OVIPOSITION BEHAVIOUR OF SOME APHIDOPHAGOUS SYRPHIDAE
by Anthony Eric Francis Chandler M.A.
Thesis submitted for the Degree of Doctor of Philosophy
Imperial College of Science and Technology, Field Station, Silwood Park, Sunninghill, Ascot, Berkshire. APRIL, 1967. ABSTRACT
The oviposition behaviour of various species of aphidophagous Syrphidae was investigated in the field and in cages. A key for the determination of 35 species from their eggs is given, together with descriptions and ecological notes.
The relationship between syrphid oviposition and aphid infestation was studied. Some aphidophagous species laid freely in the absence of aphids and the significance of this is discussed. The role of the host plant in attracting syrphids and influencing the site of oviposition was investigated. Height preferences for oviposition were related to the ecology of various species. The effect of ageing of females and interactions between stimuli were also considered.
Ways in which an understanding of the behaviour of different species may help in Biological and Integrated Control of aphids are discussed. TABLE OF CONTENTS
INTRODUCTION 1
SPECIES LIST 3
SECTION A. A Dreliminarx key to the eggs of some of the commoner aphidophagous syrphids occurring in Britain 5 1. Introduction 6 2. Key 14 3. Descriptions of eggs 25 .. Discussion 55 5. Summary 63
SECTION B. Some host plant factors affecting syrphid oviposition. 614. 1. Introduction 65 2. Host plant selection 66 3. Oviposition site selection 74 4. Influence of the substrate 75 5. Discussion 81 6. Summary 86 SECTION C. The relationship between aphid infestatiOns and syrphid oviposition. • 87 1. Introduction 88 2. Field records of oviposition 89 3. Experiments on oviposition by different syrphid species . • . . . 4. Oviposition in relation to the size and distribution of aphid aggregates 99 5. Visual perception of aphids by Syrphus balteatus ...... • . • . 104 6. Discussion 106 7. Summary 112
SECTION D. Some factors influencing the occurrence and site of Syrphid oviposition 113 1, Introduction 114 2. Stimulus carry-over 111+ a.Aphid stimulus 115 b.Adult food stimulus 117 3. Stimulus inhibition 121 a.Presence of syrphid larvae . . • 121 b. Presence of syrphid gut contents • 123 c. Presence of syrphid eggs 125 4. The, precise site of oviposition 126 5. Discussion 136 6. Summary 140 SECTION E. Height preferences for oviposition. . 141 1. Introduction 1I:2 2. Methods 142 3. Oviposition height preference over grass . 11,4 4. Effect of ageing of females upon height of oviposition 11/4 5. Effect of bare soil on height preference • 148 6. Effect of various substrata on preferred height for oviposition of Syrphus balteatus 150 7. Discussion 153 8. Summary . 157
SECTION F. Discussion of the relevance of the present studies to aphid control progrnmme s 158
ACKNO'irf agsk ,NTS 168
REFERTOGES 169 1. INTRODUCTION
Studies on the ecology of Syrphidae have been primarily concerned with the aphidophagous species because of their practical importance. Although much has been published concerning syrphid predation on field crops, little quantitative or critical work has been done on the behaviour of particular species.
Since the first instar aphidophagous larvae have limited locomotory powers to assist them to find aphids, it is important to the species that the female is able to seek out places to oviposit, where the hatching larvae will have an assured source of food,
Dixon (1959) investigated the ecology of various aphidophagous species and indicated specific differences in oviposition behaviour patterns. Volk (1964.) and Dixon studied various factors affecting the choice of oviposition site, and Bombosch (1962), Volk and Peschken (1965) investigated the relative importance of the stimulus components for oviposition by Syrphus corollae Fabr. in the laboratory. 2. The present work was undertaken to study under field conditions the relative importance to different species of host plant and aphid factors in oviposition and the ways in which these were affected by interaction, or by ageing of the females, and also to provide information which might be helpful for choice or manipulation of species in Biological or Integrated Control of aphids. 3. SPECIES LIST The nomenclature and classification adopted in this study are those of Coe (1953) as detailed by Parmenter (1954) and revised by Coe (1967). The species considered are listed below: SYRPHINAE BACCHA Fabricius 1805 obscuripennis Meigen 1822 PYROPHAENA Schiner 1860 CHEILOSIA Panzer 1809 granditarsa (Forster 1771) PLATYCHIRUS St. Fargeau and Serville 1828 albimanus (Fabricius 1781) clypeatus (Meigen 1822) manicatus (Meigen 1822) peltatus (Meigen 1822) scutatus (Meigen 1822) XANTHANDRUS Verrall 1901 comtus (Harris 1776) MELANOSTOMA Schiner 1860 mellinum (Linnaeus 1758) scalare (Fabricius 1794) SPHAEROPHORIA St. Fargeau and Serville 1828 menthastri (Linnaeus 1758) scripta (Linnaeus 1758) XANTHOGRAMMA Sohiner 1860 citrofasciatum (Degeer 1776) LEUCOZONA Schiner 1860 SYRPHUS Fabricius 1775 lucorum (Linnaeus 1758) SCAEVA Fabricius 1805 CATABOMBA Osten-Sacken 1877 pyrastri (Linnaeus 1758) SYRPHUS Fabricius 1775 EPISTROPHE Walker 1852 EPISYRPHUS Matsumura 1917 ISCHYROSYRPHUS Bigot 1882 MELANGYNA Verrall 1901 MESOSYRPHUS Mat surnura 1917 METASYRPHUS Mat samura 1917 SIXNOSYRPHUS Mat sumura 1917 SYRPHELLA Goffe 1944 SYRPHIDIS Goffe 1933 albostriatus (Fallen 1817) auricollis (Meigen 1822) balteatus (Degeer 1776) cinctellus (Zetterstedt 1843) cinctus (Fallen 1817) compositor= Verrall 1873 corollae (Fabricius 1794) diaphanus (Zetterstedt 1843) eligans (Harris 1776) glaucius (Linnaeus 1758) grossulariae Meigen 1822 lasiophthalmus (Zetterstedt 1843) latifasciatus Macquart 1829 luniger Meigen 1822 lunulatus Meigen 1822 nitidicollis Meigen 1822 punctulatus Verrall 1873 ribesii (Linnaeus 1758) torvus Osten-Sacken 1875 triangulifer (Zetterstedt 1843) tricinctus (Fallen 1817) umbellatarum (Fabricius 1794) vitripennis Meigen 1822
CHRYSOTOXINAE CHRYSOTOXUM Meigen 1803 cautum (Harris 1776)
CHE ILOS IINAE PIPIZA Fallen 1810 noctiluca (Linnaeus 1758) PIPIZELIA Rondani 1856 varipes (Meigen 1822) CNEMODON Egger 1865 vitripennis (Meigen 1822) 5.
SEC TION A
A PRELIMINARY Kau TO THE EGGS OF SOME OF THE
COMMONER APHIDOPHAGOUS SEIPHIDS OCCURRING IN BRITAIN. 6. A PRELIMINARY KEY TO THE EGGS OF SOME OF THE COMMOMR APHIDOPHAGOUS SYRPHIDS OCCURRING IN BRITAIN
I. INTRODUCTION The importance of aphidophagous Syrphidae as potential aphid control agents and the recognition that different species show markedly different oviposition response patterns have led to the present attempt to identify syrphid species from eggs laid in the field. Previously, positive identification has required hatching of the eggs, rearing of the larvae and frequently pupation and emergence of the adult, often after prolonged diapalase, a procedure that is time-consuming and uncertain owing to larval mortality. This paper represents a preliminary attempt to describe the eggs of some of the commoner British aphidophagous Syrphidae. Although it has proved possible to identify with certainty the eggs of some species in the field (e.g. Syrphus ribesii L.), for most it is necessary to examine the eggs microscopically.
The larvae of all species described in this paper appear to be at least facultatively aphidophagous if the appropriate aphid species is available. The term laphidophagausl must however be loosely interpreted for some species, further details of.which are given in the ecological notes pertaining to each. 7. Description of the egg and terminology employed .The eggs of aphidophagous Syrphidae are laid commonly on the undersides of leaves infested with aphids, although some species may, lay on uninfested plants (Chamdler,1967a) or, as in Pipizella varipes Mg., at the base of the stem of plants with root aphids (Dixon, 1959). Most species lay eggs singly but some, notably of the genera Melanostoma and Platychirus, lay them in small batches, the eggs ranked side by side.
Typically, the eggs are about one millimetre long, white .in colour and elongate-oval in shape, with an inconspicuous micropyle and microscopic surface sculpturing. The ventral surface of the egg (that in contact with the substratum) is flattened, but the dorsal surface is strongly convex
In general, the eggs of aphidophagous syrphids may , be separated from those.of other groups laying on aphid- infested plants. Hemerobiid eggs may be distinguished by their smaller size and conspicuous micropylar cap. ..gromyzid and Anthomyid eggs may be distinguished by their pronounced reticular patterning and strongly impressed inter-reticular panels, resembling only the eggs of 8. Syrphl;s nitidcollis Ng. of those syrphid species described in this paper. However, the former may be differentiated by their more frail appearance, their host plant and their lack of any particular relationship to aphids,,S. nitidicollis laying within a few millimetres of an infestation, usually of an Aphis species.
Brief descriptions of the eggs of individual species of aphidophagous syrphids have been proviided by various authors (e.g. Metcalf, 1916; Davidson, 1922; Jones, 1922; Staniland, 1922; Scott, 1939; Bhatia, 1939; Dixon, 1958), but these are inadequate for positive identification.
Klein -Krautheim (1936) has provided descriptions and plates of the eggs of eight species of non-aphidophagaus syrphids, which show consistent differences of sculpturing between closely related species. Kabos.(l943) suggested that the structure of the chorion is characteristic for each species and may be used as a method of identification, but takes the matter no further. The present paper provides general support for his thesis.
The chorionic patterning of syrphid eggs may be of tubular outgrowths, elevated ribs,, surface in3entations or it may be obscure or absent. The structures upom which the identification and descriptions given here 9. are based are defined as they appear under the light microscope and no attempt is made to interpret them in terms of their ultrastructure, The following terminology is employed%
Patterning describes the surface appearance of the intact egg under low magnification and sculpturing refers to the structures seen when the chorion is removed and examined under higher magnification (Figs. 2-4); both consist of subregularly arranged units, which usually comprise a central axis with side branches (Figs.2.F, 2,11.1 3.J, 4.D, 4.M). Where units are obscure or side-branches extensive, the general term ramifications may be used (Figs. 3.01 3.H). In some cases the sculpturing may appear as no more than dots and rods (Figs. 2,11, 2,E, 3.B, 3.0); rods more than three times as long as wide, and sinuous, are considered strands (Figs. 2,D, 2.11) and where the sculpturing is obscure but consists of dots, rods and/or strands, it is termed particulate (Figs. +.C, 4.G). Where there is a defined region around the middle of a unit with side-branches, whether this be due to surface elevations or to other structures, it is referred to as the central area (Figs. 2.3, 3.F). 10. Other descriptive terms used are defined where they occur in the text or their meanings are self-evident. The sculpturing is usually different on the dorsal and ventral surfaces and is described for both. It may also vary slightly from either of these types laterally and towards the tips of the egg and the descriptions given refer, unless otherwise stated, to the mid-dorsal and mid-ventral sculpturing, the limitation being emphasised where the difference is critical.
To assist in rapid identification of specimens from the field, the major divisions of the key are based on superficial appearance wherever possible, rather than relying upon chorionic mounts. As little use as practicable is made of ventral sculpturing since the egg cannot always be removed intact from the substratum, so this part of the chorion may be lost.
Measurements Egg measurements were made on fresh specimens using a binocular microscope with an eyepiece graticule calibrated against a stage micrometer (standard error ± 1%): the measurements in graticule units were subsequently converted to microns (total accuracy limits ± 5,4. Overall length is used to denote the size of the egg; the width of any given egg varies far more according to its hnmldity 11. regime than does its length and there is much less variation between species in width than in length. Lengths are thus quoted for over 200 eggs for each species where possible, but width measurements are not as heavily documented. Values for n given in the text refer to the length, and the width measured is in all cases the width at the widest part of the egg.
Preparation of Chorionic Mounts Chorionic mounts were made by stripping the chorion of the egg under water on a microscope slide so that it floated off, The rest of the egg was then removed and the surplus water drawn off slowly. The chorion settled down flat on the slide and was mounted in a thin film of water under a coverslip,
In practice it was found that the chorion could more readily be removed if the eggs had previously been kept in Pampelts Fluid (6 parts 35% Formaldehyde, 15 parts 95% Ethyl Alcohol, 2 parts Glacial Acetic acid and 30 parts distilled water) and this medium was also used for preserving whole eggs permanently.
When the eggs dry of their surface appearance is not appreciably different from that of fresh eggs. The white patterning present in many species (here called frosting) results from differential refraction and is not 12. as Bhatia (1939) claims Ita powdery white material, easily displaced by contact and dissolved by immersion in alcohol and xylol".
Identification and source of material Eggs were initially identified by reference to the adult (whose species may be determined with certainty) either by rearing through to the imaginal stage or by obtaining them from gravid females laying in captivity, Host preferences recorded in the ecological notes refer only to field records made at Imperial College Field Station during the seasons 1964 - 66. where egg records are few, the notes on seasonal abundance are supplemented by information from adult flight data for various parts of the British.Isles for the seasons 1959 - 66.
Eggs have also been obtained from further species) not here described, without oviposition being necessary using the following method; The ovaries of gravid females are dissected out immediately after death. Several mature eggs float free and if these are transferred to a microscope slide and allowed to dry off, the complete chorionic patterning is visible. Mounts may be made as described above. 13. Nomenclature and Classification The nomenclature employed follows that of Coe (1953), who retains the massive genus Syrphus Fabr. 1775. Gaffe (1952) splits this up into some ten different genera and although the studies of the present author on the eggs, the larvae and the adult behaviour patterns confirm some of his groupings (e.g. Metasyrphus Mtsma 1917 and Syrphella Goffe 1944), it is not possible to agree upon the homogeneity of his genus Stenosyrphus Mtsma and certain other distinctions. For clarity, therefore, the single genus Syrphus is maintained in this study but apparent natural affinities between species within this group are indicated where relevant in the text. 14. II. KEY 1. Egg with deep unbroken longitudinal grooves dorsally and laterally, usually eight in number; rosette of overlapping spathulate 'cells' around the 2 Egg without deep longitudinal grooves or rosette of spathulate 'cells' around the micropyle...... 3
2. Mean egg length <900A. Chorionic sculpturing strongly reticulate (fig.2.I) (1) Pipizella varipes Meigen Mean egg length) 900A. Chorionic sculpturing at most faintly reticulate (2) Pipiza noctiluca Linnaeus
3. Egg with tubular projections upstanding at
least 20/4. .0 .0 oe •. oe .0 *4 .0 •. Oi 4 Egg with non-tubular projections upstanding less than 20/11 or without projections . 8
4.Projections20-45Along, cup-shaped
(figs. 1.0 - 1.E) O. GS QS .14 00000 0 'PO 01, O. 1, 0 Projections 50-65/41ong, cone-shaped
(figs. 1.A - 1.B)... o 7 15. 5.Egg yellow or greyish, -orange. Mean length >1050/h. Projections trumpet-shaped (fig.1.0). Dorsal sculpturing with branches of neighbouring units rarely touching (fig ,3 . A) . (3) Syrphus ribe sii Linnaeus Egg white or cream. Mean length 41050,a. Projections mushroom-shaped (figs.l.D & 1.R). Dorsal sculpturing with branches of neighbouring units frequently touching
(figs. 3.D & 3.0) 6
6.Egg white, slightly pointed at one end. Projections with neck much wider than long (fig. 1.D). Dorsal sculpturing with fewer than eight forked branches per unit (fig.3.D) (4) Syrphus vitripennis Meigen Egg cream, rounded at both ends. Projections with neck about as long as wide (fig.l.E). Dorsal sculpturing with more than eight forked branches per unit (fig.3.G) (5) Syrphus lasiqphthaImus Zetterstedt
7.Tip of projections flask-shaped, about 8/0 wide (fig.l.A) (6) Syrphus lunulAtus Meigen Tip of projections acuminate, about 3,0 wide (fig.l.B) (7) Syrphus tricinctus Fallen
16. 8.Mean egg length ,--,-/4"):12K0 ...... 0 .0 .0 .1P 4 110 . 9 Mean egg length 41250,44...... 10
9.Mid-dorsal patterning obscure, semi-matt but not frosted; ventral sculpturing of dots and rods; egg turns pearly-grey on development, (Spring species only)(8) Leucozona lucorum Linnaeus Mid-dorsal patterning of clearly-defined frosted units; ventral sculpturing of branches with large central area; egg remains white on development. .(9) Syrphus cinctellus Zetterstedt
10t Dorsal patterning of upraised meshwork, the interstitial, panels impressed, particularly noticeable at the micropylar 11 Dorsal patterning without upraised meshwork
and impressed panels. so so se ss so so *0 so so so so 14
11, Inter-reticular panels large (> 40,x) and deep; dorsal sculpturing of groups of dots and rods (10 Syrphus nitidicollis Meigen Inter-reticular panels small (4444 and shallow; dorsal sculpturing of branching strands 12 17. 12.Dorsal sculpturing with axis and branches of equal thickness (fig.3.J); ventral sculpturing of large dots evenly distributed, egg turns brown on development (11) Syrphus umbellatarum Fabricius Dorsal sculpturing with axis and branches of unequal thickness; ventral sculpturing of small dots and rods aggregated into well- separated groups; egg remains white on
development 13
13.Dorsal sculpturing with axes lacking common orientation, neighbouring units greatly dissimilar in size (fig.4.D). July-September occurrence (12) Syrphus glaucius Linnaeus Dorsal sculpturing with axes all orientated along long axis of egg, neighbouring units similar in size (fig.4.G). Spring occurrence (13) Syrphus eligans Harris lb,. Dorsal patterning of impressed oval-shaped rings demarcating very slightly upstanding lozenge-shaped panels, shining not frosted 15 Dorsal patterning superficial or absent not impressed 20 18. 15. Dorsal sculpturing of dots and short rods
OnlY.41.414 16 Dorsal sculpturing with definite strands 19
16.Egg pointed at one end; dorsal sculpturing of dots and rods not clearly separated into groups....(l)+) Pyrophaena granditarsa Forster Egg rounded at both ends; dorsal sculpturing of dots and rods clearly separated into groups 17
17.Egg more than three times as long as broad; eggs usually laid in batches (15) Platychirus clypeatus Meigen Egg less than three times as long as broad; eggs laid singly 18
18.Dorsal sculpturing of groups of dots and rods irregularly margined (fig.2.C), mid-ventrally with little tendency to aggregate into groups; egg remains white on development (16) Platychirus albimanus Fabricius Dorsal sculpturing of groups of dots and rods smoothly margined (fig.2.1-)7 mid-ventrally clearly aggregated into groups; egg usually turns biscuity-brown on development (17) Platychirus scutatus Meigen 19. 19.Egg turns pinkish brown at tip on development; ventral sculpturing of dots and rods not aggregated into groups; eggs usually laid in small batches (18) Platychirus peltatus Meigen Egg remains white on development; ventral sculpturing of dots and rods aggregated into more or less discrete groups; eggs laid singly (19) Eigals12102111IIII Meigen
20.Dorsal patterning of longitudinal rows of fine crescent-like crests or ridges, at least five times as long as wide 21 Dorsal patterning not of fine crests, units less than five times as long as wide
21. Mean egg length )1050µ(20).8caeva pYrastri Linnaeus Mean egg length < 10504 22
22, Ventral sculpturing of dots and rods collected into groups more than three times as long as main width; perimeter with numerous infoldings (fig.3,I) (21) Syrphus Iuxliger Meigen Ventral sculpturing of dots and rods collected into groups less than three times as long as wide; perimeter almost without infoldings (fig.3.C) (22) Syrphus corollae Fabricius 20. 2A. Dorsal patterning of conspicuous studs, upstanding at least 30/44 ventral sculpturing of units with axes; side-branches not pointed... 24 Dorsal patterning without conspicuous studs, upstanding less than 30/1; ventral sculpturing of units without axes; side-branches pointed.. 25
24.Studs evenly frosted and essentially flat- topped, comprising many strands vertically orientated and densely packed (23) Chrysotoxdm cautum Harris Studs with translucent central region elevated, not consisting of bunched strands (24) Xanthogramma citrofasciatum DQgeer
25.Patterning of dorsal surface very faintly sinuate, obscure or absent centrally, clearly evident only at the tips of the egg; dorsal sculpturing with side-branches having notably blunt tips 26 Patterning of dorsal surface clearly evident centrally as striations or oblong plates; dorsal sculpturing with side-branches having pointed tips 27 21. 26. Egg strongly tapering towards one end; egg turns yellow on development; ventral sculpturing of dots and rods aggregated into discrete groups with a few short straight side-branches (25) Syrphus latifasciatus Macquart Egg not notably tapering towards one end; egg remains white on development; ventral sculpturing of large dots evenly distributed (26) Syrphus triangulifer Zetterstedt
27. Dorsal sculpturing with pronounced central area obscuring axis, side-branches long
(figs.4.0 & 4;t4) 28 Dorsal sculpturing with, at most, slight central area, axis clearly evident, side-branches
short (figs. 2.3 8c3.M) 32
28. Ventral sculpturing aggregated into units often with small side-branches 29 Ventral sculpturing of evenly distributed large dots, and rods (Spring species) (27) Syrphus punctulatus Verrall 22. 29. Surface patterning of plates or striation. semi-matt; ventral sculpturing of poorly defined groups comprising dots and rods loosely arranged and clearly evident centrally, and small but conspicuous strands radiating outwards peripherally; egg turns brown on development 30 Surface patterning of plates or striations heavily frosted; ventral sculpturing of clearly defined but obscurely and densely particulate groups, sometimes with inconspiauous, fine-pointed side-branches; egg remains white on development 31
30. Transition zone between dorsal and ventral types of sculpturing of at least four rows, some units with central area absent and axis present (28) Sphaerophoria menthastri Linnaeus Sharp demarcation between dorsal and ventral types of sculpturing, axis never present if central area absent (29) Sphaerophoria scripta Linnaeus 23. 31. Ventral sculpturing with lateral separation between groups more than half the width of a group; mid-ventral groups with some fine, pointed side-branches (fig.4.E). (30) Syrphus balteatus Degeer Ventral sculpturing with lateral separation between groups less than half the width of a group; mid-ventral groups with at most short, blunt lateral projections (31) Syrphus auricollis Meigen
32.Eggs usually laid in batches, often remote from aphids; dorsal sculpturing with mean number of side-branches less than 12 per
unit 33 Eggs laid singly, close to aphids; dorsal sculpturing with mean number of side-branches
more than 12 per unit 31+
33.Mid-ventral sculpturing of dots, rods and fine strands aggregated into semi-discrete groups (32) Melanostoma mellinum Linnaeus Mid-ventral sculpturing of dots and rods showing no tendency to aggregate into groups (33) Melanostoma scalare Fabricius 24. 314, Ventral sculpturing of small dots and rods aggregated into discrete units (34) Baccha obscuripennis Meigen Ventral sculpturing of large dots and rods showing no tendency to aggregate into groups (35) Syrphus cinctus Fallen 25. III. DESCRIPTIONS OF EGGS
1. Pipizella varipes Meigen Pellucid white; notably small, mean length = 830/a(n=5), mean width = 320/44 pointed at both ends; deep longitddinal grooves usually eight in number. Chorionic sculpturing: strongly reticulate (fig.2.2); inter-reticular panels granulose, more elongate on dorsal surface of egg; rosette of overlapping spathulate 'cells' around the micropyle. Ecological notes: frequentieggs were found from May to August with two seasonal peaks, one at the end of May and one early in August; eggs were always found associated with subterranean aphid colonies, laid singly.
