Eur. J. Entomol. 119: 191-200, 2022 | DOI: 10.14411/eje.2022.021

Effects of population density on adult morphology and life-history traits of female Mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae)Original article

Santhi BHAVANAM ORCID..., Steven A. TREWICK ORCID...
Wildlife & Ecology, School of Natural Sciences, Massey University, Palmerston North, Manawatu-Wanganui, New Zealand; e-mails: santhypriya@gmail.com, S.Trewick@massey.ac.nz

Intraspecific competition and food shortage due to high population density during early life can have a profound effect on adult fitness. Organisms often mitigate negative effects of high population density by adjusting resource allocation to adult morphological and life-history traits. In Lepidoptera with short-lived adults that do not feed, it is predicted that females developed from dense larval aggregations invest more in reproduction and traits linked to offspring survival. Here, we investigated the effects of larval population density on adult morphology and life-history traits in the female Mediterranean flour moth, Ephestia kuehniella by raising larvae at a range of population densities. Adults from high population density (16 larvae per g of food) had smaller head, thorax, and forewing compared to other densities. The allometric slope of forewing length with body mass did not differ among population densities, indicating no changes in adult wing morphology at high population density. However, we found that females emerged from larvae at high population density had bigger abdomens relative to body mass, indicating resource investment in reproduction, probably to mitigate the negative effects of crowding on egg production. Ovipositor length did not differ among population densities, indicating conservation of resources to structures with egg-laying function that affect offspring survival. Taken together, these results suggest that female E. kuehniella responding to high larval population density invest relatively more in reproduction, a life-history strategy that could alleviate negative effects of population density on fitness. This study also highlights the importance of a species' reproductive strategy in its adaptive response to environmental conditions, which is relevant to many capital breeders dependent on larval resources for reproduction.

Keywords: Reproduction, allometry, trade-off, nutrition

Received: April 14, 2021; Revised: April 22, 2022; Accepted: April 22, 2022; Published online: May 24, 2022  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
BHAVANAM, S., & TREWICK, S.A. (2022). Effects of population density on adult morphology and life-history traits of female Mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae). EJE, 119, Article 191-200. https://doi.org/10.14411/eje.2022.021
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Almbro M. & Kullberg C. 2012: Weight loading and reproductive status affect the flight performance of Pieris napi butterflies. - J. Insect Behav. 25: 441-452. Go to original source...
    2. Anderson P. & Lofqvist J. 1996: Asymmetric oviposition behaviour and the influence of larval competition in the two pyralid moths Ephestia kuehniella and Plodia interpunctella. - Oikos 76: 47-56. Go to original source...
    3. Bauerfeind S.S. & Fischer K. 2008: Maternal body size as a morphological constraint on egg size and fecundity in butterflies. - Basic Appl. Ecol. 9: 443-451. Go to original source...
    4. Bauerfeind S.S., Fischer K., Hartstein S., Janowitz S. & Martin-Creuzburg D. 2007: Effects of adult nutrition on female reproduction in a fruit-feeding butterfly: the role of fruit decay and dietary lipids. - J. Insect Physiol. 53: 964-973. Go to original source...
    5. Berdegue M., Reitz S.R. & Trumble J.T. 1998: Host plant selection and development in Spodoptera exigua: do mother and offspring know best? - Entomol. Exp. Appl. 89: 57-64. Go to original source...
    6. Bhavanam S. & Trewick S. 2017: Effects of larval crowding and nutrient limitation on male phenotype, reproductive investment and strategy in Ephestia kuehniella Z. (Insecta: Lepidoptera). - J. Stor. Prod. Res. 71: 64-71. Go to original source...
    7. Bhavanam S., Wang Q. & He X. 2012: Effect of nutritional stress and larval crowding on survival, development and reproductive output of Mediterranean flour moth, Ephestia kuehniella Z. - N. Z. Plant Prot. 65: 138-141. Go to original source...
    8. Boggs C.L. 1981: Nutritional and life-history determinants of resource-allocation in holometabolous insects. - Am. Nat. 117: 692-709. Go to original source...
    9. Boggs C.L. 2009: Understanding insect life histories and senescence through a resource allocation lens. - Funct. Ecol. 23: 27-37. Go to original source...
    10. Boggs C.L. & Niitepold K. 2016: Effects of larval dietary restriction on adult morphology, with implications for flight and life history. - Entomol. Exp. Appl. 159: 189-196. Go to original source...
    11. Bonduriansky R. 2001: The evolution of male mate choice in insects: a synthesis of ideas and evidence. - Biol. Rev. 76: 305-339. Go to original source...
