<oological Journal of the Linnean Society (1986) 88: 201-216. With 3 figures

Colour, shape and defence in aphidophagous syrphid larvae (Diptera)

GRAHAM E. ROTHERAY

Royal Museum of Scotland, Chambers Street, Edinburgh E H l 1JF

Received February 1985, accepted for publication September 1985

Colour patterns, shape and behaviour are analysed in 22 species of aphidophagous syrphid larvae in relation to their possible role in defence against,visually hunting predators. Crypsis is the most important method of primary defence. There is much variation in colour pattern. Some species are translucent, others green, brown or otherwise coloured. Most have disruptive stripes, bars or other markings that break up the body outline at short range. There is one example of a bird dropping resemblance. Behavioural requirements for effective crypsis include diurnal immobility, resting in sites that provide maximum concealment, and slow interrupted locomotion. Secondary defences are less variable and involve catalepsis, attack with saliva, and rolling and dropping from the plant.

KEY WORDS:-Syrphid larva - colour pattern - crypsis - shape - defence.

CONTENTS

Introduction . . . . . . . . . . . . . . . . . . . 201 Larval descriptions . . . . . . . . . . . . . . . . . 202 Discussion of colour patterns . . . . . . . . . . . . . . . 207 Behavioural requirements for crypsis . . . . . . . . . . . . . 2 10 Secondary defence . . . . . . . . . . . . . . . . . . 2 12 Final discussion . . . . . . . . . . . . . . . . . . 2 13 Acknowledgements . . . . . . . . . . . . . . . . . 215 References. . . . . . . . . . . . . . . . . . . . 2 15

INTRODUCTION

That animals use colour, shape and behaviour to avoid visually hunting predators has long been recognized (Poulton, 1890; Cott, 1940; Ruiter, 1952; Robinson, 1969; Edmunds, 1974). Robinson (1969) divided such defences into two categories: primary defences which function regardless of whether the predator has been perceived by the prey and secondary defences which are initiated by an encounter with a predator. Typical primary defences include crypsis or camouflaging coloration; protective resemblance or masquerade (Endler, 1978), e.g. a similarity to sticks, leaves, thorns or faeces; and aposematism or warning coloration.

Facilitating primary defences are various behavioural traits such as spacing out to avoid search image formation, selection of appropriate backgrounds on which to rest, diurnal inactivity, adopting resting postures that provide

20 1 00244082/110201+ 16 SOS.OOj0 0 1986 The Linnean Society of London

202 G. E. ROTHERAY

maximum concealment and dash-then-freeze or uniformly slow locomotion (Tinbergen, 1965; Robinson, 1969).

In comparison with other insects on plants, syrphid larvae might be especially vulnerable to predation. Most occur on a wide range of plants which may complicate background selection. At any one aphid colony there are usually several species occurring contemporaneously (Bombosch, 1963; DuSek & Lbska, 1959; Rotheray, 1979), so that for predators of syrphid larvae, high densities of potential prey are readily available at aphid colonies. Furthermore, they are soft, slow moving and because they lack eyes, cannot see an approaching predator.

The majority of Diptera larvae are uniformly coloured (see Peterson, 1960). Even other Diptera larvae that live on plant surfaces tend to be uniform in colour, e.g. Cylindrotominae (Tipu1idae)-green, Chamaemyiidae-grey, and Aphidomysa (Cecidomyiidae)-red. However, the larvae of aphidophagous Syrphidae are unique amongst Diptera in being patterned.

LARVAL DESCRIPTIONS

Existing morphological descriptions of syrphid larvae (Duiek & Lbska, 1959; Dixon, 1960; Goeldlin de Tiefenau, 1974) do not give details of the colour patterns precise enough to enable analysis. A similar problem was found by Herrebout, Kuyten & Ruiter (1963) in their studies of colour patterns in pine tree caterpillars. Their re-descriptions emphasize the general appearance of caterpillars to human observers with an analysis of individual colour pattern elements. A similar approach is adopted here.

Larvae were either collected from the field and identified using the reared adult or were obtained from eggs laid by subsequently identified gravid females. Colour patterns are usually similar in the three larval stages and only the third stage is considered here.

