Abstract
Sedentary insect herbivores, such as gallformers and leafminers, are usually non-randomly distributed among and within host plants. Dispersion of these insects is largely a function of female oviposition choice. In field experiments and observations spanning two growing seasons, we tested the hypothesis that selective oviposition on individual leaves within trees by the dominant herbivore of Emory oak, the monophagous leaf-miner Cameraria sp. nov., is determined by the probability of colonization by endophytic fungi. These fungi are alleged to act as plant mutualists by deterring, killing, or inhibiting the growth of insect herbivores. We found that leaves selected by females for oviposition and paired, unmined leaves were equally likely to be colonized by fungal endophytes. Furthermore, condensed and hydrolyzable tannin levels, purported inhibitors of fungal infection, and protein content did not vary between leaves selected by females and unmined leaves, or between leaves with and without endophyte infections. We conclude that female Cameraria do not choose leaves within trees for oviposition on the basis of propensity for endophytic fungal infection or on phytochemical parameters that might indicate probability of future infections. At this spatial scale at least, fungal endophytes do not explain the highly aggregated distribution of Cameraria among leaves and associated costs in terms of increased larval mortality. Fungal endophytes may, nevertheless, affect leafminer dispersion and abundance at larger spatial scales, such as host plant populations or species. We did find, however, that the amount of mining activity on leaves is positively associated with increased colonization by fungal endophytes. We suggest that mining activity increases endophyte fungal infections by facilitating spore germination and hyphal penetration into the leaf or by altering leaf phytochemistry. The facilitation of endophyte colonization by leafmining activity coupled with the lack of predictability of endophyte infections based on leaf phytochemistry and almost 100% infectivity of all oak leaves during sporadic wet years may prevent female leafminers from discriminating leaves for oviposition on the basis of current or future levels of endophytes in leaves.
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References
Auerbach MJ (1991) Relative impact of interactions and between trophic levels during an insect outbreak. Ecology 72: 1599–1608
Auerbach MJ, Simberloff D (1989) Oviposition site preference and larval mortality in a leaf-mining moth. Ecol Entomol 14: 131–140
Auerbach MJ, Connor EF, Mopper S (1995) Minor and major miners: Population dynamics of latent and eruptive leafmining insects. In: Cappucino N, Price P (eds) Population dynamics. Academic Press, Orlando, pp 83–110
Bate-Smith EC (1977) Astringent tannin of Acer species. Phytochemistry 16: 1421–1426
Bernstein ME, Carroll GC (1977) Microbial populations in Douglas fir needles. Microbiol Ecol 4: 41–52
Breen JP (1994) Acremonium endophyte interactions with enhanced plant resistance to insects. Annu Rev Entomol 39: 401–423
Broadhurst RB, Jones WT (1978) Analysis of condensed tannins using acidified vanillin. J Sci Food Agric 29: 788–794
Bultman TL, Faeth SH (1986) Selective oviposition by a leaf miner in response to temporal variation in abscission. Oecologia 69: 117–120
Bultman TL, Faeth SH (1988) Abundance and mortality of leaf miners on artificially shaded Emory oak. Ecol Entomol 13: 131–142
Butin H (1992) Effect of endophytic fungi from oak (Quercus robur L.) on mortality of leaf-inhabiting gall insects. Eur J For Pathol 22: 237–246
Carroll GC (1986) The biology of endophytism with particular reference to woody perennials. In: Fokkema J, Hueval J van den (eds) Microbiology of the phyllosphere. Cambridge University Press, Cambridge, pp 205–222
