Eur. J. Entomol. 117: 1-17, 2020 | DOI: 10.14411/eje.2020.001

Oviposition preference maximizes larval survival in the grass-feeding butterfly Melanitis leda (Lepidoptera: Nymphalidae)Original article

Freerk MOLLEMAN1,2, Sridhar HALALI2,3, Ullasa KODANDARAMAIAH2
1 Department of Systematic Zoology, Institute of Environmental Biology, Faculty of Biology, A. Mickiewicz University, Ul. Uniwersytetu Poznañskiego 9, PL-61-614 Poznañ, Poland; e-mail: fremol@amu.edu.pl
2 IISER-TVM Centre for Research and Education in Ecology and Evolution (ICREEE), Indian Institute of Science Education and Research, Thiruvananthapuram, Kerala, 695016, India; e-mails: sridharhalali@gmail.com, Ullasa@iisertvm.ac.in
3 Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

Phytophagous insects may be expected to prefer host-plant species on which their larvae perform best, but this has rarely been explored in grass-feeding butterflies. We explored links between oviposition preferences, larval food preferences, and performance (larval survival and development time, pupal mass, and adult longevity) on 18 species of grass in the common evening brown, Melanitis leda L. (Nymphalidae: Melanitini), a tropical butterfly that has been recorded from a large number of species of grass. Melanitis leda oviposited on all of the grass species offered in choice experiments, and larvae were able to develop to the adult stage on almost all of them. Oviposition preferences were for species of plants on which larval survival was higher, but were not correlated with larval development. The mother's choice of host plant appeared to affect performance of the resulting adults as large butterflies had longer life spans. Ovipositing females appeared to adjust clutch size and position of their eggs on a plant depending on plant traits. Larval survival was only marginally correlated with larval growth rate on the different species of plants. Larvae showed host-plant preferences that were not correlated with adult oviposition preferences, larval survival, or larval growth. Overall, while M. leda can utilize a large number of species of grass, it shows marked oviposition preferences. Apparent fine-tuning of clutch size and positioning of eggs on plants with different traits might be another adaptation associated with using a large number of species of plants. We conclude that this grass feeding butterfly selects oviposition sites that maximize the chances of their larvae surviving.

Keywords: Lepidoptera, Nymphalidae, caterpillar, growth rate, larval choice, larval survival, longevity, host plant, oviposition behaviour, polyphagy

Received: July 13, 2019; Accepted: December 6, 2019; Published online: January 13, 2020  Show citation

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MOLLEMAN, F., HALALI, S., & KODANDARAMAIAH, U. (2020). Oviposition preference maximizes larval survival in the grass-feeding butterfly Melanitis leda (Lepidoptera: Nymphalidae). EJE, 117, Article 1-17. https://doi.org/10.14411/eje.2020.001
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    References

    1. Barbehenn R.V. & Bernays E.A. 1992: Relative nutritional quality of C3 and C4 grasses for a graminivorous lepidopteran, Paratrytone melane (Hesperiidae). - Oecologia 92: 97-103. Go to original source...
    2. Barbehenn R.V., Kapila M., Kileen S. & Nusbaum C.P. 2017: Acquiring nutrients from tree leaves: effects of leaf maturity and development type on a generalist caterpillar. - Oecologia 184: 59-73. Go to original source...
    3. Bates D., Maechler M., Bolker B. & Walker S. 2015: Fitting linear mixed-effects models using lme4. - J. Stat. Softw. 67: 1-48. Go to original source...
    4. Beaver R.A. 1979: Host specificity of temperate and tropical animals. - Nature 281: 139-141. Go to original source...
    5. Bergman K.O. 2000: Oviposition, host plant choice and survival of a grass feeding butterfly, the Woodland Brown (Lopinga achine) (Nymphalidae: Satyrinae). - J. Res. Lepid. 35: 9-21. Go to original source...
