Serotonin depresses feeding behaviour in ants

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Abstract

Feeding behaviour is a complex functional system that relies on external signals and the physiological state of the animal. This is also the case in ants as they vary their feeding behaviour according to food characteristics, environmental conditions and – as they are social insects – to the colony’s requirements. The biogenic amine serotonin (5-HT) was shown to be involved in the control and modulation of many actions and processes related to feeding in both vertebrates and invertebrates. In this study, we investigated whether 5-HT affects nectar feeding in ants by analysing its effect on the sucking-pump activity. Furthermore, we studied 5-HT association with tissues and neuronal ganglia involved in feeding regulation. Our results show that 5-HT promotes a dose-dependent depression of sucrose feeding in Camponotus mus ants. Orally administered 5-HT diminished the intake rate by mainly decreasing the volume of solution taken per pump contraction, without modifying the sucrose acceptance threshold. Immunohistochemical studies all along the alimentary canal revealed 5-HT-like immunoreactive processes on the foregut (oesophagus, crop and proventriculus), while the midgut and hindgut lacked 5-HT innervation. Although the frontal and suboesophageal ganglia contained 5-HT immunoreactive cell bodies, serotonergic innervation in the sucking-pump muscles was absent. The results are discussed in the frame of a role of 5-HT in feeding control in ants.

Highlights

► Serotonin (5-HT) depresses sucrose feeding in Camponotus mus ants. ► Intake rate decreases in a dose-dependent manner. ► This occurs by a diminution in the volume of solution taken per pump contraction. ► Oesophagus, crop and proventriculus present 5-HT innervation but sucking-pump does not. ► Frontal and suboesophageal ganglions contain 5-HT immunoreactive cell bodies.

Introduction

Feeding is a very complex behaviour and its regulation requires the integration of a wide range of factors. Not only do external conditions such as the season, the time of day and the quality of food determine the feeding behaviour of an animal, but also its physiological state. Biogenic amines play an important role in the control and modulation of many actions and physiological processes in both vertebrates and invertebrates. Particularly the monoamine serotonin (5-hydroxytryptamine, 5-HT), which is found in all phyla that possess nervous systems (Weiger, 1997), orchestrates diverse behaviours and processes controlling energy balance in species as disparate as nematodes and humans (Tecott, 2007). While in vertebrates it has an inhibitory effect on feeding-related activities, in some invertebrates such as annelids, molluscs and nematodes it promotes an activation of such behaviours (reviewed in Gillette, 2006, Tecott, 2007).

In insects, monoamines can act as neurotransmitters, neuromodulators or neurohormones, exerting their effects at the central or peripheral level (Bicker and Menzel, 1989, Roeder, 1999, Blenau and Baumann, 2001, Scheiner et al., 2006, Orchard, 2006). Pharmacological studies on different insects have demonstrated that the alteration of haemolymph or neuronal levels of 5-HT modifies feeding behaviour (Kaufmann et al., 2004, Neckameyer et al., 2007, Haselton et al., 2009). In the flies Phormia regina and Neobellieria bullata and the cockroach Rhyparobia madera, administration of 5-HT promotes a decrease in sucrose consumption (Long and Murdock, 1983, Cohen, 2001, Dacks et al., 2003). It has been suggested that this effect could be due to a decrease of the sucrose sensitivity, raising the sucrose response threshold of the insect, and consequently, diminishing its food intake (Dacks et al., 2003). The effect of 5-HT on the dynamics of ingestion and the underlying mechanism have not yet been identified for insects. Does 5-HT only affect the total amount of food consumed? Or could 5-HT rather be acting – either at a peripheral or central level – on the activity of the feeding apparatus?

Immunohistochemical studies performed in several insect species revealed that the serotonergic system is involved in the main centres that control feeding – the suboesophageal ganglion (SEG) and the frontal ganglion (FG) – as well as in the salivary gland, the mouthparts and the alimentary canal (Nässel and Elekes, 1984, Davis, 1985, Klemm et al., 1986, Nässel, 1988, Orchard et al., 1988, Lange et al., 1988, van Haeften and Schooneveld, 1992, Ali et al., 1993, Ali, 1997, Miggiani et al., 1999, Dacks et al., 2003, Molaei and Lange, 2003, Orchard, 2006, Tsuji et al., 2007, Siju et al., 2008). This strongly suggests that 5-HT plays an important role in the control and integration processes involved in feeding modulation. However, the distribution and function of this amine seem to vary widely among taxa.

Insects achieve fluid intake by the sucking-pump; its anatomy was described for two ant species: Lasius niger (Janet, 1905) and Pachycondila villosa (Paul et al., 2002). It is composed of different sets of muscles that act by dilating, retracting and adducting the pharynx and the buccal tube; the contraction of the dilator muscles expand the pharynx generating the negative pressure that drives the fluid into the mouth. Sucking-pump activity was characterized for the nectivorous ant Camponotus mus (Josens et al., 2006, Falibene and Josens, 2008, Falibene et al., 2009). This ant is able to vary the velocity of sucrose solution intake depending on the sugar starvation level of the colony (Josens and Roces, 2000). Carbohydrate-starved ants reach higher intake rates by increasing pumping frequency while maintaining the volume taken per pump contraction almost constant for a given concentration (Falibene and Josens, 2008, Falibene et al., 2009).

Although many aspects of feeding behaviour and feeding regulation have been studied in ants, there is no available information about 5-HT with regard to feeding in this insect. Considering the role of the physiological state on the modulation of ingestion, the aim of the present work was

  • (1)

    to analyse the effects of this amine on feeding behaviour and sucking-pump activity, and whether the observed effects are due to changes in the sucrose perception and

  • (2)

    to study by immunohistochemical techniques the 5-HT association with the alimentary canal, the sucking-pump muscles and the major neuronal centres involved in feeding regulation.

Section snippets

Insects

Six colonies of C. mus (Roger) composed of around 1000 workers and one or more queens were used in the experiments. The colonies were captured in Buenos Aires (34° 32′ S, 58° 26′ O) and Santiago del Estero province (27° 49′ S, 64° 03′ W), Argentina, and transported to the laboratory. Each colony was reared in an artificial nest or container consisting of a plastic box (30 × 50 × 30 cm) with its base coated with plaster and its walls painted with fluon to prevent animals from escaping. Colonies were

Time-dependency of effects

The sucking-pump activity recorded throughout the time after treatments did not show any differences between 5-HT and control groups until 3:30 h. From approximately 40 min to 3:30 h after treatment, pumping frequency increased with the time in both groups (Fig. 1A). From thereon, the control ants kept pumping frequencies constant until the end of the experiment (6:30 h) while 5-HT treated ants tended to pump at lower frequencies. Considering these results, we separated the 5-HT effect in two

5-HT and feeding behaviour

The present study indicates that 5-HT promotes a depression on nectar feeding in the ant C. mus. Orally administered 5-HT to starved ants reduced the volume of sucrose solution ingested, either when administered as individual treatment or to the group and shared by trophallaxis. Depressant effects of this amine on feeding have also been demonstrated in other insects. The plant-sap feeding aphid disrupts the stylet penetration behaviour when treated with exogenous 5-HT (Kaufmann et al., 2004).

Acknowledgements

We thank the two anonymous referees for their helpful comments to improve the manuscript. A.F. thanks Dr. Claudia Groh, Thomas Münz and Cornelia Grübel for their fruitful comments and help with the immunohistochemical experiments. This work was supported by ANPCYT – FONCyT (PICT 1319), CONICET and a fellowship to A.F. (DAAD, Germany with the Argentine Ministry of Education).

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