Baker (1970), in his study of Brassica-feeding caterpillars and their avian predators, emphasizes different long- and short-range elements in predator perception of prey. Thus, in examining the colour patterns of syrphid larvae their overall appearance was judged from about 100 cm, and short-range details from about 15 cm. Final resolution of pattern elements was made by mounting a larva on a glass slide in a drop or two of water and coverslip for examination with a binocular miproscope. This technique enabled a clearer view into the interior of the larva.

Pattern elements result from: (1 ) Coloured material in the haemolymph; (2) Coloured adipose ( = fat) tissues-these can be sheet-like or particulate in form; (3) Brown or black spicules on the integument; and (4) Black material in the hind-gut (Goeldlin de Tiefenau, 1974). The standardized terminology used for the various pattern elements and regions of the larva is shown in Fig. 1.

The species descriptions are presented in order of the latest checklist to deal with the British fauna (Stubbs & Falk, 1983). The figures in parentheses following species names indicate the approximate number of larvae examined.

Baccha obscuripennis Meigen (60) This species occurs on grasses and ground layer plants in sheltered and shady

sites; thin and rectangular in cross-section; integument and haemolymph

DEFENCE IN SYRPHID LARVAE

d o r s a l

< 9 >

203

v e n t r a l

Figure 1 . Diagrammatic cross-section through a syrphid larva showing the position of the elements making up the colour patterns. 1, Mid-dorsal; 2, dorsal; 3, upper lateral; 4, lower lateral; 5 , haemolymph; 6, adipose tissue surrounding gut; 7, gut; 8, integument; 9, dorsal field; 10, lateral field.

translucent; laterally, white sheet-like adipose tissue surrounds and obscures the mid- and hind-gut, dorsally these tissues appear as two broad stripes partially obscuring the hind-gut; short mid-dorsal white stripe on the thorax and head; upper and lower lateral stripes.

Overal appearance (from approximately 100 cm) : A thin, translucent larva with white and black markings.

Melanostoma scalare (Fabricius) (50) This species occurs on various herb layer plants; elongate oval and

subcylindrical; integument translucent smooth and shining; haemolymph pale green; small amount of adipose tissue partially surrounding the hind-gut.

Overall appearance: An oval shaped, shining, pale green larva.

Platycheirus manicatus (Meigen) (30) This species occurs on herb layer plants; rectangular in cross-section;

integument and haemolymph translucent; light brown adipose tissue. surrounds mid- and hind-gut dorsally and laterally; lateral field flecked with pale adipose tissue; abdomen with pairs of small, lightly formed, triangular markings in the dorsal field, these formed from aggregated particles of brown adipose tissue.

Overall appearance: A pale brown, somewhat translucent larva.

Platycheirus scutatus (Meigen) (500) This species occurs on herb layer plants; rectangular in cross-section;

integument and haemolymph translucent; green adipose tissue surrounds and obscures mid- and hind-gut; abdomen with conspicuous pairs of triangular markings in the dorsal field formed from aggregated particles of white adipose tissue; colour variants are common with particulate adipose tissue pink or purple, and sheet-like adipose tissue pink tinged and light brown; during diapause there is a tendency for the adipose tissue to become light brown.

Overall appearance: A green or dark pink larva with white markings; diapausing individuals mottled pale brown and white.

a

a

DEFENCE IN SYRPHID LARVAE 205

Dasysyrphus albostriatus (Fallen) (30), Dasysyrphus tricinctus (Fall&) ( lo), Dasyyphus venustus (Meigen) ( 15)

These species occur on trees ( D . venustus was only reared in the laboratory and not recorded from the field); tapering anteriorly and dorsoventrally flattened; lateral and posterior projections break up the body outline when viewed from above and dorsal projections do so in lateral view; integument covered with black spicules that partially obscure the grey adipose tissue and hind-gut; spicules most dense along the numerous transverse folds of the body except on narrow, downwardly inclined pairs of bars on segments 6-1 1; these bars pink or grey from underlying adipose tissue; underneath and abutting each bar is a black stripe of aggregated spicules, these stripes extending beyond the bar to fuse with an undulating lateral black stripe each side of the body.

Overall appearance: Mottled grey and black, flattened larvae with irregular outlines (Fig. 2C).

Epistrophe eligans (Harris) (80), Epistrophe grossulariae (Meigen) (50) These species occur on trees and other plants where aphids form colonies on

open leaves; elongate oval; markedly dorsoventrally flattened and smooth in outline; integument and haemolymph translucent; gut obscured by green adipose tissue; dorsal field flecked white, orange and green; mid-dorsal white stripe tapering anteriorly; in E. eligans there is a tendency for a white line of aggregated particles of adipose tissue to extend around the margin of the larva; during diapause the haemolymph becomes translucent and the adipose tissue orange-brown.

