Table of contents
Functional differentiation - Chewing mouthparts - Mouthparts of Diptera - Labrum and epipharynx - Mandibles - Maxillae - Hypopharynx - Labium - Bibliography - Web resourcesThe mouthparts are the assemblage of the appendages of the head that are articulated to the peristome and used for collecting and taking food. After any chemical and mecchanical treatment, food is introduced by mouthparts into the oral cavity. Like all Insects, the mouthparts of Diptera are composed of external appendages, exposed and projected outwards (ectognathous type).
The ground plan of Insects, identified in the chewing type, in Diptera disapperars completely, even in the most primitive groups, meeting with drastic morphological, anatomical, and functional changes.
Functional differentiation
The mouthparts of adults flies is adapted for sucking liquid food, sometimes represented by solid particles. This happens by a food channel, structured in different ways according to systematic groups and the adaptation is called sucking mouthparts. The sucking functions is completed by other which are mutually alternatives and imply a clear relation between the anatomical structure, the functional properties and, finally, the feeding behavior. Apart from the wide heterogeneity found within the order, for Diptera we can discern between two basic types of sucking mouthparts:
- a type that can pierce or lacerate the integument of animals in order to feed the internal fluids, represented by blood of vertebrates or hemolymph of arthropods. This type is called piercing and sucking mouthparts;
- a type able to lick the surface of substrate that collects fluid food, directly from the surface of liquids, from exudates, or produced by previous dissolution. This type is called sucking mouthparts or no biting sucking mouthparts.
The association of sucking with piercing or licking functions, reflects the nature of food that composes the diet of adults. The piercing function is associated to bloodsucking or predator flies. Adults provided with this adaptation behave as epizootic parasites on vertebrates (bloodsucking flies) or like predators of other arthropods (insects and spiders). The carnivorous component of diet can be unique or has a complementary function; in this late case, the hematophagy or the insectivory are designed to meet the protein requirements for reproduction and they complete unbalanced diets, generally with high carbon/nitrogen ratio, like those based on nectar or sugar. For this reason, the carnivory sensu lato falls sometimes in context of behavioral sexual dimorphisms: for example, it is commonly known that females of mosquitoes bite and suck blood, while males are exclusively vegetarian. The opposite condition (vegetarian females and carnivorous males) does not occur and this confirms the hypothesis that the carnivorous adaptation is associated with specific physiological needs of females.
The no biting sucking function is associated with various liquid diets. In these cases, food is represented by vegetable juices of animal fluids, which escapes from glands, natural orifices or wounds (nectar, serum, lymph, etc.), or alternatively by organic liquids as must, milk, urine, etc. These feeding behaviors are associated to a simple sucking function. Otherwise the liquid food must be obtained from the oozing of a solid substrate or previous dissolution. In this last case, the sucking function is preceded by a chemical or mechanical action, executed by the labella of the proboscis. This action is intuitively matched to the idea of licking. In this case, the diet may have various components, more or less exclusive within the systematic groups, which involve saprofagy, glycophagy on honeydew, pollinivory, necrophagy, etc. Apart from a few exceptions, a distinction between the strictly sucking and the licking-sucking functions is not well defined, so we consider these behaviors as a whole opposed to piercing and sucking function.
An interesting aspect is the absence of associations between the piercing function of mouthparts and the phytophagy, contrary to other orders, as Hemiptera and Tysanoptera. Within the Diptera there are instances of females of phytophagous species in the larval stage, that supplement their diet with vegetable juices of plants attacked by the larvae. The piercing of vegetable integument is made by the ovopositor: often the female practices bites to eat juices using the ovopositor but without laying eggs.
The variability of adults' diet of Diptera occurs across the entire order with no apparent specificity: groups without relationships can be include saprophagous, insectivorous, nectarivorous, and bloodsucking species, for example, and the diet is associated to a singular adaptation of the mouthparts structure (Oliveira & Serra, 2008). An obvious example of this condition is the piercing function related to hematophagous or insectivorous diets which occur among nematocerous taxa (i.e. Culicidae, Ceratopogonidae, Psychodidae), lower brachycerous (i.e. Tabanidae, Asilidae), but also Calyptratae (i.e. Glossinidae and tribe Stomoxydini within the Muscidae). Because they are derived characters, these diets must be considered as convergences, at least in high-level taxa, as shown by strong differences between the structures of mouthparts: for example, the piercing function is permormed by mandibles and maxillae in the Culicidae, by the hypopharynx in the Asilidae, and by the labium in the Glossinidae.
