Distribution des œufs de la Diane Zerynthia polyxena (Lepidoptera, Papilionidae)

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par P. BATÁRY (1,2), N. ÖRVÖSSY (1), Á. KŐRÖSI (3) and L. PEREGOVITS (1), 2008. In Acta Zoologica Academiae Scientiarum Hungaricae, 54 (4) : 401-410.

• 1 Department of Zoology, Hungarian Natural History Museum H-1088 Budapest, Baross u. 13, Hungary
• 2 Current address: Agroecology, Georg-August University Waldweg 26, D-37073 Göttingen, Germany
• 3 Animal Ecology Research Group of the Hungarian Academy of Sciences and the Hungarian Natural History Museum, H-1083 Budapest, Ludovika tér 2, Hungary

RÉSUMÉ

Nous avons étudié les facteurs environnementaux qui influencent, à différentes échelles, la répartition spatiale des œufs d'un papillon, la Diane Zerynthia polyxena sur son unique plante-hôte [en Hongrie] l'Aristoloche clématite Aristolochia clematitis. Deux ensembles de variables ont été considérées : la nature de l'habitat (plantations de Robinier faux-acacia, clairières, coteaux) et la répartition des plantes-hôtes. Nous avons enregistré la distribution des œufs sur les plantes. Nous avons compté enregistré l'évolution de la végétation autour des pontes. Nous avons également mesuré la taille des feuilles et compté le numéro des feuilles sur chaque plant portant des pontes. L'apparence des pieds à été caractérisée en fonction de la différence de hauteur entre les tiges portant des œufs et les tiges périphériques. Deux variables ont été enregistrées sur les pontes (importance de la nourriture / taille des pieds) : nombre de feuilles et emplacement des œufs dans l'ordre des feuilles. Le type d'habitat affecte la distribution des œufs : les plantations de Robinier faux-acacia et les coteaux sont plus attractifs de les clairières. A une échelle semblable, une plus grande densité de plantes et l'apparence des pieds a une incidence sur la distribution des œufs. Au niveau des plantes, le nombre d'œufs augmente avec le nombre de feuilles sur chaque pied, et la position des œufs est relatif au nombre d'œufs par pieds : un nombre d'œufs réduit implique des pontes plus hautes sur la plante. En conclusion, les relations spatiales dans la distribution spatiale des œufs ne peuvent être analysées qu' avec une analyse des différents facteurs environnementaux.

Mots-clés

Zerynthia polyxena, oviposition, intéraction plante–insecte, Aristolochia clematitis, plante-hôte, échelle spatiale

INTRODUCTION

La ponte est une intéraction écologique particulièrement importante entre les insectes phytophages et leurs plantes-hôtes (RABASA et al. 2005). De plus, les préférences dans le choix du support de ponte et donc du développement larvaire sont au centre des relations biologiques entre l'insecte et la plante (XUE et al. 2007). Les imagos femelles sont capables de faire la différence entre différents sites de pontes, en fonction de leurs régimes climatiques, de leurs qualité d'alimentation pour les chenilles, ou des niveaux potentiels de concurrence et de prédation (BERNARDO 1996). La variation de ces aspects environnementaux affecte ainsi la performance de production d'une descendance. Chez les papillons, la ponte peut présenter des préférences envers certaines espèces, en particulier pour certaines en particulier, voire certaines parties des plante-hôtes, ce qui permet de déterminer les caractéristiques physiques et chimiques auxquels les insectes réagissent (THOMPSON & PELLMYR 1991, BERNAYS&CHAPMAN 1994). Etant donné que les chenilles émergentes sont relativement immobiles, la clé de leur survie et leur développement réside dans le choix de l'emplacement de la ponte par la femelle (PORTER 1992). En dehors d'études expérimentales (e.g. SINGER et al. 1993), il existe deux méthodes répandues d'études des sites de pontes des femelles de papillons. L'une d'entre-elles est basée sur le suivi des femelles et de l'observation visuelle de l'oviposition (e.g. GRUNDEL et al. 1998, BERGMAN 1999, ZIMMERMANN et al. 2005, KŐRÖSI et al. 2008). L'autre méthode consiste à observer la présence-absence ou encore la distribution visibles des œufs sur les plantes-hôtes (e.g. FLOATER&ZALUCKI 2000, ELLIS 2003, RABASA et al. 2005). Cette méthode indirecte est plus souple car elle permet au chercheur de planifier son plan d'échantillonnage et d'obtenir un échantillon beaucoup plus grand (sous réserve d'une certaine visibilité et de la possibilité d'identification des œufs). Cependant, l'inconvénient évident de cette méthode par rapport à la première, c'est que l'on ne tient compte que des plantes-hôtes habituellement utilisées par le papillon (DE BOER & HANSON 1984).

