This chapter is concerned primarily with responses to such stimuli as light, sound, chemicals and touch. Other aspects of behaviour are discussed in the appropriate chapter: locomotion in Chapter 2, feeding behaviour in Chapter 10, reproductive behaviour in Chapter 17, defensive behaviour including meeting behaviour in Chapter 19 and rhythms of activity and social behaviour in Chapter 21.

Reactions to light

Plateau (1886) showed that Lithobius forficatus, Necrophloeophagus longicornis, Cryptops hortensis and Cryptops punctatus were negatively phototactic (taxes are directed responses dependent on discrimination of the direction of the stimulus). Chilopods in general appear to be negatively phototactic although Demange (1956) noted that in captivity Lithobius piceus gracilitarsus Bröl. does not appear to seek darkness: if the light is not too bright it will leave its hiding place and behaves normally. It hunts in the middle of the day and reproduces in the light. Demange maintained that it was forced underground in order to seek the required humidity.

Klein (1934) showed that Lithobius forficatus ran towards a black screen at the side of an arena (skototaxis). Unilateral blinding did not affect the result. When illuminated from one side it showed a negative phototaxis which overruled the skototaxis. Görner (1959) demonstrated that Lithobius forficatus, Scutigera coleoptrata and Scolopendra cingulata exhibit a skototactic response. Neither Scutigera nor Scolopendra modify their runs when illuminated from the side but L. forficatus reacts to lateral artificial light by a negative phototaxis.

Centipedes (members of the arthropodan class Chilopoda) are common and relatively familiar animals which are found in soil and litter or under stones or bark. They are soft-bodied and dorsoventrally flattened having from 15 to 181 pairs of legs, one pair to each trunk segment. Species from temperate regions are usually of moderate size, varying from 1 to 10 cm in length and of drab brownish or yellowish coloration. Many tropical species of the order Scolopendromorpha are large, one reaches a length of 26 cm, and are brightly coloured: red, black and orange, green or violet.

Like other arthropods, the centipedes are bilaterally symmetrical, metamerically segmented animals with a double ventral nerve cord, typically with a ganglion in each segment and concentrations of nervous tissue above and below the gut at the anterior end of the body. A circulatory system is present carrying blood forwards in a dorsal vessel and backwards in a ventral vessel. The body is covered by a non-living layer, the cuticle, which is secreted by the epidermis. The cuticle is in the form of relatively rigid sclerites separated by flexible arthrodial membranes; it is shed periodically to allow growth, a phenomenon known as moulting or ecdysis. The anterior part of the body is differentiated to form a head which bears a pair of antennae, a pair of jaws (mandibles) and two pairs of jointed legs modified to form mouthparts (the first and second maxillae).

Epidermis and gland cells

In centipedes, epidermal glands occur both singly and in groups. The head glands are dealt with in Chapter 15, the poison glands in Chapter 9. The remaining epidermal glands are dealt with in this chapter.

Geophilomorpha

There are no detailed accounts of the epidermis and single epidermal glands in geophilomorphs. Blower (1951) showed that there is a continuous layer of gland cells in Haplophilus subterraneus interspersed with small epidermal cells set in a very thick basement membrane (Fig. 48).

In many geophilomorphs the metasternites often bear pores, either singly or in groups (Fig. 19). These are the openings of unicellular glands that frequently produce luminous secretions (see below).

The inflated coxae of the terminal legs frequently bear pores, the openings of the coxal glands (Fig. 14). An electron microscope study of the coxal glands of Clinopodes linearis, Necrophloeophagus longicornis and Haplophilus subterraneus shows that the canal leading inwards from each pore is slightly dilated at its base like a drum stick and the intima is here somewhat thicker and of different texture from the cuticle of the body surface. Epidermal cells are radially arranged around the proximal dilation: they represent a typical transport epithelium. The nuclei as well as the poorly developed Golgi zones are located in the basal third of the cells.

Deep infoldings of the cell apex extend as far as the nuclear region.

