Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-24T02:46:27.983Z Has data issue: false hasContentIssue false

Host plant stimuli effects on survival and duration of dormancy of Rhagoletis zoqui, Rhagoletis completa (Diptera: Tephritidae) and associated parasitoids

Published online by Cambridge University Press:  10 March 2022

J. Rull*
Affiliation:
PROIMI Biotecnología-CONICET, LIEMEN-División Control Biológico de Plagas, Av. Belgrano y Pje. Caseros, T4001MVB San Miguel de Tucumán, Tucumán, Argentina
R. Lasa
Affiliation:
Instituto de Ecología, A.C., - INECOL, Clúster Científico y Tecnológico BioMimic®, Carretera Antigua a Coatepec 351, Colonia el Haya, CP 91073 Xalapa, Veracruz, México
S. Aguas-Lanzagorta
Affiliation:
Instituto de Ecología, A.C., - INECOL, Clúster Científico y Tecnológico BioMimic®, Carretera Antigua a Coatepec 351, Colonia el Haya, CP 91073 Xalapa, Veracruz, México
M. Aluja
Affiliation:
Instituto de Ecología, A.C., - INECOL, Clúster Científico y Tecnológico BioMimic®, Carretera Antigua a Coatepec 351, Colonia el Haya, CP 91073 Xalapa, Veracruz, México
*
Author for correspondence: J. Rull, Email: pomonella@gmail.com

Abstract

Tephritid fruit flies in the genus Rhagoletis bridge between predictable periods of fruit availability by becoming dormant. To cope with acyclic unpredictable events (e.g., frost, mast seeding, etc), a proportion of the population can undergo prolonged dormancy. In the case of walnut infesting Rhagoletis, host plant-derived cues such as juglone soil concentration vary seasonally in predictable patterns. Here, we examined the effects of host plant parts and derived compounds on emergence rates and dormancy duration of Rhagoletis completa (Cresson), Rhagoletis zoqui (Bush) (Diptera: Tephritidae), and associated parasitoids. Pupae of both species were exposed to walnut leaves, fruit, or fruit and leaves and compared to a control. In a second experiment, R. zoqui were exposed to 10 mg l−1 of juglone applied to pupation medium during four consecutive 4-week time periods under variable combinations of temperature and frequency of exposure. Overall, the presence of fruit resulted in greater overwintering survival of R. completa but had no effect on the duration of dormancy of either fly species. Application of juglone over two consecutive periods produced greater mortality of R. zoqui than the control. Three parasitoid species emerged from R. completa and one from R. zoqui. Duration of dormancy for parasitoids was longer than that of fly hosts. Regardless of treatment, 13.3–18.4% of R. completa pupae and 1.3–2.8% R. zoqui engaged in prolonged (>year) dormancy. Our results indicate that host plant derived cues have little or no effect on survival and duration of dormancy of walnut infesting Rhagoletis, and at the tested concentration juglone is toxic to R. zoqui pupae. Testing the effect of juglone at lower concentrations is necessary to rule out its role as an environmental cue for regulation of dormancy. So far, host plant fruiting phenology appears to play a greater role than host plant derived cues in selecting for fly eclosion times.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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

