Entomol. exp. appl. 43: 4 9 - 5 4 , 1987 49 �9 Dr W. Junk Publishers, Dordrecht - Printed in the Netherlands

Larval morphology and searching efficiency in aphidophagous syrphid larvae

Graham E. Rotheray Royal Museum of Scotland, Chambers Street, Edinburgh, EH1 1JF, UK

Keywords: larval morphology, locomotive efficiency, capture efficiency, plant substrates, Epistrophe eligans, Metasyrphus luniger, syrphid

Abstract

The effects of larval morphology and substrate quality on the searching efficiency of third stage larvae of Epistrophe eligans (Harris) and Metasyrphus luniger (Meigen) were examined. E. eligans has a smooth, flat undersurface and was able to grasp smooth, flat substrates where it achieved high casting rates and cap- ture efficiencies. It is probably best suited to exploiting leaf-feeding, rather than stem-feeding aphids. Howev- er, M. luniger did best on stems and petioles where it used a special U-shaped grasping organ and lateral movements to hold on and move. On these substrates, as opposed to smooth, flat surfaces, it achieved high casting rates and capture efficiencies.

Introduction

One of the barriers to the colonisation of plants by insects is attachment or holding on (Southwood, 1973). Many aphid predators actively hunt for prey on plants but how their searching efficiency is af- fected by the attachment barrier is little under- stood.

Attachment and locomotion are influenced by plant surface qualities. For instance leaf waxs (Ar- zet, 1973; Shah, 1982), hairs (Banks, 1957) and the smoothness of leaves (Carter et al., 1984) interfere with the movements of aphid predators and may cause them to fall off the plant. Coccinellids (Banks, 1957), chrysopids (Arzet, 1973) and an- thocorids (Evans, 1976) preferentially search for aphids along leaf veins and margins but it is not known if this is because attachment is only effec- tive at these sites.

Another important factor affecting locomotive efficiency is predator morphology such as the na- ture of the locomotive organs and body shape (Giller, 1982). Although predaceous syrphid larvae lack the legs and anal claspers of many other aphidophagous insects, locomotive prominences

may be present (Heiss, 1938; Bhatia, 1939). These structures vary in form and degree of development among different species. For example, at one ex- treme, they are lacking in the larva of Epistrophe eligans and at the other extreme, are large and com- plex in the larva of Metasyrphus luniger. This pa- per considers the effects on searching efficiency of these two morphological varients.

Materials and methods

Larvae were obtained from eggs laid by gravid fe- males caught in the field and placed in Petri dishes with Sitobion fragariae (Walker) aphids on Rubus fruticosus L. leaves. Larvae were subsequently reared on this aphid. Both E. eligans and M. lu- niger feed on S. fragariae in nature.

The morphology of the undersurface of third stage E. eligans and M. luniger larvae was exam- ined with a dissecting microscope. At least 15 larvae of each species were examined.

The movements of third stage larvae on Acer pseudoplatanus L. leaves and petioles were record- ed to determine the locomotory mechanisms used

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by each species. These leaves have smooth surfaces except for five raised veins on the undersurface of the lamina. A A. pseudoplatanus leaf (approximate size-lamina area = 118 cm2; petiole 9 cm long • 2 -3 .5 mm in diameter) was clamped in ap- proximately parallel position to the horizontal and diffusely lit from above. Observations began when a larva was placed at the base of the petiole. If a larva fell off the leaf it was replaced by a fresh in- dividual until nine larvae of each species had been observed continuously for 1 h. Prior to each repli- cate, each larva was starved for 24 h after initially feeding them with aphids until they were consis- tently refused.

To catch aphids, syrphid larvae raise the anterior part of the body and expand it forwards or side- ways in a characteristic movement referred to as casting (Chandler, 1969; Rotheray, 1983). The sig- nificance of casting in evaluating locomotive effi- ciency is that without a firm grasp of the substrate with the posterior part of the body, casting may be inhibited or the larva may fall from the plant. Sites where casting took place and the number of casts made during 5 mins following a 2 min initial peri- od on the petiole and the upper and lower surfaces of the lamina were, therefore, recorded.