    12. Calvert I. & Corbert S.A. 1973: Reproductive maturation and pheromone release in the flour moth Anagasta kuehniella Z. - J. Entomol. (A) 47: 201-209. Go to original source...
    13. Campero M., De Block M., Ollevier F. & Stoks R. 2008: Metamorphosis offsets the link between larval stress, adult asymmetry and individual quality. - Funct. Ecol. 22: 271-277. Go to original source...
    14. Chapman R.F. 1998: The Insects: Structure and Function. Cambridge University Press, New York, 770 pp. Go to original source...
    15. Cheng Y.X., Luol L.Z., Sappington T.W., Jiangl X.F., Zhang L. & Frolov A.N. 2016: Onset of oviposition triggers abrupt reduction in migratory hlight behavior and flight muscle in the female beet webworm, Loxostege sticticalis. - PLoS ONE 11: e0166859, 15 pp. Go to original source...
    16. Corbet A.S. & Tams W.H.T. 1943: Keys for the identification of the Lepidoptera infesting stored food products. - Proc. Zool. Soc. Lond. (B) 113: 55-145. Go to original source...
    17. Davis R.B., Javois J., Kaasik A., Ounap E. & Tammaru T. 2016: An ordination of life histories using morphological proxies: capital vs. income breeding in insects. - Ecology 97: 2112-2124. Go to original source...
    18. De Gasperin O., Duarte A., English S., Attisano A. & Kilner R.M. 2019: The early-life environment and individual plasticity in life-history traits. - Ecol. Evol. 9: 339-351. Go to original source...
    19. Dmitriew C., Carroll J. & Rowe L. 2009: Effects of early growth conditions on body composition, allometry, and survival in the ladybird beetle Harmonia axyridis. - Can. J. Zool. 87: 175-182. Go to original source...
    20. Dudley R. 1999: The Biomechanics of Insect Flight: Form, Function, Evolution. Princeton University Press, NJ, 496 pp. Go to original source...
    21. Edwards R.L. 1954: The effect of diet on egg maturation and resorption in Mormoniella vitripennis (Hymenoptera, Pteromalidae). - Q. J. Microsc. Sci. 95: 459-468. Go to original source...
    22. Elliott C.G. & Evenden M.L. 2012: The effect of flight on reproduction in an outbreaking forest lepidopteran. - Physiol. Entomol. 37: 219-226. Go to original source...
    23. English S., Fawcett T.W., Higginson A.D., Trimmer P.C. & Uller T. 2016: Adaptive use of information during growth can explain long-term effects of early life experiences. - Am. Nat. 187: 620-632. Go to original source...
    24. Evenden M.L., Whitehouse C.M. & Jones B.C. 2015: Resource allocation to flight in an outbreaking forest defoliator Malacosoma disstria. - Environ. Entomol. 44: 835-845. Go to original source...
    25. Ferguson H.J., Eaton J.L. & Rogers C.E. 1997: Larval rearing density effects on lipid reserves and wing-loading in fall armyworm adults (Lepidoptera: Noctuidae). - J. Agric. Entomol. 14: 369-384.
    26. Fox J. & Weisberg S. 2019: An R Companion to Applied Regression. Sage, Thousand Oaks, CA, 472 pp.
    27. Garrad R., Booth D.T. & Furlong M.J. 2016: The effect of rearing temperature on development, body size, energetics and fecundity of the diamondback moth. - Bull. Entomol. Res. 106: 175-181. Go to original source...
    28. Gibbs M. & Van Dyck H. 2010: Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. - Oecologia 163: 341-350. Go to original source...
    29. Gibbs M., Van Dyck H. & Breuker C.J. 2018: Flight-induced transgenerational maternal effects influence butterfly offspring performance during times of drought. - Oecologia 186: 383-391. Go to original source...
    30. Haeler E., Fiedler K. & Grill A. 2014: What prolongs a butterfly's life?: Trade-offs between dormancy, fecundity and body size. - PLoS ONE 9: e111955, 10 pp. Go to original source...
    31. Heisswolf A., Klemola T., Andersson T. & Ruohomäki K. 2009: Shifting body weight-fecundity relationship in a capital breeder: maternal effects on egg numbers of the autumnal moth under field conditions. - Bull. Entomol. Res. 99: 73-81. Go to original source...
    32. Hill D.S. 2002: Pests of Stored Foodstuffs and their Control. Kluwer Academic Publishers, New York, 496 pp.
    33. Hoffmann A.A. & Loeschcke V. 2006: Are fitness effects of density mediated by body size? Evidence from Drosophila field releases. - Evol. Ecol. Res. 8: 813-828.