2. Pipiza noctiluca linna'eus Pellucid white; mean length = 1047/6(r=629 range= 910 . 12150, mean width = 423p Pointed at both ends; deep longitudinal grooves usually eight in number. Chorionic sculpturing: surface evenly granulose, at most only faintly reticulate; rosette of overlapping spathulate icel..1.st- around the micropyle. Ecological nptes: frequent; eggs were found from May to September, the main peak occurring in June and a minor one towards the end of August; eggs laid singly. 26. 3. Syrphus ribesii Linnaeus Yellow turning greyish-orange on development; mean length = 1200m. (n=)+1)+, range=905-136(0), mean width = 493A; bulbous and rounded at both ends; pronounced surface projections dorsally and laterally, egg sometimes appearing echinate even to the naked eye. Chorionic sculpturing: dorsally, projections trumpet-shaped with neck about as long as wide (fig.l.C); dendritic ramifications with branches of neighbouring units rarely touching (fig.3.A); ventrally, sculpturing of large dots and rods not aggregated into discrete groups. Ecological notes: abundant; eggs found from May to October; very wide host acceptance range; eggs occasionally laid in small batches of two to four eggs, but usually singly.
4. Syrphus vitripennis Meigen White, greying slightly on development; mean length = 9571&(n = 230, range =1 820 - 1110,L), mean width = 427/6; slightly pointed at one end; marked surface projections dorsally and laterally. Cha2ionic sculpturing: dorsally, projections mushroom- shaped, neck wider than long (fig. 1..5)), appearance of units dendritic, ramifications with extensive contact between branches of neighbouring units (fig.3.D); 27. ventrally, sculpturing of large dots and rods not aggregated into discrete groups. Ecological notes; common; eggs found from May to October; wide host acceptance range; eggs laid singly.
5, Syrphus lasiophthalmus Zettersbedt White or cream, darkening slightly on development; mean length = 1043/t (n = 51, range = 970 - 11594, mean width = 387k; rounded at both ends; pronounced surface projections dorsally and laterally. Chorionic sculpturing: dorsally, projections mushroom- shaped with neck about as long as wide (fig. 1.E); dendritic ramifications with more than five forked branches per unit (fig.3.G); ventrally, sculpturing of large dots and rods not aggregated into discrete groups. Ecological notes: common spring species; eggs found from April to June; wide host acceptance range, eggs laid singly.
6. Syrphus lunulatus Meigen White, greying on development; mean length = 1087/& (n = 22, range = 1000 - 1175,41 mean width = 573/t9 bulbous and strongly rounded at both ends; projections forming a dense fine pile over the dorsal and lateral 28. surface of the egg, each arising from a discrete, polygonal, basal plate. Chorionic sculpturing: Projections 50 - 65/41ong„ conical, constricted just before tip (fig. 1.A); dorsally, irregular reticulum of strands of uneven thickness comprising large dots and fine straight threads, individual units not separable (fig.3.E); ventrally, same structures present but less organised into a network. Ecological notes: eggs not found in the field, but laid under caged conditions in response to Aphis fabae Scop. and laid singly; recorded as aphidophagous by Degeer (1776); larvae found by Degeer on pine and by the author on oak; gravid females found frequently in May and June.
7. Syrphus tricinctus Fall6n White; mean length = 1233/o(n = 6), mean width = 573/11 slightly tapering towards one end; projections forming a dense, fine pile over the dorsal and lateral surface of the egg, stiffer-looking than those of Syrphus lunulatus and the basal plates less conspicuous. Chorionic sculpturing; Projections 50 - 65/tlong, conical, finely tapering towards tip (fig. 1.B); sculpturing otherwise as for Syrphus lunulatus. 29. Ecological notes: eggs not found in the field, but gravid females found from April to September with peaks in May and August. (The larva has been observed feeding on Lepidopterous and Hymenopterous larvae but rejecting aphids (Gabler, 1938; Friederichs et al, 1940). However, the related species S. albostriatus Fallen is recorded as aphidophagous (Schneider, 1948; Brauns, 1953) and it seems possible that S. tricinctus may be facultatively so if a suitable aphid species is presented.)
8. Leucozona lucorum Linnaeus Shining white, turning pearly-grey on development; mean length = 13751t(n = 113, range = 1280 - 1470.4, mean width = 493*1 rounded at both ends; surface lightly Idustedl, patterning of small irregularly-shaped, ill-defined units tightly packed together. Chorionic sculpturing: dorsally, short branching units irregularly orientated (fig. 4.A) with no contact between neighbours; ventrally, sharply defined groups of characteristic shape (fig. 4.B), comprising densely-packed dots and rods. Ecological notes: common spring species; eggs found from May to July, notably on plants infested with Aphis spp.; laid singly. 3o.
9. Syrphus cinctellus Zetterstedt Chalk-white; mean length = 1472Ab(n = 19, range = 1330 - 1590/i), mean width = 53461 tapering towards one end; surface patterning of irregularly-contoured but clearly separated, frosted white units, slightly upstanding. Chorionic sculpturing: dorsally and ventrally, extensive particulate areas with straight side-branches that are finely pointed and themselves unbranched; axes not present (fig.4.1,),central areas larger ventrally. Ecological notes: frequent; gravid females found from May to September with peaks in late May and late August; eggs found on spruce, pine and oak; laid singly.
10. Syrphus nitidicollis Meigen Chalk white, turning slightly greyer on development; mean length = 1113/4(n = 54, range = 1040 - 1240/01 mean width = 42714 egg tapering strongly towards one end; surface patterning comprising an upraised latticework with the interstitial panels angular and strongly. indented. Chorionic sculpturing: very sharply demarcated groups of dots and rods both dorsally and ventrally with thin strands around the periphery (figs. 4.J, 4.-x). Ecological notes: frequent; eggs found from May to July, notably in association with Aphis spp on a variety of plants; laid singly. 31. 11. Syrphus umbe/latarum Fabricius Pale whites turning deep biscuity-brown on development; mean length = 951/6(n = 125, range = 840 l000/40, mean width = 373/4; egg rounded at both ends; surface appearance of faint angular teens' that are small and lightly dusted. Chorionic sculpturing: dorsally, conspicuous axis with medium length side-branches that taper towards the tips but are not finely pointed, occasional contact between branches of neighbO4ring units (fig.3.J);. ventrally, large dots evenly distributed (fig.3.K). Ecological notes: frequent; eggs found from June to September; wide host acceptance range; eggs laid singly.
12. Syrphus glaucius Linnaeus Mid white; mean length = 1172/a(n = 221, range = 1025 - 1390,4), mean width = 480,46; slightly rounded at both ends; surface patterning of fine upraised reticulums particularly noticeable above the micropyle, inter- reticular panels frosted and irregularly shaped, obscure mid-dorsally. Chorionic sculpturing: dorsally, irregularly-orientated and irregUlarly-shaped axes with short side branches often with spathulate tips (fig.4.D); ventrally, well- separated and clearly demarcated groups of rods and dots (fig. 4.3). 32. Ecological notes: frequent; eggs found from July to September but only on umbellifers; laid singly.
13. Syrphus eligans Harris White; mean length = 1172/h(n = 90, range = 1010 1215/41 mean width = 467/44 slightly rounded at both ends; surface patterning of fine upraised reticulum clearly evident over whole dorsal surface of egg, but units are small and appearance of egg is rugose. Chorionic sculpturing; dorsally, branching units, axes obscure or absent, small particulate central area, branches short with only occasional contact between those of neighbouring units (fig. 4.G); ventrally, well-separated groups of rods and dots (fig. 4,H). Ecological notes: common spring species; eggs found during May and June; wide host acceptance range; eggs laid singly.
14. Pyrophaena granditarsa Forster White; mean length = 817/4.(n = 23, range = 705 - 906A, mean width = 329/44 egg markedly pointed at one end; surface patterning of faintly impressed oval rings, ghiny. 33. Chorionic sculpturing: dots and rods both dorsally and ventrally with only slight tendency to aggregation into groups. Ecological notes: eggs never found in the field, but gravid females frequent from June to October notably in wet, grassy habitats; eggs laid singly in the laboratory. (It is assumed (e.g. Lundbeck, 1916; Coe, 1953) that the larva is aphidophagous, but this is not yet definitely established.)
15. Platychirus clypeatus Meigen Yellowish when laid, turning bisouity-brown on development; notably long in relation to width, mean length = 1103/0(n = 86, range = 1025 - 1230A, mean width = 333A rounded at both ends; surface patterning of faintly impressed oval rings, shiny. Chorionic sculpturing: well separated groups of rods and dots dorsally, but not aggregated into discrete groups ventrally. Ecological notes: frequent; eggs found from May to September, with a small peak at the end of May and a larger one at the end of August and early in September; strong adult habitat preference for areas with long grasses, but eggs found on other herbaceous plants,. notably brassicas, often in the absence of aphids; eggs usually laid in batches. 34. 16. Platychirus albimanus Fabricius Pellucid white, remaining so on development; mean length = 931/4(n = 83, range = 865 - 990/0, mean width = 387/4; rounded at both ends; surface patterning of faintly impressed oval rings, shiny. Chorionic sculpturing: dots and rods both dorsally and ventrally, clearly separated into groups dorsally though these are irregularly-margined (fig. 2.C), ventrally with little tendency to aggregation. Ecological notes: common; eggs found from April to October; wide host acceptance range; eggs laid singly.
17. Platychirus scutatus Meigen Pellucid white usually turning biscuity-brown on development; mean length = 924/1-(n = 182, range = 840 - 10419107 mean width = 387, rounded at both ends; surface patterning of faintly impressed oval rings, shinY. Chorionic sculpturing: groups of dots and rods both dorsally and ventrally, more regularly margined dorsally (figs . 2.A, 2.B). Ecological notes: comon; eggs found from May to October; wide host acceptance range; eggs laid singly. 35. 18. Platychirus peltatus Meigen Off-white, turning pinkish-brown at tip on development; mean length = 107210(n = 143, range = 960 - 1255,#) mean width = 4090; tapering slightly towards one end; surface patterning of faintly impressed oval rings, shiny. Chorionic sculpturing: dorsally, units are of dots and rods centrally and strands radiating outwards around the periphery (fig. 2.D); ventrally, dots and rods unevenly distributed but not grouped (fig.2.E). Ecological notes: frequent; eggs found from May to October, increasing in, abundance as the season progresses. Marked preference for brassicas. Eggs usually laid in small batches, sometimes in the absence of aphids.
191 Platvchirus manicatus Meigen Off white, darkening too greyish white on development; mean length = 1088/6,(n = 140, range = 920 - 1175/4 mean width = 427A; bulbous and rounded at both ends; surface patterning of obscure, faintly impressed oval rings, shiny. Chorionic sculpturing: dorsally, dots, rods and strands not divided up into groups (fig.2.0; ventrally dots and rods aggregated into clearly defined groups (fig.2.H). Ecological notes: frequent; found from May to September, with a peak late in August; wide host acceptance range; eggs almost invariably laid singly. 36. 20. Scaeva pyrastri Linnaeus White, becoming greyer on development; mean length = 1135/11,(n = 2119 range = 1000 - 123*), re= width = 4110A; tapering towards one end; surface patterning cristulate, the crests frosted and the supporting lamina translucent. Chorionic sculpturing: dorsally, branching strands arising from axis overlain by central area; frequent contact between branches of neighbouring units (fig.3.14); ventrally groups of dots and rods with the margin strongly infolded and with occasional fine, pointed side-branches (fig.3.0). Ecological notes: common; found from June to October; wide host acceptance range; eggs laid singly.
21. Syrphus luniger Meigen White, darkening slightly on development; mean length = 976/4(n = 233, range = 890 - 1135,4, mean width = 373/4; tapering slightly towards one end; surface patterning cristulate, the crests frosted and the supporting lamina translucent. Chorionic sculpturing: dorsally, branching strands arising from axis overlain by central area; frequent contact between branches of neighbouring units (fig.3.F); ventrally groups of dots and rods with the margin substantially infolded (fig.3.I). 37. Ecological notes: common; found from April to November; wide host acceptance range; eggs laid singly.
22. Syrphus corollae Fabricius 'White, darkening slightly on development; mean length = 965,0(n = 212, range = 800 - 1109u), mean width = 373/44 tapering slightly towards one end; surface patterning cristulate, the crests frosted and the supporting lamina translucent. Chorionic sculpturing: dorsally, branching strands arising from axis overlain by central area, frequent contact between branches of neighbouring units; ventrally, groups of dots and rods with the margin only slightly infolded (fig.3.0). Ecological notes: common; found from May to October; wide host acceptance range; eggs laid singly.
23.Chrysotoxum cautum Harris Nhite; mean length = 885/14(n = 56, range = 745 - 1175/0, mean width = 387, rounded at both ends; surface patterning of studs that are frosted and clearly defined, consisting of many strands vertically orientated and densely packed. Chorionic sculpturing: extensive ramifications, very similar dorsally and ventrally, consisting of axes with side-branches, overlain by central areas, branches 38. rather blunt..ended (fig.3,H); central areas particulate, less evident ventrally. Ecological notes; eggs were not found in the field but gravid females were taken frequently from May to September, with a peak in early June; eggs laid singly in the laboratory. (The larval nutrition of the genus Chrysotoxum is unknown, but from the morphology of the larva (e.g. Heiss, 1938) and the adult (Glumac, 1960), it is thought to be aphidophagaus.)
24. Xanthogramma citrofasciatum Degeer White, darkening slightly on development; mean length = 875/4(n = 62, range = 820 - 920,4)7 mean width = 4oqm rounded at both ends; surface patterning definitely knobbled, consisting of studs with the translucent central area upraised. Chorionic sculpturing: extensive ramifications, very similar dorsally and ventrally, consisting of axes with side-branches, overlain by central areas, branches rather blunt-ended; central areas translucent, less evident ventrally. 39. Ecological notes: eggs were not found in the field, but gravid females were frequently taken from May to August, with a peak in May; eggs usually laid in the laboratory in response to Aphis fabae Scop. and laid singly. (Hoalldober (1929) describes the larvae of this species as living in Lasius nests nurtured by the worker ants and refusing aphids when these were offered, but other species in the genus have been recorded as undovptedly aphidophagous - X, divisa (Metcalf,1917), X.(= Ischiodon) aegyptium (Barbosa,1953), X grandicornis (Hughes, 1963), X. ornatum (Sharma,1966) - and it is to be expected that X. citrofasciatum is facultatively so.)
25, Syrphus latifapciatus Macquart Cream or yellow, deepening in colour on development; mean length = 933)4(n = 256, range = 770 - 1040A, mean width = 369/4; tapering strongly towards one end; surface patterning often not all evident dorsally, but traces of sinuous ridges usually discernible at the tips of the egg and faint white plates laterally. Chorionic sculpturing: dorsally, axis with simple branches rarely contacting those of neighbouring units; 40. branches blunt-ended, essentially confined to two dimensions (fit;.2.M)3 ventrally, units particulate, margins infolded and some short, straight side-branches. Ecological notes: frequent; eggs found from May to October; strong preference for Aphis fabae Scop.; eggs laid singly.
26. Syrphus triangulifer Zetterstedt Pellucid white; mean length = 980/4.(n = 41, range = 880 - 1089A, mean width = 373,4 elongate; dorsal surface shiny, patterning at most faintly sinuate dorsally, more evident laterally. Chorionic sculpturing: dorsally, axis with simple branches rarely contacting those of neighbouring units; branches square-ended, essentially confined to two dimensions (fig.2.N); ventral sculpturing of large dots evenly distributed. Ecological notes: infrequent; eggs found from May to August, primarily a spring species, but a small second generation in August/ found most frequently on shrubs; eggs laid singlY. 41. 27. Syrphus punctulatus Verrall White; mean length = 1115/t (n = 54, range = 1010 . 1215a.), mean width = 3810:5 slightly rounded at both ends; surface patterning of frosted white plates with quite sharply defined edges. Chorionic sculpturirig: dorsally, axis with extensive branches overlain by central area, frequent contact between branches of neighbouring units (fig.4.I); ventrally, large dots and rods evenly distributed. Ecological notes: common spring species; eggs found during May and June; restricted host acceptance range, primarily found on Pine and Spruce; eggs laid singly.
28. Sphaerophoria menthastri Linnaeus Off-white, turning brown on development; mean length = 897/1-(n = 127, range = 840 - 979Q, mean width = 32/4 rounded at both ends; surface patterning of opaque plates slightly upstanding, usually about twice as long as wide, but sometimes hunched up laterally and patterning appears crest-like as in Syrphus luniger, although the units are less than five times as long as wide. Chorionic sculpturing: dorsally, axis irregularly thickened with extensive branches overlain by central area, frequent contact between branches of neighbouring units (fig.4.M); ventrally, irregular groups with few 42. large dots and rods centrally and branching strands peripherally (fig.4.N). Transition zone between dorsal and ventral types of sculpturing of at least four rows, some units with central area absent and axis present. Ecological notes: frequent; eggs found from May to October but predominantly at the start of the season; wide host acceptance range; eggs laid singly, not infrequently on the upper surface of the leaf.
29. Sphaerophoria scripta Linnaeus Offawhitel ,turning brown on development; mean length = 888/e (n = 221, range = 800 - 1100/4, mean width = 373/44 rounded at both ends; surface patterning of opaque plates slightly upstanding, usually about twice as long as wide, but sometimes hunched up laterally and patterning appears crest-like as in Syrphus luniger, although the units are less than five times as long as wide. Chorionic sculpturing: as in Sphaerophoria menthastri but sharp demarcation between dorsal and ventral types of sculpturing, axis never present if central area absent. Ecological notes: common; eggs found from May to October; wide host acceptance range; eggs laid singly, not infrequently on the upper surface of the leaf. 1+3 30.Syrphus balteatua Degeer White, usually greying slightly on development; mean length = 1029(n = 233, range = 880 11a0JQ, mean width = 35a; slightly rounded at both ends, surface patterning of frosted white plates with wavy edges. Chorionic sculpturing: dorsally, particulate central area with fine side branches frequently in contact with those of neighbouring units, axes obscure or absent (fig.4.C); ventrally, discrete particulate units, more irregularly margined than in Syrphus auricollis and with fine-pointed, inconspicuous side-branches mid ventrally as well as latero-ventrally (fig.4.F), Ecological notes: found from March to October; not common during.spring but abundant from June to August; very wide host acceptance range; eggs not always laid singly.
