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Urophora Jaceana (Hering) Dispute

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I I39 1 THE NATURAL CONTROL OF POPULATION BALANCE IN THE KNAPWEED GALL-FLY (UROPHORA YACEANA) BYG. C. VARLEY,King's College,Newcastle upon Tyne (With i i Figures in the Text) CONTENTS PAGE PART I . 140 I. INTRODUCTION I. 40 2. THE CENSUS I. 14 3. THE LIFE HISTORY OF THE KNAPWEED GALL-FLY 2. I4 PART 2. THE FACTORS WHICH AFFECT THE ADULT GALL-FLIES AND THEIR FECUNDITY 146 i. THE FECUNDITY OF THE GALL-FLIES IN THE FIELD. I46 2. THE EXPERIMENTAL MEASUREMENT OF FECUNDITY. I. 48 (a) The effect of mating on fecundity . 149 (b) The effect of feeding on fecundity . - . 149 (c) The effect of combinations of temperature and humidity on fecundity . 50 3. FIELD OBSERVATIONS ON THE ADULT GALL-FLIES . I52 (a) The population density of the gall-flies and its bearing on their fecundity. I52 (b) Experiment on the dispersal of adult gall-flies . I53 (c) The effect of weather on the behaviour of the gall-flies . I54 (d) The rate of oviposition in the field . 155 (e) The effect of weather on fecundity . 157 PART 3. THE FACTORS WHICH AFFECT THE SURVIVAL OF THE EGGS, LARVAE AND PUPAE OF THE GALL-FLY . I57 i. THE MORTALITY UP TO THE FORMATION OF THE GALL . 58 (a) The egg mortality in 1935 . 158 (b) The mortality of the larvae up to the formation of the gall in 1935 . 58 (c) The egg mortality in 1936 . i6o (d) The mortality of the larvae up to the formation of the gall in 1936 . i6o 2. THE MORTALITY AFTER THE FORMATION OF THE GALL . i6i (a) Winter disappearance . I6I (b) Mortality due to mice . I63 (c) Mortality due to unknown causes . I63 (d) Mortality due to chalcid parasites . I64 (I) Eurytoma curta . I64 (2) Eurytoma robustar. I67 (3) Habrocytus trypetae. 68 (4) Torymuscyanimus . 71 (5) Macroneuravesicularis .1 . .. I7 I (6) Tetrastichussp. B 172 (e) Mortality due to caterpillars . 173 (i) Eucosma hohenwartiana . 173 (2) Metzneria metzneriella . I174 (3) Euxanthisstraminea . .1 . I74 PART 4. DISCUSSION AND CONCLUSIONS . I74 SUMMARY . I82 ACKNOWLEDGEMENTS . I 82 REFERENCES . I86 This content downloaded on Fri, 8 Mar 2013 13:36:49 PM All use subject to JSTOR Terms and Conditions I40 Natural control of population balancein the knapweedgall-fly PART I The knapweed gall-fly, Urophorajaceana(Hering)* (Diptera, Trypetidae), is a member of a large and I.INTRODUCTION complex insect community which lives in the In this contribution to insect ecology the theory of flower-heads of the black knapweed Centaurea balance of animal populations, formulated by nemoralis-Jordan (Compositae). Owing to a happy Nicholson (I933) and Nicholson & Bailey (1935), is series of peculiarities in its life history, the gall-fly used for the first time in the interpretation of the provides particularly suitable material for the study results of a field survey. The conclusions are of population problems in the field. sufficiently striking to claim the attention both of The problem considered here is formulated thus: ecologists and economic zoologists, and their im- What factors control the population density of Uro- portance goes beyond that of the insect material on phora jaceana in nature, and how do they operate? which they are based. Nicholson (I933, p. 135) states that 'a controlling It is now more than twenty years since Lotka factor should act more severely against an average published his mathematical studies on the inter- individual when the density of animals is high, and action between predators and prey which were less severely when the density is low. In other words, applied by Gause (1934) to the oscillations in the the action of the controlling factor must be governed population densities of protozoan predators and by the density of the population controlled.' Control- prey under constant environmental conditions in ling factors, with or without the help of other factors, vitro. Nicholson & Bailey's formulation of the can therefore maintain a species in a state of balance simpler situation which arises when a sp-ecific insect at such an average population density that over a parasite and its host have synchronized generations period of years these factors kill the surplus popula- was first shown to apply under idealized laboratory tion. Where other factors permit its survival it is the conditions by the neat experiment of de Bach & controlling factors which mainly determine whether Smith (I94i), where the oscillations in the population a species shall be rare or common. density of parasite and host agreed excellently with Two groups of controlling factors can be distin- the theory over a period of eight generations. guished. The first have been termed density dependent The present work provides the first attempted factors by Smith (I935). They may be recognized by confirmation from field data of the basic assumptions the fact that at any time