Overall appearance: Broad, flat, green larvae with white stripes; diapausing individuals pale brown (Fig. 2B).

Episyrphus balteatus (Degeer) (500) This species is found on various herbs, shrubs and trees; narrow,

subcylindrical and smooth in outline; integument and haemolymph translucent; white sheets of adipose tissue partially obscure the mid- and hind-gut; at close range red Malpighian tubules are conspicuous in the dorsal field.

Overall appearance: A narrow, translucent larva with white and black markings.

Melangyna umbellatarum (Fabricius) (80) This species occurs on hogweed, Heracleum sphondylium L. and Angelica sylvestris

L.; tapering anteriorly; dorsoventrally flattened and smooth in outline; integument and haemolymph translucent; gut surrounded by white adipose tissue, this extending almost to the lateral margins; mid-dorsal white stripe tapering anteriorly; undulating and interrupted upper and lower lateral stripes formed from aggregated particles of adipose tissue; a colour variant occurs in which the lateral and posterior margins are broadly and densely flecked rufous.

Overall appearance: A flat, white or white and rufous-edged larva.

Meligramma cincta (Fallkn) (60) This species occurs mostly on Fagus sylvatica L. but occasionally on Quercus

robur L., Tilia europaea L. and Acer pseudoplatanus L.; narrow and somewhat

206 G. E. ROTHERAY

dorsoventrally flattened; integument and haemolymph translucent; mid- and hind-gut partially obscured by triangular markings of white adipose tissue.

Overall appearance: A translucent larva with white and black markings.

Meligramma triangulzjera (Zetterstedt) (1 5) This species occurs mostly on Prunus spp., but also Rubus sp., Betula sp. (N. J.

Mills, pers. comm.) and Ribes sp. (data from specimens in the collection of Mrs A. F. G. Dixon housed at the Royal Museum of Scotland); tapering anteriorly; dorsoventrally flattened; abdomen with a broad white, triangular marking over the dorsal surface, almost reaching the lateral margins posteriorly; this marking completely obscuring the hind-gut; an interrupted white stripe on thorax and head; lateral and posterior margins dark matt brown due to dark pigments in the haemolymph.

Overall appearance: A white and brown larva, similar to a bird dropping (Fig. 2D).

Parasyrphus vittiger (Zetterstedt) (10) This species occurs mostly on conifers; narrow and subcylindrical; integument

and haemolymph translucent; mid- and hind-gut surrounded by white adipose tissue; a broad rufous mid-dorsal stripe; on either side of this is a broad white stripe, then another rufous stripe and finally a lower lateral white stripe; these stripes formed from aggregated particles of adipose tissue.

Overall appearance: A narrow, white and rufous striped larva.

Metasyrphus corollae (Fabricius) (25), Metasyrphus luniger (Meigen) (400) These species occur mostly on ground layer plants; narrow, tapering

anteriorly; subcylindrical and smooth in outline; haemolymph translucent; broad pale brown dorsal stripes, these partially obscured by overlying segmentally arranged, white, triangular-shaped mid-dorsal markings; undulating and interrupted white upper and lower stripes; lateral field densely flecked brown; abutting the dorsal edge of each upper lateral a further pale brown stripe which at the posterior margin of each segment fuses with the dorsal stripe leaving a pair of rectangular central markings on each abdominal segment, these incline outwards and are black in colour from the underlying hind gut; integument covered with brown or black spicules, these most dense on transverse folds of the body.

Ouerall appearance: Narrow, mottled mostly brown and white larvae.

Scaeva pjrasfri (Fabricius) ( 100) This species occurs mostly on ground layer plants; tapering anteriorly and

subcylindrical; integument with pale brown spicules, but these do not contribute to the overall colour pat tern; haemolymph translucent; green adipose tissue surrounding gut; dorsal and lateral fields flecked white; a mid-dorsal white or pink tinged stripe; a colour varient infrequently occurs which is pink instead of green.

Overall appearance: A subcylindrical green or pink larva with a white stripe.

