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The Prothoracic Gland of the Chrysopidae (Neuropteroidea: Planipennia)

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The Prothoracic Gland of the Chrysopidae (Neuropteroidea: Planipennia) Proceedings of the 4th ECE/Xll/. SIEEC, Godol/61991 The Prothoracic Gland of the Chrysopidae (Neuropteroidea: Planipennia) R. Giisten and K. Dettner Key words: green lacewings, defensive secretions, SEM, GC/MS, evolution, phylogeny Introduction Some species of green lacewings (Planipennia: Chrysopidae) produce a distinc- tive scent during molestation, usually described as allylic or faecal-like. As the source of the secretion causing the odour, paired prothoracic glands were deter- mined (McDunnough 1909), but later investigations were restricted to a detailed morphological and anatomical description of the glands in Chrysopa per/a by Sulc (1914). An analysis of secretion chemistry in Chrysopa oculata by Blum et al. (1973) revealed the presence of skatole (3-methylindole) as a gland content, which is responsible for the odour. Up to now, all references to the prothoracic glands assume their existence in the strong-smelling species only; a statement by Sulc (1914, p. 3) that they also occur in Chrysoperla carnea, which is inodorous/ was obviously overlooked. In order to record the actual distribution of these glands within the family, we examined 20 European chrysopid species for the occurrence of these organs. Besides 18 species of the tribe Chrysopini (Chrysopinae), ltalochrysa italica (Chry- sopinae: Belonopterygini) and Nothochrysa fulviceps (Nothochrysinae) were also included in the study. We present the results of investigations of gland morphology and secretion chemistry, and we discuss the probable function of the prothoracic secretion, the morphological, chemical and functional evolution of the gland, and its possible significance for phylogeny and systematics of the family. Methods Morphological investigations of the prothoracic gland were carried out by scanning electron microscopy (SEM) of macerated halves of prothoraces, showing the gland reservoir as well as properties of the reservoir opening and fine structure of glandular units. For chemical analysis, we used a gas chromatography/mass spectrometry coup- ling (GC/MS), which provides separation of secretion compounds and gives spe- cific mass spectra which help identify individual substances. Morphological and chemical characters of the prothoracic gland evaluated in this study were entered 60 into a numerical phenetic analysis, creating a phenetic tree of the investigated species. For this operation, we used the program NTSYS-pc 1.50 (Rohlf 1988) on a personal computer. Results The prothoracic gland proved to be present in all the 20 species studied. The three suprageneric taxa showed a number of differences in gland morphology. The most significant of these was the shape of the reservoir (Fig. 1): it is divided into two lobes in all 18 species of Chrysopini, into three less clearly separated lobes in Italochrysa (Belonopterygini), but undivided in Nothochrysa (Nothochrysinae). Another difference shown in Fig. 1 is the position of the gland opening, which .is partly concealed by the pronotum in Chrysopini, situated just below it in Italochry- sa and much more ventrally so in Nothochrysa. The reservoirs of the investigated species of Chrysopini, while very similar in shape, differ considerably in size. In Peyerimhoffina, Chrysoperla and most species of Chrysopa, they nearly fill out the prothorax, while they are nearly 4 times smaller (relative to body size) in the species of Nineta. Chrysopidia, Mallada, Cunctochrysa and Chrysopa viridana are intermediate. Fig. 1. Position of gland opening slit and reservoir shape in three species of Chrysopidae: Nothoch,ysa fulviceps (top), ltalochrysa italica (middle), Chrysopa per/a (bottom). (The three species are not drawn to scale. Abbreviations: gr - glandular reservoir; go- gland opening; ps - pleural sclerites · 61 The chitinous elements of the glandular units - functional units of a gland cell and accessory cells, which create a cuticular ductule - are observable in macerated SEM-preparations (for detailed discussion of glandular units, see Noirot and Quennedey 1974). We found that in Chrysopidae, glandular units associated with the prothoracic gland reservoir are extremely similar to dermal glandular units distributed over the integument. lnterspecific differences concerning shape and fine structure of glandular units could be shown only in the length of the cuticular duct. In this trait, species of Chrysopa (except Ch. viridana) are most divergent, having ducts of about 80 µm length, compared with 10-30 µm in other species. Secretion chemistry was analyzed in 13 species from 5 genera of the tribe Chrysopini. The 30 substances found can be arranged in 7 groups according to their chemical structure. A fraction