Plusieurs études ont testé les facteurs influençant la distribution des œufs à différences échelles spatiales. MCKAY (1991) a étudié les exigences de ponte du Citron Gonepteryx rhamni dans des boisements humides, en tenant compte de la distribution spatiale des plantes-hôtes, des facteurs physico-chimiques et a trouvé que la plupart des œufs étaient pondus sur de jeunes arbres poussant dans les endroits ensoleillés. De plus, les papillons semblaient préférer les arbres avec un sous-bois peu dense. De même, FLOATER and ZALUCKI (2000) ont étudié la qualité des arbres-hôtes et des préférences de la mite Australienne Ochrogaster lunifer. Ils ont trouvé plus d'amas d'œufs sur les arbres de grande qualité dans les habitats ouverts mais homogènes, tandis que dans les habitats présentant des boisement mixtes, les pontes occupaient des arbres de moins grande qualité. Dans le cas de la ponte du Collier des hélianthèmes Aricia artaxerxes ELLIS (2003), a décrit les effets

Il a décrit les incidences des différentes plantes-hôtes sur les pontes en fonctions des facteurs du micro-environnement, comme le niveau de couverture du sol par la plante-hôte ou la hauteur de végétation. Les œufs de ce papillon ont été plus fréquents sur les feuilles des plantes-hôtes les plus jeunes et plus et plus dans les sites non gérés que dans les sites gérés (végétation plus courte), tandis que la densité de plantes-hôtes ou le niveau de recouvrement du sol n'a pas d'incidence sur les pontes.


Furthermore, FARTMANN (2006) studied the effects of food-plant, microenvironment and microclimate
on the egg distribution of the Duke of Burgundy Fritillary (Hamearis lucina). He found a lower deposition height of eggs on the host-plant (Primula veris) and that majority of egg clutches situated at sites that receive direct insolation between
09:00–17:00, and which have more than 60% herb cover. DENNIS (1996) studied the oviposition in Zerynthia cretica in relation to food-plant leaves, shoots and patches. He found that females laid more eggs on large plant patches with large leaves, typically at the plant patch margin. We found only two studies that focused on monophagous butterflies and used the presence-absence data of butterfly eggs in relation to factors at different spatial scales in hierarchical nested models. KÉRY et al. (2001) studied the presence of Maculinea rebeli eggs across Gentiana cruciata fruits, genets and populations, and found that the factors measured at the genet level were more important than those measured at population level. RABASA et al. (2005) used a similar nested design to investigate the egg presence of Iolana iolas on the Colutea hispanica shrubs at fruit, plant and patch levels. They showed important factors influencing the egg presence in each level. In the present study we aimed to investigate hierarchically structured environmental factors influencing the density and distribution of Z. polyxena eggs in a black locust – poplar plantation complex, where the food-plant of this butterfly was abundant.

MATERIALS AND METHODS

Study species

The southern festoon (Zerynthia polyxena DENIS et SCHIFFERMÜLLER, 1775) is a papilionid species that reaches its northern range in Central Europe (TOLMAN 1997). The species is protected by law in Hungary. It is a monophagous species in Hungary feeding on a herbaceous plant, the birthwort (Aristolochia clematitis LINNEAUS, 1753, Aristolochiaceae). This food-plant is common on disturbed habitats, like flood plains, orchards, roadsides or black locust (Robinia pseudoacacia LINNEAUS, 1753, Fabaceae) and hybrid poplar (Populus × euramericana, Salicaceae) plantations. The flight period of the butterfly starts from mid/end April and lasts until the mid/end of May. The females oviposit on the abaxial surface of the food-plant leaves, laying either a single egg, or a smaller or larger cluster of eggs. Contrary to Zerynthia rumina LINNEAUS, 1758 which has two food-plant species (Aristolochia baetica LINNEAUS, 1753, Aristolochiaceae and Aristolochia longa LINNEAUS, 1753, Aristolochiaceae), the Z. polyxena is monophagous at least in Hungary; both eggs and larvae were observed only on A. clematitis (ROTHSCHILD et al. 1972, JORDANO&GOMARIZ 1994,ÖRVÖSSY et al. unpubl.)