Chewing mouthparts
an: antenna; cl: clypeus; li: labium; ls: labrum; md: mandible; ms: maxilla; oc: eye; pl: labial palpus; pm: maxillary palpus.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
The mouthparts of Insects, in the primitive structure, derive from the differentiation of three postoral segments. The structure is composed of articulated appendages called gnathites, represented by two pairs of symmetrical appendages (mandibles and maxillae) and a posterior (labium), unpaired and median. The gnathites are connected to the peristome of head by fixed or flexibles articulations and surround and delimite the mouth opening from the side and the back.
The anterior part of mouth is closed by the epipharynx, a morfological and anatomical structure identified with the internal side (or ventral or oral) of the labrum. Strictly speaking, the labrum does not belong to mouthparts, because it derives from a preoral segment; however, the epipharyx is more or less closely related to true mouthparts, because it bounds the opening from the front and contributes to feeding.
There is another unpaired piece that arises from the oral cavity, called hypopharynx or prepharynx. It is more or less developed and usually is confined in the lumen of mouth, between the external gnathites. It divides the oral cavity in two parts: the cranial one is the wider and is called cibarium, the ventral one is smaller and is called salivarium. The cibarium represents the beginning of the alimentary canal and continues in the pharynx, while the salivarium is the end of the efferent ducts of salivary glands.
To understand the structural homologies between the mouthparts of Diptera and the primitive chewing mouthparts, a basic description of typical pieces of the chewing type is needed:
- Mandibles. The mandibles are generally paired and symmetrica and are formed by one sclerite with a pyramidal shape, squat in phytophagous insects, slender and sharp in the predators. Each mandible connects to peristome in its antero-lateral part (pleurostome) by flexible articulation which vary in structure and number according the systematic groups. The primary function of mandibles is grinding solid food, but they may take part also in food collecting or begin raptorial or defensive organs.
- Maxillae. The maxillae form the second pair of mouth pieces and they connects to posterior-lateral part of the peristome (hypostome). Their shape can vary greatly according to systematic groups, but the basic structure is composed by two sclerites: the proximal one, called cardo, is provided of a condile inserted into a peristomial acetabulum, the distal one, called stipes, forms the main body of maxilla. The stipes bears three appendages: on to lateral prominence, called palpifer, there is a 1-more segmented appendage, the maxillar palp, that has a sensory function. At the distal of each maxilla there are two lobes (endites); the medial is called lacinia, the lateral galea. The maxillae contributes to the collecting and assist the mandibles in the mastication.
- Labium. The labium is the posterior appendage, unpaired and median with bilateral symmetry referring to the median sagittal plane. Authors believe it derives form the fusion of a second pair of maxillae( Snodgrass, 1935; Servadei et al., 1972; McAlpine, 1981). Also this appendage may change deeply according the systematic groups, but is basically composed of two sclerites: the proximal one, called postlabium (or postmentum if is not divided), is the basis connected by a fixed articulation to hypostomal margin of head; the distal one is called prelabium or prementum and could derive from the fusion of stipes of the posterior maxillae. At the sides of prementum there are two paired and symmetrical appendages, called labial palpi, composed by 1 or more segments. At the tip of the prementum there are two symmetrical pairs of lobes: the lobes of medial pair are called glossae, the lateral ones paraglossae.
Mouthparts of Diptera
an: antenna; cl: clypeus; ip: hypopharynx; li: labium; ls: labrum (epipharynx); md: mandibles; ms: maxillae; oc: eye; pd: pedicel; plp: palpus.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
A part from heterogeneity of mouthparts of Diptera, the basic differences from the chewing type are the following:
- loss of primitive functions in collecting and crushing solid food;
- adaptation of the pharynx and muscular system to improve the sucking function by a structure called cibarial pump, placed before the pharyngeal pump;
- structural reduction of mandibles and maxillae to complete atrophy;
- structural and morphological modification of the labium, by the loss or the strong reduction of some sclerites, except to prementum and palpi;
- anatomical and morphological adaptation of the palpi to licking function or some gnathites to piercing function;
- structural and functional involvement of clypeolabral region in the mouthparts;
- development of the hypopharynx.
In most primitive groups, that belong to lower Diptera (Nematocera and Orthorrhapha), the mouthparts are composed of three median and unpaired appendages and two pairs of symmetrical appendages. The first ones, from cranial to ventral, are represented by the epipharynx, the hypopharynx and the labium; the paired appendages are the mandibles and the maxillae. In several groups of lower Diptera, the mandibles and part of maxillae are strongly reduced, vestigial or loss.
The shape of epipharynx, mandibles, maxillae, and hypopharynx is usually narrow and less or more elongated. In piercing mouthparts they are called also stylets. The labium is more developed and concave in the dorsal side, so it can allow the stylets. Due its form, the labium is usually called proboscis.