the severity of their action of the theory of Nicholson & Bailey. The theory is increases as the population density rises. Intra- subsequently used to interpret the interaction be- specific competition for limited food supply or tween the various factors destroying the knapweed limited space operates in this way, and the sigmoid gall-fly. The quantitative effect of each factor can population curves obtained by Pearl (I925) for be examined separately. The clarification of a com- Drosophila cultures, and by many subsequent plex situation achieved in this way may provide workers for other species, are explicable on this view the economic entomologist with a new and powerful (see Crombie, 1945). According to Nicholson's technique. And the rather paradoxical nature of theory, limitation of host population density acts in the conclusions reached may well revolutionize the the same way on the increase of parasites and pre- methods of assessing the probable value of different dators. However, the parasites and predators also projectedcontrolmeasures to be applied to insectpests. exercise a reciprocal influence on the numbers of the If the cause operating to produce balance in the species on which they feed. population density of a species is known to be a This reciprocal reaction provides a second type of parasite, workers seeking either to reduce, conserve, controlling factor, to which it is proposed to apply or increase the population density of the species can the new term delayed density dependent factor. A use Nicholson & Bailey's theory to investigate the parasite acts as a delayed density dependent factor long-term effects on the balance which may be if its fecundity or its effective rate of increase is expected from any alteration of conditions. strongly correlated with host density. Nicholson * Until I937 the knapweed gall-fly was known in this the genus Euribia Latreille i802 as valid. This is closely country as Urophora solstitialis (L.), but it had long been bound up with the very vexed question of the validity of known that continental U. solstitialis was usually a gall-fly Meigen's I8oo names, of which Euribia is one (see of thistles. However, gall-flies bred from the continental Collin, 1946). knapweed Centaurea jacea were found to differ from the Both Seguy (I934) and Kloet & Hincks (I945) accept thistle species, and were described as new by Hering the genus Urophora of Robineau-Desvoidy I830, and (I935) under the name jaceana. Collin (1937) has found they are followed here. So it comes about that the knap- that the British specimens from knapweed are in fact weed gall-fly was called Urophora solstitialis (L.) by jaceana, and not solstitialis. Varley & Butler (I933), Euribia jaceana Hering by The generic name of the knapweed gall-fly is a point of Varley (I937a, b, I94I), and Urophora jaceana (Hering) dispute. Collin (I937) follows Hendel (I927) in accepting in this present paper ! This content downloaded on Fri, 8 Mar 2013 13:36:49 PM All use subject to JSTOR Terms and Conditions G. C. VARLEY 14I assumes that if the host density rises above the dry up, and finally their remains fall off in a lump, density of the steady state in which host and parasite leaving the ripening fruits behind. The fruits, when are in equilibrium, the percentage of hosts destroyed ripe, get squeezed out as the bracts dry and con- by the first parasite generation will not increase, but tract. Towards the end of the summer some of the remain unchanged. The number of hosts killed, and flower-heads fall to the ground. As the winter therefore the number of parasites emerging in the advances more and more flower-heads fall, until in next generation, will be proportionately greater. the following June less than a third of them remain Only after this delay of one generation will the on the dry and bleached stems. increased parasite population begin to destroy a greater proportion of hosts. Eventually after two or more generations the host density will be reduced. This fall in host density will in turn be followed by a fall in parasite density, which will allow the hosts to increase once more. These oscillations are essentially similar to those predicted independently by Lotka (I925) and Volterra (I926, I93 I) (for more complete references see Thompson, 1939). They have been observed experimentally by de Bach & Smith (I94I). In order to find how the mortality factors control ,..,#w:;:~~~~X W l, OOD LAND the population density of the knapweed gall-fly the following programme of work has been carried out. The natural rate of increase of the gall-fly has been measured under field conditions, and the factors which influence this have been studied. The mortality due to all causes has been assessed, and an HAY examination made to determine which are density dependent factors, and which delayed density de- pendent factors.
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