Would Mothers Relax Their Degree of Selectivity for Supports Suitable for Egg-Laying When the Local Density of Conspecific Females Increases? A Case Study with Three Common Lepidopteran Leaf Miners
Selecting suitable supports for egg-laying, among host species and host individuals, as well as between leaves of various qualities within a preferred host, is a major component of prehatching maternal care in herbivore insects. This feature is especially important for those species having a tightly concealed larval stage, such as leaf miners. Yet, increasing density of neighbouring conspecific females may possibly induce ovipositing mothers to relax their degree of selectivity, so as to distribute their eggs more evenly among host leaves and reduce the risk of future scramble competition between larvae within a same leaf. We test this hypothetical prediction for three common leaf-mining moths: Phyllonorycter maestingella, Phyllonorycter esperella, and Tischeria ekebladella. The prediction was supported by none of the three tested species. This suggests that, in these tiny insect species, mothers are either unable to account for the local density of neighbouring conspecific females and/or they have no effective motivation to react accordingly. In addition, this also suggests that host individuals differing by the average quality of their leaves yet exert no differentiated attractivity towards mothers at a distance. In turn, this emphasizes the role of contingent factors in the patterns of spatial distribution of insects' densities. 1. Introduction Prehatching maternal care is common place among herbivore insects since, usually, the larval stage is hardly mobile and the diet of larvae is often limited to a rather narrow range of host plants [1, 2]. Accordingly, ovipositing mothers ordinarily share the entire and double responsibility of (i) making available the best resource for offspring by selecting appropriately the supports to be egg-laid and (ii) preventing the risk of scramble competition within the brood by limiting the size of egg clutch. This stands all the more strictly for those insects with larval stage tightly concealed within a narrow part of the host plant, such as mine-forming insects [3]. For mothers, in leaf-mining species, the selection of supports to be egg-laid consists not only in reaching the proper host species but, further on, by selecting the most appropriate host individuals and, eventually, the more promising subsets of host leaves that will thus satisfy at best the minimum requirements of mothers after careful probing. The later selective choice is often decisive since leaf quality may vary at least as much within individual hosts than between them [4–9]. In quantitative term, let “ ” be the proportion of host leaves that,
References
[1]
P. Jolivet, Insectes et Plantes: Evolution Parallèle et Adaptation, Société Linnéenne de Lyon, 1983.
[2]
Dajoz, “Quelques aspects des relations plantes-insectes, leur importance dans la dynamique des populations d’insectes phytophages,” Cahiers des Naturalistes, vol. 48, pp. 87–103, 1993.
[3]
S. H. Faeth, “Novel aspects of host tree resistance to leaf miners,” in Forest Insects Guilds: Patterns of Interaction with Host Trees, Y. N. Baranchikov, W. J. Mattson, F. P. Hain, and T. L. Payne, Eds., Tech. Rep, NE-153, pp. 219–239, United States Department of Agriculture. Forest Service, 1991.
[4]
J. C. Schultz, P. J. Nothnagle, and I. T. Baldwin, “Seasonal and individual variation in leaf quality of two northern hardwoods tree species,” American Journal of Botany, vol. 69, no. 5, pp. 753–759, 1982.
[5]
J. C. Schultz, “Habitat selection and foraging tactics of caterpillars in heterogeneous trees,” in Variable Plants and Herbivores in Natural and Managed Systems, R. F. Denno and M. S. McClure, Eds., pp. 61–90, Academic Press, New York, NY, USA, 1983.
[6]
J. J. Boomsma, H. Timmermans, C. P. M. Corvers, and J. Kabout, “Monophagous leaf-mining larvae of Stigmella (Lepidoptera: Nepticulidae) on birch: patterns and differentiation in exploitation of the host,” Holarctic Ecology, vol. 10, no. 3, pp. 206–218, 1987.
[7]
M. V. Kozlov and Y. G. Koricheva, “The within-tree distribution of caterpillarmines,” in Forest Insects Guilds: Patterns of Interaction with Host Trees, Y. N. Baranchikov, W. J. Mattson, F. P. Hain, and T. L. Payne, Eds., Tech. Rep, NE-153, United States Department of Agriculture. Forest Service, 1991.
[8]
T. Roslin, S. Gripenberg, J.-P. Salminen et al., “Seeing the trees for the leaves—oaks as mosaics for a host-specific moth,” Oikos, vol. 113, no. 1, pp. 106–120, 2006.