Study area and sampling design

The study area was situated on the Hungarian Great Plain near Csévharaszt (Central Hungary, 47°18’N, 19°26’E), in a landscape comprising of tree plantations, mainly black locust and poplar cultivar plantations interrupted by clearings. The 0.02–0.03 km2 large plots were separated by hummocks originating from the last harvest of the plantations and consisted of stumps and roots covered by soil, providing an ideal place for the birthwort. A clump of food-plants consisting of at least five shoots per m2 and separated by at least 10 m from other food-plants was considered as a patch. We chose 4–4 food-plant patches for sampling in the three available habitat types, i.e. in black locust plantations, in clearings and in hummocks. In our earlier study on the same study area, we found that the imagoes avoided the poplar plantations (ÖRVÖSSY et al. 2005). Each of these food-plant patches
were covered by several thousands of birthwort shoots. We randomly selected 10 points within each patch, where we checked food-plant shoots for eggs in a 5-meter radius circle. Since relatively few food-plant shoots had leaves loaded by eggs, we stopped further searching after finding the first shoot with eggs. These circles were covered by an average of 775 food-plant shoots. From the total of 120 randomly chosen circles, 98 contained eggs, and circles without eggs were excluded from the analyses. The flight period (26 April to 15 May) ended before the egg searching (17–23 May), thus new ovipositions during the sampling period could not cause a bias. No larvae were found during the egg survey.

During the egg-survey several environmental variables were measured in the close proximity of the egg-bearing shoots. We grouped these variables according to spatial scales. The habitat type of a given food-plant shoot (black locust plantation, clearing or hummock) was interpreted as a patch level variable, and incorporated into the model as a factor. To characterise the habitat types we counted the food-plant shoot density on 20 randomly selected 2×2 m squares in each food-plant patches. We measured the size of patches. To characterise the microenvironment of the selected food-plant shoots, we counted the number of shoots and measured the mean shoot height in a 1×1 m square. We also measured the height and counted the leaves of egg-bearing shoots. We expressed food-plant apparency as the height difference between an egg-bearing shoot and the mean of sur-
rounding shoots in the 1×1 m square. On the egg-bearing shoots two variables were measured; the number of food-plant leaves and the position of the egg or the egg cluster (hence we call the scale of these variables as food-plant level to differentiate from the scale of variables measured in the direct proximity of the egg-bearing shoots, i.e. microenvironment level). The latter one was expressed as the number of leaves below the leaf bearing the egg(s) divided by the total number of leaves. Statistical analysis The effects of above mentioned environmental variables on egg distribution were analysed in general linear mixed-effects models with the Restricted Maximum Likelihood method. The normality of the distribution of eggs per leaf was assessed using normal quantile plots. Log-transformation was applied to handle non-normal distribution. The following non-correlated variables were considered in the statistical model: 1) habitat type as a factor and patch size as a co-variable at patch level; 2)
at the microenvironment level, the food-plant shoot density around the egg-bearing shoot and apparency; 3) the number of food-plant leaves and the position of eggs at food-plant level. Since food-plants were nested within food-plant patches, the latter was used as a random factor. Although food-plant leaves were also nested within food-plants, we could not include food-plant as a random factor in the model, because it would have had too large effect relative to the residual. Altogether there were only five food-plant shoots with eggs on two leaves and one food-plant shoot with eggs on three leaves. Leaves without eggs (1036) were excluded from the analysis. Furthermore, we compared models with and without the inclusion of food-plant as a random factor. We found that the two models were significantly different (L-ratio = 59.8; P < 0.0001), and the model without food-plant
had smaller AIC value, indicating that this model was more supported. By right of these, we decided to apply the latter model. The calculations were made using R (version 2.2.1; R DEVELOPMENT CORE TEAM 2006) and the nlme package for R (version 3.1, PINHEIRO et al. 2007).

RESULTS

We registered 597 eggs of Z. polyxena laid either singly, or in small (2–8 eggs) or large (10–99 eggs) clusters on the underside of food-plant leaves. During the survey we did not find any larvae nor hatched eggshells. The habitat type significantly affected the distribution of eggs (Table 1). When we compared the food-plant shoot density between habitat types with a one-way ANOVA, we found significant difference between them (F = 23.207, P < 0.001, N = 240, Fig. 1, Tukey HSD post-hoc tests showed that all habitat types differed significantly from each other regarding food-plant shoot density). There were significantly more eggs on
food-plants in black locust plantations and hummocks than in clearings (Fig. 2). At the microenvironment level, neither food-plant shoot density, nor food-plant apparency affected the egg distribution (Table 1). At the food-plant level, the number of eggs increased significantly with the number of food-plant leaves/shoot (Table 1). Finally, the position of eggs also affected significantly the number of eggs ; there were more eggs on the lower part of the food-plants than upward (Fig. 3).

Table 1. Linear mixed models for testing the effects determining the egg-laying preference of Z. polyxena at different levels. Bold p values indicate significant effects.