Differences in locomotive efficiency on the peti- ole and lamina may influence the effectiveness with which prey are captured. To investigate this possi- bility, 24 h starved, third stage larvae were placed at the base of R. fruticosus leaves (lamina area ap- proximately 35 cm z) or sections of stem (approxi- mately 9 cm long • 4 to 6 mm diameter) on which 20 early stage S. fragariae aphids had been placed previously. The R. fruticosus leaves used were smooth with a single raised vein on the undersur- face. Thorns were removed from the plant material prior to being clamped in an approximately parallel position to the horizontal. If a larva fell from the leaf or stem it was replaced by a fresh individual until nine larvae of each species had been observed continuously for 90 min. A larva was introduced only when all the aphids had settled and were feed- ing. The upper and lower surfaces of the lamina were tested separately. The numbers of casts and aphid captures were recorded. Captured aphids were replaced with fresh individuals so that 20 aphids were always present.

Results

Morphology of the ventral surface in the third stage larva. E. eligans. The undersurface is smooth, shiny and without raised locomotory prominences. However, along each side of the first seven abdomi- nal segments are discs defined by five to eight shal- low grooves which radiate out from a central point. A network of similar grooves occurs round the tip of the anal lobe at the end of the abdomen (Fig. la).

M. luniger. The conspicuous feature of the un- dersurface in this species are the raised locomotory prominences. There are seven pairs along the sides of the abdomen and they increase in complexity and size towards the end of the body. They are bi- lobed on segment 1, tri-lobed on segments 2 to 4 and divided into four lobes on segments 5 to 7 (Fig. lb). The tip of each lobe on segments 1 to 4 are coated with numerous flattened spicules. On segments 5 to 7 the tips are smooth, without spic- ules and have grooves radiating from a central point.

The locomotory prominences on segments 5 and 6 are bent over so that their tips project backwards. The tip of the anal lobe is long, smooth and co- vered with a network of grooves. It forms a 'U' shaped grasping organ with the locomotory promi- nences on segments 5 and 6 (Fig. lc).

Locomotory mechanisms on A. pseudoplatanus leaves. E. eligans. On the petiole forward move- ments were slow and interrupted frequently by pauses during which the larva either smeared saliva on the petiole or made minor alterations to its posi- tion. Forward movements were made with the body parallel to the longitudinal axis of the petiole and were similar to those of the larva of Syrphus ribesii (L.), i.e. the posterior end of the body is raised and a wave of contraction passes forward to the head (Roberts, 1971). On the lamina, all regions were searched and the raised leaf veins were crossed over without the larva falling off. Significantly fewer pauses occurred on the lamina than the petiole (mean number of pauses on the undersurface of the lamina = 5.8 ___ 2.3 v the petiole = 11.2 + 3.3 in a 17 min period on each site, t = 4.4, P < 0.002). Sig- nificantly fewer casts were made on the petiole than the lamina (Table 1). There was no significant difference between the number of casts made on

a 8

7

3 4 5

51

l 0 3 4 5

Fig. la-c. (a) the undersurface of the third stage larva of Epistrophe eligans; (b) the undersurface of the third stage larva of Metasyr- phus luniger, actual length = 11 mm; (c) U-shaped grasping organ of M. luniger, lateral view.

the upper and lower surfaces o f the lamina (Ta- ble 1).

M. luniger. Movements on the petiole occurred with few pauses. In contrast to E. eligans, the larva

o f M. luniger moved sideways along the petiole. This was achieved by curling round the petiole in a semi-spiral and using the 'U ' shaped grasping or- gan and mouthpar t s to hold on. A movement cycle

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Table 1. Mean number (_+s.d.) of casts per 5 min period by third stage larvae o fE . eligans and M. luniger on the petiole and upper and lower surface of A. pseudoplatanus leaves.