Sphaerophoria menthastri (L.) (25), Sphaerophoria scripta (L.) (100) These species occur on a variety of ground layer plants; narrow and

subcylindrical; integument translucent; haemolymph bright green; broad dorsal

DEFENCE IN SYRPHID LARVAE 207

white stripes, these appearing pale green due to overlying green haemolymph; posteriorly, flecked white in the lateral field.

Overall appearance: Narrow, green larvae.

Syrphus ribesii (L.) (2000) This species is found on a great variety of herbs, shrubs and trees; tapering

anteriorly; subcylindrical and smooth in outline; integument and haemolymph translucent; mid- and hind-gut surrounded laterally by white adipose tissue; abdomen with five pairs of white, triangular-shaped markings, the anterior and posterior margins sometimes fused to form an irregular shaped stripe; a very thin interrupted stripe either side of the heart line and ending on the thorax; mid-dorsally a thin white stripe on the thorax and head; black colour of the gut obvious between markings in the dorsal field; lateral field flecked white; colour varieties occur, commonly the inner edges of the triangular markings are orange giving the impression of dorsal orange stripes; occasionally individuals occur that have all orange adipose tissue.

Ouerall appearance: A subcylindrical, translucent larva with white, orange and black markings (Fig 2A).

P@a luteitarsis Zetterstedt (50) This species is found in galls of Schizoneura spp. aphids on Ulmus glabra L.

leaves. Pipzza noctiluca (L.) (9). This species is found in leaf curls caused by Brachycaudus helichrysa

(Kaltenbach) on Prunus spp. The closely related Pipizella uaripes Meigen was reared from root-dwelling aphids by Dixon ( 1959). All these species have brown or black coloured heamolymph and no brightly coloured adipose tissue.

DISCUSSION OF COLOUR PATTERNS

The colour patterns of all species suggest that crypsis is the primary defence. Homochromy (i.e. a resemblance to the background) and disruptive or obliterative coloration (i.e. stripes, bars and other markings that obscure the body outline; Cott, 1940) were the most common categories (Table 1) . Despite the wide variety of colour patterns, four groups can be recognized: (1) translucent species; (2) those that are green; (3) brown species; and (4) species that are otherwise coloured.

Translucent species are similar in shape and pattern, being subcylindrical with white adipose tissue (orange in Syrphus ribesii colour varieties). At long range, the body outline is difficult to see because the background colour is visible through it. At short range, the eye is drawn to the strong contrast between the black colour of the gut and the overlying white adipose tissue which partially obscures it, thus making these markings disruptive. Translucent larvae tend to be camouflaged on many different backgrounds. This may be one of the factors facilitating the development of a wide prey range like those observed in Syrphus ribesii and Episyrphus balteatus (Rotheray, 1979).

Green species have either green pigments in the haemolymph or green adipose tissue. The black gut is usually completely obscured by adipose tissue,

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210 G. E. ROTHERAY

and most have disruptive stripes or triangular marks on the body. During diapause they often become pale brown and since most species overwinter in leaf litter and soil this is presumably also cryptic.

Epistrophe species are distinctive among green larvae in being dorsoventrally flattened. As Edmunds (1974) points out, rounded species have prominent lateral shadows and profiles which show up the body outline. Flattening reduces both lateral shadow and the profile which is probably important to species whose larvae spend most of their time on leaves (see Table 2).

The colour of brown species comes from black spicules on the integument, the gut, adipose tissue and haemolymph pigments. Dasysyrphus larvae rest in crevices on bark (see Table 2), where they are well concealed by their dark coloration. Concealment is enhanced at these sites by the lateral and posterior projections that blur the body outline against the bark, and also by the dorsoventral flattening which reduces the lateral profile and the dorsal projections which disrupt it. Other brown larvae, e.g. Platycheirus manicatus, tend to rest in dead leaves at the base of plants or in the leaf litter.

Pipiza and Pipizella species have poorly developed colour patterns compared with other syrphid larvae. However, they live in concealed situations, e.g. in leaf curls or on roots, where there may be little predation pressure from visually hunting predators. Their brown and black coloration probably conceals them in the soil and leaf litter in which they overwinter.