    34. Hou Z.H., Zhong H.Y., Nansen C. & Wei C. 2019: An integrated analysis of hyperspectral and morphological data of cicada ovipositors revealed unexplored links to specific oviposition hosts. - Zoomorphology 138: 265-276. Go to original source...
    35. Huang B., Shi Z.-H. & Hou Y.-M. 2019: Tradeoff between triglyceride consumption and ovariole development in Plutella xylostella (L.) released in mixed-host environments. - J. Integr. Agric. 18: 865-872. Go to original source...
    36. Jacob T.A. & Cox P.D. 1977: Influence of temperature and humidity on life-cycle of Ephestia kuehniella Z. (Lep. Pyralidae). - J. Stor. Prod. Res. 13: 107-118. Go to original source...
    37. Jannot J.E., Brunea E. & Wissinger S.A. 2007: Effects of larval energetic resources on life history and adult allocation patterns in a caddisfly (Trich. Phryganeidae). - Ecol. Entomol. 32: 376-383. Go to original source...
    38. Jaumann S. & Snell-Rood E.C. 2017: Butterflies do not alter conspecific avoidance in response to variation in density. - Integr. Comp. Biol. 57: 396-406. Go to original source...
    39. Jaumann S. & Snell-Rood E.C. 2019: Adult nutritional stress decreases oviposition choosiness and fecundity in female butterflies. - Behav. Ecol. 30: 852-863. Go to original source...
    40. Jervis M.A., Boggs C.L. & Ferns P.N. 2007: Egg maturation strategy and survival trade-offs in holometabolous insects: a comparative approach. - Biol. J. Linn. Soc. 90: 293-302. Go to original source...
    41. Jiang X.F., Luo L.Z. & Sappington T.W. 2010: Relationship of flight and reproduction in beet armyworm, Spodoptera exigua (Lepidoptera: Noctuidae), a migrant lacking the oogenesis-flight syndrome. - J. Insect Physiol. 56: 1631-1637. Go to original source...
    42. Johnson C.G. 1969: Migration and Dispersal of Insects by Flight. Methuen, London, 763 pp.
    43. Johnson H., Solensky M.J., Satterfield D.A. & Davis A.K. 2014: Does skipping a meal matter to a butterfly's appearance? Effects of larval food stress on wing morphology and color in Monarch butterflies. - PLoS ONE 9: e93492, 9 pp. Go to original source...
    44. Jyothi P., Aralimarad P., Wali V., Dave S., Bheemanna M., Ashoka J., Shivayogiyappa P., Lim K.S., Chapman J.W. & Sane S.P. 2021: Evidence for facultative migratory flight behavior in Helicoverpa armigera (Noctuidae: Lepidoptera) in India. - PLoS ONE 16: e0245665, 13 pp. Go to original source...
    45. Karlsson B., Stjernholm F. & Wiklund C. 2008: Test of a developmental trade-off in a polyphenic butterfly: direct development favours reproductive output. - Funct. Ecol. 22: 121-126. Go to original source...
    46. Khuhro N.H., Biondi A., Desneux N., Zhang L., Zhang Y. & Chen H. 2014: Trade-off between flight activity and life-history components in Chrysoperla sinica. - BioControl 59: 219-227. Go to original source...
    47. Kivela S.M., Valimaki P., Carrasco D., Maenpaa M.I. & Manttari S. 2012: Geographic variation in resource allocation to the abdomen in geometrid moths. - Naturwissenschaften 99: 607-616. Go to original source...
    48. Kong H.L., Luo L.Z., Jiang X.F. & Zhang L. 2010: Effects of larval density on flight potential of the beet webworm, Loxostege sticticalis (Lepidoptera: Pyralidae). - Environ. Entomol. 39: 1579-1585. Go to original source...
    49. Kong H., Zhang Y., Zhu S., Kong Y., Wu L. & Hu R. 2013: Effects of larval density on growth, development and reproduction of diamondback moth (DBM), Plutella xylostella L. - J. Eco-Agric. 21: 474-479. Go to original source...
    50. Le Roy C., Debat V. & Llaurens V. 2019: Adaptive evolution of butterfly wing shape: from morphology to behaviour. - Biol. Rev. 94: 1261-1281. Go to original source...
    51. Lenth R.V. 2016: Least-squares means: The R Package lsmeans. - J. Stat. Softw. 69: 1-33. Go to original source...
    52. Lima Filho M., Favero S. & de Lima J.O.G. 2001: Produção de Anagasta kuehniella Z. (Lep. Pyralidae) com a utilização de fubá de milho na dieta artificial. - Neotrop. Entomol. 30: 37-42. Go to original source...