Carroll GC (1988) Fungal endophytes in stems and leaves: from latent pathogen to mutualistic symbiont. Ecology 69: 2–9
Carroll GC (1991a) Fungal associates of woody plants as insect antagonists in leaves and stems. In: Barbosa P, Krischik PA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 253–272
Carroll GC (1991b) Beyond pest deterrence. Alternative strategies and hidden costs of endophytic mutualisms in vascular plants. In: Andrews JH, Monano SS (eds) Microbial ecology of leaves. Springer, Berlin Heidelberg New York, pp 358–375
Cheplick GP, Clay K (1988) Acquired chemical defenses in grasses: the role of fungal endophytes. Oikos 52: 309–318
Clay K (1988) Fungal endophytes of grasses: a defensive mutualism between plants and fungi. Ecology 69: 10–16
Clay K (1990) Fungal endophytes of grasses. Annu Rev Ecol Syst 21: 275–297
Clay K (1991a) Fungal endophytes, grasses, and herbivores. In: Barbosa P, Krischik PA, Jones CG (eds) Microbial mediation of plant-herbivore interactions. Wiley, New York, pp 199–226
Clay K (1991b) Endophytes as antagonists of plant pests. In: Andrews JH, Monano SS (eds) Microbial ecology of leaves. Springer, Berlin Heidelberg New York, pp 331–357
Clay K (1992) Fungal endophytes of plants: biological and chemical diversity. Nat Toxins 1: 147–149
Clay K, Marks S, Cheplick GP (1993) Effects of insect herbivory and fungal endophyte infection on competitive interactions among grasses. Ecology 74: 1767–1777
Courtney SP, Kibota TT (1990) Mother doesn't know best: selection of hosts by ovipositing insects. In: Bernays EA (ed) Insect-plant interactions, vol II. CRC Press, Baton Rouge, pp 161–189
Cruickshank IAM (1980) Defense triggered by the invader: chemical defenses. In: Horsfall JG, Cowling ED (eds) Plant disease, vol 5. Academic Press, New York, pp 247–267
Faeth SH (1985) Quantitative defense theory and patterns of feeding by oak insects. Oecologia 68: 34–40
Faeth SH (1986) Indirect interactions between temporally-separated herbivores mediated by the host plant. Ecology 67: 479–494
Faeth SH (1990) Aggregation of a leafminer, Cameraria sp. nov. (Davis): consequences and causes. J Anim Ecol 59: 569–586
Faeth SH (1991) The effect of oak leaf size on abundances, dispersion, and survival of the leafminer, Cameraria sp. nov. (Lepidoptera: Gracillariidae). Environ Entomol 20: 196–204
Faeth SH (1992) Interspecific and intraspecific interactions via plant responses to folivory: an experimental test. Ecology 73: 1802–1813
Faeth SH, Bultman TL (1986) Interacting effects of increased tannin levels on a leaf-mining insect. Entomol Exp Appl 40: 297–300
Faeth SH, Hammon KE (1997a) Fungal endophytes in oak trees. I. Long-term patterns of abundance and associations with leafminers. Ecology (in press)
Faeth SH, Hammon KE (1997b) Fungal endophytes in oak trees. II. Experimental analyses of interactions with leafminers. Ecology (in press)
Faeth SH, Wilson D (1996) Induced responses in plants: mediators of interactions among macro-and micro herbivores? In: Gange AC (ed) British Ecological Society Symposium. Blackwell, London (in press)
Faeth SH, Mopper S, Simberloff S (1981) Abundances and diversity of leaf-mining insects on three oak host species: Effects of host-plant phenology and nitrogen content of leaves. Oikos 37: 238–251
Fisher PJ, Petrini O (1990) A comparative study of fungal endophytes in xylem and bark of Alnus species in England and Switzerland. Mycol Res 94: 313–319
Gange AC (1995) Positive effects of endophyte infections on sycamore aphids. Oikos 75: 500–510
Gaylord ES, Preszler RW, Boecklen WJ (1996) Interactions between host plants, endophytic fungi, and a phytophagous insect in an oak (Quercus grisea × Quercus gambelii) hybrid zone. Oecologia (in press)
Hammon KE, Faeth SH (1992) Ecology of plant-herbivore communities: a fungal component? Nat Toxins 1: 197–208
