Click here for the original journal page (in Acrobat pdf format).

The text below is grayed out because it is not intended to be read. It is a necessarily imperfect OCR of the original and is only used by a search engine.

Jonriuihif the Lvpulttptcrisls' Society 58(1), EOM. 44-47

HOST BREADTH AND VOLTINISM IX GALUNDUCING LEPIDOPTERA

William E. Miller

Depart in mi I of Entomology, University of Minnesota. St. Paul, Minnesota 55108, USA, email: inilleOL4@umn.eilu

ABSTRACT, because of specialized life systems and host relations, gall-indacing insects are believed to have narrower host breadth and lesser voltinism than other endophagous insects. These expectations were tested here using a sample of 136 species of British Lepidoptera consisting of 29 gallers in 11 families ami 107 tasonomically matched endophagous nungaller controls. Callers and nongallers were compared using biological data assembled and published by A. M. Emmet. Host breadth, scored ;is number of host genera, averaged 1.21 for the rallers, and 1.48 for the nongallers, and the difference is statistically significant, thus confirming host breadth expectation for this sample of Lepidoptera. This di lie re nee was generated mostly among C el echiidae. Nepticulidac, Tortricidae, and Sesiidae. Voltinism. scored as number of generations developing per year, did not dilfer between gallers and nongailers. This outcome does not necessarily refute the hypothesis underlying the expectation. The cool British climate may inhibit muliivoltinisni. and thereby minimize differences in voltinism between gallers and nongallers.

Additional key words: Gelcchiidae, Neptinilidae, Tortrieidae, Sesiidae, firitain.

Galls induced by Lepidoptera vary from simple swellings to fruitlike bodies that bear little resemblance to supporting host parts. The galls are organ specific, most developing on host stems, but some developing on host reproductive structures, leaves, and roots. With few exceptions, larvae rather than ovipositing adults induce the galls. Worldwide, ,352 uiorpho-species of gall-inducing Lepidoptera are known, of which 179 have been identified to genera and species in 20 families (Miller 2004). Greater numbers and tax-onomjc diversity of lepidopteran gallers are anticipated as tropical areas are explored.

Gall-inducing insects, including Lepidoptera, are believe id to have narrower host breadth and to develop fewer annual generations than other endophagous insects (Gomel! 1990, Raman L994, Miller 2004). Narrow host breadth is expected because evolutionary adjustments between gall inducer and host foster ioodplaut specialization, a corollary of the reputed host specificity of gall inducers (Mani 1964, Short-house & Rohfritsch 1992, Harris & Shorthouse 1996). Lesser voltinism is expected because gall inducers seem to synchronize their phenology with that of their hosts, which would ensure that larvae have access to reactive tissues necessary for gall development, its during rapid plant growth in spring. Physiological mechanisms that might mediate this synchrony have not been investigated. These host breadth and voltinism expectations for lepidopteran gall inducers would acquire added strength if empirical tesls confirmed them.

Cornell (1990) compared voltinism and other life history traits between gall inducers and leaf miners. His voltinism sample consisted of 28 species-12 leaf miners, mostly lepidopteran, and 16 gall inducers, mostly dtpteran and hvmenopteran. He (timid that voltinism averaged 1,4 gene rati on s/yr for (he gall inducers and 2.5 generations/yr for the leaf miners, which is consistent with the expectation of lesser voltinism among gall inducers. In contrast to voltinism, host

breadth of gall inducers in one or any combination oi insect orders does not seem to have been compared empirically with that of endophagous nongallers.

Reported here are comparisons of host breadth and voltinism between gallers and nongallers in a large .siunpli- ol i .epidoptera, an order noorh represented in previous cecidological studies (Miller 2004), The source of the data analyzed is Emmet's (1991) extensive life history tabulation for more than 2400 species of British Lepidoptera, the most extensively known lepidopteran fauna in the world,

Materials and Methods

To test the hypotheses that gall-inducing Lepidoptera have narrower host breadth and lesser voltinism than other endophagous Lepidoptera, I assembled a study sample of 29 gallers and 107 endophagous iiougallcr controls, 136 species in all. All known British gallers were included, as listed by Spooner and Bow-drey (1995), with emendations as follows: Argijrenthia rc.tindla Zeller, unaccountably absent from the list, was atlded (Bobbins 1992), and Parantltrenc labtmiformis rhingltieforme (Hiibner), now considered synonymous with P tabaniformis (Rottemburg), was removed (Spatenka et al. 1999),

The 107 endophagous nongallers were those marked in Emmet's (1991) tabulation exclusively with /) for borer or m for miner, and, for Heliozela only, also with c for ease bearer to match the ease bearing Heliozela gallers. Taxonomie matching was possible at the generic level for gallers in 10 genera, and at the subfamily level for gallers in six genera, in line with principles of the comparative method (Harvey & Pagel 1991). For example, matches for the two Ectoedemia (Nepticulidae) gallers consisted of the 15 nongalling endophagous Ectoedemia, and the match for the galler Adaina mterodactyla (Hiibner) (Tterophoridae, l'latyptiliinae), which has no British congeners, was l^eioptilus carphodactyla (Hiibner), the only other endophagous British memherof the subfamily Platyptili-

Volume 58, Number 1

• tr,

Table 1, Host breadth and voltinism of British gall-inducing Lepidoptera and taxonomioally matched endophagous nongallers. Data from Emmet '1991) except where noted othenvise. Family sequence follows Kristensen (1999).