Alonso-Pimentel, H, Korer, JB, Nufio, C and Papaj, DR (1998) Role of color and shape stimuli in host-enhanced oogenesis in the walnut fly, Rhagoletis juglandis. Physiological Entomology 23, 97104.CrossRefGoogle Scholar
Baker, CRB and Miller, GW (1978) The effect of temperature on the post-diapause development of four geographical populations of the European cherry fruit fly (Rhagoletis cerasi). Entomologia Experimentalis et Applicata 23, 113.CrossRefGoogle Scholar
Berlocher, SH (2000) Radiation and divergence in the Rhagoletis pomonella species group: inferences from allozymes. Evolution 54, 543557.CrossRefGoogle ScholarPubMed
Boller, EF and Prokopy, RJ (1976) Bionomics and management of Rhagoletis. Annual Review of Entomology 21, 223246.CrossRefGoogle Scholar
Boyce, AM (1931) The diapause phenomenon, in insects, with special reference to Rhagoletis completa Cress. (Diptera: Trypetidæ). Journal of Economic Entomology 24, 10181024.CrossRefGoogle Scholar
Bush, GL (1966) The taxonomy, cytology, and evolution of the genus Rhagoletis in North America (Diptera, Tephritidae). Bulletin of the Harvard Museum of Comparative Zoology 134, 431562.Google Scholar
Coder, KD (1983) Seasonal changes of juglone potential in leaves of black walnut (Juglans nigra L.). Journal of Chemical Ecology 9, 12031212.CrossRefGoogle Scholar
Cosmulescu, SN, Trandafir, I, Achim, G and Baciu, A (2011) Juglone content in leaf and green husk of five walnut (Juglans regia L.) cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 39, 237240.CrossRefGoogle Scholar
Dambroski, HR and Feder, JL (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, 21012112.CrossRefGoogle ScholarPubMed
Dana, MN and Lerner, BR (2001) Black walnut toxicity. Department of Horticulture, Purdue University, Cooperative Extension Service.Google Scholar
Dean, RW (1973) Bionomics of the apple maggot in eastern New York, Cornell University. Volume 3, 64p.Google Scholar
Denlinger, DL (1986) Dormancy in tropical insects. Annual Review of Entomology 31, 239264.CrossRefGoogle ScholarPubMed
de Scisciolo, B, Leopold, DJ and Walton, DC (1990) Seasonal patterns of juglone in soil beneath Juglans nigra (black walnut) and influence of J. nigra on understory vegetation. Journal of Chemical Ecology 16, 11111130.CrossRefGoogle Scholar
Dudley, R (2004) Ethanol, fruit ripening, and the historical origins of human alcoholism in primate frugivory. Integrative and Comparative Biology 44, 315323.CrossRefGoogle ScholarPubMed
Feder, JL and Filchak, KE (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. In: Proceedings of the 10th International Symposium on Insect-Plant Relationships (pp. 211–225). Springer, Dordrecht.CrossRefGoogle Scholar
Feder, JL, Stolz, U, Lewis, KM, Perry, W, Roethele, JB and Rogers, A (1997) The effects of winter length on the genetics of apple and hawthorn races of Rhagoletis pomonella (Diptera: Tephritidae). Evolution 51, 18621876.CrossRefGoogle Scholar
Filchak, KE, Roethele, JB and Feder, JL (2001) Effects of photoperiod and light intensity on the genetics of diapause in the apple maggot (Diptera: Tephritidae). Annals of the Entomological Society of America 94, 902908.CrossRefGoogle Scholar
Numerical Algorithms Group (1993) In Francis, B, Green, M, Payne, C (eds.), The GLIM System: Release 4 Manual. (821p) Oxford, UK: Oxford University Press.Google Scholar
Gill, HK, Goyal, G and Chahil, G (2017) Insect diapause: a review. Journal of Agricultural Science and Technology 7, 454473.Google Scholar
Hodek, I, Bonet, A and Hodkova, M (1981) Some ecological factors affecting diapause in adults of Acanthoscelides obtectus from Mexican mountains. In Labeyrie, V (ed.), The Ecology of Bruchids Attacking Legumes (Pulses). Dordrecht: Springer, pp. 4355.CrossRefGoogle Scholar
Islam, AKM and Widhalm, JR (2020) Agricultural uses of juglone: opportunities and challenges. Agronomy 10, 1500.CrossRefGoogle Scholar
Jamovi Statistical Software, , Version 0.9.1.12. Available online: https://www.jamovi.org (accessed on 14 April 2019).Google Scholar
Jose, S and Gillespie, AR (1998) Allelopathy in black walnut (Juglans nigra L.) alley cropping. I. Spatio-temporal variation in soil juglone in a black walnut–corn (Zea mays L.) alley cropping system in the midwestern USA. Plant and Soil 203, 191197.CrossRefGoogle Scholar
Kelly, D and Sork, VL (2002) Mast seeding in perennial plants: why, how, where? Annual Review of Ecology and Systematics 33, 427447.CrossRefGoogle Scholar