The final group of distinctively coloured species consists of various aphid- feeding specialists. The white or white and brown larva of Melangyna umbellatarum is most common amongst the white flowerheads of Heracleum sphondylium. Parasyrphus vittiger is found mostly on pine trees and rests at the base of pine needles or on terminal branches (Table 2) where, at long range, its stripes merge it into the background of pine needles. At short range, the strong contrast between the white and rufous stripes is disruptive to the eye. Meligramma triangulifera is the only example noted here of special protective resemblance or masquerade. It seems to resemble a bird dropping ( 15 out of 18 people identified it as such from photographs). Unusually for syrphid larvae, but consistent with the suggestion that it is a bird-dropping mimic (Edmunds, 1974), it occasionally rests on the upper surface of leaves (Table 2).

BEHAVIOURAL REQUIREMENTS FOR CRYPSIS

Diurnal immobility Syrphid larvae were usually motionless during daytime. To investigate this

further diurnal activity was monitored in six species. Larvae were individually placed in Petri dishes containing aphids in an outdoor insectary. After 24 h, observations were made every 2 h over a 24 h period. At the beginning of every 2 h period each larva was observed for up to 5 min and was scored as inactive if it was not feeding or moved less than one body length, otherwise it was recorded as being active. The results support the field observations that larvae are active at night (Fig. 3).

The only larvae recorded as active during daytime were those from colonies where there were few aphids. The empty fore-guts of these individuals (Syrphus ribesii, Episyrphus balteatus and Platycheirus scutatus) suggested starvation, and they

DEFENCE IN SYRPHID LARVAE 21 1

Daily cycle (hours)

Figure 3. Daily activity patterns in third-stage syrphid larvae. A, Syrphus ribesii; B, Episyrphus bafteatus; C , Platycheirus scutatus; D, Epistrophe eligans; E, Melanostoma scalare; F, Metasyrphus luniger, N = 10 for each species.

fed voraciously on being given aphids. Furthermore, in cultures, larvae starved for about 16 h were active during daytime. Thus, starved larvae will apparently 'risk' daytime activity.

Daytime resting sites T o record resting sites, aphid-infested plants were hand searched and a note

taken of the position of each motionless larva. Results are presented for the seven most frequently searched plant species (Table 2) .

The most frequent resting sites were leaf folds and curls. Larvae were also commonly found parallel or close to (within one body width) raised leaf veins underneath leaves. However, some species did not use leaf folds, e.g. Epistrophe

212 G. E. ROTHERAY

eligans and Epistrophe grossulariae rested underneath open leaves, Dasysyrphus albostriatus and Dasyyrphus tricinctus were on branches or in bark crevices and Meligramma triangulifera larvae were sometimes on the top of leaves (Table 2).

T o determine if larvae actively enter leaf folds, aphid-infested, pot-grown bean plants, approximately 40 cm high, were placed outdoors and at 09.00 hours on the day of the experiment a resting larva from laboratory cultures was put a t its tip. Subsequent larval movements were monitored for 2 h. Nine larvae each of Syrphus ribesii, Platycheirus scutatus, Epistrophe eligans and Epiyrphus balteatus were tested. After 30 min all the larvae had moved on to the stem or undersurface of a leaf. Thirty minutes later, five Syrphus ribesii, seven Platycheirus scutatus and six Episyrphus balteatus larvae had entered a leaf fold near the tip of the plant. After 2 h only two Platycheirus scutatus and all nine Epistrophe eligans larvae remained outside leaf folds. They were motionless against raised leaf veins on the underside of a bean leaf. Larvae quickly moved to new leaf folds or veins when the leaf folds that contained them were held open (mean time between opening leaf fold and initiation of movement = 7.34k3.21 min). These results show that larvae actively search out daytime resting sites when placed in an exposed situation.

Palterns of mouement In many syrphid larvae forward movements are frequently interrupted by

short periods of immobility or pauses. For example, in approximately 30 cm of movement on aphid-free Urtica dioica L. plants, satiated Syrphus ribesii larvae paused a mean of 1 1.2 & 3.2 times with a mean pause duration of 9.3 + 4.3 min

Pausing usually followed contacts with potential obstacles to movement, e.g. raised leaf veins, leaf margins and sharply angled stems or leaf petioles. Contacts with these obstacles were unpredictable and pausing did not conform to any obvious pattern: when the number and frequency of pauses was plotted against their duration no significant relations were evident from regression analyses

( N = 5).

( P > 0.10).