Family

Species as numbered in Emmet's tabulation

Nepticulidae Galley Nongallers

Heliozelidae Gallers

\ii]l-;[ll;l

Incurvariidae Gallers Nongallers

Yponomeutidae Gallers Nongallers

Elaehistidae Caller Nongaller

Coleophoridiie Gallers Nongallers

(.i-Vclliiilir Gallers Nongallers

Sesiidae

Gallers

Nongallers Tortricidae

Gallers Nongallers

Pterophoridae

Galler

Nongaller Crambidae

Galler

Nongallers Summary

Gallers

N'onga Iters

23,24 25-32,54-39.41

151, 157 1S6

138, 139 133, 136

411,415

401, 404, 405, 407,410,412,418, 420, 422

906 905

486,889,891,892,893ai

4S7, 830-884, 887, 888, 890

728, 755

723-727, 727a, 729, 730, 735, 737, 744. 744a,

746-748, 753, 757,808, S11-S13, 816, 817, 821, 822,

823a, 825

372, 377, 380 373-^79, 381

966, 1137, 1167, 1190, 1195, 1256, 1258, 1266 962,964,965,967,1168, 1192,1194.1196, 1197, 1199, 1200, 1200a, 1201, 1202, 1240, 1242, 1243, 1245-1247, 1249, 1253-1255, 1257, 1259-1261, 1264, 1265, 1267, 1268-1270

1517 1519

[359

1375

1 Mtmiphti bratlletji Riedl, whose discovery in Britain (Harper 1994) postdates Emmet (1991). * Mann-Whitney V irHHr = 1280.0, ponc|jM < 0,05.

inae. Nongallers outnumber gallers in the study because plausible matches were often more numerous than the gallers matched, all being included to avoid selection bias.

Host breadth and voltinism data were extracted for both the gallers and nongallers from Emmets (1991) tabulation. Data for one galler subsequently discovered in Britain, Mompha breulleiji Riedl, was obtained from Harper (1994). Host breadth was scored as number of recorded host genera. This is a stringent measure in that no distinction was made between one and

more than one host species in the same genus; however, the problem of appropriately scaling and integrating genus and species scoring was thereby avoided. Scoring by species alone could not be done because the source did not consistently list numbers of host species within genera. Voltinism was scored as number of annual generations, with the case of less than one annual generation (one generation every two years) being scored as 0.5. This case had minimal impact because it occurred in only 3 of the 29 gallers (2 sesiids and 1 tortricid) and 4 of the 107 nongallers (all sesiids).

41 >

Journal ok the Lepirofterists' Society

Student's £, Mann-Whitney U, and statistical summaries were computed with SYSTAT (1992) software. Homogeneity of variance between galler and nongaller groups was examined before analysis as outlined bv Sokal and Rohlf (1981).

Re suits

The 29 British gall inducers represent 11 of the 20 families of identified lepidupteran gall inducers worldwide (Table 1; Miller 2004). Stem galls are induced by 21 of the gallers, petiole galls by 5, and reproductive-structure galls by 3 (Bobbins 1992, Spooner & Bow-drey 1995).

Mean host breadth was 1.21 genera for gallers compared to 1.48 genera for endophagous nongallers. The difference, 0.27, is in the expected direction of fewer host genera for gall inducers, and is significant !(■' test, Table 1). The nonparametric [./-test was used because galler and control variances proved divergent. Host breadth ranged 1-2 for the gallers, and 1^ for the

nongallers.

The difference in host breadth between the two groups originated mainly within Geleehiidae, Nepticul-idae, Tortricidae, and Sesiidae. In these families, host breadth means for nongallers exceeded those for gallers by 0.71, 0.27, 0.19, and 0.17, respectively (Table 1).

Mean voltinism was 1.07 annual generations for the gall inducers, compared to 1.11 annual generations for the nongallers (Table 1). The difference, 0.04, although in the expected direction, is not significant (f 114l]r = -0,53, p ,.,_,= 0.30), Galler and nonsaller variances

L uiir EilJcd                                                                O

for voltinism proved to be homogeneous, which permitted the use of the parametric f-test. Voltinism ranged 0.5-2 for both gallers and nongallers.

Discussion

Analysis of number of host genera supports the expectation of narrower host breadth for gall inducers than for endophagous nongallers among British Lepidoptera. This result (Table 1) might have been stronger had more elaborate scoring captured the intrageneric component of host breadth, but no objective method for combining or integrating genus and species scoring was available, and species counts alone could not be used because the source did not fully elaborate host species. Actual host breadth might also be stronger than indicated by the analysis for vet another reason: galls undoubtedly attract more interest and attention than other signs of insect infestation, so that host breadth of nongallers might be underreported compared to that of gallers, which could reduce the apparent difference,

Narrow host breadth is a trait that is highly desirable in biological control agents of weeds, one which,

other things being equal, enhances the biological control potential of gallers (Harris & Shorthouse 1996, MeEvoy 1990). Geleehiidae and Tortricidae, which are among the four families here with strongest differences between gallers and nongallers in host breadth (Tabic I), are also the families with the greatest numbers of known gallers (Miller 2004).