[9]
S. Gripenberg, Spatial ecology of a specialist insect herbivore—the leaf-mining moth Tischeria ekebladella on the pedunculate oak Quercus robur [Ph.D. thesis], Helsinki, Finland, 2007.
[10]
D. Reavey and K. J. Gaston, “The importance of leaf structure in oviposition by leaf-mining microlepidoptera,” Oikos, vol. 61, no. 1, pp. 19–28, 1991.
[11]
D. T. Quiring and J. N. McNeil, “Exploitation and interference intraspecific larval competition in the dipteran leaf miner, Agromyza frontella (Rondani),” Canadian Journal of Zoology, vol. 62, no. 3, pp. 421–427, 1984.
[12]
T. L. Bultman and S. H. Faeth, “Experimental evidence for intraspecific competition in a lepidopteran leaf miner,” Ecology, vol. 67, no. 2, pp. 442–448, 1986.
[13]
T. Cornelissen and P. Stiling, “Clumped distribution of oak leaf miners between and within plants,” Basic and Applied Ecology, vol. 9, no. 1, pp. 67–77, 2008.
[14]
A. J. M. Tack, O. Ovaskainen, P. J. Harrison, and T. Roslin, “Competition as a structuring force in leaf miner communities,” Oikos, vol. 118, no. 6, pp. 809–818, 2009.
[15]
A. J. M. Tack, Spatial ecology of an oak-associated herbivore community [Ph.D. thesis], University of Helsinki, Helsinki, Finland, 2010.
[16]
M. Auerbach, E. F. Connor, and S. Mopper, “Minor miners and major miners: population dynamics of leaf-mining insects,” in Population Dynamics: New Approaches and Synthesis, N. Cappuccino and P. W. Price, Eds., pp. 83–110, Academic Press, New York, NY, USA, 1995.
[17]
T. Ohgushi, “Indirect interaction webs: herbivore-induced effects through trait change in plants,” Annual Review of Ecology, Evolution, and Systematics, vol. 36, pp. 80–105, 2005.
[18]
T. Sugimoto, “Models of the spatial pattern of egg population of Ranunculus leaf mining fly, Phytomyza ranunculi (Diptera: Agromyzidae), in host leaves,” Researches on Population Ecology, vol. 22, no. 1, pp. 13–32, 1980.
[19]
M. Auerbach and D. Simberloff, “Oviposition site preference and larval mortality in a leaf-mining moth,” Ecological Entomology, vol. 14, no. 2, pp. 131–140, 1989.
[20]
T. A. Green and R. J. Prokopy, “Oviposition behaviour of the apple blotch leafminer, Phyllonorycter crataegella (Clemens) (Lepidoptera: Gracillariidae),” Journal of the New York Entomological Society, vol. 99, no. 4, pp. 654–663, 1991.
[21]
T. P. Craig, J. K. Itami, C. Shantz, W. G. Abrahamson, J. D. Horner, and J. V. Craig, “The influence of host plant variation and intraspecific competition on oviposition preference and offspring performance in the host races of Eurosta solidaginis,” Ecological Entomology, vol. 25, no. 1, pp. 7–18, 2000.
[22]
J. T. Cronin, W. G. Abrahamson, and T. P. Craig, “Temporal variation in herbivore host-plant preference and performance: constraints on host-plant adaptation,” Oikos, vol. 93, no. 2, pp. 312–320, 2001.
[23]
H. Kagata and T. Ohgushi, “Effects of multiple oviposition on clutch size in a leaf-mining moth, Paraleucoptera sinuella (Lepidoptera: Lyonetiidae),” Entomological Science, vol. 5, no. 4, pp. 407–410, 2002.
[24]
S. C. Digweed, “Oviposition preference and larval performance in the exotic birch-leafmining sawfly Profenusa thomsoni,” Entomologia Experimentalis et Applicata, vol. 120, no. 1, pp. 41–49, 2006.
[25]
S. Gripenberg and T. Roslin, “Host plants as islands: resource quality and spatial setting as determinants of insect distribution,” Annales Zoologici Fennici, vol. 42, no. 4, pp. 335–345, 2005.
[26]
J. Béguinot, “Comparison of the severity of selection among beech leaves prior to egg-laying between a leaf-mining and two gall-inducing insects,” European Journal of Entomology, vol. 108, no. 1, pp. 71–78, 2011.
[27]
J. Béguinot, “Quantifying the gap between the actual incidence of leaf-mining or leaf-galling insects and the proportion of host-leaves potentially acceptable by them,” Annales Société Entomologique de France, vol. 48, no. 1-2, pp. 216–224, 2012.
