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Influence of Altitude and Host-Plant Species on Gall Distribution in Colliguaja Spp

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Influence of Altitude and Host-Plant Species on Gall Distribution in Colliguaja Spp Revista Chilena de Historia Natural 72: 305-313, 1999 Influence of altitude and host-plant species on gall distribution in Colliguaja spp. (Euphorbiaceae) in central Chile Influencia de la altitud y la especie de planta hospedadora sobre la distribuci6n de cecidias en Colliguaja spp. (Euphorbiaceae) en Chile central EDUARDO FUENTES-CONTRERAS, ERNESTO GIANOLI, PAULA P. CABALLERO & HERMANN M. NIEMEYER Departamento de Ciencias Ecologicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile ABSTRACT The shrub genus Colliguaja (Euphorbiaceae) shows a characteristic pattern of altitudinal distribution in central Chile. At lower altitudes it is represented by C. odorifera, at middle elevation by the putative hybrid C. salicifolia and at upper altitudes by C. integerrima. Flower buds of Colliguaja spp. are galled by gall-midges and also show the presence of associated parasitoids and hyperparasitoids. In this study we evaluated the effect of altitude and Colliguaja species on the distribution and abundance of flower galls resulting from parasitoid attack. Analysis of leaf morphology was used to represent either putative hybridisation or a host-plant species transition at different altitudes, while gall prevalence and relative abundance were measured as dependent variables. Gall prevalence and relative abundance decreased significantly as altitude increased, and leaf morphology indicated a host-plant transition from C. odorifera through C. salicifolia to C. integerrima. Path analysis revealed that altitude had a stronger direct effect on relative abundance of galls than host-plant, while the influence of host-plant hybridisation or species transition was mainly mediated by changes in elevation. Key-words: Mediterranean matorral, elevation, flower galls, Colliguaja. RESUMEN El genero Colliguaja (Euphorbiaceae) presenta un patron de distribucion altitudinal caracterfstico en Chile central. A altitudes bajas está representado por C. odorifera, a altitudes intermedias por el hfbrido putativo C. salicifolia y a altitudes mayores por C. integerrima. Los brotes florales de C. odorifera son atacados por moscas formadoras de cecidias, encontrandose tambien parasitoides e hiperparasitoides asociados. En este estudio evaluamos el efecto de la altitud y la especie de Colliguaja sobre la distribucion y abundancia de cecidias florales, producto de la accion de parasitoides. Se realizaron analisis de morfologfa foliar para representar ya sea la hibridacion putativa o la transicion entre especies de plantas hospedadoras, y se midió como variables dependientes la prevalencia y la abundancia relativa de cecidias. La prevalencia y abundanciarelativade cecidias disminuyeron significativamente amedida que incremento la altitud y la morfologfa foliar represento una transicion en la planta hospepadora desde C. odorifera pasando por C. salicifolia hasta C. integerrima. Un analisis de vias revelo que la altitud tuvo un efecto directo másfuerte que la planta hospedera sobre la abundancia relativa de cecidias, y que la influencia de la hibridacion o transicion en las plantas hospedadoras fue mediado principalmente por cambios en la altitud. Palabras clave: matorral mediterraneo, altitud, cecidias, Colliguaja. INTRODUCTION (Dreger-Jauffret & Shorthouse 1992). El- evation gradients normally produce transi- Most gall-maker insects are highly organ tions between closely related host-plant and host-plant specific. Hence, they have species, frequently regarded as putative attracted special attention for the evalua- hybrids, which show differences in their tion of variables affecting host-plant range susceptibility to gall makers (Whitham (Received 29 September, 1997, accepted 20 January, 1999; managed by M. George-Nascimento) 306 FUENTES-CONTRERAS ET AL. 1989, Boecklen & Spellenberg 1990, dominant representative of this genus. The Aguilar & Boecklen 1992, Moorehead et hybrid status of C. salicifolia has been al. 1993). postulated in the botanical literature (Navas Influences ofthe host-plant on gall-maker 1976). However, in the absence of experi- susceptibility to parasitoid attack (Price & mental crosses or suitable molecular mark- Clancy 1986, Clancy & Price 1986) and ers to recognise hybridisation is not pos- subsequent survival and abundance ofpara- sible to discern the actual status of the sitoids (Fritz 1995, Roininen et al. 1996) intermediate phenotypes (Paige & Capman have been previously shown. Further- 1993). Thus, it is possible that the altitu- more, elevation gradients can influence dinal distribution already described for "tritrophic" interactions when closely re- Colliguaja spp. represents just a transition lated host-plant species change their distri- between closely related species showing bution with changes in altitude (Preszler & variation in leaf morphology associated Boecklen 1996) with environmental heterogeneity caused The shrub genus Colliguaja Mol. by elevation. (Euphorbiaceae) is