Analysis does not support the expectation of lesser voltinism among gallers. This result (Table 1) contradicts Cornell's (J990) finding of lesser voltinism in gallers than leaf miners, but does not necessarily refute the hypothesis giving rise to the expectation. The British climate is eool-temperate and rainy, with the warmest month averaging less than 22°C (I>cwis 1994). Such a climate may inhibit mnltivoltinism so that differences in voltinism between gallers and nongallers are minimized. By contrast, in eastern North America, a temperate land mass much larger than Britain, lepi-dopteran voltinism markedly increases as latitude decreases (Fracker 1920, Tauber et al. 1986). Multivol-tinisrn in lepidopteran gall inducers, when it occurs, seems influenced more indirectly than directly by climate; that is, protracted growth seasons in warm temperate regions and in tropical wet cycles expand temporal availability of reactive host tissues for gall development (Miller 2004). Although Cornell (1990) did not taxonomically match gallers and leaf miners in comparing their voltinism, he reported no statistical connection between taxonomy and analytical outcome, and his result unequivocally shows lesser galler voltinism. Further testing of the voltinism expectation would be desirable. Possible mechanisms underlying galler-host phonological synchrony might include higher thermal thresholds for galler than nongaller development, and differing diapause reactions.

Acknowledgments

1 thank R. C. Venette. D, W fiagsdale, R. W. Hodges and K. A Schick for useful re\iews of ilie manuscript,

Literature Cited

Cornell, ELY 1990. Survivorship, life history, and concealment: a comparison of" leaf miners and gall formers. Amer Nat. 136; 581^597.

Emmet, A. M. 1991. Chart showing the life history and habits of tin- British lepidoptera, pp. 61-301. in Emmet, A. M. & J. Heath (eds.). The moths and butterflies of Great Britian and .Ireland. Vol. 7, Pt 2. I lai lev, C Colchester, United Kingdom.

FbaCKER, S. B. 1920. The life cycle of the Lepidoptera. Ann. En-tomol. Soc. Amer. 13:167-173.

HahI'ER, M.W. 1994. Simnplui bimildiji Kiedl (Lepidoptera: Mom-phidae) new to Britain, with some initial observations on its life history. Entomol. Gay. 45:151-156.

Harris, P. & J. |). Shorthouse, 1996. Effectiveness of gall inducers in weed biological control. Can. Entomol. 128:1021-1055.

Harvev, P H & M. D. Pacel. 1991. The comparative method in evolutionary biology. Oxford. Oxford, United Kingdom.

VolumeSS, Number 1

17

Kristensev, N. P, (ed.). 1999. Lepidoptera, moths and butterflies. Evolution, systematics, and biogeography. Handbook of Zoology. Vol. 1. f)e Grayter, New York.

Lewis, H. A. C. 1994. The Times atlasof the world 9th ed. Times Books. London.

Manf, M. S. 1964. Ecolo» of plant galls. Dr Walter Junk, The Hague, The Netherlands.

McEvoy, P. B. 1996. Host specificity and biological control. BioSci. 46:401-405.

Miller, W. E, 2004. Gall-inducing Lepidoptera, pp. 429-462. In Raman, A., C. \V. Schaefer & T. M. Withers (eds,). Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Enfield, New Hampshire. USA.

Hamas, A. 1994. Adapt at ional integration between gall-inducing insects and their host plants, pp. 249-275. In Ananthakrishuan, T. N. (ed,). Functional dynamics of phytophagous insects. Science Publishers, Lebanon, New Hampshire, USA.

ROFJBfNS, J. 1992. Argyresthia retinella Ze[[. (Lepidoptera: Ypono-ineutidae) a gall causer. Cecidology 7:53.

SHORTHOt'SE, J. D. & O. ROnfRrrSCH (eus.). 1992. Biology of insect-induced galls, Oxford University Press. New York.

Sokal, R. R. & F. j. Roiilk. 198l'. Biometry. 2nd ed. Freeman, New York. USA.

SPATENKA, K., O. GOBBITNOV, Z. LaSTUVKA, 1, TOSEVSKt & Y, AfUTA.

1999. Handbook of Palaearctic macrolepidoptera. Vol. I. Sesi-idae-Clearwing moths. Gem, Wallingford, England.

SFOONEB, B. M & j. P. Bowdrey. 1095. Checklist of British galls and gall-causing organisms. 1. Lepidoptera: preliminary' list. Cecidology 10:84-100.

SYSTAT 1992. Statistics version 5.2 cd. SYSTAT Inc.

Tauber, M. J., C. A. Taubeb & S. Masaki. 1986. Seasonal adaptations of insects. Oxford, New York.

Received for puiilication 10 March 2003. revised and accepted for publication 19 September 2003