31.Syrphus auricollis Meigen Alta, sometimes greying slightly on development; mean length = 956,10,(n = 59, range = 890 - 1010A, mean width 373p; slightly rounded at both ends; surface patterning of frosted white plates with wavy edges. Chorionic sculpturin4g: dorsally, particulate central area with fine side branches frequently in contact with those of neighbouring units, axes obscure or absent; 44. ventrally, discrete particulate units, more regularly margined than in Syrphus balteatus and without inconspicuous side-branches mid-ventrally although these are present latero-ventrally. Ecological notes: frequent; eggs found from May to September, but always much less commonly than those of Syrphus balteatus; usually found on shrubs, particularly Berber's and Sarothamnus; eggs laid singly.
32. Melanostoma mellinum Linnaeus White; mean length = 98l/b(n = 240, range = 890 - 1o7w, mean width = 387p4 rather bulbous, strongly rounded at both ends; surface patterning of small, frosted white plates or striations. Chorionic sculpturing; dorsally, axis with short side - branches, no contact between neighbouring units, central area small and inconspicuous (fig.2.J); ventrally, sinuous strands, dots and rods irregularly arranged, mid-ventrally aggregated into semi-discrete groups (fig.2,10. Ecological notes: common; eggs found from May to Octobers quite wide host acceptance range) eggs often found in the absence of aphids, usually laid in batches. 45. 33. Melanostoma scalare Fabricius White; mean length = 1056 (n = 264, range = 850 - 1270,,.), mean width = 440/4 notably bulbous and strongly rounded at both ends; surface patterning of small frosted white plates or striations. Chorionic sculpturing: as for Melanostoma mellinum but mid-ventrally dots, rods and strands showing no aggregation into discrete groups (fig.2.L). Ecological notes.: common; eggs found from April to October;, very wide host acceptance rangei eggs often found in the absence of aphids, often laid in batches.
34. Baccha obscuripennis Meigen White, darkening slightly on development; mean length = 1051/b (n = ) 4, range = 990 11350, mean width = 400/43 rather bulbous, rounded at both ends; surface patterning of rows of inconspicuous, small whitish striations very slightly upraised. Chorionic sculpturink: dorsally, axes with side branches only occasionally in contact with those of neighbouring units; slight, non-particulate central areas, axes clearly visible (fig, 3.M); ventrally, groups of dots and rods (fig.3.N). Ecological notes: frequent; eggs found from May to October, with peaks in May and August-September; adult habitat preference for shaded regions; wide host acceptance range; eggs laid singly, 1+6. 35. Syrphus cinctus Fallen White; mean length = 1072/6(n = 13, range = 1010 !- 1129Q, mean width = 387)4i slightly rounded at both ends; surface patterning of small whitish plates or striations. Chorionic sculpturing; dorsally, axes with side branches only occasionally in contact with those of neighbouring units; slight, non-particulate central areas, axes clearly visible (fig.2.F); ventrally, large dots and rods not aggregated into groups. Ecological notes: frequent; eggs found from May to August; primarily a spring, speciesbut with a small second generation in August; marked association with Phyllaphis fagi L, on Beech, but found also on Oak and Sycamore; eggs laid singly. 47 .
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M N 550 IV. DISCUSSION There is a high degree of structural diversity in the chorionic\pculpturing of the eggs of those species of aphidophagous Syrphidae described above, varying from simple dots fairly evenly distributed over the whole chorion, as in Pyrophaena granditarsa, to intricate, three-dimensional branching networks as in Chrysotoxum cautum. It is possible to see how the more complex patterns might be derived from the simpler ones, as, for example, in the following series, which refers only to the sculpturing of the dorsal surface of the egg.
In Platyclarus scutatus (fig.2.A) the dots are aggregated into groups and in P, manicatus (fig.2.G) they have apparently coalesced or extended into rods and short branches; in P. peltatus (fig.2.D) this is even more evident; in Syrphus glaucius (fig.4.D) there are irregular branching units of greater extent and 1ielanostoma mellinum (fig.2.J), Baccha obscuripennis (fig.3.N) and Syrphus umbellatarum (fig.303) show a series in which the same basic type of structure is progressively more developed.. In Sphaerophoria menthastri (fig. 4.M) the ramifications extend upwards into the surface folds and in Chrysotoxum cautum (fig.3.H) the units are extensively interlinked and the sculpturing even more 56.
intricate. It is not suggested that this sequence represents in any way a specific evolutionary series, but it appears likely that the more complex sculpturing has arisen from the simpler type along such general lines during the course of evolution.
It may be noted that according to our present understanding . of the phylogeny of the aphidophagous Syrphidae (Glurnac,1960) based on larval morphology and the structure of the adult male genitalia, the main genera are derivable from Platychirus and helanostama and that Sphaerophoria is probably the most recently evolved genus of those studied in this paper. Although Glumac placlesXanthogramma with the Syrphini rather than the Sphaerophorini, it is elsewhere (Verrall,l901, Lundbeck,1916) considered to be most closely allied to Sphaerophoria. There is some evidence, therefore, that the increasing complexity of the sculpturing of the egg in the aphidophagous Syrphidae parallels, in the most general terms, the phylogeny of the group.
No attempt has been made by the author to correlate the properties of the chorion with its structure. Although Bhatia (1939) has shown that syrphid eggs will hatch as normal if the chorion is removed during 57. development and hence that this is not vital for successful maturation of the embryo, Hinton (1960, 1962) has described the sculpturing of the eggs of various Diptera in relation to the operation of the chorion as a plastron and sculpturing may have a similar role in Syrphidae.
Since the eggs of aphidophagous syrphids are laid in essentially similar microhabitats (on the stem or underside of leaves of growing plants) and since the environmental conditions faced by those species studied here are essentially similar, it may be valid to consider the increased complexity and depth of sculpturing primarily as a general trend towards improvement of the protective capacity of the egg-shell rather than as a series of specific evolutionary responses by individual species to local conditions; in which case similarity of structure suggests evolutionary affinity or equivalent level of evolutionary development.
The great range of form seen in the species examined is indicative of the plasticity of the basic system and likelihood of two quite unrelated species showing similarity of structure is low, though present, and is proportionately lower the more intricately patterned the chorion i.e. unrelated species at the same level of 58. evolutionary development would be unlikely to have similar sculpturing and the latter, therefore, implies phylogenetic affinity.
It is a striking feature of the sculpturing of the eggs that on the ventral surface the structure is very often simpler than that on the dorsal surface, rarely the same and never more complex. This provides support for the view that the sculpturing has a protective capacity since the dorsal surface is the more exposed, but it also provides, particularly in those species where the transition between dorsal and ventral types of sculpturing is gradual, indications of the way in which modifications in structure take place and the lines along which different species have developed.
These points may be summarised into the following hypothesis: 1. The more complex the sculpturing, the more recently has the species evolved.
2. Similarity of sculpturing between different species indicates a natural affinity between them.
3.-Where pre sent, gradual change in sculpturing from dorsal to ventral surface of the egg provides an insight into the phylogeny of the species. 59. In general our existing knowledge of group affinities is confirmed by this study and structural resemblances are very marked in the eggs of known closely-related species. Some similarities between the chorionic sculpturing of different species are considered below.
Platychirus albimanus, P. scutatus and P. clypeatus have similar structures and Pyrophaena granditarsa has sculpturing more closely related to these than have Platychirus peltatus and P, manicatus.
The sculpturing in Syrphus nitidicollis is notably simple and remarkably similar to that of P. scutatus. It is almost identical with that in S. grossulariae Mg. and S diaphanus Zett. (uncommon species not included in the key) and confirms Goffe (1952) in grouping them together into the genus Epistrophe Wlkr, 1852. However, his fourth member, S. eligans has a markedly different structure, one that has evident similarity to Syrphus glaucius and Leucozona lucorum. The difference in structure between the eggs of Syrphus eligans and S. nitidicollis is surprising in view of the close conformity in their adult (Goffe„ 1952) and larval (Dixon, 1960) morphology and their close relationship must be considered established. 60. The other surprising difference in egg sculpturing in species clearly related in larval morphology is between Syrphus latifasciatus and S, luniger; Scaeva pyrastri has a chorionic structure much more similar to that of Syrphus luniger and S. corollae than does S. latifasciatus, which shows features more in common with S. triangulifer and S. cinctus, This placing of Scaevt pyrastri is in agreement with Hull (1949).
Syrphus balteatus, S. auricollis and S. cinctellus form a natural grouping which agrees with Goffets genus Episyrphus Mtsma, 1917, but S. auricollis and S, balteatus are more similar to each other than to S. cinctellus.
Goffets genus Stenosyrphus Mtsma, 1917, however, contains species with grossly different chorionic patterning, Syrphus lasiophthalmus shows in both dorsal and ventral sculpturing a similarity to S. ribesii and S. vitripennis that is most unlikely to be accidental; it shows no great similarity to any of the other species examined in the genus Stenosyrphus. Syrphus umbellatarum and S. compositarum Verrall appear identical, but cannot obviously be related to any other Syrphus species studied, except perhaps S. cinctus. The dorsal sculpturing of S. punctulatus is quite distinct from 61. that of S.JAaiophthalmu and S. umbellatanum, its nearest similarity being to the S, balteatus group.
The integrity of Goffets genus Syrphella Goffe, 1944 (S. alhostriqtus Fall., S. tricinctus, S. arcuatus Fall., S. venustus Mg. and S. lunulatus), is confirmed in toto, with the exception that eggs of S. arcuatus have not been seen.._ The chorionic sculpturing is notably complex.
As with both adult and larval studies, there is no clear indication from the egg sculpturing of the affinities of the genus Chrysotoxum.
The chorionic structure is very similar in the genera Melanostoma and Baccha and also in S. cinctus, but since the patterning is very simple, the similarity may be incidental,
The sculpturing of the egg in the genera Pipizella and Pipiza is interesting in that it is quite unlike that found in any of the other aphidophagous Syrphidae studied. However, it resembles that in the genus Volucella Geoffroy 1762 in the following particulars: 62 1)indication of longitudinal grooving 2)overall fine, granular stippling of the chorion 3)'cellular' sculpturing (fig.2.,I) in those species where the pattern is at all evident.
Again, in view of the simplicity of structure, no close relationship can be adduced,
The surface patterning is very similar to that of the egg of Cnemodon vitripennis Mg. as figured by Delucchi et al. (1957). 63 . VI SUMMARY
A key to the eggs of 35 species of aphidophagous Syrphidae occurring in Britain is given, followed by a fuller description of each and figures of the ma3.or forms of chorionic sculpturing. Ecological notes are provided and the emphasis is on rapid identification of eggs from the field.
The validity of using variations in chorionic microstructure as an indicator of phylogeny is discussed and an hypothesis presented which is considered in relation to our existing knowledge of group affinities; it provides some support for Goffels attempt (1952) to subdivide the vast genus Syrphus Fabricius 1775, but indicates a marked heterogeneity of the proposed genus Stenosyrphus Matsumura 1917, and predicts that natural affinities-will be found between certain species hitherto unrelated by systematists. 64,
SECTION B,
SONE HOST PLANT FACTORS AFFECTING SIRPHID OVIPOSITION 65.
SOME HOST PLANT FACTORS AFFECTING SYRPHID OVIPOSITION
I. INTRODUCTION
Volk (1959) found that aphid odour was the most important component of the stimulus pattern for oviposition by Syrphus corollae Fabr. and that host plant factors were of little significance. Wadley (1931), Banks (1952), Rattan Lal and Lal Gupta (1953), George (1957), Bombosch (1958) and Hughes (1963) observed syrphid oviposition only on infested plants close to aphids. Metcalf (1916), Heiss (1938) and Dunn (1949) found an occasional egg on uninfested plants. Schneider (1948) records that eggs laid in the absence of aphids are sterile. Peschken (1965) claimed that neither "the species of plant nor probably its colour" influenced oviposition. However, Dixon (1959) has shown the attraction of gravid S. luniger Mg. females to green poles and Chandler (1967b) records marked syrphid oviposition on uninfested plants. The role of the plant is studied in this paper. 66.
II. HOST PLANT SELECTION
1. Oviposition on uninfested plants Syrphid oviposition was recorded weekly throughout the season from July to October 1965, on a plot of brussels sprouts (Brassica oleracea gemmifera L.), 12 x 12 plants, 3i ft apart. One half of the plot was maintained aphid-free by treatment with Menazon wettable powder as a root application at a dosage rate equivalent to 4 lb/acre (recommended agricultural application rate = 1 lb/acre). The other half was untreated and open to natural attack by aphids, predominantly Brevicoryne brassicae L. Syrphid eggs were counted each week on 20 uninfested and 10 infested plants, all randomly selected. The eggs were removed from the plants with a fine brush and identified to species (see Section A.). The results, summarised in Table 19 show the response of each species to the two categories of plant.
The experiment shows that many eggs were laid on the uninfested plants, mostly by Platychirus peltatus Mg. and Melanostoma spp. The Syrphus species laid more eggs than these on the infested plants, but far fewer on the uninfested ones. TABLE I. Syrphid oviposition on infested and uninfested brussels sprout plants INFESTED PLANTS UNINFESTED PLANTS Frequency with which I Frequency with which eggs were found of Total Total eggs were found of Total stated batch size no. x 2 stated batch size no. Species of of eggs , eggs 1 2 51 6+1 laid 1 2 bf laid Syrphus balteatus Deg. k 7 8 10 1 0 0 308 616 37 2 0 0 0 0 41 S.luniger/ corollae 79 0 0 0 0 79 158 0 0 0 0 0 0 0 S.ribesii L. 30 3 0 0 0 36 72 1 0 0 0 0 0 1 Sphaerophoria scripta L. 49 0 0 1+9 98 4 0 0 0 0 0 34 Platychirus clypeatus Mg .• 1 4 3 1 3 51+ 108 0 0 0 1 0 0 4 P.alhimanus Fabr/ scutatus Mg. 90 0 0 0 90 180 3 0 0 0 0 0 13 P.peltatus Mg. 9 37 27 9 3 222 444 7 50 49 10 2 1 320 M.spalare Fabr/ mellinum L. 11+ 11+ 7 63 126 15 17 6 0 0 o 67 TOTAL NO. OF EGGS 901 1802 480 the conversion makes the counts for the 10 infested plants directly comparable with those for the 20 uninfested plants per sample. 68. The possibility that the Menazon treaLment had affected syrphid oviposition other than by destroying aphids was investigated. Two experiments were carried out from September 1st - 17th, 1964 to compare oviposition on Menazon-treated aphid-free plants (dosage rate 4 lb/acre as above) with that on untreated aphid-free plants. The untreated "control" plants were kept free of aphids by daily removal of immigrants.
In the first experiment potted field beans (Vicia faba L.) were used and in the second potted brussels sprouts. In both experiments 12 Menazon-treated plants were set up in a row in a fallow field 1 ft. apart. A parallel row of 12 "control" plants was set up 15 ft. away. Five counts of syrphid eggs on the plants were made at 3-4 day intervals. The results are presented in Table II.
TI.,BLE II. Comparison of syrphid oviposition on Menazon-treated and untreated aphid-free plants
Host plant No.eggs laid No.eggs laid on Menazon- on untreated treated plants plants Field Beans 0 0 Brussels Sprouts 47 42 It is concluded that the insecticidal treatment did not alter the attractiveness of the host plant to ovipositing syrphids. 69. 2. The species of host plant Although P. peltatus eggs were laid freely on uninfested brussels sprouts (Table I), none was found on uninfested beans (Table II). The direct response of this species to the two host plants was therefore studied further in the absence of aphids under caged conditions.
Gravid females of P. peltatus taken from the field were confined in a field cage approximately 12, x 61 x 81 with terylene net sides and polythene roof. A bucket of flowers (Solidago virgaurea L.) was provided as a source of pollen and nectar for adult nutrition. The experiment was conducted from September 21st - October 10th, 1965. 12 pots of aphid-free bean plants and 3 of aphid-free brussels sprouts, giving approximately equal leaf areas, were provided for oviposition.
In a total of 5 counts, 271 eggs were found on the brussels sprouts and 7 on the beans. It is concluded that P, peltatus markedly preferred the sprout plants.
3. The appearance of the host plant Oviposition by various species of aphidophagous Syrphidae on two colour forms of the same variety of brussels sprout was investigated. In addition to the 70 . normal form of the commercial variety Irish Elegance, a 'glossy' form lacking the superficial waxy bloom (North & Priestley, 1962) was used. Plants of the latter type have a slightly different growth form, minimised under potted conditions, and appear notably lighter green in colour.
Equal numbers of potted plants of each type were placed on the ground in a large field cage. In some cases the plants of both categories were infested, in other uninfested. The numbers of eggs laid on these plants by different species were recorded at intervals during the seasonsl965 and 1966. The totals are given in Table III and the relative preferences of the different species are shown in Figure 1.
Syrphus species normally lay very few eggs on uninfested plants (Table I), but under caged conditions as the females age progressively more eggs may be laid on suitable host plants in the absence of aphids (Chandler 1967a). Advantage was taken of this behaviour to investigate the response to the two types of plant independent of the aphid stimulus. 71.
TABLE III. Numbers of eggs laid by different svphid species on two forms of the same variety of brussels sprout plant
Aal, INFESTED PLANTS UNINVESTED PLiiNTS WEED' laid LAYING SPECIES Waxy Glossy / Waxy Glossy. Uaid ON on INFESTED Glossy glossy PLANTS 1 , young S.balteatus 400 419 51.2 9 80 89.9 S. ribes14 83 80 49.1 20 48 70.6 S.vitripennis Mg. 54 66 55.0 - - _ S.luniger 382 325 45.8 77 81 51.3 S.corollae 30 24 44.4 - - - P.scutatus 89 57 39,0 47 5 9.6 P.peltatus 84 32 27.6 393 40 9.2 P.manicatus Mg. 19 7 26.9 9 1 10.0 Sphaerophoria spp. 10 6 37.5 22 3 12.0 Melanostoma spp. 60 16 21.1 82 28 25.5
old S.luniger 223 207 48.1 - - - S.ribesii 19 87 82.1 - - . S.balteatus 139 382 73.3 - - -
72.
UNINFESTED INFESTED
P. PELTATUS P. SCUTATUS 10 P. MANICATUS -/j SPH. SCRIPTA
- 20 MELANOSTOMA SPR
MELANOSTOMA SPR 3dd A
3 P. MANICATUS
38 P. PELTATUS ▪ 30 3 N 3
SPH. MENTHASTR I P. SCUTATUS - 40
S. COROLLAE - S. LUNIGER S. RIBESII - SO S. LUNIGER S. BALTEATUS
S. VITRIPENNIS
- 60 r 0
S. RIBESII - 70
ld k
- SO 383d3 30N
S. BALTEATUS - 90
PERCENTAGE OF EGGS LAID ON GLOSSY PLANTS
FIG.I COMPARISON OF NUMBERS OF SYRPHID EGGS LAID ON WAXY AND GLOSSY FORMS OF THE SAME VARIETY OF BRUSSELS SPROUT PLANT 73. The results show that:- 1) The Platychirus species all had a tenfold preference for waxy over glossy plants if they were uninfested, but this preference was much less marked if the plants were infested.
2). Syrphus balteatus and S. ribesii preferred the glossy plants when both types were uninfested, but not if the plants were infested, unless the females were very old.
3)Syrphus luniger had no particular preference even when induced to lay on uninfested plants.
4)Melanostoma spp. preferred the waxy plants and were relatively unaffected by the presence or absence of aphids.
5)Sphaerophoria spp. responded more similarly to the Platychirus species than to the Syrphus species.
Thus the different species showed different preferences and some could seemingly discriminate and select plants on the basis of their appearance, although a differential contact stimulus may also have mediated oviposition (see Section IV). 74. III OVIPOSITION SITE SlURCTION
Fluke (1929), Dunn (1949) and George (1957) describe oviposition by aphidophagous Syrphidae as normally confined to the underside of leaves, although Campbell and Davidson (1924) record it as occurring indiscriminately over infested plants. However, the distribution of eggs on the plant was not studied quantitatively. This is investigated in this section, as far as possible independent of the aphid stimulus, which itself influences the site of oviposition (see Section D.).
The experiment was conducted in a 20°C, 16 hour daylength controlled environment room using about 20 laboratory-reared S. balteatus females provided with potted bean plants for oviposition. Six different sites were considered on the host plant: the dorsal and ventral surfaces of the leaf, dorsal and ventral surfaces of the stipules, the growing shoot and the stem,
Oviposition on plants heavily infested with Lrhis fabae Scop. was compared with subsequent oviposition on uninfe seed plants . The experiment lasted from May 26th - June 8th, 1965 and the results are given in Table IV. 75. TABLE IV. Sites on bean plant chosen for oviposition by, Syphus balteatus
OVIPOSITION . OVIPOSITION INEhSTED BEAN UNINFESTRID PEAN SIEE SITE AS % NO.OF OF PLANT Nu. OF SURFA10E EGGS EGGS LiIIDgo LAID %
Leaf ventral 29.6 237 44.1 134 43.9 Leaf dorsal 29.6 42 7.8 33 10.8 Stipule ventral 6.3 144 26.8 75 24.6 Stipule dorsal 6.3 8 1.5 '10 3.2 Shoot 14.6 81 15.1 39 12,8 Stem 13.6 26 4.8 14 4.6
TOTAL 100.0 538 100.0 305 100.0
There was no evident difference in the distribution of eggs on the plant whether aphids were present or absent. However, both distributions varied markedly from random oviposition over the plant surface, many more eggs being laid on the ventral surface of the leaves and stipules than would occur by chance.