    6. Bernays E.A., Singer M.S. & Rodrigues D. 2004: Foraging in nature: foraging efficiency and attentiveness in caterpillars with different diet breadths. - Ecol. Entomol. 29: 389-397. Go to original source...
    7. Brakefield P.M. 1987: Tropical dry and wet season polyphenism in the butterfly Melanitis leda (Satyrinae): Phenotypic plasticity and climatic correlates. - Biol. J. Linn. Soc. 31: 175-191. Go to original source...
    8. Casas J. & Djemai I. 2002: Canopy architecture and multitrophic interactions. In Tscharntke T. & Hawkins B.A. (eds): Multitrophic Level Interactions. Cambridge University Press, Cambridge, pp. 174-196. Go to original source...
    9. Cayssials V. & Rodríguez C. 2013: Functional traits of grasses growing in open and shaded habitats. - Evol. Ecol. 27: 393-407. Go to original source...
    10. Chew F.S. 1980: Foodplant preferences of Pieris caterpillars (Lepidoptera). - Oecologia 46: 347-353. Go to original source...
    11. Craig T.P. & Itami J.K. 2008: Evolution of preference and performance relationships. In Tilmon K.J. (ed.): Specialization, Speciation, and Radiation. The Evolutionary Biology of Herbivorous Insects. University of California Press, Berkeley, CA, pp. 20-28. Go to original source...
    12. Damman H. 1987: Leaf quality and enemy avoidance by the larvae of a pyralid moth. - Ecology 68: 88-97. Go to original source...
    13. Davis R.B., Õunap E., Javoi¹ J., Gerhold P. & Tammaru T. 2013: Degree of specialization is related to body size in herbivorous insects: a phylogenetic confirmation. - Evolution 67: 583-589. Go to original source...
    14. De la Masselière C.M., Facon B., Hafsi A. & Duyck P.-F. 2017: Diet breadth modulates preference - performance relationships in a phytophagous insect community. - Sci. Rep. 7: 16934, 9 pp. Go to original source...
    15. Edwards E.J., Osborne C.P., Strömberg C.A., Smith S.A. & C4 Grasses Consortium 2010: The origins of C4 grasslands: integrating evolutionary and ecosystem science. - Science 328: 587-591. Go to original source...
    16. Ehrlich P.R. & Raven P.H. 1964: Butterflies and plants: a study in coevolution. - Evolution 18: 586-608. Go to original source...
    17. Faeth S. & Bultman T.L. 2002: Endophytic fungi and interactions among host plants, herbivores, and natural enemies. In Tscharntke T. & Hawkins B.A. (eds): Multitrophic Level Interactions. University of Cambridge, Cambridge, 282 pp. Go to original source...
    18. Friberg M. & Wiklund C. 2009: Host plant preference and performance of the sibling species of butterflies Leptidea sinapis and Leptidea reali: a test of the trade-off hypothesis for food specialisation. - Oecologia 159: 127-137. Go to original source...
    19. Friberg M. & Wiklund C. 2016: Butterflies and plants: preference/performance studies in relation to plant size and the use of intact plants vs. cuttings. - Entomol. Exp. Appl. 160: 201-208. Go to original source...
    20. Gamberale-Stille G., Söderlind L., Janz N. & Nylin S. 2014: Host plant choice in the comma butterfly: larval choosiness may ameliorate effects of indiscriminate oviposition. - Insect Sci. 21: 499-506. Go to original source...
    21. García-Barros E. & Fartmann T. 2009: Butterfly oviposition: sites, behaviour and modes. In Settele J., Shreeve T., Konvicka M. & Van Dyck H. (eds): Ecology of Butterflies in Europe. Cambridge University Press, Cambridge, pp. 29-42.
    22. Gilbert L.E. 1979: Development of theory in the analysis of insect-plant interaction. In Horn D.J., Mitchell R.D. & Stairs G.R. (eds): Analysis of Ecological Systems. Ohio University Press, Columbus, pp. 210-240.
    23. Godfray H.C.J. 1986: Clutch size in a leaf-mining fly (Pegomya nigritarsis, Anthomyiidae). - Ecol. Entomol. 11: 75-81. Go to original source...