Fig. 1. Mean (±SE) number of food-plant shoots per m2 in the three habitat types. The different letters indicate significant differences at P < 0.05

Fig. 2. Mean (±SE) number of eggs of Z. polyxena per food-plant leaf in the three habitat types. The different letters indicate significant differences at P < 0.05

Fig. 3. Egg position on the plant’s leaf-storeys (the number of leaves below the leaf bearing the egg(s) divided by the total number of leaves) is plotted against log number of eggs. Smaller value of egg position indicates that the eggs are on lower leaves. The solid line represents the fix effect of egg position of the fitted model

DISCUSSION

The behaviour leading to oviposition, i.e. selection of oviposition site, is a complex process, because successful oviposition greatly contributes to individual fitness (SCHOWALTER 2006). However, females do not always select the most appropriate host and newly hatched larvae may reject the plant on which they hatch (BERNAYS&CHAPMAN 1994). So egg-laying females can make errors and larvae can correct it to some degree, but if they are to survive, i.e. to maximise their fitness, the females’ preference and the larvae’s performance should overlap as much as possible. In the current study, the egg distribution of Z. polyxena was affected on two levels, basically by habitat type and also by characteristics at food-plant level, but not by factors at the microenvironment level.

The habitat differences found in the present study, i.e. the black locust plantation and hummocks were more preferred than clearings, may well be interpreted as the butterflies’ preference against areas that were more exposed to direct sunshine
or cold. FARTMANN (2006) reported that H. lucina preferred those sites for oviposition in calcareous grasslands, where the food-plant (Primula veris) potentially received direct insolation between 09:00 and 17:00. MCKAY (1991) found that most eggs of G. rhamni were laid on isolated juvenile trees (Frangula alnus) growing at sunny sites. These studies show that oviposition site preferences may ensure an optimal microclimate for the development of the larvae.

In our case, patch size did not affect the number of eggs laid, while in the case of Z. cretica DENNIS (1996) showed that larger food-plant patches had more eggs. However, we have to call the attention to the fact that in the latter study the patches
were mapped on a much finer scale (food-plant patch size range: 25 to 2400 cm2) than in our case (food-plant patch size range: 661 to 11954 m2, mean: 3384 m2). At the microenvironment level, neither food-plant shoot density, nor foodplant apparency seemed to act as a limiting factor on egg density. However, we have to mention that food-plant shoots occurred in a very large number in each habitat. Moreover, food-plant shoot density was highest in the clearings, generally two times higher than in the black locust plantation and about 15% higher than in he hummocks (Fig. 1). This also suggests that the habitat type effect is not connected with the food-plant availability. In contrast to our results, DENNIS (1996) found in his fine scale study that food-plant shoot number was one of the most important factors affecting the egg density of Z. cretica. Regarding food-plant apparency,
the height of egg-bearing shoots were significantly higher than those in the microenviroment (paired t-test, t = 8.956, P < 0.001), however, it probably influences only the food-plant selection of butterflies, but not the egg load.

The number of food-plant shoot leaves showed a positive effect on egg numbers and more eggs were found on the lower leaves of food-plant shoots. In our earlier study, we observed that at the beginning of flight period the food-plants were quite scarce and just started to develop, therefore, the first females had limited choices (ÖRVÖSSY et al. 2005). This probably means that early sprouting food-plants have some advantage compared to the late sprouting ones, therefore, they could be more apparent. Since food-plant shoots receive eggs at a younger stage, the eggs are situated on lower leaves. Moreover, at this period the females have large egg load, which could also cause that they lay eggs in clusters rather than single eggs. This result suggests that temporal aspects are also important in oviposition. DENNIS (1996) also emphasized the importance of the duration of food-plant patches; he suspected that food-plant patches available for longer periods are more likely to have more larvae. Investigating a congeneric species, Z. rumina, JORDANO & GOMARIZ (1994) found that the freshly hatched larvae consumed the younger and
softer leaves of the food-plants. This could stand behind that the observed Z. polyxena females also laid the eggs on young leaves, however, with egg searching it was not possible to investigate the temporal effects. Another potential explanation
for the young leaf selection could be that females select these because of lower concentrations of some defence chemicals. However, ROTHSCHILD et al. (1972) described that Z. polyxena contained and stored efficiently two aristolochic acids
which were presumably present in its food-plant, in A. clematitis.

In this short study we showed that the egg distribution of Z. polyxena was affected by several components acting at different spatial levels. We have to emphasise that such a complex process, like oviposition, should also be investigated by the direct tracking of females, which could illuminate further aspects of egg distribution. As a conclusion, we also underline that spatially correlated data in egg distribution studies need to be analysed considering an intrinsically hierarchical structure of environmental factors (RABASA et al. 2005).

Acknowledgements

Two anonymous referees provided constructive remarks that considerably improved the manuscript.We are indebted to LAJOS RÓZSA for valuable comments and linguistic revisions on the manuscript. The study was supported by the National R&D Programme, entitled “The origin and genezis of the fauna of the Carpathian Basin: diversity, biogeographical hotspots and
nature conservation significance” (contract no. 3B023–04).

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Traduction proposée par Christophe Bernier, le 1er septembre 2010.

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