IV. T[ INFLUENCE OF THE SUBSTRATE Eggs of aphidophagous Syrphidae are usually laid singly, although species of Melanostoma and Platychirus often lay small batches of eggs (Metcalf 1916, 1917; Campbell and Davidson l924; Fluke 19299 Dixon 1959). 76 . The tendency of various species to lay in batches and the extent to which the surface upon which the eggs are laid might affect the batch size are investigated here.
The term "batch" is defined as the number of eggs
laid side by side at one time by one female. Eggs laid end to end or near to but not touching one another are not considered as being in one batch.
The numbers of syrphid eggs laid per batch on A. fabae infested potted bean plants was recorded throughout the season of 1965 in the field and during 1966 in field cages. The results are given in Table V.
The numbers of eggs laid per batch was also investigated on brussels sprout plants (infested and uninfested2 waxy and glossy) and on the walls of transparent polystyrene cages. Oviposition on polystyrene usually occurred when gravid females were confined for several days in small boxes of the transparent material with muslin-covered holes in the side and provided with an adequate supply of hazel pollen2 sugar solution and water for nutrition. Since oviposition occurred in the absence of both host plant and aphids, it is assumed that the major external influence upon the batch size was the contact made with the substrate. The results are given in Table VI. 77. TABLE V. The numbers of eggs laid in batches by various syrphid species on Aphis fabae-infested bean plants
Total Mean no Species no. eggs h ,. ,. h ,- Per/ 0 0 0 o eggs tc -I- -P tc -P -P laid batch cd cd cj c3 /ba 6/ba H c\i 3 —I Is%
Scaeva pyrastri L 1032 1 - - 1034 1.001 Syrphus luniger 691 1 - - - - 693 1.001 S. corollae 1751 4 - - - - 1759 1.002 S.latifasciatus Macq. 1331 6 1343 1.005 S.ribesii 1504 97 13 5 1 1 1768 1.091 S.vitripennis 1048 7 . - 1062 1.007 S.balteatus 271937 5 - - 2808 1.017 S.auricollis Mg. 259 5 269 1.019 S.punctulatus Verrall 37 - - - 37 1.000 S.lasiophthalmus Zett. 58 , - - - - 58 1.000 S.triangulifer Zett. 40 - - - - - 40 1.000 S,umbellatarum Fabr. 87 - - - - - 87 1.000 S.eligans Harris 83 - - 83 1.000 S.nitidicollis Mg. 124 - - - - - 124 1.000 Leucozona lucorum L. 379 2 - - - 383 1.016 Baccha obscuripennis Mg. 42 - - - 42 1,000 Sphaerophoria scripta 297 - - - 297 1.000 Platychirus scutatus 850 3 - - - 856 1.004 P.albimanus 335 4 _ _ _ - 343 1.012 P.manicatus 269 1 - - - - 271 1.004 P.peltatus 851 11 5 1 2 - 136 1.308 Melanostoma scalare 71130 1 2 - - 142 1.365 Kanthogramma citrofasciatum Deg. 59 2 - 63 1.033 Pipiza noctiluca L. 154, 1 - - - - 156 1.007 Ti,KE VI. The mean batch size of eggs laid by various syrphid species on different substrates
Polystyrene .L.fabae.init B.brassicae- uninfested infested and beans infested waxy waxy sprouts uninfested --sprouts glossy SPECTRS routs No Mean No Mean No Mean No Mean No Mean eggs no. : eggs no. eggs no. eggs no. eggs no. laid eggs/ laid eggs/ laid eggs/ laid eggs/ laid eggs/ batch batch batch batch batch Seluniger 433 1.016 693 1.001 1499 1.002 83 1.025 461 1.002 S.ribesii 157 1.137 1768 1.091 402 1.098 69 1.151 50 1.111 S.balteatus 62 1.033 '808 1.017 1673 1.0;9 424 1.053 96 1.055 Sph.scripta 375 1.000 297 1.000 97 1.000 76 1.000 - _ P.scutatus 93 1.000 856 1.004 1290 1.006 47 1.000 57 1.000 P.manicatus 66 1.031 271 1.004 424 1.014 183 1.011 - _ P.peltatus 115 1.278 136 1.308 682 2.545 2011 2.652 120 1.414 M.scalare 149 1.290 142 1.365 80 1.702 123 1.685 - _ M.mellinum 108 2.700 - - 505 3.686 110 3.793 100 3.571 79. There is no appreciable difference in the mean number of eggs per batch laid on the polystyrene or infested beans. However, on average P. peltatus and M. scalare laid more eggs per batch on brussels sprouts than on beans and P. peltatus also lays more per batch on the waxy than the glossy sprout plant. The mean batch size of eggs laid by M. scalare on sugar beet leaves (Beta vulgaris L.) (mean = 1.33, n = 72) and on oak leaves (Quercus robur L.) (mean = 1.31, n = 55) is similar to that found on polystyrene and on bean (Table VI).
In an experiment in which females of M. mellinum L. and M. scalare were confined in separate small polystyrene boxes with a brussels sprout leaf lightly infested with Brevicoryne brassicae, the mean batch size was recorded for eggs laid on the sprout leaf and on the base, sides and top of the container. The results are given in Table VII. 80. TOLE VII. The mean batch size of eggs laid by Melanostoma scalare and M. mellinum under the same conditions on brussels sprout leaves and on polystyrene
Polystyrene Brussels Sprouts Species No. of Mean no. No. of Mean no. eggs eggs/ eggs eggs/ laid batch laid batch
N. scalare 70 1.273 38 2.533 M. mellinum 151 2.041 409 3.298
The mean batch size for each species was notably higher on the brussels sprout leaf.
M. mellinum females were observed whilst ovipositing. Sometimes eggs were laid on the brussels sprout leaves whilst the females were clinging to the polystyrene walls or resting on the cage base. The mean batch size for such eggs was similar (m = 3.20, n = 48) to that for all the eggs laid on the brussels sprout leaf rather than the polystyrene (Table VII). 81. —V. DISCUSSION
It is surprising that some aphidophagous syrphid species lay fertile eggs freely on uninfested plants. Platychirus peltatus shows a positive oviposition response to brussels sprout plants per se, yet the larva is aphidophagous, the author having reared it successfully in the laboratory on Aphis fabae, Brevicoryne brassicae and Acvrthosiphon pisum Harris. However, it may be only facultatively so. Other aphidophagous species have been recorded as feeding on alternative foods: Xanthandrus comtus Harris on larvae of Lepidoptera (Smith, 1936; Lucchese, 1942; Schneider, 1953) and Coleoptera (KAger, 1926); Melanostoma mellinum on adults of Musca domestica L., Chortophilla pusilla Mg. (Giard,l896) and larvae of Philedone hyerana Mill. (Chapman 1905); Melanostoma obscurum on decomposing chickweed (Davidson, 1922), and Metasyrphus and Allograpta species on healthy brassica plant tissue (Hamrum 1967). The ability to subsist on diets other than aphids would no doubt increase the chances of survival of species like Platychirus peltatus that often lay in their absence. Observations by the author indicate that the larvae are less voracious and larval development takes longer in 82. Melanostoma species and P. peltatus than in the common aphidophagous Syrphus species.
Oviposition on effectively uninfested plants might result in the utilisation of aphid colonies that are too small to attract the Syrphus species ( Section C.IV ) and would thus decrease inter-specific competition. Perhaps also brassicas, as releasers for P. peltatus oviposition, may by intensive cultivation have become super-releasers (Chandler 1967 b).
The importance of the host plant in oviposition has been shown for P. peltatus. It is suggested that for any aphidophagous syrphid species there is a balance between aphid and host plant factors goberning oviposition. If the aphid stimulus is reduced, by scarcity or absence or because the females are old, the host plant factors become more important. Evidence for this is summarised below.
1) Some species were more dependent upon aphids than others. Under the same circumstances Syrphus luniger laid only near to aphids whereas P. peltatus laid frequently on uninfested plants (Table I) 83 . 2)In general, the species showing least response to aphids showed most to host plant factors, e.g. P. peltatus had a tenfold preference for the uninfested waxy over the uninfested glossy plants, whereas, S, luniger had little or no preference (Table III).
3)Any preferences shown for the waxy or glossy plants when infested were greater when both were uninfested (Fig.l), suggesting an increased reaction to the host plant in the absence of an aphid stimulus.
1.) Old S. balteatus and S. ribesii females preferred infested glossy plants more when they were old than when they were young (Table III). klso old syrphids laid more eggs on uninfested plants than did young syrphids (Chandler 1967a), indicating that ageing decreased more the importance of the aphid stimulus.
The genus Melanostoma is intermediate between purely phytophagous syrphids (e.g. Cheilosia spp.) and purely aphidophagaus ones (e.g. Syrphus spp) (Davidson, 1922; Telford, 1939; Glumac, 1960) and is closely related to the genus Platychirus (Verrall, 1901; Lundbeck, 1916; Glumac, 1960). Possibly the genera diverged, amongst other features, in host plant preference, Platychirus species preferring plants like the waxy brussels sprouts, 81+. Syrphus species preferring those like the glossy plants and Melanostoma species having an intermediate preference. This divergence would help to reduce inter-specific competition. The superimposition of increased orientation to aphids would account for the situation today as summarised in Table III.
If this hypothesis is correct, the plant-location system is the older-established and the aphid-location system gradually replaced it in the evolution of the truly aphidophagous Syrphinae. The development of aphid detector systems may have resulted not only in reduction of the response to the host plant when aphids are present, but in some cases in the loss of some plant responses altogether, as shown by the lack of preference for waxy or glossy brussels sprout plants by S. luniger even in the absence of aphids,
Those species whose adults are markedly aphid- orientated in the field may be referred to as Group I species and comprise largely Syrphus species. They usually lay single eggs close to aphids. Those that are markedly plant-orientated may be termed Group II species and it is to this group that the Melanostoma species and P. peltatus belong. Eggs are often laid in 85. batches on uninfested plants. The separation between the two groups is not absolute, but the distinction has proved helpful in studies on oviposition behaviour.
There was a difference in the mean batch size of eggs laid by M. scalare and M. mellinum on brussels sprout leaves and on polystyrene under the same conditions (Table VII). P. peltatus laid more eggs per batch on sprouts than on beans (Table VI). It is evident that the nature of the substrate influenced the number of eggs laid per batch. When M. mellinum laid on brussels sprout leaves whilst looking at and clinging to polystyrene; the batch size was appropriate to the sprout leaf and not the polystyrene. Whilst it is not possible to discount visual influence; it seems likely that there was a stimulus to the ovipositor from the underlying substrate. The larger batch size laid by M. scalare in response to brussels sprout but not to bean, sugar beet or oak leaves suggests a specific stimulus from the sprout leaves. 86.
VI. SUMMLRY
Although aphidophagous Syrphidae usually lay close to aphids, Platychirus peltatus Mg., Melanostoma scalare Fabr. and M. mellinum L. lay freely on uninfested sprout plants. The existence of a group of species that will lay in the absence of aphid stimulus provides a useful tool for the investigation of oviposition stimuli independent of aphids. Both plant species and plant appearance are important factors in P. peltatus oviposition. More eggs are laid per batch by M. scalare, M. mellinum and P. peltatus on brussels sprout leaves than on bean leaves or polystyrene. 87 .
SECTION C.
THE RELATIONSHIP BETWEEN APHID INFESTATIONS
AND SYRPHID OVIPOSITION. 88.
THE RELATIONSHIP BETWEEN APHID IlahSTATIONS AND SYRPHID OVIPOSITION
I. INTRODUCTION Banks (1953) showed that t1-.ere was a positive correlation between the number of syrphid eggs laid on a bean shoot (Vicia faba L.) and the number of aphids (Aphis fabae Scope) present, but that very heavy aphid infestations were avoided. Dixon (1959) found that eggs were laid very close to Acyrthosiphon spartii Koch on broom (Sarothamnus scoparius L.) and that more eggs were laid the larger the aphid colony. However, van Emden (1963) working on brussels sprout plants (Brassica oleracea gemmifera L.)infested with Brevicoryne brassicae L. found no correlation between the number of syrphid eggs and the number of aphids present; nor did Bombosch (1963) in relation to colony size of Aphis fabae on sugar beet (Beta vulgaris L.) except at very high levels of general crop infestation. Such contrasting results indicate a need for further study.
The current investigation was conducted in four stages: firstly, the response of the species complex as a whole to different levels of aphid infestation was studied in 89. a field experiment. Secondly, the response of different syrphid species to the size of aphid populations was studied under caged conditions. Thirdly, an attempt was made to investigate the importance of the distribution of aphids as distinct from ,their - density, on the host plant. Fourthly, visual responses to aphids were studied.
II. FIELD RECORDS OF OVIPOSITION BY SYRPHIDAE 1. Oviposition on brussels sprouts infested with Brevicoryne brassicae 96 brussels sprout seedlings, variety Irish Elegance, were planted on May 25th, 1964 as eight plots of 12 plants each, surrounded by at least 20 yards of fallow soil which was regularly ploughed. (The plot layout was determined by the requirements of another experiment) ( see page 118). Each plot was caged with a wide-meshed nylon net to exclude birds, but permitting free passage to insects. The plants were artificially infested with B. brassicae on July 20th and supplemented on July 22nd. Counts were taken on July 24th, 26th and 28th, and August 3rd and 7th; the same four plants per plot were examined at each count. The weather remained fine and sunny throughout the experiments.
Aphid infestations on each plant were categorised visually as shown in Table I. 90. TABLE, I. Categories of aphid infestation in 1965 experiment on syrphid oviposition on brussels sprouts
ICAT&GORY INFESTATION ESTIkATa OF APHID NUMBERS
1 Extremely light 50 - 300 2 Very light 301 - 700 3 Light 701 - 1,500 4 Light - medium 1,501 - 3,000 5 Medium 3,001 - 5,000 6 Medium - heavy 5,001 - 10,000
7 Heavy 10,001 +
Syrphid eggs were carefully counted on each plant. The numbers laid in batches and the relationship of each egg or batch to the nearest aphid colony were recorded. Three categories of proximity were distinguished: eggs laid close to aphids (V), eggs laid on the same leaf as aphids but not clearly in relation to them (S) and eggs laid on leaves without aphids CO.
160 plants were examined and a total of 1801 eggs Vas recorded from the 145 plants considered in this study (15 were excluded owing to marked attack by Cecidomyids or other causes). 91. Equivalent counts of syrphid eggs were also made on a large plot of brussels sprouts of the same variety, treated with soil-applied Menazon to maintain the plants free of aphids, which was situated on the same field less than 100 yards away (Infestation Category = 0). The results are presented here for comparison with the oviposition response on the infested plants. loll results are summarised in Table II which shows that the total number of eggs laid by syrphids rose with increasing level of aphid infestation up to a maximum level (about 5,000 aphids), beyond which it decreased progressively. Some oviposition occurred even when the plants were uninfested.
2. Oviposition on sugar beet infested with Lphis fabae Syrphid oviposicion on sugar Leet was recorded throughout the season in 1965. 18 sugar beet seedlings were planted out into the field on May 10th and counts were taken weekly from June 21st until October 25th. Syrphid eggs were identified to species (see Section A.) and the natural level of aphid infestation was estimated for each count. The results are given in Table III.
The table shows that oviposition by the Syrphus species was closely related to the presence of aphids while Melanostoma scalare was largely responsible for the eggs laid on plants without aphids. TABLE II. Fj J,d ovip os it ion by syrphids on uninfested and *bras sicae infested sprout s
INFESTATION NO .OF TOTAL SINGLE BATCHED NO .OF mEAN I MEAN MEAN MEAN MEAN CATEGORY PILiaTT4 NO .OF EGGS EGGS BATCIES NO. , NO. NO. NG . NO. i EGGS EGGS/1 SINGLE BATCHED BATCHES/ BATCHED PLANT EGGS/ EGGS/ PLANT EGGS/ PLANT PLANT BATCH
0 220 314 66 248 78 1.43 0.30 1.13 0.35 3.18 1 2 if 2 2 1 2 ,,00 1.00 1.00 0.50 2.00 2 14 74 61 13 5 5.29 4.36 0.93 0.36 2.60 3 23 207 140 67 21 9.00 6.09 2.91 0.91 3.19 If 70 91+7 763 181+ 63 33.53 10.90 2.63 0.90 2.92 5 17 350 293 57 19 ,20.59 17.21+ 3.35 1.12 3.00 6 10 150 11+1 9 3 15.00 11+.2.0 0.90 0.30 3.00 7 9 69 63 6 2 7.67 7.00 0.67 0.22 3.00
TOTAL 365 2115 1529 586 192 5.79 4.19 1.61 0.53 3.05 -__ 93. TOLE III. Syrphid oviposition on sugar beet, 1965.
Number of eggs per 18 plants I Group I :1G roupII
9
cd H F.4 al tus tus Kean no. CI) H H tus F-1 of tto H v) W ta ta H 0 0 tea H roup Group l l Aphis z ro ,c? u c e V) I II s p fabae/ r9 9 11 ba rn. ggs eggs Date • • • .
plant P S . m P . Z
21.JUN 33 0 0 0 0 6 0 0 6 30JUN, c.200 0 0 5 0 9 0 0 14 0 7. JUL c.300 2 0 5 6 1 0 0 ( 14 0 13 .JUL c.250 1 1 11 3 1 0 0 117 0 19 ,JUL 61 0 0 0 0 1 0 0 1 0 30.JUL 7 0 0 0 1 0 0 2 1 2 5. AUG 7 0 0 0 2 1 0 0 3 0 13..UG 0 0 0 0 0 0 0 4 0 4 20.AUG 0 0 0 0 0 0 0 18 0 8 26.0G 0 0 0 0 6 0 I 0 0 0 0 2. SEP 0 0 0 0 0 0l 0 14 0 14 9. SRP 0 0 0 0 0 0 0 7 0 7 15.SEP 0 0 0 0 0 0 2 10 0 221SEP 0 0 0 0 0 0 0 8 0 29.SEP 0 0 0 0 0 0 0 7 0 7 7. OCT 0 0 0 0 0 0 0 2 0 2 14.0CT 0 0 0 0 0 0. 0 0 0 0 25.0CT 0 0 0 0 0 0 . 0 0 0 0 94.
III. EXPERIKENTS ON OVIPOSITION BY DIFFERENT SYRPHID SPECIES
In view of the differences in syrphid behaviour found in the sugar beet experiment, oviposition by individual species was investigated in large field cakes. 1. Cage experiments on oviposition on sprouts Four wooden-framed cages each measuring 121 x 61 x 81 were used in these experiments. Each had a roof covered with polythene sheeting and walls of terylene net. Buckets of cut flowers (usually Senecio jacobaea L. or Solidago virgaurea L.) and dishes with pads soaked in water and sugar solution (with 0.255, nipagin to inhibit growth of micro-organisms) were provided as food for syrphid adults.
The experimental plants comprised B. brassicae- infested potted sprouts about 9" high. The aphid populations were estimated carefully, and to facilitate assessment the heart leaves and buttons of the sprouts were removed before the experiments so that aphid infestations were fully exposed.
Two experiments were conducted with sprouts. Seven plants were used per experiment with levels of infestation increasing in steps (see Tables IV and V) 9 5 . from 0 to about 400 aphids in the first and 0 to about 5,000 in the second experiment. Care was taken to try and keep the aphid populations !healthy' and the plant growth vigorous, but for dense populations this was not easy. The uninfected plants were kept aphid-free by root treatment with a systemic insecticide (Menazon) which is known not to alter the attractiveness of the plants (..see page 68 ).
A minimum of 3 counts was made for each species studied. Females were obtained from the field and the number present during each experiment varied between about 4 and 15 according to the species. The eggs were removed with a fine brush during each count and transferred to a moist, black filter-paper on which they were subsequently identified in the laboratory.
The experimental pots were randomly distributed about 1 ft. apart. The relative positions were changed after each count. The results of the two experiments are given in Tables IV and V.