Protocerebral neurosecretory cells and cerebral gland

Holmgren (1916) described the cerebral gland of centipedes calling it the frontal organ. Fahlander (1938) realised that it was endocrine in nature and proposed for it the name cerebral gland. Gabe (1952) showed that axons from a group of lateral neurosecretory cells on each side of the protocerebrum carried secretory material to the cerebral glands. This was confirmed by Palm (1955).

In Lithobius forficatus the cerebral gland appears to be a hollow sac which is bathed by a stream of haemolymph and innervated by a nerve from the optic stalk, also receiving a pair of nerves originating from lateral neurosecretory cells in the protocerebrum (Palm, 1955) (Fig. 105a). The lateral neurosecretory cells are of two types, large and small, the former being far more numerous than the latter. In addition to these lateral cells there is a group of small neurosecretory cells in the posterior median region of the protocerebrum which corresponds to the pars intercerebralis of insects (Scheffel, 1961) (Fig. 105a). The nerve from the optic nerve to the cerebral gland in L. forficatus runs from the optic lobe to the gland in Lithobius calcaratus C. L. Koch. The nerve is absent in geophilomorphs and scolopendromorphs (Joly & Descamps, 1970). The large lateral neurosecretory cells (Type 1) are phloxinophil after Gomori staining, the smaller cells (Type 2) stain with haematoxylin.

Insects, which have a very well-developed tracheal system, have a much reduced blood system but in the Chilopoda both systems are well developed (Fahlander, 1938). The dorsal tubular heart is connected by one or more pairs of commissures to a ventral supraneural vessel. The blood flows forward in the heart which is continued anteriorly as the anterior aorta. This vessel, the commissures, supraneural vessel and latero-dorsal arteries of the heart supply the organs with blood through open ended arteries. There is little evidence of a venous system. Blood returns to the heart through paired ostia which are typically arranged one pair to each segment.

The heart

In Scolopendra cingulata the heart is suspended from two connective tissue sheets which enclose the dorsal sinus (Fig. 138a). It is attached laterally on each side to a double sheet of connective tissue which encloses the lateral sinus containing the pericardial cells. The lateral sheets join and continue outwards as a single layer. Fan-shaped alary muscles which attach to the heart spread through these lateral sheets (Fig. 138b). The dorsal sinus communicates widely with the perivisceral coelom through large openings between successive alary muscles (Jangi, 1966). Herbst (1891), Duboscq (1898) and Fahlander (1938) regarded the cavity of the dorsal sinus and the lateral sinuses as representing the pericardium: Heymons (1901) considered that the pericardium consisted of two very large cavities enclosing the dorsal longitudinal muscles.

Malpighian tubules

In centipedes the Malpighian tubules are a pair of long, forwardly running, blind tubules which originate at the junction of the mid- and hind-gut (Figs. 110, 111).

Lithobiomorpha

The Malpighian tubules of Lithobius forficatus have been described by Plateau (1878), Palm (1953) and Rilling (1968). The tubules open into the gut by way of a distinct urinary bladder or ampulla, the inner portion of which is a narrow tube piercing the intestinal wall (Fig. 151a). Palm failed to identify distinct sphincter muscles but thought it probable that the muscular coat of the intestine which surrounds the inner portion of the ampulla functions as a sphincter. Rilling (1968) stated that the ampullae show a typical mid-gut musculature but annexe the circular muscles of the hind-gut. In some specimens the tubules terminate in a small thin-walled transparent vesicle, Palm was unable to determine whether this was caused by physiological conditions or whether it was a morphological variation.

The epithelium of the ampulla has a strong basement membrane along which run very thin longitudinal muscle fibres; a few circular and oblique fibrils are also present. In many places connective tissue cells occur around the ampullae, either situated directly on the basement membrane or connected with it by fine cytoplasmic processes. The ampulla cells are tall and narrow with basal nuclei. The apical parts of the cells contain indistinct granules and more or less prominent vacuoles. There is no cell cuticle or brush border.