SECONDARY DEFENCE

Secondary defence mechanisms are initiated during encounters with a predator. Since syrphid larvae are blind they are probably only elicited in response to tactile cues. No encounters with potential predators were observed. However, responses to parasitoids have been recorded (Rotheray, 198 1) and similar responses were elicited by stroking and pinching with forceps. Thus,

Table 3. Secondary defence mechanisms of third stage syrphid larvae

Stimulus Response during stimulation Response after stimulation

Stroking with a catalepsis (frozen posture) head relaxes, usually

Gently pinching moves to a new resting

Repeated pinching rolls over repeatedly; moves to a new resting

brush with the head contracted remains still

with forceps saliva emitted at attacker site

with forceps falls from the substrate site

head raised and sticky

DEFENCE IN SYRPHID LARVAE 213

there is probably no discrimination between various agents with larvae responding to visually hunting predators in the same way as to parasitoids or forceps. Three responses have been recorded (Table 3). Which response occurred depended on the intensity of the stimulus. Stroking produced catalepsis or frozen posture. Gentle pinching caused a larva to raise its head and emit saliva. Repeated pinching resulted in the larva rolling over rapidly and losing contact with the substrate.

FINAL DISCUSSION

Colour patterns in animals are used for intraspecific communication, thermoregulation and defence (Endler, 1978). I n syrphid larvae it is unlikely that colour patterns function in communication, nor is it likely that animals, which are presumably alike in their physiology, would have developed such a multiplicity of thermoregulatory mechanisms as to demand such diverse colour patterns. Their colour patterns do, however, conform to the expectations of crypsis. This suggestion is strengthened by the occurrence of behavioural traits similar to those displayed by known cryptic animals.

For instance, cryptic animals tend to be nocturnal or crepuscular (Robinson, 1969; Edmunds, 1974). This is necessary because movement is a powerful prey- seeking stimulus in visually hunting predators, many of which are active in the daytime (Robinson, 1969). Many syrphid larvae were nocturnal (Fig. 3) . Vickerman & Sunderland (1975) and Holmes (1985) also recorded nocturnal activity in syrphid larvae. Furthermore, cryptic animals tend to adopt concealing patterns of movement. Some move rapidly then freeze (Robinson, 1969). The frequent pauses observed in locomotion of syrphid larvae are consistent with this move-then-freeze tactic.

During daytime cryptic animals usually become inactive in resting sites that match their colour patterns (Sargent, 1966, 1968; Edmunds, 1974). Thus, to be concealed on a wide range of plants, syrphid larvae must either develop the means to be cryptic on a variety of backgrounds or find similar matching sites on many plants. Syrphid larvae use both means of achieving concealment. Mention has already been made of translucence as a mechanism enabling crypsis on various backgrounds, and colour varieties in Syrphus ribesii, Platycheirus scutatus and Scaeva pyrastri may be another means of achieving crypsis on different substrates.

However, the degree to which an animal needs to be cryptic on a particular background obviously depends on how much of the animal is open to view (Baker, 1970). Many crevices occur on plants where larvae would be completely hidden. Commonly these consist of leaf curls or folds, either as part of the natural contours of the fully developed leaf or as young, unopened leaves or dead and crumpled ones. Where available, they are used by many species (Table 2) which obviates the need to be cryptic on these plants.

Thigmokinesis, that is the negative relationship between locomotion and amount of contact with a substrate (Sutton, 1972), is probably the mechanism underlying entry into leaf folds. Satiated Syrphus ribesii larvae are thigmokinetic (Rotheray & Martinat, 1984) and the behaviour of other species is similar. Inside leaf folds, stimuli eliciting thigmokinesis probably occur through contacts with the closely surrounding substrate.

214 G . E. ROTHERAY

However, the colour and shape patterns of Dasysyrphus and Epistrophe larvae conceal them most effectively against bark and leaves respectively and they were not recorded in leaf folds (Table 2). Resting site selection is probably more complex in these species, involving factors other than thigmokinesis. Resting against a raised leaf vein is another common behaviour (Table 2). Here, only one side of the body is hidden from view but the longitudinal stripes present on many larvae are aligned with the vein, which may enhance concealment as part of homochromy.

Dispersion is another factor affecting crypsis. Tinbergen ( 1965) suggested that cryptic animals should be overdispersed or scattered at random so as to avoid searching image reinforcement from the higher frequency of encounters that predators could be expected to have with aggregated (clumped) prey. Also, many predators intensively search the surrounding area following contact with prey (Croze, 1970; Hassell, 1976). The extent to which syrphid larvae can optimize their dispersion may be limited by the aggregated nature of their own prey and the risk of losing contact with it.