Labrum and epipharynx
The labrum is a region derived from preoral somites, but in Diptera it takes part of mouthparts. From frontal view it appears as a sclerite more or less elongated. In lower Diptera it connects to clypeus by the clypeolabral suture, in higher Diptera by a membrane more or less wide, called clypeolabral membrane. The internal side of labrum is called epipharynx, term used to indicate the first unpaired appendage of mouthparts. The lateral edges of epipharynx are revolute and extend laterally, so they form a concave surface that close part of the food canal at the dorsal and lateral sides.
Shape and sclerotization of the labrum vary according to several groups. In Culicidae, the bending of lateral edges of epipharynx is complete so that the epipharynx close entirely the lumen of the food canal; in most of Diptera, instead, the food canal is closed by the contraposition of the epipharynx with the mandibles or the hypopharynx. In lower Diptera with piercing mouthparts, the epipharynx is stylet-shaped and more or less sclerotized, while in Diptera with no piercing mouthparts is usually membranous. A singular structure occurs in the Dolichopodidae: the distal part of epipharynx extends laterally with short and cutting plaques, called epipharyngeal blades or epipharyngeal armatures, which represent the piercing organs in this family.
an: antenna; cl: clypeus; ip: hypopharynx; li: labium; ls: labrum (epipharynx); md: mandibles; ms: maxillae; oc: eye; pm: maxillary palpus.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
In lower Diptera, at the sides of the basis of the epipharynx, often there are two symmetrical sclerites (tormae) that connect to lateral egdes of the clypeus, near th clypeolabral suture. The development of these sclerites would be related to piercing function of mouthparts of lower Diptera, because they are present in several bloodsucking or predaceous nematocerous and orthorrhaphous, while they are absent among the higher Diptera (McAlpine, 1981).
The involvement of the epipharynx in taking food, in most Diptera, is limited to formation of the food canal. In bloodsucking or predaceous Diptera, usually, the epipharynx does not take part to piercing function, except the Culicidae, where this appendage is well elongated and is inserted into the bite with the other stylets. In Dolichopodidae, finally, the epipharyngeal blades are used to lacerate the cuticle of the prey, so in this family the epipharynx is the piercing organ.
Mandibles
The mandibles are paired and symmetrical appendages stylet-shaped, present only among lower Diptera. In the Nematocerca, they occurs sometimes in part of Culicomorpha and in Blephariceridae, Tanyderidae, and Psychodidae families. In Orthorrhapha they occurs only in few families of Tabanoidea. In other groups, the mandibles are vestigial or loss, like in all Muscomorpha. The presence of the mandibles is functionally significant only in bloodsucking or predaceous females, where they become pierging organs. In Culicidae, the mandibles are long and slender and have the medial margin finely serrated; instead, in bloodsucking and insectivorous females of other groups, the mandibles appears as short blades. In males of these species, the mandibles may be present but are reduced or otherwise they are not functional. In Tabanoidea, when present, the mandibles close the ventral part of the food canal, by approaching to the epipharyx.
Maxillae
The maxillae are usually present, but with a structure deeply differentiated among the various groups, according to the development of maxillary stylets. Structurally, they are composed of a basal part, little evident, formed by the cardo and the stipes; this late bears the maxillary palp and sometimes the distal stylet.
an: antenna; cl: clypeus; ip: hypopharynx; li: labium; ls: labrum (epipharynx); m: mystax; ms: maxillae; oc: eye; pm: maxillary palpus.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
The maxillary palpi are sensory organs present in most Diptera and appear as appendages more or less evident which arise from the basis of the proboscis and porrect. In most Nematocera the palpi are composed of five segments, two in most Orthorrhapha, and a unique segment in most Cyclorrhapha. The shape and size may be useful keys to taxonomic determination and, in some groups, are elements of sexual dimorphism.
The maxillary stylets, when present, are articulated at the distal of stipes. In the past, some Authors believe that maxillary stylets derive from the differentiation of the lateral lobes (galeae), but in more recent works Authors assign the origin to the laciniae (Hennig, 1973, McAlpine, 1981, Merz & Haenni, 2000). The presence, shape, and functionality of laciniae are similar to the mandibles: they lost in higher Diptera, while in lower Diptera are developed and functional in bloodsucking or insectivory forms. Females of Culicidae have long maxillary stylets, shaped as serrated blade in the distal, while in other groups they appear as short blades.