represented in Santiago While C. odorifera suffers low defolia- valley (central Chile) by three species with tion in relation to other shrub species of the a characteristic pattern of altitudinal dis- Chilean mediterranean matorral (Montenegro tribution. In this area, from 600 to 1200 et al. 1980), it is strongly attacked by gall- meters above sea level (hereafter masl) makers (Martinez et al. 1992). From the Colliguaja odorifera Mol. is a major com- beginning of this century the identity of ponent of the Mediterranean matorralland- gall inducer species has been under debate scape. It is gradually substituted by (Porter 1928, Martfnez et al. 1992), having Colliguaja salicifolia Gill. et Hook. at mid been solved only recently (Nuiiez & Saiz elevations (1200-1500 masl), while at up- 1994, Saiz et al. in press). These latter per altitudes (1600-2000 masl) Colliguaja studies definitively showed, as initially integerrima Gill. et Hook. becomes the stated, that the insects Riveraella TABLE I Means and standard deviations (SD) of morphological variables of populations of C. odorifera, C. salicifolia and C. integerrima utilised in the discriminant analysis. Sample size = 10 Medias y desviaciones estiindar (SD) de !as variables morfo16gicas utilizadas en el aniilisis discriminante de poblaciones de C. odorifera, C. salicifolia y C. integerrima. Tamaiio muestral = 10 Variable C.odorifera C.odorifera C. salicifolia C. salicifolia C. integerrima 1150 masl 1300 masl 1450 masl 1600 masl 1650 masl Mean SD Mean SD Mean SD Mean SD Mean SD Leaf length (I) 2.99 0.47 2.98 0.27 3.59 0.50 5.03 0.76 8.44 0.51 (cm) Leaf width (w) 1.27 0.32 1.30 0.16 0.69 0.08 0.86 0.17 0.47 0.06 (cm) lw-1 2.42 0.26 2.33 0.18 5.31 0.96 6.05 0.92 18.82 2.36 Leaf perimeter (p) 8.72 1.67 8.64 0.95 9.18 1.72 14.13 3.61 21.57 5.20 (cm) Leaf area (a) 2.80 1.21 2.77 0.57 1.76 0.29 3.13 0.25 3.20 0.42 (cm2) Leaf shape ( 4n a p-2) 0.46 0.04 0.48 0.05 0.29 0.06 0.21 0.06 0.10 0.03 Glands per leaf (g) 37.06 5.11 38.14 6.00 18.73 3.71 32.1 13.41 0 0 g p-1 4.37 0.43 4.50 0.66 2.11 0.44 2.30 0.76 0 0 FLORAL GALLS OF Colliguaja spp. 307 colliguayae Kieffer & Herbst and At each altitude, ten mature shrubs were Promikiola rubra Kieffer & Herbst randomly selected regardless of the pres- (Diptera: Cecidomiiydae) are the inducers ence of galls. On each individual shrub of the ament (male flower) gall in C. sampled, two branches were chosen at ran- odorifera. Both gall-midges can be attacked dom and the largest ten fully expanded by the ectoparasitoid Exurus colliguayae leaves on them were collected for morpho- Philippi (Hymenoptera: Eulophidae) which metric studies. At the laboratory, the leaves kills the gall-midge larvae after the gall has were placed within glass plates and scanned been induced (Saiz et al. in press). This in a Scanjet 3p® for further analysis with parasitoid wasp species remains in the gall the SigmaScan® software. Finally, the while it shows lignification until the typi- shrubs were identified to the species level cal floral galls are formed, as described by following the key of Navas (1976). Nufiez & Saiz ( 1994) and Saiz et al. (in The morphological measures of the leaves press). Furthermore, an ectohyperparasi- (Table 1) were subjected to a canonical toid wasp, Torymus laetus Philippi (Hy- discriminant function analysis to evaluate menoptera: Torymidae), may attack and if the a priori classification by altitude or consume the eulophid larvae (Saiz et al. in by Colliguaja species reflected any mor- press). Those gall-midges not attacked by phological change. Furthermore, follow- E. colliguayae leave the gall while the gall ing the approach proposed by Moorehead tissues are still soft, in early spring (Au- et al. (1993) to order hybrids and parental gust-September) (Saiz et al. in press). host-plant species, the canonical scores Therefore, typicallignified galls observed from the first discriminant function were on C. odorifera during the late summer re-scaled to obtain a modified leaf mor- season are the result of a tritrophic interac- phology index (LMI). This measure, which tion, since they would not be formed with- varies between 0 and 1, represents a mor- out the action of E. colliguayae. phological continuum, with values near 1 We studied Colliguaja spp. (Euphor- for C. odorifera, close to 0 for C. biaceae) along an elevation gradient to integerrima and intermediates for C. evaluate whether "tritrophic" effects, re- salicifolia. lated with either putative hybridisation or an altitudinal transition between host-plant Gall prevalence and relative abundance in species, and environmental heterogeneity the field associated with elevation, affect the distri- bution and relative abundance of floral The same shrubs selected for morphomet- galls. ric analysis were used to estimate the preva- lence and relative abundance of flower galls. Sampling was performed during Feb- MATERIALS AND METHODS ruary-March of 1996, the end of the sum- mer season, when all the flower galls at- Morphological analysis of the leaves of tacked by parasitoids-hyperparasitoids are Colliguaja species fully developed (Martfnez et al.
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