Species Leaf

Petiole Upper Lower surface surface

E. eligans 4.7-+ 2.6a* 19.9+ 2.0b 20.2+ 3.8b n = 9

M. luniger 38.0+ 4.3a* 12.6+ 2.9b 36.0_+ 5.6a n = 9

* Values in rows are significantly different at P < 0 . 0 5 if fol- lowed by different letters (SNK tests). One way ANOVA indi- cated significance at P < 0.005.

started by expanding the anterior part of the body forwards along the petiole and gripping it with the mouthparts. The posterior part of the body was subsequently contracted and the grasping organ placed round the petiole close to the head. This cy- cle was then repeated. Underneath the lamina, lar- vae moved along the raised leaf veins by grasping the vein alternately with the grasping organ and mouthparts.

On top of the lamina movements were similar to those of E. eligans except that when moving larvae rocked conspicuously from side to side and some- times fell off the leaf (n = 7). Larvae moved along the leaf margin using the grasping organ and mouthparts to grip the edge. Significantly fewer casts were made on the upper surface of the leaf (Table 1).

Prey capture efficiency. In E. eligans prey capture efficiency was significantly lower on stem sections than on the lamina. Also no significant differences in capture efficiencies were recorded between upper and lower surfaces of the lamina. In contrast, cap- ture efficiency in M. luniger was significantly lower on top of the lamina (Table 2).

Discussion

Insects use frictional or meniscus forces to ad- here to surfaces (Edwards & Tarkanian, 1970; Stork, 1980a, b). Of these, meniscus forces seem more important in syrphid larvae since larvae smear saliva in front of them and move through it (Bhatia, 1939; Roberts, 1971). The presence of grooves on the undersurfaces of E. eligans and M. luniger possibly help to maintain meniscus forces by filling with saliva and increasing the surface area available for contact with the substrate.

However with differences in the development of locomotory prominences the distribution of these grooves differs between larvae of E. eligans and M. luniger. This probably influences how well particu- lar substrates are grasped. The smooth, flat under- surface of the larva of E. eligans suits it to grasping laminas where a high degree of contact between the larva and the plant surface is possible. On stems and petioles only a narrow strip of the undersur- face is in contact with the plant. E. eligans larvae appear to compensate for a poor grasp of stems and petioles by moving slowly, pausing frequently to adjust position and smearing saliva, which,

Table 2. Mean number (_+ s.d.) of casts, aphid captures and capture efficiencies (captures - casts x 100) of third stage larvae of E. eligans and M. luniger on stems and upper and lower surfaces of leaves of Rubusfruticosus infested with 20, early stage S. fragariae aphids.

Species Rubus fruticosus

Stem Upper leaf surface Lower leaf surface

Casts Captures Cap. eff.* Casts Captures Cap. elf. Casts Captures Cap. eff.

E. eligans 11.8_+1.9 1.5+1.1 9.1 __. 4.9a 31.2_+5.4 20 .9+2.1 69.7 +__ 2.6b 27.8_+3.1 19.9:t:2.0 73.0_+ 1.5b n = 9

M. luniger 46 .7+3 .8 26.5_+2.9 67.4_+ 6.7a 11.0+_4.1 1.2_+0.9 9.5 + 4.4b 45.4_+3.2 24.0-+3.3 62.7 + 2.9a n = 9

* Capture efficiency values in rows are significantly different at P <0.05 if followed by different letters (SNK tests). One way ANOVA on arcsin t ransformed data was significant at P<0 .005 . Means in the table are back-transformed.

when the larva moves forward, coats the undersur- face and may help to maximise attachment.

In contrast, the grasping organ and narrow, sub- cylindrical shape of M. luniger allows larvae of this species to curl round stems and petioles and grasp raised leaf veins. On top of the lamina, the larva of M. luniger seems unable to use its grasping organ. This is probably because of the backwardly direct- ed locomotory prominences on segments 5 and 6 which not being in contact with the substrate, result in a reduction of grasping ability. This could ac- count for the unsteady rocking motion and fre- quent falls from the lamina. A minimal grasp of the lamina is further indicated by larvae which al- ways fell off when the leaf was turned upside- down. E. eligans larvae, however, never fell off when the leaf was turned upside-down.

These differences in attachment probably in- fluence searching efficiency by affecting where and how larvae search for prey. The parallel movements of E. eligans on stems and petioles mean that only one side of the substrate is searched for prey. How- ever the lateral movements of M. luniger enable all faces of the stem or petiole to be searched. On the lamina E. eligans searched all regions whereas M. luniger is restricted to leaf margins and veinal regions if raised veins are present. It can also search on top of the lamina but with reduced efficiency. However few aphids form colonies on top of leaves.