Hypopharynx
The hypopharynx has a particular importance in Diptera due to following reasons:
- in all Muscomorpha and in most lower Diptera with vestigial maxillae and mandibles, the hypopharynx close ventrally the lumen of the food canal, by opposing to the epipharynx;
- the saliva is excreted through the salivary canal, which passes within the hypopharynx.
This last character is essential to the functionality of both the biting and no biting mouthparts: food sucking is generally preceded by the release of saliva, that performs several functions:
- in bloodsucking Diptera, the saliva contains anticoagulants and other substances that aim to reduce the time of suction or delay the reaction of the host: for example, rubefacient substances, which causes the dilation of capillaries and speed up the blood flow, and anesthetic substances;
- saliva of predators has hydrolytic enzymes, needed to dissolve and make more flowing the hemolymph, and neurotoxic substances which paralize the prey during the feeding;
- saliva of dipterans with licking-sucking mouthparts facilitates the dissolution of nutrients, condition required by the functionality of labella. For example, the glyciphagous muscoids are able to take the crystallized sugar from the honeydew by capillarity through the pseudotracheae after they are dissolved with the saliva.
an: antenna; cl: clypeus; ip: hypopharynx; lbl: labella; li: labium; ls: labrum (epipharynx); oc: eye; plp: maxillary palpi; prm: prementum.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
Usually, the hypopharynx is foil-shaped, more or less elongated and poorly sclerotized. It is placed between the epipharynx and the dorsal groove of the proboscis. In Culicidae it is long and slender like other stylets and takes part to the penetration in the bite, while in other groups is usually short. The consistency of hypopharynx has a great importance in the Asilidae: in this family it represents also the pierging organ, so it is sharp and strongly sclerotized.
Labium
The labium or proboscis is the appendage most evident due the conformation and the size. Compared with the labium of chewing mouthparts, the proboscis of Diptera is characterized by the postmentum reduced, modified articulation between postmentum and prementum, palpi strongly modified, and distal lobes (glossae and paraglossae) lost. Sclerotized areas are reduced to plaques separated by extended fleshy or membranous areas. Therefore, labium of Diptera appears as a fleshy and flexible appendage than a segmented sclerite.
In front at the chewing mouthparts, the labium of Diptera has a reduced postmentum, the articulation of the prementum modified, palpi modified, and finally the glossae and paraglossae are lost. The sclerotized areas are reduced to plates separed from membranae, that make the labium as a fleshy appendage more than a segmented sclerite.
From a morphological point of view, the proboscis is divided into three parts:
- basiproboscis or rostrum: it is the proximal portion, shaped as a truncate cone, often retractile;
- medioproboscis, called from some Authors hautellum or theca (McAlpine, 1981, Tremblay, 1991): it is the middle portion, forming a groove in the dorsal side and a sclerotized area in the ventral, identified as the prementum;
- distiproboscis: this is a bilobed expansion of the proboscis, derived from the modification of labial palpi. The two lobes, generally fleshy and elastic, are called labella (singular of labellum).
The whole proboscis appears as a flexible and fleshy organ, with a more or less deep groove in the dorsal side. In Culicidae, the labium is elongated and serves as case the stylets are accomodated when they are not used. In other groups, the proboscis is not a true theca, but allows the other appendages in its groove. So, from lateral view all appendages are poorly visible, except to maxillary palpi, because hidden by the fleshy expansion of the labium.
In Diptera with no biting sucking mouthparts, the labella are wide expansions fleshy and elastic, variously shaped, often forming an angle with the axis of prementum. In most groups, the labella form a squat distal expansion, roughly isodiametric, while in certain groups they may be very elongated. Labella derive from a strong modification of bisegmented palpi, condition assumed as plesiomorphic of entire order, but this originary structure is visible only in few primitive families of Nematocera (McAlpine, 1981). The most important character of labella is the anatomical structure of their surface. This is composed of a system of microtubules present in most Brachycera but rarely in Nematocera. These microtubules have a complex structure, characterized by a wall composed of incomplete sclerotized rings, quite similar to sclerotization of tracheae in the respiratory system. For this reason, the tubules of labella are called pseudotracheae, despite having no relations with the respiratory system. The pseudotracheae arise from a median cavity, the prestoma, where the food canal and salivary canal end. From prestoma, the pseudotracheae radiate to medial side of labella and open in their surface. This tubular system has a dual function:
an: antenna; ip: hypopharynx; li: labium; ls: labrum (epipharynx); oc: eye; plp: maxillary palpus.
Author: Giancarlo Dessì
(License: Creative Commons BY-NC-SA)
- the pseudotracheae collect the salivary secret from the hypopharynx and distribute it on the surface of the labella so that dissolve the food;
- the liquid food is capillary absorbed by the pseudotracheae and transferred to the food canal.
