, K.E., Rull, J. & Aluja, M. (2003) Allopatric genetic origins for sympatric host-plant shifts and race formation in Rhagoletis. Proceedings of the National Academy of Sciences 100, 10314–10319.Google Scholar
Feder, J.L., Xie, X., Rull, J., Velez, S., Forbes, A., Leung, B., Dambroski, H., Filchak, K.E. & Aluja, M. (2005) Mayr, Dobzhansky, and bush and the complexities of sympatric speciation in Rhagoletis. Proceedings of the National Academy of Sciences 102, 6573–6580.Google Scholar
Filchak, K.E., Roethele, J.B. & Feder, J.L. (2000) Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739–742.Google Scholar
Forbes, A.A., Powell, T.H.Q., Stelinski, L.L., Smith, J.J. & Feder, J.L. (2009) Sequential sympatric speciation across trophic levels. Science 323, 776–779.CrossRefGoogle ScholarPubMed
Forrest, J. & Miller-Rushing, A.J. (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philosophical Transactions of the Royal Society B 365, 3101–3112.CrossRefGoogle Scholar
Frick, K.E., Simkover, H.G. & Telford, H.S. (1954) Bionomics of the cherry fruit flies in eastern Washington. Bionomics of the Cherry Fruit Flies in Eastern Washington 13, 66 pp.Google Scholar
Geng, J., Li, Z.H., Rajotte, E.G., Wan, F.H., Lu, X.Y., & Wang, Z.L. (2011) Potential geographical distribution of Rhagoletis pomonella (Diptera: Tephritidae) in China. Insect Science 18, 575–582.CrossRefGoogle Scholar
Gourbière, S. & Menu, F. (2009) Adaptive dynamics of dormancy duration variability: evolutionary trade-off and priority effect lead to suboptimal adaptation. Evolution 63, 1879–1892.Google Scholar
Hood, G.R., Forbes, A.A., Powell, T.H., Egan, S.P., Hamerlinck, G., Smith, J.J. & Feder, J.L. (2015) Sequential divergence and the multiplicative origin of community diversity. Proceedings of the National Academy of Sciences USA 112, E5980–E5989.Google Scholar
Hough, A.F. (1965) Black cherry (Prunus serotina Ehrh.). pp. 539–545 in Fowells, H.A., (ed.) Silvics of Forest Trees of the United States. Washington, DC, Comp. U.S. Department of Agriculture, Agriculture Handbook 271.Google Scholar
Johannesen, J., Keyghobadi, N., Schuler, H., Stauffer, C. & Vogt, H. (2013) Invasion genetics of American cherry fruit fly in Europe and signals of hybridization with the European cherry fruit fly. Entomologia Experimentalis et Applicata, 147, 61–72.CrossRefGoogle Scholar
Klassen, W. (2005) Area-wide integrated pest management and the sterile insect technique. pp. 39–68 in Dyck, V.A., Hendrichs, J. & Robinson, A.S. (eds) Sterile Insect Technique. Netherlands, Springer.CrossRefGoogle Scholar
Köppler, K., Kaffer, T. & Vogt, H. (2009) Substantial progress made in the rearing of the European cherry fruit fly, Rhagoletis cerasi. Entomologia Experimentalis et Applicata 132, 283–288.Google Scholar
Koštál, V. (2006). Eco-physiological phases of insect diapause. Journal of Insect Physiology 52, 113–127.Google Scholar
Martínez, B.O.U.M. & Ruiz, C. (2005) Riesgo de heladas para la agricultura en la región sureste del estado de Coahuila. INIFAP-CIRNE. Campo Experimental Saltillo. Coahuila, México, Publicación Especial Núm. 5, 6.6p.Google Scholar
McVaugh, R. (1951) A revision of the North American black cherries (Prunus serotina Ehrh., and relatives). Brittonia, 7, 279–315.Google Scholar
Menu, F. (1993) Strategies of emergence in the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia 96, 383–390.CrossRefGoogle ScholarPubMed
Menu, F. & Debouzie, D. (1993) Coin-flipping plasticity and prolonged diapause in insects: example of the chestnut weevil Curculio elephas (Coleoptera: Curculionidae). Oecologia 93, 367–373.CrossRefGoogle ScholarPubMed
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2012) Prolonged pupal dormancy is associated with significant fitness cost for adults of Rhagoletis cerasi (Diptera: Tephritidae). Journal of Insect Physiology 58, 1128–1135.Google Scholar
Moraiti, C.A., Nakas, C.T. & Papadopoulos, N.T. (2014) Diapause termination of Rhagoletis cerasi pupae is regulated by local adaptation and phenotypic plasticity: escape in time through bet-hedging strategies. Journal of Evolutionary Biology 27, 43–54.Google Scholar
Nestel, D., Rempoulakis, P., Yanovski, L., Miranda, M.A. & Papadopoulos, N.T. (2016) The evolution of alternative control strategies in a traditional crop: economy and policy as drivers of olive fly control. pp. 47–76 in Horowitz, A.R. & Ishaaya, I. (eds) Advances in Insect Control and Resistance Management. Springer International Publishing.Google Scholar
Neven, L.G. & Yee, W.L. (2017) Impact of prolonged absence of low temperature on adult eclosion patterns of western cherry fruit fly (Diptera: Tephritidae). Environmental Entomology 46, 708–713.Google Scholar
Ortiz, W.R., Ruiz, S.G. & Fierro, R.S. (1992) Localización microclimática de zonas óptimas para la introducción del cultivo de la soya en el estado de Tlaxcala. Atmósfera 5, 169–179.Google Scholar