The alimentary canal of centipedes is a straight tube which is clearly divided into fore-gut, mid-gut and hind-gut. The fore-gut originates as an ectodermal invagination, the stomodaeum, and hence is lined by cuticle. It comprises the pharynx and oesophagus, the latter sometimes differentiated into crop and gizzard or proventriculus. The mid-gut is of mesodermal origin (mesenteron) and the hind-gut is formed from a posterior ectodermal invagination, the proctodaeum. A pair of Malpighian tubules originate at the junction of the mid- and hind-gut and run forwards towards the head (Figs. 110, 111). They are described in Chapter 16. The so-called ‘salivary glands’ are described in Chapter 15.

The pre-oral cavity is bounded anteriorly by the labrum, anterodorsally by the membranous epipharyngeal surface, laterally by the mandibles and ventrally by the anterior portion of the hypopharynx, a delicate lobed structure which usually bears dense fields of hairs and the pores of unicellular glands. The mouth opens into the pharynx.

Geophilomorpha

The epipharynx is very poorly developed in geophilomorphs and the hypopharynx is reduced to a small bilobed structure covered with fine hairs. The pharynx is very short, its wall showing lateral longitudinal thickenings to which are attached the pharyngeal dilator muscles (Fig. 112) (Verhoeff, 1902–25).

The alimentary canal posterior to the pharynx has been described for Haplophilus subterraneus gervaisi (Plateau) and Necrophloeophagus longicornis (Fig. 110a) by Plateau (1878). The oesophagus is long and narrow, its folded cuticular lining lacking spines.

Newport (1844) was the first worker to recognise that the forcipules of centipedes, which he termed the mandibles, contained a poison gland. Despite this, many nineteenth-century workers confused the poison glands with other head glands (Duboscq, 1898): their true nature was recognised by MacLeod (1878). He examined Scutigera coleoptrata, Lithobius forficatus, Cryptops savignyi and various Scolopendra species and geophilomorphs noting the gland duct and pore. He demonstrated that whereas a bite from the poison claws of L. forficatus produces almost instantaneous death in flies, extracts of the ‘salivary glands’, when injected, did not.

Structure of the gland and discharge of poison in Scolopendra

The structure of the poison glands has been described for Scolopendra subspinipes by MacLeod (1878), for S. cingulata by Duboscq (1898), for S. morsitans by Pawlowsky (1913) and Dass & Jangi (1978), and for S. viridicornis by Barth (1967). Cornwall (1916) described the poison gland in Ethmostigmus platycephalus spinosus and Bücherl (1946) described the gland of a number of scolopendrids.

The gland is situated in the distal part of the trochantero-prefemur and extends into the poison claw on which its duct opens subterminally. It is innervated by a nerve from the suboesophageal ganglion and is well supplied with tracheae. In S. cingulata it is bluish white in colour. Transverse sections show a central duct surrounded for three-quarters of its circumference by elongated gland cells which open into the duct by pores (Fig. 121a).

The literature on the parasites of centipedes was reviewed by Cloudsley-Thompson (1949) and additional data were provided by Remy (1950).

Ectoparasites

Acari

Like other arthropods, centipedes are frequently found to have mites attached to them but these have received little attention. The six-legged larvae of trombidiids occasionally attach themselves to the legs of centipedes. It seems that they feed on the host as their soft-skinned abdomens increase in size the longer they remain attached. Gamasid mites, which are normally free-living humus-dwellers, are sometimes specific parasites of myriapods: none are found on centipedes in South Africa although Antennophorus and related genera occur on tropical Scolopendras and ants in other parts of the world (Lawrence, 1953).

The resting stage (deutonymph or hypopus) of several species of Tyroglyphidae is found on the appendages of almost all orders of ground-living arthropods. They are minute and do not harm their hosts as they have no mouth parts for feeding; they attach themselves by means of suckers at the posterior end of the body (Fig. 208). Although they are not, strictly speaking, parasites it is convenient to deal with them here.

Lewis (1960) reported that the littoral geophilomorph Strigamia maritima frequently carried hypopi of the tyroglyphid Histiostoma sp. Specimens normally carried up to ten hypopi, the largest number on one specimen was 43, but the number often becomes much greater in laboratory cultures. Adolescens I Strigamia are far less heavily infested than other stages, possibly because they offer less suitable attachment sites due to their small size.