Table IV shows that the Syrphus species, Scaetra pyrastri L. and Platychirus albimanus Fabr. laid more eggs with increasing aphid infestation per plant and few or no eggs in the absence of aphids. Platychirus peltatus Mg. and P„manicatus Mg., however, showed no TABLE IV. Variation in syrphid oviposition with Brevicoryne brassicae infestation on brussels sprouts, 6-16th September 1966
0 1-1 U) 4-) 4-3 U) U) ii a.) 4-) -P cd
ca s -P P4 wri 0 cts F-i -H 4-)
ibe 4-)
Ci(A • r -H cd a) . F-1 cd S H CQ Ca cD. •r-i 7._ of No.of No:..of No No c? No No No ac eggs eggs eggs 5 eggs eggs % eggs % eggs % eggs % <4 - 0 0 0 0 0 0 0 0 0 2 0.87 2 2.98 9 11.69 22 8.03 1 50 11 4.95 4 4.71 •13 4.98 2 1.94 25 10.97 5 7.46 20 25.97 46 16.79 2 100 11 4.95' 4 4.71 18 6.90 2 1.94 27 11.84 8 11.94 6 7.79 43 15.69 3 150 21 9.46 10 11.76 26 9.96 5 4.85 34 14.92 12 17.91 17 22.08 33 12.05 4 200 26 11.72 14 16.47 53 20.31 17 16.51 35 15.3514 20.90 9 11.69 57 20.80 5 300 67 30.18 23 27.06 54 20.69 36 34.95 40 17.54 11 16.42 6 7.79 26 9.49 6 400 86 38.74 30 35.29 97 37.16 41 39.81 65 28,5115 22.39 10 12.99 47 17.15
TIL 100.0 85 100.0 261 100.0 103 100.0 228 100.0 67 100.0 77 100.0 274 100.0 97. clear densitp.dependent oviposition response and laid many eggs on the uninfested plant.
At high aphid densities (Table V) the Syrphus species, Scaera pyrastri and Platychikts scutatus laid increasing numbers of eggs with increasing aphid population up to an optimum beyond which the numbers laid decreased. P. manicatus seemed to prefer about 100 B. brassicae per plant, P. scutatus about 1000 and S. ribesii about 2000 aphids. The numbers of eggs of 121 , peltatus laid on a plant and the level of aphid infestation were not clearly related.
2. Cage experiments on oviposition on beans A similar experiment to the above was conducted using pots of bean plants infested with A. fabae. 6 pots were used and the infestation per pot increased from 0 to about 500 aphids in five steps as shown in Table VI. Counts were taken on August 4th, 7th, 9th and 11th, 1966.
4s for brussels sprout plants, P. manicatus seemed to prefer about 100 aphids per plant, whereas St balteatus preferred at least 500 aphids. TABLE V. Variation in syrphid oviposition with Brevicoryne brassicae infestation on brussels sprouts 25th August - 11th September 1966
d r ion tion 6.1uniger Sc.pyrastri,S.ribesiiJ P.scutatus P.manicatus P.peltatus te t ri - ta la d d
u No. i No. No. No.; No. No. t eo fes tima hi hi
op of of j of of 1 of of ----- ap in ca Ap p Es
, - eggs 5o egg eggs' % eggs cA eggs 6:, eggs ,::
0 0 0 0 0 0 0 0 7. 3.78 19 6.99 30 26.09 1 50 13 2.17 5 3.07 10 1 3.36 10 5.41 53 19.49 14 12.17 2 100 62 10.35 20 12.27 25 8.39 12 6.49 63 23.16 24 20.87 3 400 119 19.87 32 19.63 33 11,07 2010.81 51 18.75 14 12.17 .1+ 000 165 27.54 36 22.09 64 21.48 63 34.05 31 11.39 13 11.30 5 000 160 26.71 47 28.83 98 32.88 46 24.86 34 12.50 6 5.23
6 F5000 80 13.36 23 14.11 68 22.82 27 14.60 21 7.72 14 12.17. TOTAL 599 100.0 163 00.0 29a 200.0 185 100.0 272 100.0 115 100.0 99. TABLE VI Variation in syrphid oviposition with Aphis fabae infestation on field beans, 4th 11th Aug. 1966
LPHID ESTIMATED S.BALTEATUS P.MANICATUS INFESTATION APHID No. OF No.OF CATEGORY POPULATION EG GS $ EGGS %
0 0 3 0.43 18 15.'3 1 50 61 8.76 23 20,35 2 loo 87 12.50 24 21.24 3 200 112 16.09 19 16.81 4 400 180 25.86 11 9.74 5 500 253 36.36 18 15.93
TOTAL 696 100.0 113 100.0
IV SYRPHID OVIPOSITION IN RELATION TO THE SIZE AND DISTRIBUTION OF APHID AGGREGATES In the last section it was shown that oviposition by most of the syrphid species studied was closely related to the size of the aphid population. It was not established whether the response was influenced by the way in which the aphid population was distributed on the plapt.
This was investigated by (a) studying the oviposition response to aphid aggregations of different sizes and 100. (b) offering a simple choice between plants with similar numbers of aphids distributed in the form of large and small aggregations.
1.Field observations Records of oviposition by individual syrphid species on brussels sprouts were taken on 54 plants in a half-acre plot for the period July 26th - .Lugust 20th, 1965. The sprout seedlings were planted out in the field on May 11th and were about 2ft, high at the time of the experiment. The general level of B. brassicae infestation was low. The aggregates were usually discrete and were categorised as in Table VII.
Table VII indicates preferences for aphid aggregates of different sizes by the various syrphid species. P, peltatus seemed to prefer the smaller aggregates, P. scutatus aggregates of about 21 - 50 aphids and S. balteatus and S. luniger the largest ones. Sphaerophoria scripta L. had no evident preference.
2. Cage experiments (a) The previous experiment was repeated under more controlled conditions, in which the total number of aphids per plant was kept approximately equal, so that the importance of the distribution could be studied irrespective of the population size per plant. TABLE VII. Numbers of eggs laid by syrphids in relation to different sized B . bras sicae aggregates 26th July - 20th August 1965
S .baltea.tus S .1uniger S .scripta P .scutatus P .peltatus
te --- G.) a t te te te
a a
a a s
s eg s s
s
bio g g eg g r eg s g g til s g eg 's s a) r g
r
re — r g
a) te eg . te
g te •ao te o 4-) a o.
a a eg o. c1 o an a f f ag f eg f f f eg g f f eg 0 f o /ag cH to n - eg f g /agg n e /agg no. eg /ag n s
e ••. oa) s n r n o o s r - s o n r o
n P o o o
0 ti) g o o g o . g C3 tO *LID u . . e map 0 tx0 No. egg Mea ag No. egg No. Mea No egg No. Mea No. No agg
No. eg Z 03
No Z(1) Mea iz ag I L ag S i
)
\- r 29 1.16 2 2 1 .00114- 17 1.21 15 17 1.13 9 25 • 0 00
j
16 23 • 58 1.76 6 7 1.17 5 6 1.20 1.44 4 13 \J L c.
)
Iv n. • 93 1.94 10 10 1.00 10 12 1.20 9 17 1.89 3 7 co 0o
1 l x
1
o 1.83 1 1 1.00 2 6 3.00 \ tT 28 1.87 6 11 0 0
rt
o cI 2 .14-0 5 6 1.20 8 13 1.63 ‘.. 19 2.71 5 12 0 0 N 1--
1
+ Of 1- ry 26 2.17 2 4 2.00 0 0 - 1 1 1.00 0 0 TOTAL 140 253 1.81 31 46 1.48 35 42 1.20 51 77 1.51 16 45 2.81 102. Six potted sprout plants about 90 high were selected and the heart leaves removed. Known numbers of B, brassicae were enclosed on the laminae in leaf cages until established. The cages were then removed and the aphids thinned out as necessary. Three plants each with four colonies of about fifty aphids were compared with three each with 10 colonies of about 20 aphids. In practice the aphids could not be reliably restricted to discrete colonies, but the two infestation patterns were readily distinguishable. The experiment was conducted in a large field cage. About three female syrphids per species were taken from the field and the eggs that they laid on the six plants were recorded on August 27th, 29th and September 1st. The results are presented in Table VIII. TABLE VIII, Comparison of the number of eggs laid by syrphids in response to the same number of B. brassicae per sprout plant distributed in large or small aggregates Syrphus luniger Syrphus balteatuA Platychirus 1 peltatus Date Large Small !Large Small Large Small colonies colonieS colonies colonies icolonies colonies i 27.AUG.66 29 21 i 12 19 8 5 29 ,AUG.66 37 26 1 28 32 17 10 1.SEPT.66 51 26 I 12 29 12 7 Total . 117 73 1 52 80 37 22 103. Table VIII shows that, for a given aphid population Syrphus luniger preferred a small number of large colonies to a larger number of small ones 2 = 11.32, p< 0.05) but S. balteatus preferred the opposite (e = 8.90, p 40.05). Accepting a 5% probability level as significant, it is evident that the two species show contrasting preferences. Like S. luniger, P. peltatus laid more eggs on the plants with large colonies, but the difference was not significant = 3.84, p). 0.05).
(b) The above procedure was repeated, but with the aphid aggregations more variable in size. Six potted sprout plants 9" high were used, the heart leaves were removed and infestations of approximately equal size per plant (150 aphids) were established using leaf cages as before. The syrphids used were those remaining from the previous experiment. Counts were taken on September 6th, 8th and 10th, 1966, and the results are given in Table M.
Table DC. shows that, for a given aphid population, S. luniger sought out the largest aggregates present on the plants whereas under the conditions of the experiment, P. peltatus selected smaller colonies. The results agree with those obtained from the field experiment (Table VII). 104. TABLE IX. Numbers of syrphid eggs laid in relation to aphid aggregates of different sizes, the total number of aphids per plant being approximately equal Size of Syrphus luniger Platychirus peltatus aphid aggregate No. of No .-of Mean no. No. of No.of Mean no. aggregates- eggs eggs/ aggregates eggs -eggs/ aggregate aggregabe
0 - - - 7' 18 2.57 1-10 13 14 1.08 10 52 5.20 11-20 13 25 1.92 8 42 5.25 21-30 lo 33 3.30 5 23 4.60 31-40 4 15 3.80 2 4 2.00 41-50 10 4a 4.20 0 0 51+ 4 22 5.50 0 0 _ TOTAL 54 152 2.76 32 139 4,34
V. VISUAL PERCEPTION OF APHIDS BY SYRPHUS BALTEATUS Oviposition by S. balteatus in response to two colour forms, green and pink, of Acyrthosiphon pisum Harris on potted bean plants was investigated. The aphids attacked, the shoots as well as the undersides of the leaves and were therefore readily visible from above. About fifteen S. balteatus females collected in the field were enclosed in a large field cage and the experiment was conducted in four parts from July 6th-20th, 1966. Counts were taken every 1-2 days. 105. 1)Equal numbers of potted beans were infested with the green aphid and with the pink aphid and the numbers of eggs laid in response to each counted. Table X, row 1 shows that there was a marked preference for the pink form.
2)Small red dots were painted onto the shoots of three pots of beans. The plants were then infested with the green aphid and the numbers of eggs laid on the red-dotted plants compared with those on three pots of unpainted plants infested with the green form and three with the red form. The results (Table X, row 2) indicate that the paint spots together with the green aphids stimulate oviposition as much as the pink aphid.
3) The procedure was repeated using plants with white dots instead of red ones, and a similar distribution of eggs was found (Table X, row Therefore it seems that the conspicuousness of the dots and not their colour was responsible for increased oviposition.
1+) A fourth category of plant infested with green aphids and with the upper surf ace of many of the leaves conspicuously red-banded was included, there being more paint on the red-banded leaves than the red-dotted shoots. Oviposition was recorded for all four categories and 106. the results (Table X, Tow 4) show that the syrphids laid no more eggs on the red-striped plants than on the unpainted plants infested with green aphids. It was not possible to continue the experiment as the females had now ceased laying.
TABLE X. Eggs laid by Syrphus balteatus in response to visual stimuli
-P
H U) U) 4- to P U) rd 4—ct -P rd + rn•r-1 0 a) 4 4-) 4 ca,0 o) re) RI 0 p4 0 •ri tiCs g m cd -P 0 cd 0 ca car-I 0 ca ri .• F-t id 0 a) 0 .0 0 a) h0 •W O (1)O a) ri) Sri rd a) -I-I 4-) -Pctl 0 tIC) cd r•A 114 OOk Pr El a) P-1 g
1 499 306 ONO Ole 805 1.63 2 155 71 161 387 2.18
3 lao 59 gimp 127 1.10 306 2.03 Li- 90 22 64 20 196 4.09
VI. DISCUSSION Ovipositing Syrphus balteatus females laid more eggs on plants infested with the pink form than the green form of Acyrthosiphon pisum. If the shoots of bean plants infested with the green aphid were painted with red or white dots, as many eggs were laid as on the plants infested with the pink aphid. However, increasing the 107. conspicuousness of plants by banding the upper surfaces of leaves with red paint did not affect the numbers of eggs laid on them. Apparently the syrphids were attracted by a specific optical pattern that resembled aphids.
As the females aged, there was an increasing tendency to lay amongst the pink aphids rather than the green ones (Table X). It has been suggested that the importance of the aphid stimulus relative to the plant stimulus declines as syrphids age ( see page 83 ). Seemingly, also, the olfactory component of the aphid stimulus decreases in importance relative to the optical component as S. balteatus ages.
It is evident that the optimum size of aphid population for oviposition by young syrphids varies according to the species. The preferences are not as clear in the Platychirus species as in the Syrphus species, the latter showing a density-dependent response except at very high aphid densities (Table V) when they tend to avoid aphids.
It appears that even after a plant has been selected for oviposition there is still selection for suitable aphid colonies on that plant (Table VIII), 108. so, there are not only different optimm population sizes for different syrphids, but also different optimum colony sizes, resulting in selection of specific sites for oviposition on the chosen plant.
Evidence has been presented that aphidophagous syrphids may conveniently be divided into two categories differing in oviposition behaviour ( see page 84 ). Members of the first group, comprising mostly the Syrthus species, tend to lay single eggs in the near vicinity of aphids. Members of the second group, comprising certain Melanostoma and Platychirus species, tend to lay eggs in small batches often on uninfested plants.
At the time of the initial field experiment on brussels sprouts (Table II), the method for identifying syrphid eggs had not been developed. However, the graph comparing the responses of syrphids laying single eggs with those laying batched eggs (Figure 1), and that comparing the numbers of eggs laid close to and distant from the aphids (Figure 2)7 are very similar and give an approximate indication of the response that would have been shown by Group I and Group II syrphids. 20 20 TOTAL EGGS — TOTAL EGGS •••• SINGLE EGGS •••• V+S EGGS
--- BATCHED EGGS • • --- X EGGS • • • 1
• • • I5 I 5
: 10 1 0
5 5
....•• • 40.--...... "‘ • • .... ---. ..."' • • z • -.. S. e • •••. • ------• -- _, •,_ _..... S. .-• i I I t I I I. t t t t• .. O I 0 I 0 I 2 3 4 5 6 7 0 I 2 3 4 5 6 7 CATEGO RY OF APHID INFESTATION CATEGORY OF APHID INFESTATION H FIG I GRAPHS SHOWING THE RELATIONSHIP BETWEEN SYRPHID OVI POSITION AND THE LEVEL OF 2 APHID INFESTATION CATEGORISED ACCORDING TO (a) BATCH SIZE OF EGGS (b) PROXIMITY OF EGGS TO APHIDS. (SEE TEXT) 110. The overall response appears to have been largely due to the Group I species, although at low levels of infestation the behaviour of the Group II species, which are much less density-dependent (Tables IV and V) is important.
The data presented earlier in this paper concerning syrphid oviposition on B. brassicae-infested brussels sprouts show that density-dependent oviposition would be expected when there are more than a few hundred aphids per plant, but not when there are very few. Thus the lack of correlation between the presence of B. brassicae and syrphid oviposition recorded by van Emden (1963) is no doubt related to the relatively small aphid infestations that he studied.
The Group II species lay only rarely on beans ( see page 115) and syrphid oviposition is due almost entirely to Group I species. It is to be expected, therefore, that studies involving beans as host plant would show at all times a density-dependent syrphid oviposition and this has been found by Banks (1953) and Peschken (1965). On broom Dixon (1959) records, where species were identified, that Syrphus luniger, S. vitripennis Mg., S. nitidicollis Mg. and Platychirus scutatus Mg. laid most eggs. All, including P. scutatus which lays single eggs near aphids, are Group I species. Moreover, the eggs on broom were laid close to aphids. It is inferred from this data that Group II oviposition was at most low and hence that the overall response would be density-dependent, as was recorded.
The finding of Bombosch (1963) that syrphid oviposition and A. fabae population size on sugar beet were correlated only when there was a high general level of aphid infestation, suggested that there was a marked Group II response at the lower densities as on brussels sprouts. The experiment on sugar beet described earlier (Table II) confirms the response of Group II species to this host plant; the Group I species were attracted when the level of aphid infestation was high, but later in the season when the aphids had disappeared, the Group II species alone were attracted.
The evidence of differential oviposition behaviour obtained in this work has therefore helped to explain the discrepancies between the results of previous investigations on the relationship between syrphid oviposition and aphid population size. 112 . VI. SUMMARY Oviposition by aphidophagous Syrphidae varies with the size of aphid infestations. The reponses of different syrphid species were investigated and it was found that they have different optimum aphid population sizes for oviposition. In one experiment using potted brussels sprout plants infested with Brevicoryne brassicae
L., Platychirus manicatus Mg. seemed to prefer about 100 aphids per plant, P. scutatus Mg. about 1000 and Syrphus ribesii L. about 2000 aphids, These preferences are not as clear in certain Platychirus species, notably P. peltatus Mg., as they are in the Syrphus species (e.g. S. luniger Mg.). Above the optimum level of aphid infestation the response falls away.
Once a plant has been selected for oviposition there may still be selection of suitable colonies on that plant. Fox a given aphid population, S. luniger significantly preferred a small number of large aggregates to a larger number of small ones, whereas S. balteatus Deg. significantly preferred the opposite. The tendency of the different species to select aphid populations of different size is likely to decrease interspecific competition. 113 .
SECTION D .
SOME FACTORS INFLUENCING THE OCCURRENCE
AND SITE OF SYRPHID OV IP OS ITION . 114.
SOME FACTORS INFLUENCING TI OCCURRENCE AM OF SIRPHID OVIPOSITION
I. INTRODUCTION
Some of the independent effects of host plant and aphid factors on oviposition by aphidophagous syrphids have already been described (Sections B &C). Interactions between factors are now considered, with particular reference to the interacting effects of aphid and plant on the site at which the eggs are laid and on the possibility of stimulus carry-over, defined as occurring when a stimulus received at one site influences a respon,ze at another.
II. STIMULUS CARRY-OVER
Ibbotson (1960) has shown that Oscinella frit L. females, although attracted by oat seedlings, nevertheless lay most eggs on neighbouring soil, which provides a better tactile stimulus for oviposition. The possibility of an analogous situation in which syrphids are attracted by one plait and lay elsewhere is investigated in this section. 115.
1. Aphid stimulus Pairs of potted bean plants (Vicia faba L.), one pot heavily infested with Aphis fabae Scop. and the other maintained free of aphids by treatment with Menazon, were set up 6" apart over an area of about twenty acres and a range of arable and wooded habitats. In six counts taken from August 1st - 18th, 1965, a total of 124-pots in each category was examined. Syrphid eggs were removed from the plants, counted and identified (Table I). Those of Platychirus scutatus Mg. could not be reliably separated from P t albimanus Fabr., or of Syrphus Iuniger Mg. from S. corollae Fabr.
TABLE I. Syrphid oviposition =pairs of bean plants, one infested and one uninfested.
No. of eggs No. of eggs Species laid on laid on infested plants uninfested plants Syrphus balteatus Deg. 327 0 S.luniger/corollae 41 0 S. ribesii L. 132 0 S.latifasciatus Macq. 287 0 S.umbellatarum Fabr. 1 0 S.triangulifer Zett. 2 0 Scaeva pyrastri L. 2 0 Sphaerophoria, scripta L. 13 1 Platychirus peltatus Mg. 0 1 P. manicatus 0 3 P.albimanus/scutatus 24; 2 Melanostoma scalare 1 0 Baccha obscuripennis Mg. 10 0 TOTAL 1109 7 116,
It is evident that in general there is no effective carry-over stimulus to the uninfested plants. However, Platychirus manicatus laid only on the uninfested plants and this coupled with other records of eggs on uninfested plants in the field suggested that its behaviour should be investigated further.
Six gravid P. manicatus females taken from the field were confined in a field cage approximately 121 x 61 x 8' with terylene net sides and polythene roof. Pots of flowers (Potentilla recta macrantha) were provided for adult nutrition. Twelve uninfested potted bean plants or six heavily A. fabae-infested plants and six uninfested ones were provided for oviposition during the period July 30th - August 16th, 1966. The pots were distributed in random order with a space of 62 between each. The numbers of eggs laid on the two categories of plant were recorded and the results are presented in Table TABLE II. Oviposition by Platychirus manicatus on infested rind uninfested bean plants Day No.of potted bean plants No. of eggs laid on Infested Uninfe sted Infested Uninfested
4 0 12 1 7 6 6 2 12 8 6 6 7 16 6 6 2 9 11 6 6 8 14 13 0 12 1 16 0 12 0 17 6 6 6 23 117.
In the absence of. aphids in the cage there was negligible oviposition. When infested plants were present eggs were laid on both infested and uninfested plants, but predominantly on the latter. It appears that the response to the uninfested plants is increased by the presence of aphid infestations in the vicinity and that for this species there is a carry-over of the aphid stimulus.