Harborne JB, Ingham JL (1978) Biochemical aspects of the coevolution of higher plants with their fungal parasites. In: Harborne JB (ed) Biochemical aspects of plant and animal coevolution. Academic Press, New York, pp 343–405
Juniper B, Southwood TRE (1986) Insects and the plant surface. Edward Arnold, London
Kearney TH, Peebles RH (1960) Arizona flora. University of California Press, Berkeley
McNeil JN, Quiring DT (1983) Evidence of an oviposition-detering pheromone in the alfalfa blotch leafminer Agromyza frontella (Rondani) (Diptera: Agromyzidae). Environ Entomol 12: 990–992
Mopper S, Simberloff DS (1995) Differential herbivory in an oak population: the role of plant phenology and insect performance. Ecology 76: 1233–1241
Petrini O (1986) Taxonomy of endophytic fungi of aerial plant tissues. In: Fokkema NJ, Hueval J van den (eds) Microbiology of the phyllosphere. Cambridge University Press, Cambridge, pp 175–187
Petrini O, Sieber TN, Toti L, Viret O (1992) Ecology, metabolite production, and substrate utilization in endophytic fungi. Nat Toxins 1: 185–196
Potter DA (1985) Population regulation of the native holly leaf-miner, Phytomyza ilicicola Loew (Diptera: Agromyzidae), on American holly. Oecologia 66: 499–505
Powell RG, Petroski RJ (1992) Alkaloid mycotoxins in endophyte-infected grasses. Nat Toxins 1: 163–170
Preszler RW, Gaylord ES, Boecklen WJ (1996) Reduced parasitism of a leaf-mining moth on trees with high infection frequencies of an endophytic fungus. Oecologia (in press)
Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62: 244–251
Quiring DT, McNeil JN (1984) Exploitation and interference intraspecific larval competition in the dipteran leaf miner, Agromyza frontella (Rondani). Can J Zool 62: 412–427
Saikkonen K, Helander M, Ranta H, Neuvonen S, Virtanen T, Suomela J, Vuorinen P (1996) Endophyte-mediated interactions between woody plants and insect herbivores. Entomol Exp Appl (in press)
Simberloff D, Stiling PD (1987) Larval dispersion and survivorship in a leaf-mining moth. Ecology 68: 1647–1657
Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, San Francisco
Stiling PD, Simberloff DS (1989) Leaf abscission: induced defense against pests or response to damage? Oikos 55: 44–49
Stiling PD, Brodbeck BV, Strong DR (1982) Foliar nitrogen and larval parasitism as determinants of leafminer distribution patterns on Spartina alternaflora. Ecol Entomol 7: 447–452
Stiling PD, Simberloff DS, Anderson LC (1987) Non-random distribution patterns of leaf miners on oak trees. Oecologia 74: 102–105
Taper ML, Case TJ (1987) Interactions between oak tannins and parasite community structure: unexpected benefits of tannins to cynipid gall-wasps. Oecologia 71: 254–261
Taper ML, Zimmerman EM, Case TJ (1986) Sources of mortality for a cynipid gall-wasp (Dryocosmus dubiosus (Hymenoptera: Cynipidae)): the importance of the tannin/fungus interaction. Oecologia 68: 437–445
Whitham TG (1980) The theory of habitat selection examined and extended using Pemphigus aphids. Am Nat 115: 449–466
Williams AG, Whitham TG (1986) Premature leaf abscission: an induced defense against gall aphids. Ecology 67: 1619–1627
Wilson D (1993) Fungal endophytes: out of sight but should not be out of mind. Oikos 68: 379–384
Wilson D (1995a) Endophyte-the evolution of a term, and clarification of its use and definition. Oikos 73: 274–276
Wilson D (1995b) Fungal endophytes which invade insect galls: insect pathogens, benign saprophytes, or fungal inquilines? Oecologia 103: 255–260
Wilson D, Carroll GC (1994) Infection studies of Discula quercina, an endophyte of Quercus garryana. Mycologia 86: 635–647
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Faeth, S.H., Hammon, K.E. Fungal endophytes and phytochemistry of oak foliage: determinants of oviposition preference of leafminers?. Oecologia 108, 728–736 (1996). https://doi.org/10.1007/BF00329049
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DOI: https://doi.org/10.1007/BF00329049