The antennal lobe of Libellula depressa (Odonata, Libellulidae)
Introduction
Research on the olfactory neurobiology of insects has focused on many Neoptera such as flies, cockroaches, honeybees, moths and locusts. In these insects the general organization of the central olfactory pathway has been studied in detail (Strausfeld et al., 1998, Schachtner et al., 2005, Galizia and Rössler, 2010, Martin et al., 2011, Strausfeld, 2012).
The antennal lobe (AL) is the first integration center for odor information in the brain (Strausfeld and Hildebrand, 1999). It is part of the deutocerebrum and receives sensory innervations from olfactory sensory neurons (OSNs) on the antennae. In the AL these afferents form dense spherical structures, called olfactory glomeruli, which are functional morphological subcompartments. Detailed investigations on the honeybees revealed that 3–5 antennocerebral tracts (axons of projection neurons) connect each AL with higher brain areas (mushroom bodies and lateral horn) (Hansson and Anton, 2000, Galizia and Rössler, 2010).
Ephemeroptera and Odonata are classified as Palaeoptera (old wings), the remainder of the pterygote insects constitutes the larger clade Neoptera (new wings). The earliest branching event in winged insects is one of the core problems regarding early insect evolution and paraphyly of Palaeoptera could be a possibility in hexapod phylogeny. However, in a recent paper by Blanke et al. (2012) parsimony analyses of the head data unambiguously supported a clade Palaeoptera. Odonata and Ephemeroptera show big eyes and reduced antennae with a short flagellum, and they are considered mainly visually oriented. While many studies have been published on their visual abilities (Sherk, 1978a, Sherk, 1978b, Sherk, 1978c, Olberg, 1981, Olberg, 1986, Olberg et al., 2000, Olberg et al., 2005, Olberg et al., 2007), little attention has been paid to other sensory modalities. In particular, the problem of olfaction in Palaeoptera cannot be considered fully elucidated until now. Their brain seems to lack glomerular antennal lobes and they do not possess mushroom body calyces, a major target area of olfactory input originating in the antennal lobe (Strausfeld et al., 1998, Strausfeld et al., 2009, Farris, 2005). Strausfeld et al. (1998) reported that Thysanura, Ephemeroptera and Odonata are probably all anosmic with respect to air-borne odors. The same authors reported in 2009 that Palaeoptera are basal taxa characterized by possessing reduced “setaceous antennae” that supply axons to mechanosensory neuropils. In an overview on the primary olfactory brain centers in Crustacea and Hexapoda, Schachtner et al. (2005) reported that dragonflies and mayflies show small antennae and a small deutocerebrum, suggesting only a poorly developed olfactory system and that the area in the brain receiving sensory input from the antennae in both orders lacks a glomerular neuropil (Baldus, 1924, Hanström, 1928, Strausfeld, 1998). Studies in adult Aeshna cyanea revealed that even the bipartite organization typical of other insects is missing (Baldus, 1924).
An electron microscopic investigation of the adult dragonfly Libellula depressa (Odonata: Libellulidae) revealed sensilla located in pits on the antennal flagellum (Rebora et al., 2008), which can be categorized as sensilla coeloconica and as deeply sunken sensilla styloconica. The structure of sensilla coeloconica is in agreement with that reported for insect olfactory receptors (Steinbrecht, 1997). The deeply sunken sensilla are represented by sensilla styloconica located at the bottom of deep cavities that show features typical of thermo-hygroreceptors (Rebora et al., 2008). In these ultrastructural investigations no other sensory structure was noted on the antennal flagellum except for some occasionally observed campaniform sensilla (Rebora et al., 2008), representing mechanoreceptors likely used to inform the insect of flagellum bending. Single sensillum electrophysiological recordings from adults of L. depressa confirmed the presence of thermo-hygroreceptive neurons and olfactory neurons on the antennal flagellum of L. depressa (Piersanti et al., 2011, Rebora et al., 2012). The presence of olfactory and thermo-hygroreceptive sensilla has been shown in ultrastructural investigations in several Odonata families (Rebora et al., 2009a, Piersanti et al., 2010) and in Ephemeroptera (Rebora et al., 2009b, Rebora et al., 2010).
Except for the description of the mushroom bodies (Strausfeld et al., 2009), the available information on the organization of the Odonata brain is scarce and mainly based on old data (Baldus, 1924, Hanström, 1928) or limited to the larval brain (Svidersky and Plotnikova, 2004, Svidersky and Plotnikova, 2006). Among the most ancient Hexapoda, detailed neuroanatomical data on the antennal lobe are available for Collembola (Kollmann et al., 2011) and Archaeognatha (Mißbach et al., 2011), and some preliminary observations have been published for Zygentoma (Schachtner et al., 2005), but no studies on Odonata and Ephemeroptera antennal lobes have been published so far except for the above reported overview on the primary olfactory brain centers in Crustacea and Hexapoda by Schachtner et al. (2005).
The aim of the present paper is to describe the projections of afferent sensory neurons stemming from the antennal flagellum sensilla (OSNs and thermo-hygrosensory neurons) of the dragonfly L. depressa, in order to identify the antennal lobe and provide more information on it.
Section snippets
Study insects
Larvae of L. depressa Linnaeus, 1758 (Odonata: Libellulidae) were collected in a natural pond in Lisciano Niccone (Perugia, Central Italy) in March–April 2010 and carried to the Max Planck Institute for Chemical Ecology (Jena, Germany) in order to obtain adults. In the laboratory, the larvae were kept in plastic containers with water, detritus, flora and fauna from the collecting site at 25 ± 2 °C, LD 12:12 h light conditions, and were fed ad libitum with plankton and Diptera larvae up to the
The brain
Among the major brain areas (neuropils) of the brain of L. depressa, we reconstructed those that we were able to unambiguously delimit in all three dimensions (Fig. 1). The protocerebrum (without the optic lobes which had been removed) hosts huge mushroom bodies (MBs) and the central complex. The mushroom bodies are composed of a pedunculus, which divides into a vertical (alpha) lobe and a medial (beta) lobe. In the upper part of the pedunculus the Kenyon cell somata are visible, but there is
The antennal lobe of L. depressa and the dragonfly's ability to perceive odors
The synaptic background labeling as well as the antennal backfills showed that sensory neuron arborizations cover a great portion of the AL, which lies surrounded by clusters of cell bodies very likely representing projection neurons and local interneurons. As reported in Section 2, NC82 immunohistochemistry was used in L. depressa to outline neuropils. NC82 did stain neuropils in the dragonfly, but failed to outline AL olfactory glomeruli. We therefore additionally employed Lucifer yellow as
Acknowledgements
We are grateful to Tor Jorgen Almaas for his help in the collection of some preliminary data, to Patrizia Elena Vannucchi for her help in carrying dragonfly larvae to Jena, to Shannon Olsson for her helpful comments on the manuscript, and to the anonymous referees for their helpful suggestions. This work was supported by National Research Funds (Fondo Integrativo per la Ricerca di Base – F.I.R.B., 2010, RBFR10Z196) and by the Max Planck Society.
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