2. Adult food stimulus Mature female syrphids utilise two different host- finding mechanisms, the one directed towards a suitable adult food source and the other towards a suitable oviposition site. Nectar, or honeydew, and pollen are necessary foods for ovarial maturation and syrphids acre commonly observed feeding on flowers (Schneider, 1948).
The possibility that flowers might increase oviposition on neighbouring aphid-infested plants is of considerable practical importance (van Maiden 1964). Conversely, it is possible that satiation of feeding might lead to a repulsion from the region of the flowers and consequently to relatively low oviposition in the neighbourhood. 118. The role of flowers close to oviposition sites was investigated first by recording the number of eggs laid on small replicated plots of aphid-infested brussels sprouts with and without flowers, and secondly by recording the response to uninfested brussels sprouts with and without flowers, in the absence of a complicating aphid stimulus.
Eight plots of brussels sprouts in two blocks of four were planted 28 yards apart separated by bare soil. Each plot was 12 ft. square and comprised twelve plants, four per side. Each plot was caged with J' mesh netting to exclude birds while permitting free passage to insects. The plants were artificially infested with B. brassicae and five counts of syrphid eggs were made on four plants per plot at 4-day intervals between July 27th and August 12th, 1964.
Throughout the period of the first three counts buckets of flowers were placed in the centre of plots 2, 4, 6 and 8, the other four plots acting as controls with centres of bare soil. The plots were weeded and the flowers replaced regularly; neither weeds nor flowers were an appreciable source of aphids. Yellow flowers (Senecio jacobaea L.) were chosen because adult syrphids 119. are known to be attracted to this colour (Ilse, 1949; Parmenter, 1952; Volk, 1964) and feeding was frequently observed, During the period leading up to the fourth count flowers were removed from all plots and before the fifth the experimental and control treatments were reversed. The results are summarised in Table III. Table III. Comparison of numbers of eggs laid by syrphids on plots of aphid-infested brussels sprout plants with and without flowers
Plot Count 1 Count 2 Count 3 Count 4 Count 5
2 Y ai 1 22. 56. 45 43 4 86 2/ az 47 50 6 20 88, 60 18 13 8 41 2 41 32 47 Total 178 /DI 194 142 153
1 40 104 69 48 46 3 35 60 39 26 21 5 38 144 54 29 3.i 7 38 40 35 29 ga Total 151 348 197 132 130 Underlining indicates counts on plots with flowers
The table shows (count 4) that the plants in the two series of plots evoke a similar total oviposition response irrespective of the presence of flowers.
120. In the first three counts a total of 672 eggs was laid in the presence of flowers and 696 in their absence. In the last count, in which the control and experimental plots were reversed, the numbers of eggs laid on the two categories of plot were again very similar. Thus flowers in the near vicinity of aphid infestations did not increase syrphid oviposition.
The effect of flowers on oviposition on uninfested plants was also investigated. A. bucket of Senecio jacobaea, flowers was maintained in the middle of a plot of aphid-free brussels sprout plants previously treated with Menazon. At about 4-day intervals from July 31st . August 19th, 1964 syrphid oviposition was recorded on the surrounding 12 plants and also on an equivalent 12 plants in an adjacent aphid-free plot without flowers in the centre. The results are presented in Table IV. Table IV. Comparison of numbers of eggs laid by sYrPhids on plots of aphid-free brussels sprout plants with and without flowers
Plot 'Count ftuntOountCount Count Count t'.246tal i 1 2 3 4 5 6 With flowers 1 11 8 10 31 46 29 135 Without flowers 28 1 14 35 5 4 23 155 i The number of eggs laid on each category do not differ significantly (p >0.10), so even species that lay in the absence of aphids do not appear to be influenced by the flowers. III. STIMULUS INHIBITION
In this section the possibility is investigated that syrphids are attracted to one plant from a distance but inhibited from laying there by local factors, ovipositing instead on neighbouring plants. Thus Gupta and Thorsteinson (1960) have shown for Plutella maculipennis Curt. that although a plant may provide a sufficient stimulus for oviposition, inhibitory factors may also be present and decrease the response.
Banks (1953) observed that aphidophagous syrphids avoided very heavy aphid infestations on beans and the same has been shown for infestations on brussels sprouts ( see page 92 ), The possibility was investigated that this was because existing syrphid populations deterred further syrphid oviposition.
1. The presence of syrphid larvae Caged syrphid females were presented with six similar brussels sprout plants with approximately equal populations of B. brassicae. Three plants each had eight diapausing larvae of either Platychirus peltatus or Sphaerophoria scripta; the other three plants were free of predators. Diapausing larvae were selected 122. to obviate destruction of the infestations or fouling of the plants with larval gut contents (see next subsection).
The procedure was repeated using uninfested brussels sprout plants. Ten immature Syrphus balteatus larvae were put on three of the plants. The larvae were more conspicuous than in the previous experiment since, unlike the diapausing larvae, they actively searched the available leaf area. They frequently left the plants and were replaced every few hours. The results of both experiments are summarised in Table V.
Table V. Comparison of the numbers of eggs laid by syrphids on brussels sprout plants with and without syrphid larvae
With aphids Without aphids Species With Without With Without larVae larvae larvae larvae Syrphus balteatus 126 146 - S. corollae 53 48 _ - Platychirus scutatus 25 15 3 3 P. peltatus - 85 g6 1 - It is concluded that oviposition was unaffected by the pretence of syrphid larvae on a plant. 123.
2) The presence of syrphid gut contents Aphidophagous syrphid larvae store faeces in the hind gut until about to pupate, diapause or become quiescent, when they are voided as a black smear on the plant. The intestine may be cleared by a single evacuation or by several over a period of days. Thes® voided gut contents might act as visual or olfactory indicators of past syrphid predation and might inhibit oviposition.
Their effect was investigated by the same procedure as was used to determine the influence of syrphid larvae on oviposition. Caged females were presented with six brussels sprout plants, all either B. brassioae infested or all uninfested, three of which had about ten blobs of syrphid gut contents, applied either by the larva itself which was then removed, or by paintbrush. The results are given in Table VI. 124.
Table VI. Comparison of the numbers of syrphid eggs laid on brussels sprout plants with and without syrphid gut contents
With aphids Without aphids Species With gut Without With gut Without contents gut contents gut • contents contacts Syrphus corollae 98 96 - - S. luniger 53 32 - - .S. latifasciatus 39 20 - - S, balteatus 140 194 8 8 S. ribesii 23 24 - - Scaeva pyrastri 23 27 - - Sphaerophoria scripta 11 14 4 1 Platychirus scutatus 112 165 5 9 P. manicatus 52 48 11 7 P. peltatus - - 17 8
Although Platychirus scutatus laid more eggs on plants without gut contents, the Platychirus species as a whole did not select clean plants when there was no complicating aphid stimulus (21+ eggs on plants without and 33 on those with gut contents). Nor did Syrphus species discriminate (374 eggs laid on those with and 361 on those without gut contents). The voided contents 125. therefore do not seem to be used as a "marker" and the habit of retaining gut contents is probably based solely on requirements of hygiene.
3. The presence of syxphid eggs The possibility that gravid syrphids might be deterred from ovipositing on otherwise suitable plants by existing syrphid eggs was investigated in three experiments from August 10th - 18th, 1966. Sterile eggs were used to obviate the possibility of larvae interfering with the experiment.
In the first experiment, caged Syrphus balteatus females were presented with six similar sprout plants with approximately equal B. brassicae populations. Three of the plants had 150 sterile eggs of Scaeva Vrastri placed amongst and around the aphids. Counts of Syrphus balteatus eggs were taken daily and the results are given in Table VII, row 1.
The above experiment was repeated using S. coronae adults and sterile eggs laid naturally by ribesii. The results are given in Table VII, row 2.
The procedure was repeated using Platychirus manicatus as the test species. In one series infested and in another uninfested brussels sprout plants were 126. provided. Sterile Scaeva pyrastri eggs were put on the plants as before. The results are given in Table VII, row 3. TABLE VII, Comparison of the numbers of syrphid eggs laid on brussels sprout plants with and without syrphid eggs already present
Experiment Species With aphids Without aphids With Without With Without eggs eggs eggs eggs
1 S.balteatus 123 111 - -- 2 S.corollae 73 89 - - 3 P.manicatus 23 27 18 15
It is concluded that the presence of syrphid eggs on a suitable host plant did not influence subsequent oviposition on that plant.
IV. THE PRECISE SITE OF OVIPOSITION 1, Proximity of oviposition to edge of brussels sprout leaves In preliminary studies it was noticed that eggs tended to be laid close to the edge of brussels sprout leaves. This was investigated quantitatively. Potted sprout plants about 25 am high were used and the heart leaves and buttons removed so that only the stem and usually eight to ten leaves remained, the largest being about 80 x 80 mm and the smallest about 60 x 60 mm, 127. The plants were either all infested with B, brassic4e such that aphld:s were spread extensively over the ventral surfaces of all the leaves, or all uninfested. The distance between each egg laid and the edge of the leaf was recorded for various species confined in large field cages at intervals during the year 1966. Table VIII shows the mean distances and Fig. 1 the range of variation in position for the different species.
TABLE VIII. Mean distance between eggs and edge of brussels sprout leaf for various species of syrphid Infested plant Uninfested plant. No.of Mean No.of 'Mean eggs distance eggs distance Species laid between laid between egg and egg and edge of edge of leaf (mm) leaf (mm) Sc.pyrastri 111 6.4 S.latifasciatus 5o 6.3
S.Iuniger 319 5.1 .11 time
S.ribesii 486 5.1 IVO
S.vitripennis 29 3.3 OM. WW1
S.balteatus 228 4.9 ••••
Sph.scripta 3o 5.0 •••1 P.manicatus 170 4.0 90 4.8 P.peltatus 223 4.4 39 3.5 P.sautatus 169 2.2 36 2.5
M.mellinum 19 3.2 ft* 128. 20 (a) SCAEVA PYRASTRI 0 "11•MMIMI. U.• 10 0 0
•••=•••••• (Y)SYRPHUS LUNIGER
IL 1 O
30[ to 0 (c) SYRPHUS RIBESII 0 20
0▪ 10 ON•t! 0
to I 02 (d) SYRPHUS BALTEATUS
•11IIM•IMP PM! u. 1 0 0 o • 30 O O 20 (e) PLATYCHIRUS SCUTATUS
LL O 10
0
...1111•1•1•1•=r 30 PLATYCHIRUS PE LTATUS
0 OMR
•Mi!M=MI. 30 (0)PLATYCHIRUS MANICATUS o 20
LL O 10 ov. 0 0 I 2 3 4 5 6 7 6 9 10 >10
DISTANCE BETWEEN EGG AND EDGE OF LEAF (m m)
FIG I PROXIMITY OF SYRPHID OVIPOSITION SITE TO EDGE OF BRUSSEL 5 SPROUT LEAF. 129 . There was a marked tendency for the eggs to be laid close to the edge of the leaf, usually less than 1 cm from the periphery. However, the eggs of the Syrphus species were less restricted to the periphery of the leaf than those of the Platjehirus species (Fig.1).
2. Proximity of oviposition to nearest aphids The optimum aphid population size for eviposition differs for different syrphid species and there may also be selection for particular colonies. Syrphus luniger normally laid only close to aphids whereas Platychirus peltatus laid frequently at distances remote from aphid infestations (Sections B & C). Dixon (1959) also found specific differences in the distance of eggs from the nearest aphid on broom (Sarothamnus scoparius L.). The proximity of syrphid oviposition to aphids was investigated in detail as follows:
Experiments were conducted during the season of 1966 in large field cages using groups of about five syrphid females obtained from the field or reared in the lanoratory. A standard oviposition stimulus was provided. This comprised two potted brussels sprout plants about 24 cm high with the heart leaves removed so that all aphid infestations were exposted. One plant was infested with about 300 B. brassicae and the other, 130. about 30 cm away was uninfested and maintained free of aphids with Menazon. The distance between each syrphid egg and the nearest aphid was recorded up to 30 mm. All eggs laid at a greater distance than this or on the uninfested plant were placed in a single category.
The proximity of oviposition to aphids is shown for various species in Fig. 2, which confirms that Syrphus luniger and Scaeva pyrastri tend to lay very close to aphids whereas Platychirus and Melanostoma species tend to lay many more eggs at a greater distance from the nearest aphid, as already indicated by preliminary data ( see page 67 ).
The mean distance between egg and aphids for various syrphid species is presented in Fig. 3a. This mean value is heavily weighted by the oviposition on uninfested plants, but if such oviposition is discounted (Fig. 3b), some species still lay closer to aphids than others and the order of these as presented on the continuum is substantially unchanged. In general, the more eggs normally laid by a given species on the uninfested plants, the greater the mean distance from the nearest aphid of eggs that are laid on infested plants. 131.
6 0 r SYRPHUS LUNIG EA SCAEVA PYRASTRI 50
40
30
20
I0
0 7767,
60 SYRPHUS RIBESII SYRPHUS BALTEATUS
50
40
30
20
I0
0
50 PLATYCHIRUS SCUTATUS PLATYCHIRUS PELTATUS
40 LL 0 30
20
10
0
60 PLATYCHIRUS MANICATUS MEL ANOSTOMA SPP. 50
40
30
20 o
O 0 1-5 6-10 11-15 16-30 31+ 0 I -5 6-10 11-15 16-30 31+ DI ST ANC E BETWEEN EGG AND NEAREST APHID. DISTANCE BETWEEN EGG AND NEAREST APHID. rn) (inm)
F IG. 2 PROXIMITY OF OVIPOSITION TO APHIDS SHOWN BY VARIOUS SPECIES OF SYRPH1DAE 132 .
o; 0 z m c z - S. COROLLAE S. COROLLAE z - O S. LUNIGER S LUNIGER -n m O SC. PYRASTRI SC. PYRASTRI z S. RIBESII S RIBESII m z 0 \s. S. VITRIPENNIS v n - S. VITRIPENNIS S. BALTEATUS t.; P. SCUTATUS 1:1 • S. BALTEATUS PELTATUS r am P. MANICATUS z MELLINUM/ SCALARE 1* P. SCUTATUS m B L.—I a. SPH. SCRIPTA z T S 0 ARE
NE m 0 z P. PELTATUS
z
GGS SPH. SCRIPTA z
D E -20-
PHI m - 22- P. MANICATUS -4 SYR z M. MELLINUM/SCALARE 24 ▪3N _ - • z -26- ma m —J • CL -28- - 0 < I— -30- VI c-t O ILI LL 0 - 32- Z Z 'Er < 2 0 2 CENTRAL SCALE IN MM. 7-4 0 O
FIG.3 PROXIMITY OF SYRPHID OVIPOSITION TO APHIDS ON BRUSSELS SPROUT PLANTS. 133. 3. EfSec__.boi:2Atpffema- le i.dontheij.oQ_ition behaviour About fifteen laboratory-reared Syrphus luniger females were confined over bare soil in a large field cage in an experiment lasting from August 10th - October 12th, 1965 (Chandler, 1967a). Buckets of cut flowers, predominantly Solidago virgaurea L., were provided for food. Ten potted brussels sprout plants each infested with about 300 B. brassicae were provided for oviposition. The distance between each syrphid egg and the nearest aphid was recorded in counts taken on August 12th, 14th, 17th and 19th. The plants were removed from the cage on August 19th and put back on August 25th, and a fifth count made on August 27th. The results are given in Fig. 4, which shows that the mean distance between the eggs and the nearest aphid increased as the syrphids aged.
Such loss in response to aphids did not occur when the experiment was repeated in 1966 using the same species, at the same time of year, caged over bare soil and with Solidago flowers for food, but with only two brussels sprout plants for aviposition, one infested with about 300 B. brassicae (Table IX). 131+.
SO DAY I DAY 3 Cn =1 06) ••=••••1111, 0n=208) 40 .M1•1•1111,
30
IL 20 0 1 0 \0 1
0 7.7114.-m..-ummamt 7017773:53M1
50 DAY 6 DAY 8
Q1=254) 1=1 84) 40 .1.1••••=11,
19 30 0 20 LL 0
4)) 1 0 0 72-17Thgam
50 DAY 16
40 cr.11.25 6)
30
20
c`:( 1 0
0 O 1 —5 6-10 11-15 16-30 31+ DISTANCE BETWEEN EGG AND NEAREST APHID (mm.)
FIG 4 DECLINE IN PROXIMITY OF OVIPOSITION TO APHIDS BY SYRPHUS LuNi G ER M9. 135.
TABLE IK. Mean distance between egg-laying site and Brevicoryne brassicae in relation to the age of Syrphus luniger
Date No. of Mean distance eggs laid between eggs and nearest aphid (mm)
18.SEPT.66 254 1.32 21.SRPT.66 167 1.26 24.auT.66 108 1.53 27.smoT.66 81 0.98 30.sEpT.66 20 0.55 3.ocT. 66 112 1.84 6.0c T. 66 59 1.32 9.0cT. 66 , 16 1.31
TOTAL 808 1.38
A third experiment using S. luniger and Scaeva pyrastri was conducted with the cage on grass instead of bare soil and with seven potted sprout plants each heavily infested with about 1000 B. brassicae. The results in Table X show that the mean distance increased during the experiment. 136. TABLE X Loss in proximity to large infestations of Brevicoryne brassicae of_ eggs laid by Syrphus luniger and Scaeva pyrastri 1 Syrphus luniger 1 Scaeva pyrastri Date No. of Mean No. of Mean eggs distance eggs distance laid between laid between eggs and eggs and nearest nearest aphid(mm) aphid(mm)
29t kUG.66 107 0,92 19 0.47 5.SEPT.66 152 1.01 73 1.85 8.SEPT.66 109 6,15 82 3.71
From these experiments it appears that, as it ages, Syrphus luniger may lose precision of oviposition in response to B. brassicae, at least in the presence of large aphid infestations.
V. DISCUSSION Although ovipositing syrphids avoid very heavy aphid infestations, this is not because syrphid eggs, larvae or larval gut contents are already present on the plants and although the roles of honeydew contamination and fungus attack have not been investigated it is possible that ovipositing adults are directly deterred by the size of aphid populations ( see page 101 ), 137. Visual response to aphids has been shown for adult female S. balteatus (pages 104-106 ), but Dixon (1959) and Volk (1964) have demonstrated the importance of aphid odour over other oviposition stimuli for S. luniger and S. corollae respectively. Perhaps, therefore, the avoidance of populations larger than the optimum size results from excessive olfactory stimulus which might, in theory, lead to oviposition on neighbouring uninfested plants.
Stimulus carry-over was demonstrated by Platychirus manicatus which oviposited on uninfested beans only when infested plants were also present (Table II). However, there was no evidence of carry-over for Syrphus species (Table I) for which the aphid stimulus is paramount ( see page 84 ).
At least two factors, which interact, were involved in the precise choice of oviposition site. There was a marked tendency for eggs to be laid both close to the edge of the leaf and also close to aphids. P. scutatus, for example, laid over 90% of its eggs within 5 mm of the edge of the leaf and over 70% within 5 mm of the nearest aphids. 138. The evidence that different syrphid species lay eggs at different distances from aphids (Figs. 2 & 3) confirms earlier findings (Sections B & C) that, in general, Syrphus species show a more marked response to aphids than Platychirus or Melanostoma species. Moreover, the larger the aphid infestation preferred for oviposition (see Section C ), the closer a given species tends to lay to aphids (Figs. 2 & 3).
No evidence was found that flowers influenced nearby syrphid oviposition. This is in agreement with Peschken (1965), but contrary to the findings of Fluke (1929), Dixon (1959) and van Emden (1965). However, Dixonls data shows that although peak syrphid oviposition coincided with the flowering of broom, so also did the peak aphid infestation, which may well have been the more important factor. The investigations of Fluke and van Emden were not replicated and adequate attention may not have been given to possible variables such as wind and shade, which might bias adult syrphid distribution, and to aphid infestations on the flowers themselves.
Although close proximity of flowers may not influence syrphid oviposition, shortage of flowers might nevertheless act as a limiting factor, especially in large fields or 139. where large acreages of land are intensively cultivated. Schneider (l940, however, has shown that some syrphids can fly several kilometres a day between overnight and feeding sites. 140.
VI SUMMARY Syrphids were not deterred from ovipositing on suitable plants by the presence of other syrphid eggs, larvae or larval gut contents. Heavy infestations of Aphis fabae L. on bean plants (Vicia faba L.) induced Platychirus manicatus Mg. to lay preferentially on neighbouring uninfested plants. Such "carry-over" of stimulus from one plant to another was not found for Syrphus species. Nor did flowers, a source of adult food, stimulate oviposition nearby.
The site of oviposition in relation to Brevicoryne brassicae L. on brussels sprouts (Brassicae oleracea gemmifera L.) varied markedly according to species: in similar conditions Syrphus luniger Mg. laid over 50% of its eggs touching aphids and less than 1% on uninfested plants, whereas P. manicatus laid less than touching aphids and over 50% on uninfested plants. Most eggs were laid close to the edge of the leaf, especially by Platychirus species, e.g. P. scutatus Mg. which laid over 90% within 5 mm of the edge of the leaf. SECTION E .
HEIGHT PREFERENCES FOR °VIP OSITION 142.