Ovruski, S.M., Wharton, R.A., Rull, J. & Guillén, L. (2007) Aganaspis alujai (Hymenoptera: Figitidae: Eucoilinae), a new species attacking Rhagoletis (Diptera: Tephritidae) in the Neotropical region. Florida Entomologist 90, 626–634.Google Scholar
Padilla, R.C. (1964) Mosca del capulín, una nueva plaga descubierta en la región de Texcoco, México. Fitofilo 43: 9–18.Google Scholar
Prokopy, R.J. (1968) The influence of photoperiod, temperature and food on the initiation of diapause in the apple maggot. Canadian Entomologist 100, 318–329.Google Scholar
Prokopy, R.J. & Papaj, D.R. (2000) Behavior of flies of the genera Rhagoletis, Zonosemata, and Carpomya (Trypetinae: Carpomyina). Fruit Flies. pp. 219–252 in Aluja, M. & Norrbom, A.L. (eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Qin, Y., Paini, D.R., Wang, C., Fang, Y. & Li, Z. (2015) Global establishment risk of economically important fruit fly species (Tephritidae). PLoS ONE 10, e0116424.Google Scholar
Rull, J., Aluja, M., Feder, J. & Berlocher, S. (2006) Distribution and host range of hawthorn-infesting Rhagoletis (Diptera: Tephritidae) in Mexico. Annals of the Entomological Society of America 99, 662–672.CrossRefGoogle Scholar
Rull, J., Wharton, R., Feder, J.L., Guillén, L., Sivinski, J., Forbes, A. & Aluja, M. (2009) Latitudinal variation in parasitoid guild composition and parasitism rates of North American hawthorn infesting Rhagoletis. Environmental Entomology 38, 588–599.Google Scholar
Rull, J., Aluja, M., Feder, J.L. (2011) Distribution and basic biology of black cherry-infesting Rhagoletis (Diptera: Tephritidae) in México. Annals of the Entomological Society of America 104, 202–211.Google Scholar
Rull, J., Tadeo, E., Lasa, R. & Aluja, M. (2016) The effect of winter length on survival and duration of dormancy of four sympatric species of Rhagoletis exploiting plants with different fruiting phenology. Bulletin of Entomological Research 106, 818–826.Google Scholar
Smith, J.J. & Bush, G.L. (2000) Phylogeny of the subtribe Carpomyina (Trypetinae), emphasizing relationships of the genus Rhagoletis. pp. 187–217 in Aluja, M. & Norrbom, A.L. (eds) Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL, CRC Press.Google Scholar
Sosa, V. (1988) Staphyleaceae. Flora de Veracruz. Fascículo 57. Xalapa, Veracruz, México.Google Scholar
Stark, S.B. & AliNiazee, M.T. (1982) Model of postdiapause development in the western cherry fruit fly. Environmental Entomology 11, 471–474.Google Scholar
Schwarz, D., McPheron, B.A., Hartl, G.B., Boller, E.F. & Hoffmeister, T.S. (2003) A second case of genetic host races in Rhagoletis?. A population genetic comparison of sympatric host populations in the European cherry fruit fly, Rhagoletis cerasi. Entomologia Experimentalis et Applicata 108, 11–17.Google Scholar
Tadeo, E., Feder, J.L., Egan, S., Schuler, H., Aluja, M., Rull, J. (2015) Divergence and evolution of reproductive barriers among three allopatric populations of Rhagoletis cingulata across eastern North America and México. Entomología Experimentalis et Applicata 156, 301–311.Google Scholar
Tauber, M.J., Tauber, C.A. & Masaki, S. (1986) Seasonal Adaptations of Insects. New York, NY, Oxford University Press on Demand.Google Scholar
Teixeira, L.A., Isaacs, R. & Gut, L.J. (2007) Habitat-specific flight period in the cherry fruit fly Rhagoletis cingulata (Loew)(Diptera: Tephritidae). Environmental Entomology 36, 1339–1348.Google Scholar
Vallo, V., Remund, U. & Boller, E.F. (1976) Storage conditions of stockpiled diapausing pupae of Rhagoletis cerasi for obtaining high emergence rates. BioControl 21, 251–256.Google Scholar
Van Kirk, J.R. & AliNiazee, M.T. (1981) Determining low-temperature threshold for pupal development of the western cherry fruit fly for use in phenology models. Environmental Entomology 10, 968–971.Google Scholar
Van Kirk, J.R. & AliNiazee, M.T. (1982) Diapause development in the western cherry fruit fly, Rhagoletis indifferens Curran (Diptera, Tephritidae). Journal of Applied Entomology 93, 440–445.Google Scholar
Verheggen, F., Verhaeghe, A., Giordanengo, P., Tassus, X. & Escobar-Gutiérrez, A. (2017) Walnut husk fly, Rhagoletis completa (Diptera: Tephritidae), invades Europe: invasion potential and control strategies. Applied Entomology and Zoology 52, 1–7.Google Scholar
Xie, X., Rull, J., Michel, A.P., Velez, S., Forbes, A.A., Lobo, N.F., Aluja, M. & Feder, J.L. (2007) Hawthorn-infesting populations of Rhagoletis pomonella in Mexico and speciation mode plurality. Evolution 61, 1091–1105.Google Scholar
Xie, X., Michel, A.P., Schwarz, D., Rull, J., Velez, S., Forbes, A.A., Aluja, M. & Feder, J.L. (2008) Radiation and divergence in the Rhagoletis pomonella species complex: inferences from DNA sequence data. Journal of Evolutionary Biology 21, 900–913.Google Scholar
Yee, W.L., Goughnour, R.B., Hood, G.R., Forbes, A.A. & Feder, J.L. (2015) Chilling and host plant/site-associated eclosion times of Western cherry fruit fly (Diptera: Tephritidae) and a host-specific parasitoid. Environmental Entomology 44, 1029–1042.Google Scholar