[28]
T. Hirota and Y. Kato, “Influence of visual stimuli on host location in the butterfly, eurema hecabe,” Entomologia Experimentalis et Applicata, vol. 101, no. 2, pp. 199–206, 2001.
[29]
K. Gotthard, N. Margraf, and M. Rahier, “Geographic variation in oviposition choice of a leaf beetle: the relationship between host plant ranking, specificity, and motivation,” Entomologia Experimentalis et Applicata, vol. 110, no. 3, pp. 217–224, 2004.
[30]
S. Gripenberg, J.-P. Salminen, and T. Roslin, “A tree in the eyes of a moth—temporal variation in oak leaf quality and leaf-miner performance,” Oikos, vol. 116, no. 4, pp. 592–600, 2007.
[31]
S. Eber, “Bottom-up density regulation in the holly leaf-miner Phytomyza ilicis,” Journal of Animal Ecology, vol. 73, no. 5, pp. 948–958, 2004.
[32]
K. J. Gaston, D. R. Genney, M. Thurlow, and S. E. Hartley, “The geographical range structure of the holly leaf-miner. IV. Effects of variation in host-plant quality,” Journal of Animal Ecology, vol. 73, no. 5, pp. 911–924, 2004.
[33]
S. J. Gon？alves-Alvim, R. G. Collevatti, and G. W. Fernandes, “Effects of genetic variability and habitat of Qualea parviflora (Vochysiaceae) on herbivory by free-feeding and gall-forming insects,” Annals of Botany, vol. 94, no. 2, pp. 259–268, 2004.
[34]
J. A. Santiago Lastra, L. E. García Barrios, J. C. Rojas, and H. Perales Rivera, “Host selection behavior of Leptophobia aripa (Lepidoptera: Pieridae),” Florida Entomologist, vol. 89, no. 2, pp. 127–134, 2006.
[35]
S. P. Egan and J. R. Ott, “Host plant quality and local adaptation determine the distribution of a gall-forming herbivore,” Ecology, vol. 88, no. 11, pp. 2868–2879, 2007.
[36]
E. F. Connor, E. Hosfield, D. A. Meeter, and X. Niu, “Tests for aggregation and size-based sample-unit selection when sample units vary in size,” Ecology, vol. 78, no. 4, pp. 1238–1249, 1997.
[37]
U. Kuhlmann, D. Babendreier, T. S. Hoffmeister, and N. J. Mills, “Impact and oviposition behaviour of Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), a polyembryonic parasitoid of the apple ermine moth, Yponomeuta malinellus (Lepidoptera: Yponomeutidae),” Bulletin of Entomological Research, vol. 88, no. 6, pp. 617–625, 1998.
[38]
D. Wool and O. Ben-Zvi, “Population ecology and clone dynamics of the galling aphid Geoica wertheimae (Sternorrhyncha: Pemphigidae: Fordinae),” European Journal of Entomology, vol. 95, no. 4, pp. 509–518, 1998.
[39]
M. Vos and L. Hemerik, “Linking foraging behavior to lifetime reproductive success for an insect parasitoid: adaptation to host distributions,” Behavioral Ecology, vol. 14, no. 2, pp. 236–245, 2003.
[40]
A. R. Ives and H. C. J. Godfray, “Phylogenetic analysis of trophic associations,” The American Naturalist, vol. 168, no. 1, pp. E1–E14, 2006.
[41]
L. Kuczyński and A. Skoracka, “Spatial distribution of galls caused by Aculus tetanothrix (Acari: Eriophyoidea) on arctic willows,” Experimental and Applied Acarology, vol. 36, no. 4, pp. 277–289, 2005.
[42]
H. Kagata and T. Ohgushi, “Conflict between optimal clutch size for mothers and offspring in the leaf miner, Leucoptera sinuella,” Ecological Entomology, vol. 29, no. 4, pp. 429–436, 2004.
[43]
S. H. Faeth, “Aggregation of a leafminer, Cameraria sp. nov. (Davis): consequences and causes,” Journal of Animal Ecology, vol. 59, no. 2, pp. 569–586, 1990.
[44]
S. Gripenberg, E. Morri？n, A. Cudmore, J. P. Salminen, and T. Roslin, “Resource selection by female moths in a heterogeneous environment: what is a poor girl to do?” Journal of Animal Ecology, vol. 76, no. 5, pp. 854–865, 2007.