of alkenes is found in all species and, remarkably, its composition is very similar in all. The main compound of this fraction is (Z)-4-tri- decene. The other compound groups show various chemical compositions and might be derived from quite different biogenetic pathways. They are usually spe- cific for certain genera, e.g. terpenoids (Chrysopidia), octanoic acid (Chrysoperla), long-chain hydrocarbons (Chrysoperla and Mallada), amides (Chrysopa) a!]d ska- tole (all Chrysopa except Ch. viridana). A special case is observed in Nineta, where no substances other than the alkene fraction are present. Discussion The idea that the strong-smelling secretion of Chrysopa species has defensive function is· quite straightfoiward and was first proposed by Melander and Brues (1906) and adopted by most later authors. In view of the great olfactory sensitivity of mammals to skatole (Laffort 1963), bats (Chiroptera) seem to be likely target organisms for the defence secretion, as they are potentially important predators of the night-flying Chrysopidae. Blum et al. (1973), however, found evidence for a repellent effect not only against mammals (mice) but also against arthropods (ants). For a number of reasons, we believe that the prothoracic secretion in the inodorous species serves as a defensive allomone as well, rather than representing some kind of pheromone. Firstly, it appears that these species, just as the odorous ones, discharge their gland contents when molested, even though this is difficult to observe in most cases. Also, it is unlikely that this secretion represents a phero- mone playing a role in sexual interactions, as there is no sexual dimorphism and as there are already other pheromone glands known in these insects (male abdominal glands; Wattebled and Canard 1981). Aggregation or alarm pheromones are not to be expected in the solitary green lacewings. The glands of Nineta show the most primitive situation among Chrysopini chemically as well as morphologically. If they are regarded as a model for the initial stage in the evolution of the pro thoracic gland, it must be asked which could be the defensive value of the alkene-containing secretion. A possible hypothesis is that these hydrocarbons act as a solvent and spreading agent for gut contents which are exuded in defence. Discharging faeces or gut contents is the simplest way of chemi- cal defence in arthropods (Dettner 1989). The effect of repellent substances con- tained in gut contents can be both more potent and more prolonged if solvent 62 substances from an exocrine gland are added. A comparable phenomenon has already been shown in Opiliones (Eisner et al. 1978); in these, however, the active substances are contained in the glandular secretion. The idea that a mixing of fluids for defence is found in Nineta and other chrysopids is supported by the obsetvation that gut contents are nearly always discharged together with the prothoracic secre- tion by all inodorous species, and also, less obviously, by the odorous species. Alkenes represent ideal solvents for active substances in defensive mixtures, but have little or no repellent or toxic effect on their own (Dettner 1991 ). Derived from this hypothetical initial stage, the defensive value of the secretion could have been more and more enhanced during evolution by adding different active substances, corresponding with a stepwise enlargement of the gland resetvoir. The different kinds of multicomponent secretions might also reflect an adaptation to different predators as target organisms, like the skatole-containing secretion possibly di- rected against bats. As the prothoracic gland is obviously a groundplan character in Chrysopidae, it can be used as a valuable tool in phylogeny and systematics, and this can be done on different taxonomic levels. The subfamilies Nothochrysinae and Chrysopinae, and also the two investi- gated tribes of Chrysopinae (Belonopterygini, Chrysopini) clearly showed structu- ral differences in overall gland morphology, indicating that even a superficial examination of this character might help clarifying the relationships of supra- generic taxa within the family. For future studies, this could especially be promi- sing for the Ankylopterygini, Leucochrysini and the different lineages of Chrysopi- ni (which are probably not monophyletic), whose affinities still remain uncertain after the extensive investigation by Brooks and Barnard (1990). Chrysopidia ciliata Nineta pa/Iida ------ Ma/lada flavifrons ------------ Mal/ada picteti Mallada prasinus Mallada marianus Mal/ada zelleri I .Mallada ventrulis I ----Mallada clathratu.~ ---------------Chrysoperla camea ------------Cunctochrjsa baetica Chrysopa per/a --- Chrysopa walkeri ..---------1 ---Ch,ysopa f omwsa I ---- Chrysopa dorsalis I ..,__ _______ Clzrysopa pa/lens --------- Chrysopa abbreviata ---------- Chrysopa vin·dana
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