    24. Gripenberg S., Mayhew P.J., Parnell M. & Roslin T. 2010: A meta-analysis of preference-performance relationships in phytophagous insects. - Ecol. Lett. 13: 383-393. Go to original source...
    25. Hardy T.N., Clay K. & Hammond A.M. 1985: Fall armyworm (Lepidoptera: Noctuidae): a laboratory bioassay and larval preference study for the fungal endophyte of perennial ryegrass. - J. Econ. Entomol. 78: 571-575. Go to original source...
    26. Hartley S.E. & DeGabriel J.L. 2016: The ecology of herbivore-induced silicon defences in grasses. - Func. Ecol. 30: 1311-1322. Go to original source...
    27. Hopkins A.D. 1916: Economic Investigations of the Scolytid Bark and Timber Beetles of North America. U.S. Department of Agriculture Program of work for 1917, 353 pp.
    28. Jaenike J. 1978: Optimal oviposition behavior in phytophagous insects. - Theor. Popul. Biol. 14: 350-356. Go to original source...
    29. Kalesh S. & Prakash S.K. 2007: Additions to larval host plants of butterflies of the Western Ghats, Kerala, Southern India (Rhopalocera, Lepidoptera). Part 1. - J. Bombay Nat. Hist. Soc. 104: 235-238.
    30. Kalesh S. & Prakash S.K. 2009: Early stages of the Travancore Evening Brown Parantirrhoea marshalli Wood-Mason (Satyrinae, Nymphalidae, Lepidoptera), an endemic butterfly from the southern Western Ghats, India. - J. Bombay Nat. Hist. Soc. 106: 142-148.
    31. Karban R. & Takabayashi J. 2019: Chewing and other cues induce grass spines that protect meristems. - Arthr.-Plant Interact. 13: 541-550. Go to original source...
    32. Karlsson B. & Wiklund C. 1985: Egg weight variation in relation to egg mortality and starvation endurance of newly hatched larvae in some satyrid butterflies. - Ecol. Entomol. 10: 205-211. Go to original source...
    33. Kunte K. 2012: Butterflies of Peninsular India. Universities Press, Hyderabad, 272 pp.
    34. Kursar T.A., Wolfe B., Epps M.J. & Coley P.D. 2006: Food quality, competition, and parasitism influence feeding preference in a neotropical lepidopteran. - Ecology 87: 3058-3069. Go to original source...
    35. Larsen T.B. 2005: Butterflies of West Africa. Apollo Books, Vester Skerninge, 900 pp. Go to original source...
    36. Leiva D. & De Vries H. 2014: Steepness: Testing Steepness of Dominance Hierarchies. R Package Ver. 0.2-2. URL: https://CRAN.R-project.org/package=steepness.
    37. Leniaud L., Audiot P., Bourguet D., Frérot B., Genestier G., Lee S.F., Malausa T., Le Pallec A.-H., Souqual M.-C. & Ponsard S. 2006: Genetic structure of European and Mediterranean maize borer populations on several wild and cultivated host plants. - Entomol. Exp. Appl. 120: 51-62. Go to original source...
    38. Lindman L., Johansson B., Gotthard K. & Tammaru T. 2013: Host plant relationships of an endangered butterfly, Lopinga achine (Lepidoptera: Nymphalidae) in northern Europe. - J. Insect Conserv. 17: 375-383. Go to original source...
    39. Mattson W.J. 1980: Herbivory in relation to plant nitrogen content. - Annu. Rev. Ecol. Syst. 11: 119-161. Go to original source...
    40. Moore G.J. 1986: Host plant discrimination in tropical satyrine butterflies. - Oecologia 70: 592-595. Go to original source...
    41. Nokelainen O., Ripley B.S., Bergen E., Osborne C.P. & Brakefield P.M. 2016: Preference for C4 shade grasses increases hatchling performance in the butterfly, Bicyclus safitza. - Ecol. Evol. 6: 5246-5255. Go to original source...