The number of pseudotracheae and the structure of the sclerotization are treated by the cladistic analysis to define the relationships in certain groups of Brachycera (Sinclair & Cumming, 2006).
In several muscoid flies, the prestoma bears two series of small sclerotized teeth, called prestomal teeth. This structure is used to scrape particles from solid surfaces so that may be absorbed by pseudotracheae. That allows to take in semifluid food containing solid particles.
The structure and morphology of labella described above, have differences more or less marked in some groups. In Nematocera with no insectivorous or hematophagous diet, the labella are generally fleshy and broad, but have not pseudotracheae. Relations between the diet and the absence of pseudotracheae are poorly considered in literature, in contrast to higher Diptera, widely studied in this area. However, should be observed that the most common diet of "vegetarian" nematocerous is based on nectarivory (Labandeira, 2005). In Culicidae, the labium is elongated and terminate with two small labella; the entire appendage is flexible and poorly sclerotized and does not take part to piercing. During the biting, the proboscis is ventrally flexed and the labella are used to guide the penetration of stylets into the bite. In other lower Ddiptera with piercing mouthparts the labella may be more or less expanded and do not take part in the biting.
The bloodsucking muscoids show the closest homologies with the sucking mouthparts of higher Diptera. The piercing function, in these flies, is performed by the labium, that has obvious adaptation: it is slender and elongated, strongly sclerotized and with vestigial labella placed at the sides; in contrast, the prestomal teeth are well developed and provide to piercing function.
Bibliography
- Cerretti, P. (2010) Terminologia morfologica: 8-11. In I tachinidi della fauna italiana (Diptera Tachinidae), con chiave interattiva dei generi ovest-paleartici. Vol. II. Atlante iconografico, Work cited.
- Hennig, W. (1973) Imagines: 141-236. In Diptera (Zweiflüger), Work cited.
- Labandeira, C.C. (2005) Fossil History and Evolutionary Ecology of Diptera and Their Associations with Plants: 217-273. In Yeates, D.K. & Wiegmann, B.M. (eds.) The Evolutionary Biology of Flies, Work cited.
- Matile, L. (1993) Morphologie des Diptères: 54-96. In Diptères d'Europe Occidentale. Tome I, Work cited.
- McAlpine, J.F. (1981) Morphology and terminology - Adults: 9-63. In McAlpine, J.F.; Peterson, B.V.; Shewell, G.E.; Teskey, H.J.; Vockeroth, J.R. & Wood, D.M. (eds.) Manual of Nearctic Diptera. Volume 1, Work cited.
- McAlpine, J.F. (1989) Phylogeny and classification of the Muscomorpha: 1397-1518. In Borkent, A.; McAlpine, J.F.; Wood, D.M. & Woodley, N.E. (eds.) Manual of Nearctic Diptera. Volume 3, Work cited.
- Merz, B. & Haenni, J.P. (2000) 1.1. Morphology and terminology of adult Diptera (other than terminalia): 21-51. In Papp, L. & Darvas, B. (eds.) Contributions to a Manual of Palaearctic Diptera. Volume 1. General and Applied Dipterology, Work cited.
- de Oliveira, L.A. & Serra, A.L. (2008) Anatomia comparada do aparelho bucal de espécies pertencentes à Ordem Díptera (Arthropoda, Insecta), com ênfase na morfologia funcional, Work cited.
- Servadei, A.; Zangheri, S. & Masutti, L. (1972) Entomologia generale ed applicata, Work cited.
- Sinclair, B.J. & Cumming, J.M. (2006) The morphology, higher-level phylogeny and classification of the Empidoidea (Diptera), Work cited.
- Snodgrass, R.E. (1935) Principles of insect morphology, Work cited.
- Tremblay, E. (1991) Ordine Diptera (Ditteri): 11-20. In Entomologia applicata. Volume III Parte I, Work cited.
- Tremblay, E. (1985) Morfologia: 14-24. In Entomologia applicata. Volume Primo: Generalità e mezzi di controllo, Work cited.
Web resources
- Yeates, D.K.; Hastings, A.; Hamilton, J.; Colless, D.H.; Lambkin, C.L.; Bickel, D.J.; McAlpine, D.K.; Schneider, M.A.; Daniels, G. & Cranston, P.S. Anatomical Atlas of Flies. In CSIRO Entomology. CSIRO, Commonwealth Scientific and Industrial Research Organisation. Last access: 28 May 2019.
Creative Commons BY-NC-SA 3.0 Unported License
(BY: Attribution - NC: Noncommercial - SA: Share Alike).