HEIGHT PREFERENCES FOR OVIPOSITION IN APHIDOPHAGaUS SYRPHIDS
I. INTRODUCTION
Different species of Coccinellidas prefer particular heights of vegetation for oviposition (Blackman, 1965; Iperti, 1965) as does the moth Leucoptera spartifoliella Hb. which Agwu (1967) related to the flying height of the females and the greenness of the vegetation. Peschken(l965) found that more aphidophagous syrphid eggs were laid near the ground than at stand height in crops of wheat (Triticum sp.), sugar beet (Beta vulgaris L.) and potatoes (Solanum tubercsum). Studies on the height preferences of aphidophagous Syrphidae are described in this paper.
II. METHODS Oviposition by aphidophagous Syrphidae was recorded on potted field beans (Vicia faba L.) artificially infested with Aphis fabae Scop. throughout the season of 1965 and part of 1966. Pots were fixed to posts at heights of lft, Oft and 6ft in a range of habitats including grass, fallow field and woodland. Similar 1)+3. infestations were maintained at each height and the pots were replaced about every ten days. The eggs laid at each height were counted and identified every two or three days. After each count the pot at Eft was moved to 4ft,, that at Oft to lft and that at lft to 6ft, thereby minimising the importance of differences on aphid infestation.
During 1966 the observations were supplemented by experiments in large field cages 121 x 61 x 81 with sides of terylene net and a roof of polythene sheet; pots were fixed at lft, 4ft and 6ft and alternated after each count as in the field. Where possible, three or six counts were made with each pot at each height for the same length of time. Syrphids used in the cage experiments were either reared in the laboratory or taken from the field. Flowers (Potentilla recta macrantha, Solidago virgaurea L., Senecio jacobaea L. or Raphanus raphanistrum L.), according to the season, provided pollen for foods pads of cotton wool soaked in water and in sugar solution (with 0.25% nipagin to inhibit the growth of micro-organisms) were also provided. III OVIPOSITION HEIGHT PREFERENCE OVER CLASS
When caged over grass different species of syrphid preferred similar heights for oviposition as found for all habitats combined in the field (Fig.l). The compounded data for such cage and field studies are given in Table I. These show well-defined specific height preferences ranging from Syrphus triangulifer Zett.s which laid 69% of its eggs at 6ft and only 5% at lfts to Leucozona lucorum L. which laid only 8r at Eft but 7kio at lft.
IV EFFECT OF AGEING OF FEMALES UPON HEIGHT OF OVIPOSITION
The effect of ageing of the syrphid females on the height of oviposition was initially investigated by comparing the heights at which the first and last hundred eggs were laid by various species on the infested bean pots in the field during 1965 (Fig.2). Thebdistribution of eggs of S. latifasciatus remained the same; the last hundred eggs of S. balteatus were distributed differently from the firsts but the distribution of all the eggs laid differed little from that of the first hundred. However, the first and last hundred eggs of S. ribesii were very differently distributed and the overall height
145.
SYRPHUS BALTEATUS SYRPHUS LATIFASCIATUS
50
GGS 40 E
OF 30
AGE
T 20
RCEN 10 PE 0
FIELD (n.71111 ) CAGE (n.1632) FIELD (ns492) CAGE (n.241)
SYRPHUS COROLLAE SPHAEROPHORIA (SCRIPTA)
50
40 GGS E
OF 30
GE
A 20 T CEN
R I0 PE 0
FIELD (n.216 ) C AGE (n.1097) FIELD (p..79 ) CAGE (n:2133)
❑ 6 FT •® 4 FT 11111 FT
F I G 1 HEIGHT PREFERENCES FOR OVIPOSITION BY VARIOUS SYRPHID SPECIES IN THE FIELD AND CAGED OVER GRASS TABLE I Height preferences for oviposition in the field and when caged over grass shown by various syrphid species __ % eggs laid at lio. of eggs laid each height Species 6ft 4ft lft i Total 6ft Att ,aft Syrphus triangulifer Zett. 2 10 2 1 39 69.2 25.6 5.1 Syrphus lasiophthalmus Zett. 32 23 1 56 57.1 41.1 1.8 Syrphus punctuja;tus Verrall 25 15 2 42 59.5 35.7 4.8 eyrphus eligans Harris 46 38 9 93 49.5 40.9 9.6 Syrphus umbellatarum Fabr. 25 20 7 52 48.1 38.5 13.5 Pipiza noctiluca L. 24 29 12 65 36.9 44.6 18.5 Scaeva pyrastri L. 314 354 268 936 33.5 37.8 28.7 Syrphus corollae Fabr 332 437 328 1097 30.3 39.8 29.9 Baccha obscuripennis Mg. 49 61 53 163 30.1 37)), 32.5 Syrphus auricollis Mg. 26 37 30 93 28.0 39.8 32.3 Syrphus luniger Mg. 239 414 427. 1080 22.1 38.3 39.5 Syrphus balteatus Deg. 526 765 a.059 2350 22.4 32.6 45.1 Syrphus vitripennis Mg. 308 435 618 1361 22.6 32.0 45.4 Platychirus manicatus Mg. 85 94 183 362 23.5 26.0 50.6 Syrphus ribesii L. 390 524 935 1849 21.1 28.3 50.6 Syrphus latifasciatus Macq. 150 207 376 733 20.5 28,2 51.3 latychirus scutatus Mg. 168 379 701 22.0 24.0 54.1 Syrphus nitidicollis Mg15422 36 63 121 18.2 29.7 52.1 Sphaerophoria scripta L. 37 59 122 218 '17.0 27.1 56.0 latychirus albimanus Fabr. 60 117 233 410 14.6 28.5 56.8 Leucozona lucorum L. 3 5 29 37 8.1 13.5 78.4
11+7 .
50
40
30
20
10
0
FIRST 100 EGGS LAST 100 EGGS TOTAL (nsu 492)
SYRPHUS BALTIATUS
60 —
50
40
30
20
10
0
FIRST 100 EGGS LAST 100 EGGS TOTAL(n=718)
SYRPHUS RIBESI I
60
50
40
30
20
10
0
FIRST 100 EGGS LAST 100 EGGS TOTAL 0=1199
El 6 FT ®4 FT ill FT
FIG 2 EFFECT OF AGEING UPON THE HEIGHT OF OVIPOSITION BY VARIOUS SYRPHID SPECIES IN THE FIELD 11+8. distribution was also different from that of the first hundred eggs (Fig.2).
The changes in heights preferred by S. ribesii were investigated in detail from august 20th - September 30th, 1966 in a large field cage. Seven females which had not oviposited were collected in the field. The changing numbers of eggs laid at the three heights confirm that preference alters with age (Table 11). TABLE II Changes in the height of ovinosition in ageing Syrphus ribesii females Height Eggs laid of 1st 2nd 3rd 4th 5th l 6th 7th 8th Total .% oviposition 100 100 100 100 100 100 100 100 6ft 6 7 9 8 22 22 39 57 170 21.3 lift 20 23 26 30 38 37 50 51 255 31.9 lft 74 70 65 62 40 41 11 12 375 +6.8
V. EEQ4CT OF BARE SOIL ON HEIGHT PREFERENCE When caged over bare soil instead of grass from May 21st - June 17th, 1966, S. latifasciatus, S. ribesii, S. balteatus and Leucozona lucorum laid relatively few eggs at lft and more at 6ft, though S. corollae was unaffected (Fig. 3).
11+9 .
SYRPHUS LATIFASCIATUS SYRPHUS COROLLAE
50 O
LIJ• 40 1-
0 30 E G 20 NTA E 10 1- PERC 0 -
GRASS (n=733) SOIL (n=466) GRASS (n=1097) SOIL (n=490)
SYRPHUS R 18E511 LEUCOZONA LUCORUM
70
60 0 o 50
40 O 30 4- GE
20 NTA
RCE 10 PE 0
GRASS (n=244) SOIL( n=305) GRASS (n- 37) SOIL (n=258)
El 6 FT ®4 FT ■1 FT
FIG 3 HEIGHT PREFERENCES FOR OVIPOSITION BY VARIOUS SYR PHID SPECIES CAGED OVER GRASS AND OVER SOIL 150. Height preferences over grass and soil were investigated in the field from June 22nd until July 19th, 1966, using three pots of infested beans on each of eight posts, four over soil and four over neighbouring grassland as shown in Fig. 4a. The results, for the only species that laid significant numbers of eggs (Fig. 4b) show no marked differences in response in contrast to the results obtained in cages.
VI EFFECTS OF VARIOUS SUBSTRATA ON PREFERRED HEIGHT FOR OVIPOSITION OF SYRPHUS BAIJTEATUS. In the first of two cage experiments, bare soil, silver foil and green crepe paper (Ridgway 33 GY-G (b) Vanderpoells Green) were compared with grass, both as a complete floor cover and as a lft border only, with soil in the middle. Young gravid females were used as before and supplemented at intervals.
The results (Fig. 5) confirmed that in cages in contrast to the behaviour in the field (Fig. 4b) oviposition by S . balteatus was altered by a substratum of bare soil. The lft height preference was however restored by a lft-wide turf border and by a substratum of green crepe paper.
151.
• '.;•••••::•:••••••: 0 POST WITH INFESTED BEAN POTS • AT 6 FT. 4 FT AND 1 FT. E] GRASS
0 0 0 SOIL
30 FT 0 0
(a) FIELD PLAN OF EXPERIMENT
SYRPHUS BALTEATUS PLATYCHIRUS (SCUTATUS)
70
60
50
40
30
20
10
0 GRASS (n_407) SOIL (n=122) 1GRASS (n=92) SOIL(nni51 4)
0 6 FT 04 FT 1111 1 FT
(b) SYRPHID OVIPOSITION
FIG 4 COMPARISON OF THE EFFECTS OF GRASS AND BARE SOIL BACKGROUNDS ON THE HEIGHT PREFERENCE FOR OVIPOSITION BY TWO SYRPHID SPECIES IN THE FIELD
152.
60 —
50 S 40 EGG F 30 I. GE O
A 20 T
10 PERCEN 0-
GRASS (n=s275) SOIL (n-1434) SILVER FOIL (n=1613)
JUNE 11-13 JUNE 14-19 JUNE 20-25
50
GGS 40 F E 30 O GE 20 NTA
CE 10 PER 0
TURF BORDER (n=1357) GREEN CREPE PAPER (n -1396) GRASS (n=396)
JUNE 26— 29 JUNE 30 — JULY 2 JULY 3-5
06 FT 134 FT 111111 FT
FIG 5 EFFECT OF VARIOUS SUBSTRATA UPON THE HEIGHT OF OVIPOSITION BY SYRPHUS BALTEATUS UNDER CAGED CONDITIONS (1) 153. In the second experiment sugar beet leaves were distributed as a margin about ift wide round a cage with a soil base. The height preference for oviposition was compared with that for oviposition over both brown (Ridgway 9'" OR -O (m) Light Seal Brawn) and yellow (Ridgway 25 YG-Y (b) Light Greenish Yellow) fabric, and the females were finally confined over grass. Results are given in Fig. 6.
The females were not supplemented during the second experiment and so the effect of ageing was more marked than previously, as indicated by the height preference when caged over grass, which was less marked than for young females (Fig. 5).
The pattern of oviposition in relation to height was similar over soil (Fig. 5) and brown fabric (Fig. 6), but with green leaves in the cage, although these occupied a smaller area than did the soil, the height distribution was more similar to that over grass.
VII DISCUSSION When eggs of a given species were found at one height they were usually found also on plants at the other heights. This is taken as evidence that the height at which a species lays most eggs does not 151+.
SO S 40 GG E F 30 E O 20 - TAG
CEN 10 R PE 0-
BEET LEAVES (n =249) BROWN FABRIC (n=452) BEET LEAVES (n=702)
JULY 27— 29 JULY 30—AUGUST 1 AUGUST 2-4
50 .. GS
G 40 - E F 30 ,- E O
TAG 20 EN C
R 10 PE 0
YELLOW FABRIC ( n=290) GRASS (n=232)
AUGUST 5— 8 AUGUST 9-11
0 6 FT ESI 4 FT 11 1 FT
FIG 6 EFFECT OF VARIOUS SUBSTRATA UPON THE HEIGHT OF OVIPOSITION BY SYRPHUS BALTEATUS UNDER CAGED CONDITIONS ( 2 ) 155.
represent merely a preferred searching zone, but a definite preferred height for oviposition.
In general, the height preferences shown by various syrphid species (Table I) conform well with their habitat preferences. The uniToltins spring species (e.g. Syrphus lasiophthalmus and S. eligans) which occur when aphid infestations are present on trees and shrubs but are uncommon on herbace4,,us plants, tend to prefer 6ft.
The early summer species (e.g. nitidicollis and Leucozona lucorum prefer lft and their oviposition period corresponds approximately with the time when aphid populations on trees and shrubs are failing whereas many aphids are developing on herbaceous plants.
The syrphid species that were common throughout the year (e.g. S. ribesii and S. luniger) did not seem to prefer consistently any particular height. Such behaviour is no doubt advantageous for finding aphids in whatever zone they are most abundant at any particular time. The marked variation in height preferences of S. ribesii with age seemingly ensures exploitation in turn of all habitats. 156.
The substratum influenced height preferences of caged S. balteatus. A substratum of grass or green crepe paper stimulated oviposition at lft but bare soil or brown, silver or yellow fabric inhibited this preference which was restored by a green margin.
It is possible that green acts as a visual landmark from which the ovipositing female can gauge height. This might account for the difference in the height of S. balteatus oviposition in the field (Fig. 4b) and in cages (Fig. 5)2 since in the latter circumstances thare was no green landmark. 157.
VIII STINDIARY
Height preferences for oviposition by various species of aphidophagous Syrphidae were studied by recording eggs laid on potted field beans (Vicia faba L.) infested with Aphis fabae Scop. fixed at heights of 6ft, Oft and lft. Well-defined specific height preferences were found, ranging from Syrphus triangulifer Zett., which laid 69% of its eggs at 6ft and only 5 at lft, to Leucozona lucorum L. which laid only W at 6ft. but 78% at lft. S t ribesii L., which initially preferred 6ft, laid increasingly at lft as it aged.
In cages the colour of the substratum affected height preference. For example, S.,balteatus Deg. behaved as in the field by preferring lft if the base of the cage was covered with grass or green crepe paper, but if the base was bare soil or was covered with brown, silver or yellow fabric, this preference was obscured. 158.
SECTION F.
DISCUSSION OF THE RELEVANCE OF THE PRESENT
STUDIES TO APHID CONTROL PRO GRAIDE S . 159. DISCUSSION OF THE RELEVANCE OF THE PRESENT STUDIOS TO APHID CONTROL PROMAMMES
Syrphids have often been reported as the most important natural enemies of aphids in particular studies (Flake, 1929; Balch, 1952; George, 1957, Bombosch, 1959; van Emden, 1965; Sharma, 1966) but their importance no doubt varies substantially from year to year and place to place.
Although gravid females may search crop fields before aphids immigrate (Dunn, 1949; Bombosch, 1963, 1967), marked oviposition is usually delayed until, the pest population is firmly established (Dunn, 1949; Balch, 1952; Banks, 1953; Dixon, 1959; van Emden 1963). Although massive aphid destruction may occur and population growth be curbed (Way & Banks 1962), the restraint may still be overcome by aphid multiplication (van Emden, 1963, 1965). In such cases the check may even benefit the aphids if the predator thereby retards pest build-up until the host plant has increased in size and can support a larger aphid population (Way,1967). 160, Prolonged heavy depredation without a lasting check to increase in pest numbers is indicative of predators well adapted to their prey and represents a success for Natural Selection but potential failure for pest control programmes, because the prey population is not seriously jeopardised.
When the predator-prey system is finely balanced small changes in a single factor, such as synchronisation, may profoundly influence the size of a pest population and make the difference between control and no control (van Zmden, 1967). But in a complex system where there is marked ecological homeostasis, manipulation of existing predator populations is less likely to provide effective control of native pests than are introduced related species (Pimentel, 1963).
However, it is desirable to study first the ecology of the existing natural enemies to find their potentialities and limitations for pest control. In earlier sections the ecology and oviposition behaviour of various aphidophagous syrphids were considered, and their relevance to aphid control programmes is now discussed. 161. The larvae are voracious feeders, often eating several hundred aphids during their development (Campbell & Davidson, 1924 a and b; Dunn, 1949; Barbosa, 1953; Lal & Hague, 1955; Ninomyia, 1957a; Lgska, 1959; Bombosch, 1963; Sharma, 1966). The prey may be consumed in less than a minute (Ninomyia 1957a) and Barbosa (1953) records 116 aphids eaten in a 4-hr period by Ischiodon aogYptium Wied.
However, the first instar larvae are believed to have very limited locomotory powers and also poor host location systems, searching for aphids at random (Bansch, 1964). It would therefore seem important that the gravid female find a suitable oviposition site so that the newly-hatched larvae have an assured food supply. Moreover the adults, unlike those of Coccinellids, do not feed on aphids and so host detector systems must be well-developed in ovipositing females so that suitable sites may readily be found.
Different syrphid species prefer different optimum aphid population sizes for oviposition (Section C). Those that choose either very large or very small infestations are of particular interest in assessing control potentialities. Scaeva pyrastri L., Syrphus luniger Mg. and S. corollae Fabr. females prefer 162. large infestations (Pages 96 & 98 ), lay close to aphids (Page 131) and their larvae are very voracious (Davidson, 1916; Fluke, 1929; Yakhontov, 1967). Their destructive capacity is therefore high. Moreover the life cycles of such speOias are short and there is no obligatory diapause (Campbell and Davidson, 1924b; Schneider, 1948; Bombosch, 1957; Laska, 1959; Hamrum, 1967) so that several generations may occur each year and infestations be repeatedly and heavily attacked. They are very tgeneralisedt in their host preferences, accepting a wide range of aphid and plant species (Schneider, 1947; Bombosch, 1963; Dugek & Kaska, 1967). For widespread control of established aphid infestations such species should be investigated and Fluke (1929) has suggested the introduction of Scaeva pyrastri into Wisconsin.
The main disadvantage of such species is that they rarely attack incipient aphid populations. However, such levels may be represented to predators as heavy attacks. Bombosch (1962) and Volk (1964) have demonstrated the importance of aphid honeydew in inducing oviposition in Syrphus corollae Fabr, and Hagen & Tassan (1967) are developing a yeast hydrolysate spray, simulating the honeydew production of large aphid infestations, to attract parasites and predators. 163. Such techniques may be of great value in stimulating oviposition on small aphid populations by species whose larvae are most voracious, and in synchronising maximum syrphid attack at the critical period of aphid infestation.
Predation during the initial stages of infestation rather than after establishment would seem to offer greater possibilities for aphid control. Melanostoma scalare Fabr., M. mellinum L. and Platychirus neltatus Mg. prefer small aphid infestations and frequently lay on uninfested plants (Sections B & C). . The larvae of such species have a long developmental period (Davidson, 1922; Fluke, 1929; Dunn, 1949; Dugek & LAska, 1960) and may survive on an intermittent diet of few aphids, supplemented if necessary by non-aphid foods (Page 81). They might therefore prevent aphid population build-up by eating the aphids initially present and, since starved larvae are very active (Dixon, 1958; Bansch, 1964, 1967) and third instars can travel long distances (Kamal, 1927) by !patrolling! the plant they might eat immigrant aphids as they arrived.
Eggs of these species are usually laid in batches (Page 78). Banks (1953) has shown that the nutritive value of one coccinellid egg to a coccinellid larva is 164. equivalent to three aphids. Syrphid larvae readily eat syrphid eggs and, in the absence of aphids, the first-hatched larva may cannibalise the remaining eggs, thus sustaining itself during its search for food elsewhere.
Species preferring low infestations for oviposition may show a marked response to the host plant itself (Sections B & C). Thus small differences in the appearance of brussels sprout plants lead to a tenfold difference in oviposition by Platychirus peltatus and manicatus Mg. Studies on the role of the host plant in syrphid attraction should be pursued.
Peschken (1965) found that syrphids prefer dense stands for oviposition and preliminary experiments by the author indicate that some species, notably SYrphus balteatus Deg. and S. ribesii L. lay relatively fewer eggs on plants surrounded by areas of fallow. Perhaps green colour co-stimulates oviposition (Bombosch, 1963): the use of green backgrounds and green strips providing !channels' for ovipositing syrphids across fallow fields or to increase the greenness of crops at appropriate stages would therefore seem to be worth further study. 165. The main limitation for control purposes so far encountered for syrphids specialising in small aphid infestations is one of synchronisation. In a 3-year study of oviposition on brussels sprout plants P. peltatus laid few eggs during initial aphid infestation of the plants, but the number increased markedly in late summer when the species was more abundant (Chandler, 1967b; and Page 35). Melanostoma species laid predominantly before the sprouts were planted out in the field and again at the end of the season (Page 44). If oviposition by these species could be synchronised with aphid immigration on to brussels sprouts, their control potentialities would be greatly increased.