    42. Peña C. & Wahlberg N. 2008: Prehistorical climate change increased diversification of a group of butterflies. - Biol. Lett. 4: 274-278. Go to original source...
    43. Pijpe J., Brakefield P.M. & Zwaan B.J. 2007: Phenotypic plasticity of starvation resistance in the butterfly Bicyclus anynana. - Evol. Ecol. 21: 589-600. Go to original source...
    44. R Core Team 2017: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
    45. Renwick J.A.A. & Chew F.S. 1994: Oviposition behavior in Lepidoptera. - Annu. Rev. Entomol. 39: 377-400. Go to original source...
    46. Sahoo R.K. & Kodandaramaiah U. 2018: Local host plant abundance explains negative association between larval performance and female oviposition preference in a butterfly. - Biol. J. Linn. Soc. 125: 333-343. Go to original source...
    47. Sahoo R.K., Warren A.D., Collins S.C. & Kodandaramaiah U. 2017: Host plant change and paleoclimatic events explain diversification shifts in skipper butterflies (Family: Hesperiidae). - BMC Evol. Biol. 17: 174, 9 pp. Go to original source...
    48. Schäpers A., Nylin S., Carlsson M.A. & Janz N. 2016: Specialist and generalist oviposition strategies in butterflies: maternal care or precocious young? - Oecologia 180: 335-343. Go to original source...
    49. Schäpers A., Petrén H., Wheat C.W., Wiklund C. & Friberg M. 2017: Female fecundity variation affects reproducibility of experiments on host plant preference and acceptance in a phytophagous insect. - Proc. R. Soc. Lond. (B) 284: 20162643, 9 pp. Go to original source...
    50. Scheirs J., De Bruyn L. & Verhagen R. 2000: Optimization of adult performance determines host choice in a grass miner. - Proc. R. Soc. Lond. (B) 267: 2065-2069. Go to original source...
    51. Scheirs J., De Bruyn L. & Verhagen R. 2002: Seasonal changes in leaf nutritional quality influence grass miner performance. - Ecol. Entomol. 27: 84-93. Go to original source...
    52. Shirai Y. 1995: Longevity, flight ability and reproductive performance of the diamondback moth Plutella xylostella (L.) (Lepidoptera: Yponomeutidae), related to adult body size. - Res. Popul. Ecol. 37: 269-277. Go to original source...
    53. Showler A.T. & Moran P.J. 2014: Associations between host plant concentrations of selected biochemical nutrients and Mexican rice borer, Eoreuma loftini (Dyar) (Lepidoptera: Crambidae), infestation. - Entomol. Exp. Appl. 151: 135-143. Go to original source...
    54. Simpson S.J. & Raubenheimer D. 2012: The Nature of Nutrition: A Unifying Framework from Animal Adaptation to Human Obesity. Princeton University Press, Princeton, NJ, 256 pp. Go to original source...
    55. Singer M.C. 1986: The definition and measurement of oviposition preference in plant-feeding insects. In Miller J.R. & Miller T.A. (eds): Insect-Plant Interactions. Springer, New York, pp. 65-94. Go to original source...
    56. Singer M.C. 2004: Measurement, correlates, and importance of oviposition preference in the life of checkerspots. In Ehrlich P.R. & Hanski I. (eds): On the Wings of Checkerspots: A Model System for Population Biology. Oxford University Press, Oxford, pp. 113-137.
    57. Singer M.C. & Mandracchia J. 1982: On the failure of two butterfly species to respond to the presence of conspecific eggs prior to oviposition. - Ecol. Entomol. 7: 327-330. Go to original source...
    58. Singer M.S. & Stireman J.O. 2005: The tri-trophic niche concept and adaptive radiation of phytophagous insects. - Ecol. Lett. 8: 1247-1255. Go to original source...