    53. Malcolm S.B., Vargas N.R., Rowe L., Stevens J., Armagost J. E. & Johnson A.C. 2018: Sequential partial migration across monarch generations in Michigan. - Anim. Migrat. 5: 104-114. Go to original source...
    54. Menken S.B.J., Boomsma J.J. & van Nieukerken E.J. 2010: Large-scale evolutionary patterns of host plant associations in the Lepidoptera. - Evolution 64: 1098-1119. Go to original source...
    55. Mevi-Schütz J. & Erhardt A. 2005: Amino acids in nectar enhance butterfly fecundity: a long-awaited link. - Am. Nat. 165: 411-419. Go to original source...
    56. Moghadamfar Z., Pakyari H. & Amir-Maafi M. 2020: Age-stage, two-sex life table of Ephestai kuheniella (Lep. Pyrallidae) at different constant temperatures. - Crop Prot. 137: 105200, 6 pp Go to original source...
    57. Monaghan P. 2008: Early growth conditions, phenotypic deve­lopment and environmental change. - Phil. Trans. R. Soc. (B) 363: 1635-1645. Go to original source...
    58. Niitepõld K. 2019: Effects of flight and food stress on energetics, reproduction, and lifespan in the butterfly Melitaea cinxia. - Oecologia 191: 271-283. Go to original source...
    59. Niitepõld K. & Hanski I. 2013: A long life in the fast lane: positive association between peak metabolic rate and lifespan in a butterfly. - J. Exp. Biol. 216: 1388-1397. Go to original source...
    60. Nijhout H.F. & Grunert L.W. 2010: The cellular and physiological mechanism of wing-body scaling in Manduca sexta. - Science 330: 1693-1695. Go to original source...
    61. Norris M.J. 1934: Contributions towards the study of insect fertility. III. Adult nutrition, fecundity, and longevity in the genus Ephestia (Lepidoptera, Phycitidae). - Proc. Zool. Soc. Lond. 1934: 333-360. Go to original source...
    62. Norris M.J. & Richards M. 1932: Contributions towards the study of insect fertility. I. The structure and operation of the reproductive organs of the genera Ephestia and Plodia (Lepidoptera, Phycitidae). - Proc. Zool. Soc. Lond. 1932: 595-612. Go to original source...
    63. Pilakouta N., Halford C., Racz R. & Smiseth P.T. 2016: Effects of prior contest experience and contest outcome on female reproductive decisions and ofspring fitness. - Am. Nat. 188: 319-328. Go to original source...
    64. R Core Team 2021: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, URL: http://www.r-project.org/index.html
    65. Rainford J.L., Hofreiter M., Nicholson D.B. & Mayhew P.J. 2014: Phylogenetic distribution of extant richness suggests metamorphosis is a key innovation driving diversification in insects. - PLoS ONE 9: e109085, 7 pp. Go to original source...
    66. Rankin M. & Burchsted J. 1992: The cost of migration in insects. - Annu. Rev. Entomol. 37: 533-559. Go to original source...
    67. Rees D.P. & Rangsi T.V. 2004: Insects of Stored Products. CSIRO, Collingwood, 181 pp. Go to original source...
    68. Rhainds M. 2020: Variation in wing load of female spruce budworms (Lepidoptera: Tortricidae) during the course of an outbreak: Evidence for phenotypic response to habitat deterioration in collapsing populations. - Environ. Entomol. 49: 238-245. Go to original source...
    69. Rolff J., Johnston P.R. & Reynolds S. 2019: Complete metamorphosis of insects. - Phil. Trans. R. Soc. Lond. (B) 374: 20190063, 8 pp. Go to original source...
    70. Saastamoinen M., Van der Sterren D., Vastenhout N., Zwaan B.J. & Brakefield P.M. 2010: Predictive adaptive responses: condition-dependent impact of adult nutrition and flight in the tropical butterfly Bicyclus anynana. - Am. Nat. 176: 686-698. Go to original source...
    71. Sanghvi K., Zajitschek F., Iglesias-Carrasco M. & Head M.L. 2021: Sex- and trait-specific silver-spoon effects of developmental environments, on ageing. - Evol. Ecol. 35: 367-385. Go to original source...
    72. Scudder G.G.E. 1971: Comparative morphology of insect genitalia. - Annu. Rev. Entomol. 16: 379-406. Go to original source...