Syrphids may specialise other than in their preferred level of aphid infestation for oviposition. They may prefer different species of aphid or host plant. Ninomyia (1957b) has demonstrated larval food preferences and has shown that some species (e.g. S. balteatus) have a much wider host range than others (e.g. S. torvus 0.-S.). However, the choice is usually made by the adult in selecting a suitable oviposition site. 166. Pipizella varipes Mg. tends to oviposit on plants of Pastinaca sativa L. with root infestations of Anuraphis subterranea Walker (Heeger, 1858; Dixon, 1959). Cnemodon vitripennis Mg. prefers aphids with flocculent wax secretions on trees and shrubs (Delucchi et al., 1957; Evenhuis, 1959, 1967). Syrphus cinctus Fall4n larvae are most commonly found amongst populations of Phyllaphis fagi L. on beech trees (Dukk & L6ska, 1962; Bombosch, 1963; personal obseryations). Such specialisation concentrates attack on particular plants and monophagous species may be of more value than extreme polyphagous forms in specific control programmes. For instance, Platychirus peltatus prefers brussels sprout plants to beans for oviposition (Page 69 ) and would therefore be potentially of more use in controlling Brevicoryne brassicae I. than Aphis fabae Scop. However, Syrphus latifasciatus Macq. prefers A. fabae to B. brassicae by a factor of more than ten to one (personal observations).
There is also specialisation in height preferences for oviposition (SectionE.). In general, early season species search at 6ft in preference to Oft or lft, which well equips them to find the aphids present at that time. Similarly, other species show a marked preference for 167. oviposition near the ground. By favouring the former category in spring for orchard pests and the latter at the appropriate time of year for cereals and other low-standing crops, better use may be made of existing natural enemies.
Mass rearing of aphidophagous syrphids for field release would be much more difficult than for Chrysopids (Finney, 1950). Appropriate conditions for mating under laboratory conditions have been found for S. balteatus (Schneider, 1948), S. corollae, S. ribesii and S. vitripennis Mg. (Bombosch 1957) and S. luniger (Tokmakoglu 1965), but not for other species. Adults require pollen in addition to nectar, honeydew or sugar solution for maturation of the ovaries (Schneider, 1948), but artificial. diets may be substituted with slight loss in fecundity (Wilkening 1961). However, no synthetic alternative has yet been found for the aphids required in large numbers by developing larvae. Even if larvae are reared in the laboratory on suitable aphid species, many die from bacterial attack (Kamal, 1927; Speyer, 1936; Desek cx Ldska, 1962; Steinhaus Marsh, 1962; Clark, 1963; Tokmakoglu, 1965) and this can so far only be minimised by regular and careful attention. Much research is needed before mass rearing for field release would be practicable for syrphids. 168. ACKNOWLEDGEMENTS I should like to express my thanks to:
Professor O.W. Richards for granting facilities to carry out the work at Imperial College Field Station,
Mr. M.J. Way for supervising the project and for his advice and support,
Dr. J. Smart and the Zoology Department, Cambridge, for the use of microprojection equipment in preparation of the egg key.,
Dr. S. Bombosch, Dr. J.H. Kennedy and Mr. R.I. Coe for assistance and discussion of various parts of the work,
Mrs. M.E. van Emden for German translations, Mrs. B. Murdie for assistance in preparation of the figures, Mr. H. Devitt for photography and Mrs. D.P. Ives for the typing of the manuscript,
The Science Research Council for the provision of a Postgraduate Studentship for three years. 169. REFERENCES AGWU, S.1., 1967. The biology and population dynamics of Leucoptera spartifoliella (Hb.) on broom, Sarothamnus scoparius. Thesis (Ph.D.), London University.
BALCH, R.E., 1952. Studies on the balsam woolly aphid Adelges piceae (Rats.) and its effects on Balsam Fir, Abies balsamea (L.) Pubis. Dep. Agric. Can., 867 ; 1-76.
BANKS, C.J., 1952. The natural enemies of aphids. Rep. Rothamsted exp. Stn 1952, pp.116-177.
BANKS, C.J., 1953. Studies on the predator complex of certain Aphididae (Hem.) with particular reference to Aphis fabae (hoop.). Thesis (Ph.D.), London University.
it BOSCH, R., 1964. Vergleichende Untersuchungen zur Biologie und zum Beutefang verhalten aphidovorer Coccinelliden, Chrysopiden und Syrphiden. Zool, Jb. Syst., Ql : 271-340.
BANSCH, R., 1967. On prey-seeking behaviour of aphidophagous insects. Proc. SYmp. Ecol. aphidophagous Insects, Prqpe, 1965, pp. 123-128. 170. BARBOSA, da Silva, A.J., 1953. Ischiodon aegyptium Wied. (Syrphidae, Diptera). Notas breves sobre a sua biologia e o seu valor no control biologico dos afideos do algodoeira. Mems. Trab., 9 : 317.332.
BEATIA, M.L. 1939. Biology, 'morphology and anatomy of aphidophagous syrphid larvae. Parasitology, 11 ; 78-129.
BLACKMAN, R.L., 1965. Specificity in predator-prey relationships with particular reference to the aphidophagous Coccinellidae. Thesis (Ph.D.), London University.
BOMBOSCH, . 1957. Erfahrungen tiber Laboratoriumszuchten aphidivorer Schwebfliegen. TagBer. dt. Akad. LandwWiss. Berl., 11 : 160-162.
BOMBOSCH, S., 1958. Untersuchungen dber die AuslOsung der Elablage bei aphidivoren Schwebfliegen (Dipt. Syrphidae). XV int. Congr. Zool. Lond., p:896.
BOMBOSCH, S., 1959. Ein Beitrag zur Frage biozonoseschonender Schadlingsbekampfung im RUbenbau. Verh. IV int. Pflschtz- KonAr. Hamburg, 1957., I : 975-977. 171.
BOlvDOSCH 7 Bal 1962. Untersuchungen Uber die AuslOsung der Eiablage bei Syrphus coronae Fabr. (Dipt. Syrphidae). angaw. Ent., 51(1) 81-88.
BOMBOSCH, 1963. Untersuchungen zur Vermehrung von Aphis fabae Scop. in Samenrtbenbestanden linter be sonderer Beracksichtigung der Schwebfliegen (Diptera, Syrphidae). Z. ansew. Ent., 2(2) : 105-141.
30MBOSCH, S., 1967. Distribution of enemies in different habitats during the plant growing season. Proc. Symp. Ecol. aphidophagous Insects, Prague, 1965, pp s 171-175.
BRAUNS, A., 1953. Beitrage zur Okologie and wirtschaftlichen Bedeutung der aphidivorer Syrphidenarten (Diptera). Beitr. Ent., a : 278-303.
CAMPBELL, R.E.1 & DAVIDSON, W.M., 1924. Notes on aphidophagous Syrphidae of Southern California. Bull, S. Calif. Acad. Bei., 3-9 & 59-71.
CHANDLER, A.E.F., 1967a. Oviposition responses by aphidophagous Syrphidae (Diptera). Nature, Lond., 211 : 736, 172. CHANDIZR, 1967b. Some aspects of host plant selection in aphidophagous Syrphidae (Diptera). Proc. Symp. Ecol. aphidophagous Insects, Prague, 1965. pp. 113-115.
CHAPMAN, T.A.1 1906. Food and habits of Xanthandrus comtus Harris. Entomologist's mon. Mag., 42 : 14.
CLARK, L.R., 1963. The influence of predation by Syrphus sp. on the numbers of Cardiaspina albitextura (Psyllidae). Aust. J. Zool., 11(4):470-487.
COE, R.I., 1953. Handbooks for the identification of British Insects. X(1). Diptera: Syrphidae. London. (R. ent. Soc.). 98PP.
COE, R.L., 1967. Syrphidae (In) Kloet, G.S. & Hincks, W.D., Check list of British insects. Stockport. (In Preparation).
DAVIDSON, W.M., 1916. Economic Syrphidae in California. 3. econ. Ent., : 454-457.
DAVIDSON, WM., 1922. Notes on certain species of Melanostoma (Diptera, Syrphidae). Trans. Am. ent. Soc., 48 s 35-47. 173.
DE " C., 1776. M4moires pour servir a lihistoire des insectes. Stockholm. 6.
DELUCCHI, V ., PSCHORN-WLLCHER, H., & ZMIFER, H., 1957, Onemodon-Lxten (Syrphidae) als Rauber von Dreyfusia piceae Ratz. (i,delgidae). II Morphologie and Biologie von Cnemodon dreyfusiae Del. & nebst Beobachtungen tS.ber C. latitarsis Egger. Z, angew. Ent., 41 : 246-259.
DIXON, T.J,, 1958. .,11 ecological study of Syrphidae (Diptera) with an account of their larvae. Thesis (Ph.D.), London University. (Ls White, T.J.).
DIXON, T.j., 1959. Studies on oviposition behaviour of Syrphidae (Diptera). Trans. R. ent. Soc. Lond., 111(3) : 57-80.
DIXON, T.J., 1960. Key to and descriptions of the third instar larvae of some species of Syrphidae (Diptera) occurring in Britain. Trans. R. ent. Soc. Lond., 112(13) : 345-379. 174. DUNN, J.A., 1949. The parasites and predators of potato aphids. Bull. ent. Res., 40(1) 97-122. se DUSEK, J. & ILEA, P., 1960. Weitere unbekannte Syrphidenlarven (Diptera, Syrphidae). Cas. csl. Spot.. ent., 12(4) : 371-380. V DUSEK, J. & LASKA, P.9 1962. Beitrag zur kenntOis einiger Syrphiden-larven (Diptera, Syrphidae). Cas. esl. Spots ent., 12(4) : 348-356. V DUSEK, J. & LAMA, P., 1967. Occurrence of syrphid larvae on some aphids. 12222.3 amil.1121. aphidophagous Insects, Prague, 1965. PP. T7-3Eh
MOEN, H.F. van., 1963. A field technique for comparing the intensity of mortality factors acting on the cabbage aphid Brevicoryne brassicae (L.) in different areas of a crop. Entomologia exp. appl., 6 : 53-62.
E4DEN, H.F. van., 1964. The role of uncultivated land on the biology of W.lop pests and beneficial insects. Scient. Hort., : 121-136. 175. EMDEN, H.F. van., 1965. The effect of uncultivated land on distribution of cabbage aphid on an . adjacent crop. J. aPP1. Ecol., 2 t 171-196.
II1DEN, H.F. van., 1967. The effectiveness of aphidophagous insects in reducing aphid populations. Proc. SYmp. Ecol, aphidophagous Insects, Prague, 1965. pp. 227-235.
EVENHUISI H.H.$ 1959, Cnemodon vitripennis (Meig.) as a predator of the woolly apple aphid Eriosoma lanigerum (Hausm.) Ent. Ber. Amst,, 19 : 238-240.
EVENHUIS, H.1-1,1 1967. Syrphid predators of apple aphids and their parasites. Proc. Symp. Ecol. aphidophagous Insects, Prague, 1965, Pp.191 -193.
FINNEY, G.L., 1950. Mass-culturing Chrysopa californica to obtain eggs for field distribution. J. econ. Ent., 1 : 97-100.
FUME, C.L., 1929. The known predacious and parasitic enemies of the pea aphid in North America. Bullt Wis. agric. Exp. Stn., 21 : 1-47. 176. FRIEDERICHS, K., SCHAERFFENBERG, B. & STURM, H,, 1940. Uber die Feinde des Kiefernspanners mit Berucksichtigung des Mischwaldes. Z. angaw. Ent., ?_2 : 621-641.
GABLER, H. 1938. Die Bedeutung der Larven von Syrphus tricinctus Fall. far die Vernichtung von Raupen and Afterraupen. Tharandt. forstl,Jb., 69-74.
GEORGE, K,S., 1957. Preliminary investigations on the biology and ecology of the parasites and predators of Brevicoryne brassicae (L.). Bull, ent. Res., 48 s 619-629.
GIARD, A., 1896. Sur un changement de regime des larvee de Melanostoma mellina L. (Diet.). Bull Soc. ent. Fr., .61s 231+.
GLUMAC, S., 1960. Phylogenetic system of Syrphidae based upon the male genitalia structure and the type of the larvae with characteristics of the family and tribes, Glasn, Prirod_t Muz. Beur,(B), 16 s 69-103.
E.R.1 1952. An outline of a revised classification of the Syrphidae on phylogenetic lines. Trans. Soc, Brit. Ent., 11 : 97-124. 177. GUPTA, P.D. & THORSTEINSON, A.J.9 1960. Food plant relationships of the Diamond-back moth (Plutella maculipennis (Curt.)). II Sensory regulation of oviposition of the adult female. Entomologia exp. appl., 3 : 305-314.
HAGAN, K.S. & TASL,AN, R.L., 1967. Artificial diet for Chrypopa carnea Stephens. Proc. SYmp. Ecol. aphidophagous Insects, Prague, 1165,pp.83-87.
HAYRUM, C.11.1 1967. Food utilization of the common Minnesota Syrphinae species. Proc. Symp. Ecol. aphidophagous Insects, Prague, 1965.pp.71-73.
HEEGER„ E., 1858. Neue Metamorphosen einiger Dipteren. Sber. Akad. Wiss. Wien, al ; 295-309.
E.M. 1138. A classification of the larvae and puparia of the Syrphidae of Illinois exclusive of aquatic forms. Illinois biol. Monogr., 16 : 1-1142.
HINTON, H.E., 1960. How some insects, especially the egg stages, avoid drowning when it rains. Proc S. Lond. ent, nat. Hist. Soc., 1960, PP. 138-154. 178. HINTON, H.E., 1962. The fine structure and biology of the egg-shell of the wheat bulb-fly, leptohylemyia coarctata. Q. J.1. microsc. Sci,, 103(2) : 243-251.
OLLDOBER, K., 1929. Uber die Entwicklung der Schwirrfliege Xanthogramma citrofasciatum im neste von Lasius alienus and niger. Zdol. Anz., 82 171-176.
HUGHES, R.D., 1963. Population dynamics of the cabbage aphid, Brevicorype brasnicae (L.). J. Antm. Ecol., 32_ : 393_424.
HULL, F.M., 1949. The morphology and interrelationship of the genera of syrphid flies, recent and fossil. Trans Zool. Soc. Iond., 26 : 257-408.
IBBOTSON, A., 1960. Observations on the oviposition behaviour of frit fly (Oscinella frit L.). Entomologia exp. appl., : 84-92.
ILSE, D., 1949. Colour discrimination in the dronefly, Eristalis tenax. Nature, Lond., 163:255-256. 179. 'PERT', G,, 1961. Contribution h lietude de la specificite chez les principales Coccinelles aphidiphages des Alpes-Maritimes et des Basses-Alpes. Entompphaga, 10 159-178.
JONES, C.R., 1922. A contribution to our knowledge of the Syrphidae of Colorado. Colo. agric. Bull.,269.
KOOS, W.J., 1943. Eischaal structuren bij Syrphiden. Tijdschr, Ent., 86 : 43-44.
KAMAL, M., 1927. Biological studies on some Hymenopterous parasites of aphidophagous Syrphidae. Bull. Minist. Agric, Egypt techn. scient. Serv., 207.
KIEIN-KRAUTHEIM, F., 1936. her das Chorion der Bier einiger Syrphiden (Diptera). Biol. Zbl., 6, : 323-329.
KR6GER, F., 1926. Biologie and Morphologie einiger Syrphidenlarven. Z. Morph. okol. Tiere, 6 83-149.
LAL, R. & HAQUE, E., 1955. Effect of nutrition under controlled conditions of temperature and humidity on longevity and fecundity of Sphaerophoria scutellaris (Fabr.) (Syrphidae:Diptera) -Efficacy of its maggots as aphid predators. Indian J. Ent., 1.7: 317-325.
180. LAL, R. & GUPTA, S.B.L., 1953. Morphology of the Immature stages of Sphaerophoria sautellaris (Fabr.) (Syrphidae Diptera) with notes on its biology. Indian J. Ent., 12 : 207-218.
LASKA, P., 1959. Pi:i.sperky k pozriani aphidofe'.gnich pestrenek zvlagte k potravni ekolgii larev (Syrphidae, Diptera). Bohem cent. A-1(6) : 321-344.
LUCCHESE E. 191,2. Contributi alla conoscenza dei Lepidotteri del melo: 3. Acroclita naevana Hb. Boln. Lab. Ent. Portici, : 1-120.
LUNDBECK, W., 1916. Diptera Denies, 14 (Lonchopteridae, Syrphidae). Copenhagen. 591 pp.
METCALF, C.L.„ 1916. Syrphidae of Maine. Bull. Me, agric. Exp. Stn., ala : 193-264.
YEICCALF, C.L.:t1r19.11 7:6:Yr::::717:: Maine - Second report: Life history studies. Bull. Me. agric, Exp.
NINOMYIA, E., 1957a. On the number of aphids destroyed by syrphid larvae. Jap. J. appl, Ent, Zool., 1(2) 119-124. (Biol. Abstr. (1959) 43271.) 181. NINOMYIA, E., 1957b. On the food-habits of some aphidophagaus Syrphid larvae. Jap. J. appl. Ent. Zool., 1(3) : 186-192. (Biol, Abstr. (1959) 43409.).
NORTH, C . & PRIESTLEY, LG., 1962 . A glossy-leaved mutant of Brussels sprouts. Hort. Res., 1 : 95.
PARMNTER, L., 1952. Syrphidae (Dipt.) attracted to yellow colours. Entomologistts mon. Mag., 88 : 50.
PARMENTER, L., 1954. A list of the species of Syrphidae (Diptera) of the British Isles. Entomologistls Gaz., 135-144.
PESCHKEN, D., 1965. Untersuchungen zur Orientierung aphidophager Schwebfliegen (Diptera Syrphidae). Z. angew. Ent., 12(3): 201-235.
PIMENTEL„ D., 1963. Introducing parasites and predators to control native pests. Can. Ent., 22(8) : 785-791.
RIDGWAY, R., 1912. Colour standards and colour nomenclature. Washington. 182. SCHNEIDER, F*, 1947. air ibberwinterung von Lasiopticus pyrastri L. und Lasiopticus seleniticus l'ieig. (Dipt., Syrphidae). Mitt. Schweiz. ent, Ges., 20::306-316.
SCHEEIDSH, F., 1948. Beitrag zur Kenntnis der Generationsverhaltnisse und Diapause rauberischer Schwebfliegen (Syrphidae, Dipt.). hitt. schweiz, ent, Gas., 21 : 249-285.
SCH1EIDER, F., 1953. Syrphus nigritarsis Zett., ein ai- und larvenrauper von Melasoma (Chrysom., Col.). Tijdschr. Piziekt., : 192-194.
SCOTT, E.I., 1939. An account of the developmental stages of some aphidophagous Syrphidae (Dipt.) and their parasites (Hymenopt,). Ann. aPp1. Biol., 26 : 509-532.
M.L.2 1966. Contribution lietude de Longiunguis donacis (Pass.) (Aphididae-Homoptera) et des fluctuations de ses populations en provence maritime. Annls Epiphyt., 7(2) : 147-201. 183. SMITH, H.D.1 1936. Le syrphide Xanthandrus comptus Harris, pr4dateur de la chenille processionaire du pin (Cnethocampa pinivora Tr.). Bull, Soc. ent. Fr., 41 : 328-329.
SPEYER, W., 1936. Syrphid larvae as enemies of woolly aphids. RachrBl. dt. PflSchutzdienst, Berl., : 16.
STANILAND, L.N.1 1922. Hoverflies: their habits and economic importance. Fruit Grow.la : 143-4.
STEINHAUS, E,A. & MARSH, G.A., 1962. Report of diagnoses of diseased insects, 1951-1961. Hilgardia, aa 349-490.
TELFORD, U.S., 1939. The Syrphidae of Minnesota. Bull, Minn. agric, Exp. Stn., 140 : 1-76.
TOKMAKOGLU, 0., 1965. Erfahrungen ilber die Laboratoriumszucht mit Syrphus luniger Mg. (Dipt. Syrph.). Anz. SchadlingSk,, ,3(2) : 23-25.
VERRALL„ G.H.1 1901. Platypezidae, Pipunculidae and Syrphidae of Great Britain. 8 : 127-691. London. 181+. VOLK, S., 1964. Untersuchungen zur Eiablage von Syrphus corollae Fabr. (Diptera Syrphidae).
Z. angew e Ent., 5(4) : 365-386.
WADLEY, F.M., 1931. Ecology of Toxoptera graminum, especially as to factors affecting importance in the Northern United States. Ann. ent. Soc. Amer., a4 s 325-395.
WAY, 1967. Importance of intraspecific competition in aphids. Proc. Symp. Ecol. aphidophagous Insects, Prague, 1965. p.283.
WAY, M.J. & BANKS, C.J., 1958. The control of Aphis fabae Scop, with special reference to biological control of insects which attack annual crops. X. int. Congr. Ent., 1956, : 907-909.
WIZENING, K., 1961. Refahrungen and Beobachtungen bei der Laboratoriumszuchtvon Syrphus corollae Fhbr. Z. angew. Zool., 48 : 221-240.
YAKHONTOV, V.V., 1967. Coccinellidae and Syrphidae as predators of aphids in Uzbekistan. Proc, Symp. Ecol. aphidophagaus Insects, Praguei 1965, pp.267-269.