Moraiti, CA, Nakas, CT and Papadopoulos, NT (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, 4354.CrossRefGoogle ScholarPubMed
Neilson, WTA (1962) Effects of temperature on development of overwintering pupae of the apple maggot, Rhagoletis pomonella (Walsh). Canadian Entomologist 94, 924928.CrossRefGoogle Scholar
Neilson, WTA (1964) Some effects of relative humidity on development of pupae of the apple maggot, Rhagoletis pomonella (Walsh). Canadian Entomologist 96, 810811.CrossRefGoogle Scholar
Neven, LG and Yee, WL (2017) Impact of prolonged absence of low temperature on adult eclosion patterns of western cherry fruit fly (Diptera: Tephritidae). Environmental Entomology 46, 708713.CrossRefGoogle Scholar
Nufio, CR, Papaj, DR and Alonso-Pimentel, H (2000) Host utilization by the walnut fly, Rhagoletis juglandis (Diptera: Tephritidae). Environmental Entomology 29, 9941001.CrossRefGoogle Scholar
Oroño, L, Aluja, M, Ovruski, S, Rull, J, Interdonato, R, Prado, FE and Hilal, M (2019) Dynamics of soluble sugars and secondary metabolites in fruit of Juglans australis attacked by Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). Arthropod-Plant Interactions 13, 411421.CrossRefGoogle Scholar
Papaj, DR (2005) Ovarian dynamics in relation to host quality in the walnut-infesting fly, Rhagoletis juglandis. Functional Ecology 19, 396404.CrossRefGoogle Scholar
Prokopy, RJ (1968) The influence of photoperiod, temperature and food on the initiation of diapause in the apple maggot. Canadian Entomologist 100, 318329.CrossRefGoogle Scholar
Prokopy, RJ and Papaj, DR (2000) Behavior of flies of the genera Rhagoletis, Zonosemata, and Carpomya (Trypetinae: Carpomyina). In Aluja, M & Norrbom, AL (eds), Fruit Flies (Tephritidae): Phylogeny and Evolution of Behavior. Boca Raton, FL: CRC Press, pp. 219252.Google Scholar
Rull, J, Aluja, M, Feder, JL and Berlocher, SH (2006) The distribution and host range of hawthorn-infesting Rhagoletis (Diptera: Tephritidae) in Mexico. Annals of the Entomological Society of America 100, 213233.Google Scholar
Rull, J, Aluja, M, Guillen, L, Egan, S, Glover, M and Feder, JL (2013) Distribution, host plant affiliation, phenology, and phylogeny of walnut-infesting Rhagoletis flies (Diptera: Tephritidae) in Mexico. Biological Journal of the Linnean Society 110, 765779.CrossRefGoogle Scholar
Rull, J, Tadeo, E, Lasa, R and 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, 818826.CrossRefGoogle ScholarPubMed
Rull, J, Tadeo, E, Lasa, R and Aluja, M (2018) 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. Bulletin of Entomological Research 108, 461470.CrossRefGoogle ScholarPubMed
Rull, J, Lasa, R, Guillén, L and Aluja, M (2019a) The effect of winter length on duration of dormancy and survival of Rhagoletis completa (Diptera: Tephritidae) and associated parasitoids from Northeastern Mexico. Journal of Insect Science 19, 7.CrossRefGoogle Scholar
Rull, J, Lasa, R and Aluja, M (2019b) The effect of seasonal humidity on survival and duration of dormancy on diverging Mexican Rhagoletis pomonella (Diptera: Tephritidae) populations inhabiting different environments. Environmental Entomology 48, 11211128.CrossRefGoogle Scholar
Smith, DC (1988) Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature 336, 6667.CrossRefGoogle Scholar
Stapanian, MA and Smith, CC (1978) A model for seed scatter hoarding: coevolution of fox squirrels and black walnuts. Ecology 59, 884896.CrossRefGoogle Scholar
Thiboldeaux, RL, Lindroth, RL and Tracy, JW (1994) Differential toxicity of juglone (5-hydroxy-1, 4–naphthoquinone) and related naphthoquinones to saturniid moths. Journal of Chemical Ecology 20, 16311641.CrossRefGoogle ScholarPubMed
Von Kiparski, GR, Lee, LS and Gillespie, AR (2007) Occurrence and fate of the phytotoxin juglone in alley soils under black walnut trees. Journal of Environmental Quality 36, 709717.CrossRefGoogle ScholarPubMed
Willis, RJ (2000) Juglans spp., juglone and allelopathy. Allelopathy Journal 7, 155.Google Scholar
Yee, WL (2013) Soil moisture and relative humidity effects during postdiapause on the emergence of western cherry fruit fly (Diptera: Tephritidae). Canadian Entomologist 145, 317326.CrossRefGoogle Scholar
Yee, WL, Hernández-Ortiz, V, Rull, J, Sinclair, BJ and Neven, LG (2014) Status of Rhagoletis (Diptera: Tephritidae) pests in the NAPPO countries. Journal of Economic Entomology 107, 1128.CrossRefGoogle ScholarPubMed