    73. Shi J., Chen F. & Keena M.A. 2015: Differences in wing morphometrics of Lymantria dispar (Lepidoptera: Erebidae) between populations that vary in female flight capability. - Ann. Entomol. Soc. Am. 108: 528-535. Go to original source...
    74. Sivinski J., Vulinec K. & Aluja M. 2001: Ovipositor length in a guild of parasitoids (Hymenoptera: Braconidae) attacking Anastrepha spp. fruit flies (Diptera: Tephritidae) in southern Mexico. - Ann. Entomol. Soc. Am. 94: 886-895. Go to original source...
    75. Sota T., Hayashi M. & Yagi T. 2007: Geographic variation in body and ovipositor sizes in the leaf beetle Plateumaris constricticollis (Coleoptera: Chrysomelidae) and its association with climatic conditions and host plants. - Eur. J. Entomol. 104: 165-172. Go to original source...
    76. Stahlschmidt Z.R. & Adamo S.A. 2015: Food-limited mothers favour offspring quality over offspring number: a principal components approach. - Funct. Ecol. 29: 88-95. Go to original source...
    77. Tammaru T. & Haukioja E. 1996: Capital breeders and income breeders among Lepidoptera: consequences to population dynamics. - Oikos 77: 561-564. Go to original source...
    78. Tammaru T., Esperk T. & Castellanos I. 2002: No evidence for costs of being large in females of Orgyia spp. (Lepidoptera, Lymantriidae): larger is always better. - Oecologia 133: 430-438. Go to original source...
    79. Tigreros N. & Davidowitz G. 2019: Flight-fecundity tradeoffs in wing-monomorphic insects. - Adv. Insect Phys. 56: 1-41. Go to original source...
    80. Torsten H., Frank B. & Peter W. 2008: Simultaneous inference in general parametric models. - Biom. J. 50: 346-363. Go to original source...
    81. Walczak U., Baraniak E. & Zduniak P. 2017: Survival, body mass and potential fecundity of the invasive moth Cameraria ohridella (Lepidoptera: Gracillariidae) on its original host plant Aesculus hippocastanum and Aesculus glabra. - Eur. J. Entomol. 114: 295-300. Go to original source...
    82. Wang J., Jiang X.F., Wu D.L. & Luo L.Z. 2008: Effect of larval rearing density on development and fecundity of the beet armyworm, Spodoptera exempta (Lepidoptera: Noctuidae). - Acta Entomol. Sin. 51: 889-894.
    83. Wheeler D. 1996: The role of nourishment in oogenesis. - Annu. Rev. Entomol. 41: 407-431. Go to original source...
    84. Wickham H. 2016: ggplot2: Elegant Graphics for Data Analysis. Springer, New York, 211 pp. Go to original source...
    85. Wickman P.O. & Karlsson B. 1989: Abdomen size, body size and the reproductive effort of insects. - Oikos 56: 209-214. Go to original source...
    86. Wilke C.O. 2020: cowplot: Streamlined Plot Theme and Plot Annotations for 'ggplot2'. URL: https://wilkelab.org/cowplot/
    87. Xu J. & Wang Q. 2009: A polyandrous female moth discriminates against previous mates to gain genetic diversity. - Anim. Behav. 78: 1309-1315. Go to original source...
    88. Xu J. & Wang Q. 2010: Form and nature of precopulatory sexual selection in both sexes of a moth. - Naturwissenschaften 97: 617-625. Go to original source...
    89. Xu J., Wang Q. & He X. 2008: Emergence and reproductive rhythms of Ephestia kuehniella (Lepidoptera, Pyralidae). - N. Z. Plant Prot. 61: 277-282. Go to original source...
    90. Yanagi S.I. & Miyatake T. 2002: Effects of maternal age on reproductive traits and fitness components of the offspring in the bruchid beetle, Callosobruchus chinensis (Coleoptera: Bruchidae). - Physiol. Entomol. 27: 261-266. Go to original source...
    91. Yanagi S. & Tuda M. 2012: Female size constrains egg size via the influence of reproductive organ size and resource storage in the seed beetle Callosobruchus chinensis. - J. Insect Physiol. 58: 1432-1437. Go to original source...
    92. Yang A.S. 2001: Modularity, evolvability, and adaptive radiations: a comparison of the hemi- and holometabolous insects. - Evol. Dev. 3: 59-72. Go to original source...
    93. Yang F., Hu G., Shi J.J. & Zhai B.P. 2015: Effects of larval density and food stress on life-history traits of Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). - J. Appl. Entomol. 139: 370-380. Go to original source...

    This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content