A number of topics of an ecological nature namely behaviour, food and feeding, respiration, the reproductive system and reproductive behaviour, life-histories, predators, and defence mechanisms and parasites have been the subject of previous chapters.

Many of the remaining ecological data are fragmentary and widely scattered and any account must needs reflect the interests of the particular author and his reading and cannot be comprehensive.

Water relations of terrestrial centipedes

Water loss experiments

A number of investigators have shown that centipedes lose water rapidly at low humidities. Auerbach (1951) investigated the ‘desiccation death time’ of various centipedes from Michigan, USA (Table 17): Roberts (1956) and Vaitilingham (1960) measured ‘survival times’ of British woodland centipedes at six different humidities; their results for 55 per cent relative humidity are shown in Table 18. Lewis' (1963) results, for six British species are shown in Table 19. Palmen & Rantala (1954) found the geophilomorph Pachymerium ferrugineum in Sweden to survive for between 38 and 109 hours at 34 per cent relative humidity at 20 °C.

It is clear from these results that, by and large, geophilomorphs are more resistant to desiccation than lithobiomorphs or scolopendromorphs. Unfortunately there are no data for scutigeromorphs.

There has been considerable confusion over the nature of the glandular structures of the anterior region of centipedes: Duboscq (1898) pointed out that no two description of the anterior glands of Scolopendra were in accord and from one to three pairs of salivary or venomous glands had been figured or described for the genus. The most detailed accounts of centipede head glands are those of Herbst (1891) and Fahlander (1938). Both single and multicellular glands occur, some of the latter forming a metamerically arranged series.

Scutigeromorpha

The Scutigeromorpha have the largest number of head glands. Fahlander (1938) investigated Scutigera coleoptrata, Thereuopoda clunifera and Thereuonema tuberculata, describing from these species seven pairs of multicellular anterior glands. He distinguished two pairs of buccal glands filling the greater part of the head antero-dorsal to the mouth, the medial pair opening into the anterior region of the pharynx, the lateral pair by short ducts into the oral cavity (Fig. 147a). The mandibular or hypopharyngeal glands lie largely in the hypopharynx, their ducts opening on the hind wall of the buccal cavity. In contrast to other head glands, the lobes of these glands are long and narrow and radiate in all directions.

The first maxillary glands open immediately anterior to the basal part of the first maxillae. The secretory part of the glands lies ventral to the nerve cord and stretches from the region of the first maxillae to the second leg-bearing segment (Fig. 147a).

The embryonic development of centipedes will not be described here: it has been reviewed by Johannsen & Butt (1941). The most important work is that of Heymons (1901) on the embryology of Scolopendra spp. Verhoeff (1902–25) quoted at length from Heymons and added further data. Dohle (1970) and Knoll (1974) described the embryological development of Scutigera coleoptrata.

The Chilopoda exhibit two distinct patterns of post-embryonic development. In the epimorphic orders Geophilomorpha and Scolopendromorpha, the young hatch with a full, or almost full, complement of legs and the eggs and early post-embryonic stadia are brooded by the female. In the anamorphic orders Lithobiomorpha and Scutigeromorpha, the eggs are laid singly and are not brooded by the female. The young hatch with less than the adult number of legs and the number gradually increases during the early moults. Data for the Craterostigmus are currently very fragmentary.

Geophilomorpha

Larval stadia and brooding

Latzel (1880) gave brief notes on the larval stages of a large number of geophilomorphs. More detailed accounts have been given for Geophilus proximus and Pachymerium ferrugineum by Sograff (1883), for Dicellophilus carniolensis (C. L. Koch) together with notes on some other species by Verhoff (1902–25), for the American species Geophilus rubens by Johnson (1952), for Strigamia maritima by Lewis (1960) and for Necrophloeophagus longicornis and Clinopodes linearis by Weil (1958).

The process of hatching in geophilomorphs is a gradual process, the egg splitting into two halves to reveal the ‘last embryonic phase’.