Furthermore, not only does attachment effect where larvae search but it also affects the efficiency with which prey are captured. On stems and peti- oles E. eligans had low casting rates i.e. attempts at capturing prey, and probably as a consequence, reduced capture efficiencies (Tables 1 and 2). How- ever M. luniger had higher casting rates and cap- ture efficiencies on those sites it could most effi- ciently grasp i.e. stems, petioles and leaves with raised leaf veins (Tables 1 and 2). Overall the results suggest that E. eligans is better suited to exploiting aphids on smooth, flat surfaces such as leaves whereas M. luniger is a more effective predator of stem-feeding aphids and aphids that occur on leaves with projecting leaf veins.

The morphologies studied here are not unique to the two species studied. All known larvae of Epis- trophe ssp. and Dasysyrphus ssp. have flat under- surfaces whereas Metasyrphus ssp. and Scaeva ssp. have U-shaped grasping organs and are subcylindri- cal. Although not a true test of the association be-

53

tween morphology and searching efficiency, be- cause congeneric species having similar morphology cannot be regarded as independent data points, nonetheless, supporting evidence that the association exists in the way described comes from an analysis of the field distribution of larvae among stem and leaf feeding aphids. A survey of 25 different plant species and the larvae associated with aphids on these plants was made from 1977 to 1979 in S. Wales, UK. Of the total number of Epis- trophe and Dasysyrphus larvae recorded (n = 136), the proportion on plants with leaf-feeding aphids was 0.88 and the proportion on stem - feeding aphids was 0.12. For Metasyrphus and Scaeva lar- vae (n = 460) the proportion on stem - feeding aphids was 0.93 with 0.07 on leaf - feeding aphids. Larvae recorded on plants with both stem and leaf feeding aphids (n = 117) are not included.

Many other syrphid species were also recorded from these plants. The morphology of their ventral surfaces was, in the most common species, inter- mediate between E. eligans and M. luniger. For ex- ample, Syrphus ribesii (L.) has locomotory promi- nences but no U-shaped grasping organ (Rotheray, 1986) and the extent to which its searching efficien- cy is affected by attachment problems is uncertain. Nonetheless an attachment barrier has clearly in- fluenced searching efficiency in E. eligans and M. luniger. Future comparisons between different predator species and possibly different stages, should take attachment into account and include an analysis of morphology in relation to locomo- tive efficiency on whatever substrates are tested. Experimental studies of searching efficiency may need to control for substrate quality.

Acknowledgements

I thank Alan Bond, Francis Gilbert, Paul Gross and Ed Burrows for comments.

R~sum~

Morphologie larvaire et efficacitd de la prospection chez des larves aphidophages de syrphes

Uexamen a port6 sur les effets de la morphologie larvaire et de la nature du substrat sur les succ~s de

54

la prospection des larves de troisibme stade de E. elegans et de M. luniger. La surface ventrale de E. elegans est plate et molle, sans pro6minences locomotrices. Sur les feuilles plut6t que sur les p6ti- oles, il a mieux adh~r6 au substrat et a r6alis6 plus de captures avec une meilleure efficacit6. E. elegans est probablement mieux adapt6 ~ l'exploitation des pucerons sur des surfaces molles et plates, comme les feuilles. M. luniger pr6sente une disposition complexe de pro6minences locomotrices, com- prenant un organe de pr6hension en forme de U l'extr6mit6 du corps. Sur les tiges, les p6tioles et les feuilles avec des nervures saillantes, il est capable de se fixer efficacement et de se d6placer sur des struc- tures cylindriques en utilisant son organe de pr6- hension, ses pi6ces buccales et des mouvements lat6raux. II a r6alis6 plus de captures avec une plus grande efficacit6 sur tiges et p6tioles par comparai- son avec des surfaces molles; il peut ~tre mieux adapt6 ~ exploiter les pucerons associ6s aux sur- faces cylindriques de ce type.

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Accepted: July 29, 1986.