    59. Singer M.S., Lichter-Marck I.H., Farkas T.E., Aaron E., Whitney K.D. & Mooney K.A. 2014: Herbivore diet breadth mediates the cascading effects of carnivores in food webs. - Proc. Natl. Acad. Sci. (Biol.) 111: 9521-9526. Go to original source...
    60. Soler R., Pineda A., Li Y., Ponzio C., Loon J.J.A. van, Weldegergis B.T. & Dicke M. 2012: Neonates know better than their mothers when selecting a host plant. - Oikos 121: 1923-1934. Go to original source...
    61. Solofondranohatra C.L.,Vorontsova M.S., Hackel J., Besnard G., Cable S., Williams J., Jeannoda V. & Lehmann C.E.R. 2018: Grass functional traits differentiate forest and savanna in the Madagascar central highlands. - Front. Ecol. Evol. 6: 184, 8 pp. Go to original source...
    62. Southwood T.R.E. & Kennedy C.E.J. 1983: Trees as islands. - Oikos 41: 359-371. Go to original source...
    63. Stuhldreher G. & Fartmann T. 2015: Oviposition-site preferences of a declining butterfly Erebia medusa (Lepidoptera: Satyrinae) in nutrient-poor grasslands. - Eur. J. Entomol. 112: 493-499. Go to original source...
    64. Tammaru T. & Esperk T. 2007: Growth allometry of immature insects: larvae do not grow exponentially. - Funct. Ecol. 21: 1099-1105. Go to original source...
    65. Therneau T. 2015: A Package for Survival Analysis in S. Version 2.38. URL: https://CRAN.R-project.org/package=survival.
    66. Thomas J.A. 1984: The conservation of butterflies in temperate countries: past efforts and lessons for the future. In Vane-Wright R.I. & Ackery P.R. (eds): Biology of Butterflies. Symposium of the Royal Entomological Society of London No. 11. Academic Press, London. pp. 333-353.
    67. Thompson J.N. 1988: Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. - Entomol. Exp. Appl. 47: 3-14. Go to original source...
    68. Tscharntke T. 1988: Variability of the grass Phragmites australis in relation to the behaviour and mortality of the gall-inducing midge Giraudiella inclusa (Diptera, Cecidomyiidae). - Oecologia 76: 504-512. Go to original source...
    69. Van Bergen E., Barlow H.S., Brattström O., Griffiths H., Kodandaramaiah U., Osborne C.P. & Brakefield P.M. 2016: The stable isotope ecology of mycalesine butterflies: implications for plant-insect co-evolution. - Funct. Ecol. 30: 1936-1946. Go to original source...
    70. Vialatte A., Bailey R.I., Vasseur C., Matocq A., Gossner M.M., Everhart D., Vitrac X., Belhadj A., Ernoult A. & Prinzing A. 2010: Phylogenetic isolation of host trees affects assembly of local Heteroptera communities. - Proc. R. Soc. (B) 277: 2227-2236. Go to original source...
    71. Whitcomb R.F., Kramer J., Coan M.E. & Hicks A.L. 1987: Ecology and evolution of leafhopper-grass host relationships in North American grasslands. In Harris K.F. (ed.): Current Topics in Vector Research. Vol. 4. Springer, New York, NY, pp. 121-178. Go to original source...
    72. Wiklund C. 1975: The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon L. - Oecologia 18: 185-197. Go to original source...
    73. Wiklund C. 1984: Egg-laying patterns in butterflies in relation to their phenology and the visual apparency and abundance of their host plants. - Oecologia 63: 23-29. Go to original source...
    74. Williams I.S. 1999: Slow-growth, high-mortality - a general hypothesis, or is it? - Ecol. Entomol. 24: 490-495. Go to original source...
    75. Willis K.J. & McElwain J.C. 2002: The Evolution of Plants. Oxford University Press, Oxford, 378 pp.
    76. Zalucki M.P., Clarke A.R. & Malcolm S.B. 2002: Ecology and behavior of first instar larval Lepidoptera. - Annu. Rev. Entomol. 47: 361-393. Go to original source...

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