The integument

The integument is the outer covering of arthropods and consists of a single layer of epidermal cells (often called the hypodermis) which rests on a basement membrane and secretes the cuticle. The cuticle covers the outer surface of the animal and lines the invaginations that arise from it such as the fore- and hind-guts, the tracheae, the lower parts of the genital ducts and the ducts of the epidermal glands.

The centipede cuticle appears to consist of three main layers: an outer, thin, refractile membrane usually about 1 μm in thickness called the epicuticle; a rigid, usually amber-coloured exocuticle and an inner thick elastic layer, the endocuticle, which is colourless and lamellated. The varying terminologies that have been used for these layers by different authors are shown in Table 1. The layers below the epicuticle are sometimes termed the procuticle. The outer part of the procuticle becomes tanned and sclerotised to form the exocuticle, the remaining undifferentiated part being the endocuticle. Between the exocuticle and the endocuticle there may be a region of hardened but not fully darkened cuticle which is fuchsinophil and lamellate like the endocuticle. This layer is termed the mesocuticle. The exocuticle and endocuticle show a variety of staining reactions and Blower (1951) regarded the optical appearance of the two layers as the only criterion which constantly differentiated them.

The nervous system

The arthropod nervous system may be conveniently considered under three headings:

1. (a) the central nervous sytem, consisting of a dorsal brain connected by circum-oesophageal connectives to a double ventral nerve cord along which there are ganglia, one pair per segment,

2. (b) the visceral nervous system supplying the gut and

3. (c) the peripheral nervous system including all the nerves radiating from the ganglia of the central and sympathetic systems.

Data on the anatomy of the nervous system were reviewed by Verhoeff (1902–25) and Hilton (1930). Subsequently, detailed studies have been carried out on Scolopendra cingulata, Lithobius forficatus and Thereuopoda clunifera by Fahlander (1938), on Pseudolithobius megaloporus by Henry (1948), on Scolopendra morsitans by Jangi (1966) and on L. forficatus by Rilling (1968).

In the Lithobiomorpha the brain lies transversely above the stomodaeum. It consists of the cerebral ganglia each composed of a lateral and an antero-lateral lobe. The lateral lobe receives nerves from the ocelli and Tömösváry organ and from the protocerebral, or cerebral glands. These lobes represent the protocerebrum – the ganglion of the pre-antennary segment. The deutocerebrum, the ganglia of the antennary segment, is represented by the antero-lateral lobes which receive nerves from the antennae. The ganglia of the third head segment, the tritocerebrum are flattened lobes closely joined to the ventral side of the cerebral ganglia (Fig. 73).

Geophilomorpha

Food

It has long been believed that earthworms are an important item in the diet of geophilomorphs. Newport (1844) and Wood (1865) stated that earthworms form the diet of the Geophilomorpha and Brehm (1877) figured a Geophilus coiled round a large earthworm. Brade-Birks (1929) recovered setae, probably of a very young lumbricid worm, from the gut of a specimen of Haplophilus subterraneus. Auerbach (1951) was unable to substantiate that Geophilus rubens Say or Strigamia fulva Sager fed on worms: both species refused a selection of small arthropods although the Strigamia accepted a small beetle larva. Weil (1958) found a Necrophloeophagus longicornis under a stone attacking a lumbricid twice its length. He found that large earthworms struggle free from geophilomorphs with ease and do not appear to be harmed by their bite and concluded that centipedes are seldom successful in overcoming earthworms larger than themselves.

Johnson (1952) showed that in the laboratory, Geophilus rubens accepted Drosophila larvae and adults, mycetophilid larvae, snails' eggs and small enchytraeid worms but not mites, elaterid or buprestid beetle larvae or earthworms. Weil (1958) reported that N. longicornis takes very small earthworms, weakly sclerotised insect larvae, young lithobiomorphs and occasionally enchytraeids, and entomobryomorph Collembola but not Tomocerus. It occasionally attacks newly moulted insect larvae: a teneral Lacon murinus was stabbed with one poison claw and opened between the scutellum and the elytra.