Syrphid larvae can often be found some considerable distance from aphids. For example, 87% of third-stage Syrphus ribesii ( N = 46), 82% Platycheirus scutatus ( N = 22) and 70% Episyrphus balteatus ( N = 27) larvae were resting more than 30 cm from aphid-infested flowerheads of six Heracleum sphondylium plants examined on 14 August 1984 at Corstorphine Hill, Edinburgh. Holmes (1985) noted that large syrphid larvae did not stay close to aphids after feeding.

Nonetheless, in certain situations larvae do rest amongst aphids, e.g. in colonies of Aphis sambuci L. on Sambucus nigra L. This is a large aphid forming densely packed iggregations and larvae of Syrphus ribesii, Epistrophe eligans and Plapheirus scutatus usually rest amongst the aphids. Also, heterospecific aggregations of larvae often occur within colonies of leaf-curling aphids, e.g. Aphis rumicis L. on Rumex acetosa L., Schizoneura ulnii (L.) on Ulmus glabra and Mytus cerasi (Fabricius) on Prunus spp. Thus, apparent dispersion in syrphid larvae may be a reflection of plant topography and aphid colony characteristics rather than a mechanism for defence against visually hunting predators.

Some of these behavioural traits could be additionally influenced by thermoregulation. Larvae may rest in leaf folds more because they offer a favourable thermal environment rather than as a place to escape predators. Mitigating against this is the fact that first- and second-stage larvae, that might be particularly sensitive to environmental conditions, characteristically spend all their time exposed on the plant surface (Rotheray, 1979; Holmes, 1985). The third-stage larva of many species is also exposed, e.g. Dasysyrphus on bark, Epistrophe on leaves, Parasyrphus vittiger on pine needles, Syrphus ribesii and Platycheirus scutatus on Sambucus nigra stems and leaves, and Meligramma triangulifera on the upper leaf surface. Thus, resting site selection is probably not influenced by a need to thermoregulate.

Parasitoids of syrphid larvae are unlikely to have affected colour patterns since they do not use visual cues in host-searching behaviour (Rotheray, 1981). However, parasitoids do concentrate their searches for hosts at aphid colonies so may add to the selection pressure from visually hunting predators for diurnal immobility and resting site selection.

In this small sample of about 25% of the British fauna, a great variety of colour patterns exist (Table 1). Some of this diversity could be explained by a

DEFENCE IN SYRPHID LARVAE 215

relationship between prey specificity and colour pattern. Polyphagous species tend to be translucent, green or brown. However, specialists are often unique, with patterns that match them to particular backgrounds, e.g. the white larvae of Melangyna umbellatarurn on white Heracleum sphondylium flowers and the orange and white stripes of Parasyrphus vittiger on pine needles. Thus, where prey specificity exists the development of a more perfectly matching pattern is facilitated and diversity is increased. A similar relationship between numbers of resting sites and colour patterns in moths was suggested by Endler (1984).

When crypsis fails to deter a potential predator secondary defences may begin (Table 3) . The observed relationship between stimulus intensity and type of counter-response may be related to crypsis. At low levels crypsis and catalepsis may still work. Stronger stimuli, such as picking a larva up, suggest that crypsis has failed and a more active defence such as rolling over is needed. However, none of these responses deterred parasitoids, many of which had developed ways of dealing with them (Rotheray, 1981). Falling off the plant would seem to be the most effective means of escape but entails losing contact with aphid prey. Emitting saliva, unless distasteful, would seem unlikely to deter an insectivorous bird. It is not clear whether saliva is distasteful. Eisner (1971) states that ants withdraw immediately on contact with it. Similarly, parasitoids break off an attack and groom if their antennae or mouthparts become daubed with saliva (Rotheray, 1981).

ACKNOWLEDGEMENTS

I am grateful to all the individuals who have encouraged my studies of syrphid larvae, in particular Professor M. F. Claridge, Drs P. Stiling, M. Jervis, N. Kidd and M. Shaw. I am especially grateful for the many stimulating discussions over the past 5 years with Dr F. Gilbert. I wish to thank F. Gilbert, C. Hartley, M. Shaw and G. Swinney for helpful comments on an earlier draft of this paper.

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